Vol. 79 Wednesday, No. 175 September 10, 2014

Part II

Department of Commerce

National Oceanic and Atmospheric Administration 50 CFR Part 223 Endangered and Threatened Wildlife and Plants: Final Listing Determinations on Proposal To List 66 Reef-Building Coral Species and To Reclassify Elkhorn and Staghorn Corals; Final Rule

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DEPARTMENT OF COMMERCE ADDRESSES: Submit responses to the Mycetophyllia ferox, Oculina varicosa, request for information regarding a Pachyseris rugosa, Pavona bipartita, National Oceanic and Atmospheric subsequent ESA section 4(d) Rule and Pavona cactus, Pavona decussata, Administration critical habitat designation to National Pavona diffluens, Pavona venosa, Marine Fisheries Service, Pacific Islands Pectinia alcicornis, Physogyra 50 CFR Part 223 Regional Office, NOAA Inouye Regional lichtensteini, Pocillopora danae, Center, 1845 Wasp Blvd., Building 176, Pocillopora elegans, Porites [Docket No. 0911231415–4826–04] Honolulu, HI 96818; or National Marine horizontalata, Porites napopora, Porites Fisheries Service, Southeast Regional nigrescens, Porites pukoensis, RIN 0648–XT12 Office, 263 13th Avenue South, Saint Psammocora stellata, Seriatopora Petersburg, FL 33701. aculeata, Turbinaria mesenterina, Endangered and Threatened Wildlife Turbinaria peltata, Turbinaria and Plants: Final Listing FOR FURTHER INFORMATION CONTACT: Lance Smith, NMFS, Pacific Island reniformis, and Turbinaria stellulata. Determinations on Proposal To List 66 Eight of the petitioned species occur in Reef-Building Coral Species and To Regional Office, 808–725–5131; Jennifer Moore, NMFS, Southeast Regional the Caribbean, and 75 of the petitioned Reclassify Elkhorn and Staghorn species occur in the Indo-Pacific region. Corals Office, 727–824–5312; or Marta Nammack, NMFS, Office of Protected Most of the 83 species can be found in AGENCY: National Marine Fisheries Resources, 301–427–8469. A list of the the United States, its territories (Puerto Service (NMFS), National Oceanic and literature cited in this rule is available Rico, U.S. Virgin Islands, Navassa, Atmospheric Administration (NOAA), at http://coral.sero.nmfs.noaa.gov and Northern Mariana Islands, Guam, Commerce. http://www.fpir.noaa.gov/PRD/prd_ American Samoa, Pacific Remote Island Areas), or its freely associated states ACTION: Final rule. coral.html. (Republic of the Marshall Islands, SUPPLEMENTARY INFORMATION: SUMMARY: We, the National Marine Federated States of Micronesia, and Fisheries Service (NMFS), are Background Republic of Palau), though many occur more frequently in other countries. publishing this final rule to implement On October 20, 2009, the Center for On February 10, 2010, we published our final determination to list the Biological Diversity (CBD) petitioned us following 20 species as threatened: five a 90-day finding (75 FR 6616) that CBD to list 83 reef-building corals as had presented substantial information in the Caribbean (Dendrogyra cylindrus, threatened or endangered under the Orbicella annularis, Orbicella faveolata, indicating the petitioned actions may be Endangered Species Act (ESA) and warranted for all of the petitioned Orbicella franksi, and Mycetophyllia designate critical habitat. The 83 species ferox); and 15 in the Indo-Pacific species except for the Caribbean species included in the petition were: Oculina varicosa. We also announced (Acropora globiceps, Acropora Acanthastrea brevis, Acanthastrea jacquelineae, Acropora lokani, the initiation of a formal status review hemprichii, Acanthastrea ishigakiensis, of the remaining 82 petitioned species, Acropora pharaonis, Acropora retusa, Acanthastrea regularis, Acropora Acropora rudis, Acropora speciosa, and we solicited input from the public aculeus, Acropora acuminata, Acropora on six categories of information: (1) Acropora tenella, Anacropora spinosa, aspera, Acropora dendrum, Acropora Euphyllia paradivisa, Isopora Historical and current distribution and donei, Acropora globiceps, Acropora abundance of these species throughout crateriformis, Montipora australiensis, horrida, Acropora jacquelineae, their ranges (U.S. and foreign waters); Pavona diffluens, Porites napopora, and Acropora listeri, Acropora lokani, (2) historical and current condition of Seriatopora aculeata) under the Acropora microclados, Acropora these species and their habitat; (3) Endangered Species Act (ESA) of 1973, palmerae, Acropora paniculata, population density and trends; (4) the as amended. The two species currently Acropora pharaonis, Acropora effects of climate change on the listed as threatened (Acropora polystoma, Acropora retusa, Acropora distribution and condition of these coral cervicornis and Acropora palmata) in rudis, Acropora speciosa, Acropora species and other organisms in coral the Caribbean still warrant listing as striata, Acropora tenella, Acropora reef ecosystems over the short and long threatened. We also determined that a vaughani, Acropora verweyi, Agaricia term; (5) the effects of all other threats total of 43 proposed species do not lamarcki, Alveopora allingi, Alveopora including dredging, coastal warrant listing as endangered or fenestrata, Alveopora verrilliana, development, coastal point source threatened species, and three proposed Anacropora puertogalerae, Anacropora pollution, agricultural and land use species are not determinable under the spinosa, Astreopora cucullata, practices, disease, predation, reef ESA. We have reviewed the status of the Barabattoia laddi, Caulastrea fishing, aquarium trade, physical species and efforts being made to echinulata, Cyphastrea agassizi, damage from boats and anchors, marine protect the species, and public Cyphastrea ocellina, Dendrogyra debris, and aquatic invasive species on comments received on the proposed cylindrus, Dichocoenia stokesii, the distribution and abundance of these rule, and we have made our Euphyllia cristata, Euphyllia coral species over the short- and long- determinations based on the best paraancora, Euphyllia paradivisa, term; and (6) management programs for scientific and commercial data Galaxea astreata, Heliopora coerulea, conservation of these species, including available. We also solicit information Isopora crateriformis, Isopora cuneata, mitigation measures related to any of that may be relevant to the designation Leptoseris incrustans, Leptoseris yabei, the threats listed under No. 5 above. of critical habitat for the 20 species Millepora foveolata, Millepora tuberosa, The ESA requires us to make newly listed under this final rule. Montastraea annularis, Montastraea determinations on whether species are DATES: The effective date of this final faveolata, Montastraea franksi, threatened or endangered ‘‘solely on the rule is October 10, 2014. Responses to Montipora angulata, Montipora basis of the best scientific and the request for information regarding a australiensis, Montipora calcarea, commercial data available * * * after subsequent ESA section 4(d) Rule and Montipora caliculata, Montipora conducting a review of the status of the critical habitat designation must be dilatata, Montipora flabellata, species * * * ’’ (16 U.S.C. 1533). received by November 10, 2014. Montipora lobulata, Montipora patula, Further, our implementing regulations

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specifically direct us not to take related to the SRR and the Draft Caribbean corals (Acropora cervicornis possible economic or other impacts of Management Report prior to issuing our and Acropora palmata) warranted listing species into consideration (50 12-month finding. Thus on April 17, reclassification from threatened to CFR 424.11(b)). We convened a Coral 2012, we published a Federal Register endangered. The findings in the Biological Review Team (BRT) notice announcing the availability of the proposed rule were based on the composed of seven Federal scientists SRR and the Draft Management Report, information contained within the from NMFS’ Pacific Islands, Northwest, and specifically requested information reports described above (SRR, SIR, and and Southeast Fisheries Science on the following: (1) Relevant scientific Final Management Report). During a 90- Centers, as well as the U.S. Geological information collected or produced since day comment period, we solicited Survey and National Park Service. The the completion of the SRR or any comments from the public, other members of the BRT are a diverse group relevant scientific information not concerned governmental agencies, the of scientists with expertise in coral included in the SRR; and (2) relevant scientific community, industry, foreign biology, coral ecology, coral taxonomy, management information not included nations in which the species occur, and physical oceanography, global climate in the Draft Management Report, such as any other interested parties on our change, coral population dynamics and descriptions of regulatory mechanisms proposal. We later extended the public endangered species extinction risk for greenhouse gas (GHG) emissions comment period by 30 days, making the evaluations. The BRT’s comprehensive, globally, and for local threats in the 83 full comment period 120 days. We peer-reviewed Status Review Report foreign countries and the United States, received approximately 32,000 (SRR; Brainard et al., 2011) incorporates its territories (Puerto Rico, U.S. Virgin comments through electronic and summarizes the best available Islands, Navassa, Northern Mariana submissions, letters, and oral testimony scientific and commercial information Islands, Guam, American Samoa, Pacific from public hearings held in Dania as of August 2011 on the following Remote Island Areas), or its freely Beach, FL; Key Largo, FL; Key West, FL; topics: (1) Long-term trends in associated states (Republic of the Rio Piedras, Puerto Rico; Mayaguez, abundance throughout each species’ Marshall Islands, Federated States of Puerto Rico; Christiansted, St. Croix, range; (2) potential factors for any Micronesia, and Republic of Palau), U.S. Virgin Islands; Charlotte Amalie, decline of each species throughout its where the 82 petitioned coral species St. Thomas, U.S. Virgin Islands; Hilo, range (human population, ocean collectively occur. Further, in June Hawaii, HI; Kailua Kona, Hawaii, HI; warming, ocean acidification, 2012, we held listening sessions and Kaunakakai, Molokai, HI; Wailuku, overharvesting, natural predation, scientific workshops in the Southeast Maui, HI; Lihue, Kauai, HI; Honolulu, disease, habitat loss, etc.); (3) historical region and Pacific Islands region to Oahu, HI; Hagatna, Guam; Saipan, and current range, distribution, and engage the scientific community and the Commonwealth of the Northern habitat use of each species; (4) historical public in-person. During this public Marianas Islands (CNMI); Tinian, CNMI; and current estimates of population size engagement period, which ended on Rota, CNMI; Tutuila, American Samoa; and available habitat; and (5) knowledge July 31, 2012, we received over 42,000 and Washington, DC. of various life history parameters (size/ letters and emails. Also, we were During the public comment period, age at maturity, fecundity, length of provided with or we identified we received numerous comments on the larval stage, larval dispersal dynamics, approximately 400 relevant scientific proposed listing and the sufficiency or etc.). The SRR evaluates the status of articles, reports, or presentations that accuracy of the available data used to each species, identifies threats to the were produced since the SRR was support the proposed listing species, and estimates the risk of finalized, or not originally included in determinations. In particular, comments extinction for each of the species out to the SRR. We compiled and synthesized raised questions and provided varied, the year 2100. The BRT also considered all relevant information that we often conflicting, information regarding the petition, comments we received as identified or received into the the following topics: a result of the 90-day finding (75 FR Supplemental Information Report (SIR; (1) The proposed species’ listing 6616; February 10, 2010), and the NMFS, 2012c). Additionally, we statuses (e.g., certain species proposed results of the peer review of the draft incorporated all relevant management as endangered should be threatened); SRR, and incorporated relevant and conservation information into the (2) the sufficiency and quality, or lack information from these sources into the Final Management Report (NMFS, thereof, of the species-specific final SRR. Additionally, we developed a 2012b). Therefore, the 82 candidate information used for each species’ supplementary, peer-reviewed Draft coral species comprehensive status proposed listing determination; (3) the accuracy of the methods used Management Report (NMFS, 2012a) to review consists of the SRR (Brainard et to analyze the available information to identify information relevant to ESA al., 2011), the SIR (NMFS, 2012c), and assess extinction risk (including NMFS’ factor 4(a)(1)(D), inadequacy of existing the Final Management Report (NMFS, ‘‘Determination Tool’’) and derive regulatory mechanisms, and protective 2012b). listing statuses for each of the proposed efforts that may provide protection to On December 7, 2012, we published species; the corals pursuant to ESA section 4(b). a proposed rule (77 FR 73219) to list 12 (4) the ability of corals to adapt or The response to the petition to list 83 of the petitioned coral species as acclimatize to ocean warming and coral species is one of the broadest and endangered (five Caribbean and seven acidification; most complex listing reviews we have Indo-Pacific) and 54 coral species as (5) the reliability, certainty, scale, and ever undertaken. Given the petition’s threatened (two Caribbean and 52 Indo- variability of future modeling and scale and the precedential nature of the Pacific), and we determined 16 coral predictions of climate change; and issues, we determined that our decision- species (all Indo-Pacific) did not (6) the effect local management efforts making process would be strengthened warrant listing as threatened or have on coral resilience. if we took additional time to allow the endangered under the ESA. This was After considering these comments, we public, non-Federal experts, non- the final agency action for those species found that substantial disagreement governmental organizations, state and which we determined were not existed regarding the sufficiency and territorial governments, and academics warranted for listing. We also accuracy of the available data used in to review and provide information determined that two currently listed support of the proposed determinations.

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As a result, we determined it was Section 3 of the ESA further defines Given the precedential and complex necessary to solicit additional data from an endangered species as ‘‘any species nature of this rule-making process, we those scientists who were identified by which is in danger of extinction took extra steps to assemble the best public comments and others who may throughout all or a significant portion of available information for informing the have additional data to assist in its range’’ and a threatened species as final listing determinations. Efforts to resolving the substantial disagreement. one ‘‘which is likely to become an acquire this information first included Therefore, pursuant to the ESA section endangered species within the the formation of an expert scientific 4(b)(6)(B)(i), we determined that a 6- foreseeable future throughout all or a panel (BRT) that used the best available month extension of the deadline for significant portion of its range.’’ Section scientific information at that time in a final determinations on the proposed 4(a)(1) of the ESA requires us to structured decision-making process to rule was necessary (78 FR 57835; determine whether any species is inform and write the SRR. Further, this September 20, 2013). We completed our endangered or threatened due to any process provided numerous data collection effort in the fall of 2013, one or a combination of the following opportunities for public input, and the relevant information that we five factors: (A) The present or including a public comment period after received or collected was considered in threatened destruction, modification, or the 90-day finding in 2010 (75 FR 6616; the formulation of this final rule. The curtailment of its habitat or range; (B) February 10, 2012), a unique public data collection effort was the final step overutilization for commercial, information-gathering period (77 FR in our thorough process to assemble the recreational, scientific, or educational 22749; April 17, 2012) prior to the best available information on the status purposes; (C) disease or predation; (D) release of the proposed rule in 2012, of the species addressed in this final the inadequacy of existing regulatory and a 120-day formal public comment rule. As a result, this final rule mechanisms; or (E) other natural or period after the publication of the represents a logical evolution from the manmade factors affecting its continued proposed rule. Finally, in a targeted proposed rule, including some changes existence. We are required to make data-solicitation effort to resolve in our overall decision-making listing determinations based solely on substantial scientific disagreement in framework and a holistic the best scientific and commercial data the public comments on the proposed reconsideration of the key elements that available after conducting a review of rule, we published a 6-month extension contribute to a species’ listing status, as the status of the species and after taking in September 2013 to gather additional described in detail throughout this rule. into account efforts being made by any information to further inform our final Consequently, most of the listing state or foreign nation to protect the decisions (78 FR 57835; September 20, determinations have changed between species. 2013). Over the course of this multi-year process, we gathered and reviewed the proposed and final rules. This finding begins with an overview thousands of scientific papers, journal of coral biology, ecology, and taxonomy Listing Species Under the Endangered articles, reports, and presentations in the Corals and Coral Reefs section Species Act (bibliography and select documents below, including whether each available at http://www.nmfs.noaa.gov/ We are responsible for determining proposed species meets the definition of pr/species/invertebrates/corals.htm). In whether the 66 proposed coral species a ‘‘species’’ for purposes of the ESA. addition, we held a total of 19 public should be listed as threatened or Specifically, are the proposed species hearings in 2012 and 2013 throughout endangered under the ESA, and whether determinable under the ESA given any the Southeast and Pacific Islands the two species proposed for discrepancies between their current regions, and received and reviewed over reclassification should be listed as morphologically-based taxonomy and 75,000 public comments during the endangered under the ESA (16 U.S.C. any new genetic information that may information-gathering period in 2012 1531 et seq.). Clonal, colonial result in taxonomic reclassification. and the proposed rule public comment organisms, such as corals, are vastly Other relevant background information period in 2012–2013, combined. These different in their biology and ecology in this section includes the general efforts ensure that this final rule is than vertebrates, which are typically the characteristics of the habitats and based upon the best available focus of ESA status reviews. Therefore, environments in which the proposed information on the proposed species at concepts and terms that are typically species are found. The finding then this time, as explained in more detail applied to vertebrates have very distinct summarizes information on factors below. meanings when applied to corals. A adversely affecting and posing ‘rare’ coral may have millions of extinction risk to corals in general in the Summary of Comments Received colonies as compared to a ‘rare’ Threats Evaluation section. The Risk Below we address the comments vertebrate, which may only have Analyses section then describes the received pertaining to the proposed hundreds of individuals. To be framework applied to each of the listings or reclassifications of the 68 considered for listing under the ESA, a species that resulted in final listing coral species in the December 7, 2012, group of organisms must constitute a statuses for the proposed species. The proposed rule (77 FR 73219). During the ‘‘species,’’ which is defined in section 3 Species-specific Information and 120-day public comment period from of the ESA to include ‘‘any subspecies Determinations section provides the December 7, 2012, to April 6, 2013, we of fish or wildlife or plants, and any best available species-specific received 1,120 written and verbal distinct population segment of any information, which, coupled with the responses (including public testimony species of vertebrate fish or wildlife general portions of this final rule, during the 19 public hearings). This which interbreeds when mature.’’ In the provide the basis for the individual included 1,119 unique comments on the case of reef-building corals, the decision determinations for final listing status. proposed listings or reclassifications that a species is a listable entity is often Finally, we assessed efforts being made and 32,000 action alert responses in complicated by several aspects of their to protect the species and determined if support of the rule organized by the biology including individual these efforts are adequate to mitigate petitioner CBD, which substantively delineation, taxonomic uncertainty, impacts and threats to the extent that a constitutes one unique comment, and. identification uncertainty, and life species does not meet one of the The public comments received covered history (e.g., colonialism and clonality). statutory statuses. a wide breadth of topics, many of which

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were significant and within the scope of possible to determine the listing status these species that there is not sufficient this rule-making. We summarized the of these species with adequate evidence to support listing comments, and these summaries and confidence. determinations of threatened or our responses are organized according Response: The comments correctly endangered for either species. This is to the sections of the proposed rule on note that in some instances, lack of explained in more detail in each which those comments were based. We information, or ambiguity and species’ individual determination. have considered all public comments, uncertainty in available information, is Comment 2: Related to Comment 1, and we provide responses to all relevant so great that any listing determination one comment identified Pocillopora as a issues raised by comments. We have not on such a basis would be arbitrary. In problematic taxon and provided a recent responded to comments outside the our judgment, that is not the case for the scientific paper describing new genetic scope of this rulemaking, such as proposed species, with a few exceptions evidence of taxonomic contradictions comments regarding the potential noted below. The SRR concluded that between genetic and morphologic economic impacts of ESA listings, the 68 species in the proposed rule were results for Pocillopora species (Pinzo´n comments suggesting that certain types determinable, including the species for et al., 2013). of activities be covered in any future which the SRR found that splitting or Response: Based on information regulations pursuant to ESA section 4(d) lumping petitioned species was summarized in the SRR, the proposed for threatened species, or whether ESA necessary based on genetic studies. For rule split P. elegans into Indo-Pacific listings are appropriate for species the proposed rule, we agreed with the and Eastern Pacific nominal species, threatened by climate change. As SRR, and considered the 68 species to and proposed P. elegans (Indo-Pacific), explained in the Background above, this be determinable for purposes of P. elegans (Eastern Pacific), and P. final rule was extended by 6 months to conducting a status review and danae for listing (P. danae only occurs resolve substantial scientific determining listing status under the in the Indo-Pacific). However, after disagreement in the public comments ESA. considering new information on on six topics related to the proposed The public comments did not provide taxonomic uncertainty throughout the listing. any studies or results, nor did we find genus Pocillopora that has become any new studies or results, that available since the publication of the Comments on Taxonomic Uncertainty significantly contradict the proposed rule, including the paper in Reef-Building Corals consideration of the traditional, (Pinzo´n et al., 2013) submitted by the Comment 1: Many public comments morphologically described species as commenter, we no longer consider the on the proposed listing rule stated that determinable species, with the three Pocillopora species that were species identification uncertainties and exception of Pocillopora. We proposed for listing to be determinable taxonomic uncertainties associated with acknowledged in the proposed rule, under the ESA. A range-wide many reef-building corals are however, that the taxonomic uncertainty phylogeographic survey that included problematic for the ESA listing for reef-building corals is not only real most currently recognized pocilloporid determination process. Four comments (Brainard et al., 2011), but increasing in species found that reliance on colony specifically stated that the ability to recent years as genetics studies have morphology is broadly unreliable for determine the status of coral species advanced (Stat et al., 2012; Veron, species identification, and that several under the ESA is impeded by the 2013). In the case of Pocillopora species, genetic groups have highly limited taxonomic uncertainty of many coral the taxonomic uncertainty has recently geographic distributions. The study species. Two comments stated that increased substantially such that the concluded that ‘‘a taxonomic revision genetic and genomic science is just three proposed species in this genus are informed foremost by genetic evidence beginning for corals, and as it develops not determinable under the ESA (see is needed for the entire genus’’ (Pinzo´n it will likely show the current Comment 2). For the remaining 65 et al., 2013). Similarly, a morphologically-based taxonomy is species, the best available scientific phylogeographic survey of several incorrect, completely changing current information continues to support their currently recognized pocilloporid coral taxonomy. Therefore, management classification as species. The taxonomic species representing a range of atypical decisions based on the current uncertainty associated with each species morphologies thought to be rare or taxonomy should be approached with is considered along with other types of endemic to remote locations throughout caution. One comment stated that uncertainty when determining the status the Indo-Pacific found that: (1) The proper species identification, especially of each species in the Species-specific current taxonomy of Pocillopora based for the Indo-Pacific Acropora genus, is Information and Determinations section. on colony morphology shows little difficult and exacerbated by the use of In this way, the species identification correspondence with genetic groups; (2) outdated and inadequate information. and taxonomic uncertainty for each colony morphology is far more variable Most of these comments are based on species is acknowledged and than previously thought; and (3) there species identification uncertainties and incorporated into each of the 65 are numerous cryptic lineages (i.e., two the conflicting taxonomic results determinations in this final rule. or more distinct lineages that are between recent genetics studies and In this final rule, even though classified as one due to morphological traditional morphology-based Millepora foveolata and Montipora similarities). The study concluded that taxonomy, and comments identified two lobulata were affirmed to be valid ‘‘the genus Pocillopora is in need of potential problems: (1) Species species, and there are few if any taxonomic revision using a combination identification and taxonomic taxonomic uncertainty issues, the two of genetic, microscopic characters, and uncertainty prevents many reef-building species are so difficult to identify in the reproductive data to accurately coral taxa, especially in the Indo-Pacific, field that there is very little reliable delineate species’’ (Marti-Puig et al., from being determinable species under information available for either species 2013). Likewise, a more limited study of the ESA; and (2) even if these taxa are (Fenner, 2014b). Thus, as described in several currently recognized determinable species under the ESA, the the Species-specific Information and pocilloporid species in Moorea found taxonomic uncertainty confounds the Determinations below for M. foveolata that genetic groups do not correspond to available information regarding the and M. lobulata, the species colony morphology, and exhibit a wide status of each species, thus it is not identification uncertainty is so high for range of morphological variation

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(Forsman et al., 2013). These studies Therefore, we are withdrawing our there is insufficient information on demonstrate that colony morphology in proposal to list P. elegans (Indo-Pacific) productivity and connectivity on which pocilloporids is a poor indicator of as threatened, P. elegans (Eastern to base listing decisions. taxonomic relationships, for the Pacific) as endangered, and P. danae as Response: Coral reproduction and following reasons: (1) Morphologically threatened; these species are not connectivity are addressed generally in similar colonies may not be the same considered further in this final rule. the Reproductive Life History of Reef- species (i.e., colonies of different Comment 3: Several comments building Corals section. As each species appear similar because of objected to our agreement with the proposed coral species has a different similar environmental conditions or SRR’s (Brainard et al., 2011) lumping of reproductive life history, we more other reasons); and (2) morphologically Montipora dilitata, M. flabellata, and M. comprehensively address each species’ different colonies may be the same turgescens into a single species, as well reproduction, connectivity, and species (i.e., colonies of the same as the lumping of M. patula and M. recruitment (when that information was species appear different because of verrilli into a single species, based on available) as they relate to each species’ different environmental conditions or the results of a single genetics study by status under the ESA in the Species- other reasons). Forsman et al. (2010). specific Information and Determinations Response: The objections in the While the current literature supports section. The public comments did not public comments to lumping Montipora the taxonomic division of pocilloporids provide any studies or information on dilitata/M. flabellata/M. turgescens and geographically into Indo-Pacific and reproduction or connectivity for any M. patula/M. verrilli did not provide species except for Acropora cervicornis Eastern Pacific groups, it indicates a any new or supplemental information, (see Species-specific Information and high level of taxonomic uncertainty for nor did we find any new or Determinations section). Any all Pocillopora species that are found in supplemental information, contradicting supplemental information we found is both areas, such as P. elegans. Within the key study used by the SRR to included in Species-specific these two geographic areas, colonies consider these species as a group. We Information and Determinations section. that resemble P. elegans may be must use the best available science on different species, including possibly which to base our determinations, and Comments on Distribution and still undescribed species. That is, there is no indication that Forsman et al. Abundance of Reef Building Corals colonies may merely resemble P. (2010) is in error. However, as discussed Comment 5: We received several elegans because of similar in the response to Comment 1, we comments regarding the distribution environmental conditions or other acknowledge that coral taxonomy is a and abundance of reef-building corals, reasons, but actually may be different rapidly growing field and that is creates mainly regarding the lack of species- species. And the opposite type of uncertainty in determining a species specific information for many species’ taxonomic uncertainty also appears to under the ESA. This taxonomic geographic distributions and population be common, as colonies that do not uncertainty is considered in the abundances. There were only a few resemble P. elegans may actually be P. individual Species-specific Information comments related to determining the elegans. That is, colonies that are P. and Determination for the Montipora. distribution and abundance of reef elegans appear different because of building corals, specifically on different environmental conditions or Comments on Reproductive Life History extrapolating individual corals to other reasons (Forsman et al., 2013; of Reef-Building Corals overall population abundance and Marti-Puig et al., 2013; Pinzo´n et al., Comment 4: There were only a few distribution, on which to base a listing 2013). The recently appreciated comments related to the reproductive decision. One comment stated that coral taxonomic uncertainty is in addition to life history of corals. One comment population size and structure across the the historical morphological taxonomic stated that coral reef connectivity data world’s oceans is nearly impossible to uncertainty within the genus are sparse, and while the majority of determine with any accuracy because Pocillopora and for P. elegans published studies on coral larval we use crude substitutes for individual specifically (Veron, 2013; Veron, 2014). dispersal report evidence of local animals in determining population and While P. danae does not occur in the seeding and replenishment of reefs, range information within a species. For Eastern Pacific, similar taxonomic other models and studies report example, there is a significant difference uncertainty problems occur for this sporadic periods of longer distance between using colony population and species. That is, this species also had dispersal and recruitment events. The range estimates versus using polyp historical morphological taxonomic commenter felt that the proposed rule population and range estimates, which uncertainty (Veron, 2013), which has did not adequately address coral are essentially impossible to estimate. recently been compounded by genetic population dynamics and connectivity Another comment stated that it is not taxonomic uncertainty, leading Veron in determining the status of the accurate to equate percent coral cover (2014) to conclude that the species candidate coral species under the ESA. on reefs to population abundance (i.e., likely requires a taxonomic revision. A Another comment stated that there is numbers of individuals). Any loss of new taxonomic revision of Pocillopora almost no information on any of the coral cover often is manifest by loss of was published, in which P. danae was species’ trends or recruitment rates, and coral tissue over large portions of still found to be a synonym of P. verrucosa, the limited information available is living colonies, without the loss of the resulting in the traditional P. danae based on qualitative opinion, not individual. Furthermore, it is unclear being included within P. verrucosa quantitative data. The comment also whether the loss of many separate but (Schmidt-Roach et al., 2014). However, pointed out that the proposed rule genetically-identical colonies (‘clones’) the overall taxonomic uncertainty agreed that the term ‘recruit’ could be equates to the loss of a single but within Pocillopora, including for P. difficult to apply in the case of corals, genetically-distinct individual if some elegans and P. danae, has not been which reproduce both sexually and of the clone colonies survive. Another resolved, and in fact continues to asexually, and that the number of commenter noted that the distributions increase as more studies are conducted. recruits per spawner depends on the age of the Indo-Pacific species are largely Thus, at this time, Pocillopora species or size at which an entity is defined as unknown due to their incredibly vast are not determinable under the ESA. a recruit. These comments assert that ranges encompassing numerous

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archipelagos that include thousands of providing variability in environmental diversity of mesophotic habitat. The islands and atolls. The commenter conditions). extent of mesophotic habitat is emphasized this point by noting that Further, in the Coral and Coral Reefs addressed in the Coral Habitats sub- there are between 30,000 and 40,000 section (Individual Delineation and section. Mesophotic habitat’s potential islands in Oceania which could Species Identification sub-sections), we function as refugia for corals from ocean potentially have populations of the explain that we define a coral species as warming is addressed in the Spatial and proposed coral species. The comments the ‘‘physiological colony’’ (i.e., unit of Temporal Refugia sub-section. Where described above collectively assert that the species that can be identified as an mesophotic habitat information is listing decisions cannot be made due to individual in the field) to ensure that we available for an individual coral species the lack of species-specific information. are evaluating the individual species we have included and considered that Response: We acknowledge that it is and not coral reefs generally for information in the Species-specific difficult to quantify and qualify determining ESA status. Public Information and Determinations section. distribution and abundance for comments did not offer any information Comment 8: With regard to coral individual coral species. The ambiguity on how to define a coral species, but our habitats being divided into only two associated with the delineation of the explanations in the Individual global regions (i.e., Caribbean and Indo- individual in reef-building corals is Delineation and Species Identification Pacific), a couple of comments stated addressed in the Individual Delineation sub-sections makes clear that we do not that the Indo-Pacific region was too sub-section in the Corals and Coral consider coral reefs as species in this coarse. Specifically, the comments Reefs section, including how we final rule. However, it should be noted stated that the Hawaiian Islands should characterize the delineation of the that defining an individual coral as the be considered its own region or sub- individual for the species covered by physiological colony in this final rule region with Hawaiian species evaluated this final rule. In response to public did not change how we interpreted separately, due to Hawaii’s isolated comments, we more adequately address abundance data for any species. nature and significant number of Comment 7: A few comments stated each species’ distribution and endemic species. that the proposed rule lacked species- abundance as those characteristics relate Response: We recognize that there specific information for mesophotic to each species’ determination status may be numerous distinct sub-regions habitats (deep, lower-light areas, usually under the ESA in the Species-specific throughout the Caribbean and Indo- between 30 and 100 m deep). One Information and Determinations section. comment stated that the coral Pacific basins for some or all species, The public comments provided some communities of many Indo-Pacific and that some coral species are endemic useful information on the distribution jurisdictions have received little to Hawaii. However, under the ESA, we and abundance of specific coral species, attention, with vast areas of reef must evaluate the status of the species and we also collected supplemental remaining unexplored, especially for throughout their entire ranges. information on distribution and corals occurring in the mesophotic zone, Invertebrate species, such as corals, abundance that is included in the which likely harbors populations of cannot be divided further into Distinct Species-specific Information and species that can also be found at Populations Segments (DPS) under the Determinations section. shallower depths. Another comment ESA, since DPS specifically refer only to vertebrate species. Therefore, we cannot Comments on Coral Reefs, Other Coral stated that recent data from NOAA- identify sub-regions, such as Hawaii, as Habitats, and Overview of Candidate supported studies of mesophotic reefs its own distinct geographic range and Coral Environments found these extensive and poorly studied ecosystems serve as refugia for evaluate the status of more broadly Comment 6: Some comments asserted numerous shallow water coral species, distributed species only within that that the proposed rule focused too much yet no survey data from these ongoing specific area. In addition, as described on coral reefs rather than focusing on studies were included in the proposed in the Risk Analyses—Statutory coral species. A couple of comments rule. We also received two papers Standard sub-section of this final rule, stated that corals thrive in places that (Bridge and Guinotte, 2013; Kahng et al., we were not able to identify a are not coral reefs, even when nearby 2014) that suggested the global diversity significant portion of its range (SPOIR) coral reefs are not thriving, of some mesophotic corals may be for any of the proposed corals and underscoring the notion that reefs are underestimated and the biogeographic therefore could not evaluate whether the not species. Another couple of ranges of mesophotic corals are not fully status of the species within that portion comments stated that the focus on coral explored. of its range impacts the overall status of reefs and reef ecosystems, and the Response: The proposed rule briefly the species throughout its range. importance they have to reef-associated described mesophotic habitats and Comment 9: We received a few species, is improper for ESA listing acknowledged that the amount of comments regarding the consideration analysis and added that NMFS cannot mesophotic habitat available is and inclusion of Traditional Ecological simply decide to treat reefs as a species unknown and likely greater than the Knowledge (TEK), particularly from under the ESA simply because amount of shallow reef habitat. The local island cultures (Hawaiian, evaluating reefs is easier. proposed rule also stated there is greater Chamorro, and Samoan), as best Response: The proposed rule coral cover on mesophotic reefs in the available information for our listing acknowledged that reef-building coral Indo-Pacific than in the Caribbean. determination process. One comment species are not reef-dependent and However, more information has become noted the importance of corals and coral provided a description of non-reefal available on this habitat type since reefs to island cultures in the Pacific habitats. Public comments did not publication of the proposed rule. Two Islands region, in particular to native provide information on how to interpret papers (Bridge and Guinotte, 2013; Hawaiians. The comment criticized the non-reefal habitat in our analysis, but in Kahng et al., 2014) provided more lack of TEK in the SRR and proposed the Coral Habitats sub-section of this information on the global diversity and rule for the candidate corals, stating that final rule we clarify the relevance of biogeographic ranges of mesophotic coral biology and ecology is a non-reefal habitats in determining each corals and we have collected fundamental part of TEK, and that their species’ status under the ESA (e.g., information on the magnitude and TEK is part of best available science.

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Response: We agree that TEK provides species meets the definition of mortality of corals (Colella et al., 2012; an important and unique perspective on threatened or endangered. That is, if the Schopmeyer et al., 2012). local ecosystems, their status, threats, species is currently in danger of Response: We agree with commenters and changes over time; when relevant extinction or may become so in the and acknowledge that there is information was made available to us, foreseeable future due to any one or a uncertainty associated with climate we incorporated it into the proposed combination of the five factors under change projections. Climate change rule. We also acknowledge that this Section 4 of the ESA (in which the projections over the foreseeable future information is not necessarily accessible various threats are categorized) then the are associated with three major sources in academic peer reviewed journals or species may be listed. of uncertainty: (1) The projected rate of text books. Therefore, we requested any increase for GHG concentrations; (2) Comments on Global Climate Change— additional TEK-related information on strength of the climate’s response to General Overview the biology, ecology, threats, and GHG concentrations; and (3) large extinction risks of the 65 coral species Comment 11: We received many natural variations. The recent warming on numerous occasions for inclusion comments on the general treatment of slow-down is an example of a large within this final rule. While we received global climate change in the proposed natural variation that was not public comments and listened to several rule and supporting documents. The anticipated by previous models. public testimonies from community Global Climate Change—General However, AR4’s projections were built members in both the Pacific Islands and Overview section in the proposed rule upon scientifically accepted principles, Southeast regions that disagreed with and the global climate change portion of which fairly simulated many large scale our proposed listing determinations, we the SRR describe past, current, and aspects of present-day conditions, did not receive any TEK-related future GHG emissions and atmospheric providing the best available information information or data on the biology, concentrations and the associated past, on climate change at the time the ecology, threats, or extinction risks for current, and future general effects on proposed rule was published. The any of the 65 coral species within this coral reef ecosystems, based primarily IPCC’s Fifth Assessment Report (AR5), final rule. on the International Panel on Climate Climate Change 2013: The Physical Change’s (IPCC) Fourth Assessment Science Basis (IPCC, 2013), commonly Comments on Threats Evaluation Report (AR4), The Physical Basis (IPCC, referred to as the Working Group I Comment 10: We received a large 2007) and supporting literature. Report (WGI) became available in number of public comments on the Some comments stated that we did September 2013, and supersedes AR4; various threats to corals and coral reefs. not adequately account for the accordingly, this final rule relies on the In addition to the specific comments on uncertainty in climate change modeling. information provided in AR5’s WGI. the nine most important threats, one A few comments stated that global Despite the advance of climate change comment stated that there should be no temperature has been stable for the last science in recent years, there is still doubt that corals and coral reefs ten years or that warming has slowed complexity and uncertainty associated throughout the world are in serious down since 2000. One commenter with projections of global climate trouble and in decline due to the effects provided two recent papers (Guemas et change. However, the current state of of anthropogenic stressors. Another al., 2013; Hansen et al., 2012) that climate change science is capable of commenter asked whether the mere showed global mean surface producing informative projections that threats from anthropogenic impacts are temperatures did not increase as much provide a rational basis for considering sufficient for ESA listing. Yet another as had been predicted from 2000 to likely patterns in future climate change- commenter requested that recreational 2010. related threats to reef-building corals. boating activities should be recognized Some comments stated that GHG More detail on the overall complexity as a specific threat, even though emissions and global temperatures associated with projections of global recreational boating activities may only continue to rise unabated. One comment climate change, major sources of present a relatively minor risk to coral referenced two studies (Frieler et al., uncertainty in climate change species. 2012; van Hooidonk et al., 2013b) that projections, and a summary of AR5’s Response: As described in the projected the frequency of coral reef WGI, including the pathway that we proposed rule, there are nine threats bleaching under different levels of consider the most impactful to corals, considered to be the most significant to warming and emissions scenarios, are addressed in Threats Evaluation— the current or expected future extinction indicating that significant and Global Climate Change Overview sub- risk of reef-building corals. The immediate GHG reductions are critical section. comments and responses on these nine to prevent coral reefs from degradation We also acknowledge the observed threats (ocean warming, disease, ocean and collapse. Another comment also recent hiatus/slow-down in the rate of acidification, trophic effects of fishing, referenced van Hooidonk et al. (2013b) global surface air temperature increase, sedimentation, nutrients, sea-level rise, and stated that targets for atmospheric and we have accordingly provided a predation, and collection and trade) are carbon dioxide (CO2) concentrations description of the hiatus/slowdown and addressed individually below. We must be lower than 450 parts per its implications in the Threats acknowledged that recreational boating million (ppm) to protect coral reef Evaluation—Ocean Warming sub- activities may present some risk to coral ecosystems. Yet another comment stated section. In summary, despite species and it was included in the that scientific modeling indicates that unprecedented levels of GHG emissions description of the threat ‘‘Human- within 40 to 50 years, reef decline will in recent years, a slow-down in global induced Physical Damage’’ in the SRR. pass a tipping point, largely due to the mean surface air temperature warming However, we determined that threat’s increasing impacts of climate change, has occurred since 1998, which AR5’s contribution to the extinction risk of and may not be reversible over WGI refers to as a ‘‘hiatus.’’ Despite this corals, generally, is negligible to low. ecological time scales. Another slowdown in warming, the period since We also recognized that comment pointed out that climate 1998 is the warmest recorded and ‘‘Each anthropogenic threats are affecting coral change also could likely increase corals’ of the last three decades has been species worldwide and may be exposure to cold water stress, which successively warmer at the Earth’s sufficient for an ESA listing if the studies have shown can cause extensive surface than any preceding decade since

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1850.’’ The slow-down in global mean change models are associated with anomalies and for variations in the surface warming since 1998 is not fully uncertainty, as discussed in response to responses of individual coral species explained by AR4 or AR5 WGI’s models, comment 11 above. However, in across their ranges. Comments noted but is consistent with the substantial response to comments on ocean that coral species and their symbionts decadal and interannual variability seen warming projections, such as criticism are not uniformly susceptible and/or in the instrumental record and may of the reliance of the proposed rule and resilient to climate change across their result, in part, from the selection of supporting documents on AR4 (IPCC, ranges. That variability results in beginning and end dates for such 2007) and the lack of consideration of heterogeneous responses of coral analyses. the ocean warming hiatus, we provide a species to ocean warming both in Public comments provided review of the best available information different parts of the ranges and also at supplemental information on several on these topics, including AR5’s WGI different rates in the future. Another aspects of global climate change, as Report (IPCC, 2013), in the Threats comment provided information from described above. We also collected Evaluation—Global Climate Change van Hooidonk (2013b) regarding spatial information to inform how we assess the Overview, Representative Concentration and temporal variability of ocean effects of global climate change to Pathways (RCP) 8.5 Projections, and warming within different regions. The corals, including the IPCC Working Ocean Warming sub-sections below. commenter identified reef locations that Group II report on impacts, adaptation, These data support the conclusion in appear to be less vulnerable to and vulnerability. We maintain that the proposed rule that ocean warming is bleaching, including the southern Great global climate change is central to increasing in severity, and is likely to Barrier Reef (GBR), the western Indian assessing extinction risk for the corals in continue increasing in severity within Ocean, Persian Gulf, Red Sea, Thailand, this final rule. As described in more the ranges of reef-building corals. New Caledonia and French Polynesia, detail in the Threats Evaluation—Global However, a key difference between the as well as other locations that appear to Climate Change Overview sub-section proposed and final rule is that we now be more vulnerable to bleaching, below, the supplemental information more fully consider the ability of each including the western Pacific warm underscores the complexity and species’ spatial and demographic traits pool, northwestern Australia, west uncertainty associated with projecting to moderate exposure to threats, Papua New Guinea and the central the extent and severity of effects of including warming, and place Pacific islands of Tokelau. Another global climate change across the ranges appropriate emphasis on the non- commenter stated that the corals at of reef-building corals. uniform nature of global threats at the Flower Garden Banks National Marine Comments on Ocean Warming (High regional and local levels that allows Sanctuary seem to be less affected by Importance Threat, ESA Factor E) habitat heterogeneity to play a role in elevated sea surface temperatures that buffering a species against vulnerability Comment 12: We received several are impacting corals in other parts of the to extinction. The significance of coral wider Caribbean. comments on general future projections abundance and distribution, and habitat Response: We discussed spatial (i.e., of ocean warming levels. One heterogeneity, to this final rule is regional and/or local) variability of commenter stated that climate change described in more detail in the Corals models applied in our assessment are and Coral Reefs, Risk Analyses and ocean warming impacts to corals in the too coarse to accurately predict the Species-specific Information and proposed rule and we agree that ocean conditions reefs will experience in the Determinations sections of this rule. warming will not affect all species in all future and that real conditions are After reviewing the public comments locations uniformly over the foreseeable impacted by bathymetry, water mixing, and information provided in AR5’s WGI future, and that different regions are wind patterns, fresh water inputs, and our conclusion regarding the threat of predicted to experience the effects of other bio-geographic factors. The ocean warming remains unchanged ocean warming on different time scales commenter concluded that existing from the proposed rule. We maintain and at different magnitudes than others. projections for sea surface temperature that ocean warming is a high We provide a review of all the best are not sufficient to conclude the importance threat in assessing global available information on spatial species face an existential threat. Other extinction risk for the corals in this final variability in ocean warming, including comments also criticized the use of rule, while we also acknowledge that any information provided via public AR4’s worst-case scenario as the basis the interpretation of future climate comment or gathered ourselves since for determining the most likely future change threats to corals is associated the proposed rule was published, in the scenario with regard to ocean warming, with complexity and uncertainty, and Threats Evaluation—Global Climate and related topics such as the proposed that effects on individual species of reef- Change Overview, RCP8.5 Projections, rule’s lack of consideration for the post- building corals are difficult to determine and Ocean Warming sub-sections below. 1998 hiatus in global warming. as described in more detail in the These data support the conclusion in Response: In the proposed rule, we Threats Evaluation—Global Climate the proposed rule that ocean warming is discussed the numerous, complex Change Overview subsection below. increasing in severity, and likely to spatial and temporal factors that Comment 13: Many comments continue increasing in severity within compound uncertainty associated with criticized the proposed rule for not the ranges of reef-building corals. This projecting effects of ocean warming on accounting for spatial variability in review also underscores the complexity corals in the future, and we have ocean warming and overlooking and uncertainty associated with spatial determined that ocean warming will not regional and local variability in variability in ocean warming across the affect all species in all locations conditions leading to warming-induced ranges of reef-building corals. A key uniformly over the foreseeable future. bleaching, which may be more or less difference between the proposed and We believe that different bio-geographic severe regionally or locally than the final rule is that we now more fully factors such as bathymetry, water overall warming. For example, we consider the ability of each species’ mixing, wind patterns, and fresh water received two comments requesting us to spatial and demographic traits to will likely impact conditions corals will review the literature for information moderate exposure to threats, including experience over the foreseeable future. regarding current and projected regional warming, and place appropriate We also recognized that global climate differences in sea surface temperature emphasis on the non-uniform nature of

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global threats at the regional and local between ocean warming and corals reefs information (such as synergistic effects levels which allows habitat in the proposed rule, and concluded of ocean warming with other threats), heterogeneity to play a role in buffering that ocean warming is a severe and which has been incorporated and a species against vulnerability to increasing threat to corals. The public considered in our assessment, as extinction. The significance of coral comments and supporting papers we described in more detail in the Threats abundance and distribution and habitat received on the overview of ocean Evaluation—Ocean Warming sub- heterogeneity to this final rule is warming and coral reefs generally section. The comments and supporting described in more detail in the Corals support the conclusion in the proposed papers support the conclusion in the and Coral Reefs, Risk Analyses and rule that ocean warming is an important proposed rule that the impacts of ocean Species-specific Information and and increasing threat to coral reefs. warming on reef-building corals are Determinations sections of this rule. However, the other comments increasing in severity and likely to Comment 14: Comments on the underscore the uncertainty associated continue increasing in severity. This overview of ocean warming and coral with projecting the effects of ocean information also underscores the great reefs focused on projected effects of warming on coral reefs in the future, complexity and high uncertainty ocean warming on coral reef and as described in our response to associated with the various specific ecosystems, rather than on reef-building Comment 13, we also acknowledge that effects of ocean warming, including coral species. These comments comprise there is and will continue to be regional synergistic effects with other threats, two distinct views. Some comments and local variability in responses of across the ranges of reef-building corals. emphasized that coral reefs are likely to corals to ocean warming over the We continue to acknowledge that decline sharply in the future because of foreseeable future. We acknowledge that susceptibility of a species to a threat increasing GHG emissions, while other ocean warming will not act uniformly depends on the combination of: (1) comments emphasized that recent on all species at all times over the Direct effects of the threat on the reviews indicate a wide range of foreseeable future. Further, we species; and (2) the cumulative and possible responses by coral species. For recognize that the responses of each interactive (synergistic or antagonistic) example, one commenter cited Frieler et species to ocean warming will vary effects of the threat with the effects of al. (2012) and stated that the estimated across their ranges over the foreseeable other threats on the species. In the frequency of coral bleaching at different future. Additionally, as described in proposed rule, we considered how the levels of global warming showed that previous comment responses, a key ° cumulative or interactive effects altered limiting warming to 1.5 C above pre- difference between the proposed and the rating assigned to a threat industrial levels is unlikely to protect final rule is that we now more fully susceptibility in isolation. However, most of the world’s reefs from consider the threat-buffering capacity of upon further consideration, we need to degradation. The commenter further each species’ unique characteristics, and evaluate the extent to which one threat explained that even under the lowest of place appropriate emphasis on the non- influences the susceptibility of an the IPCC AR5 emissions scenarios uniform nature of global threats at the individual species to another threat (RCP3–PD) and optimistic assumptions regional and local levels which allows with more species-specific information, regarding thermal adaptation, habitat heterogeneity to play a role in in connection with all the other approximately one-third (range from 9 buffering a species against vulnerability elements that influence a species’ to 60 percent) of the world’s coral reefs to extinction. extinction risk. Generally, cumulative will experience long-term degradation. Comment 15: We received comments and interactive processes are complex Another commenter cited Donner (2009) on specific effects of ocean warming on and uncertain and existing information and similarly stated that the projected reef-building corals that covered various about threats interactions is only based increase in sea surface temperatures due topics, including the interactions of on a few studies on a few species. to the physical commitment from the warming-induced bleaching with other Where possible, when we have species- present accumulation of GHGs due to threats. For example, one commenter specific or applicable genus-level anthropogenic activity, as well as the noted that anthropogenic climate information on cumulative or amount of GHGs likely to be emitted, is change (e.g., ocean warming) weakens interactive effects, we have applied this sufficient to cause frequent and higher coral colonies and renders them more information to that particular species’ magnitude heat stress for the majority of susceptible to disease, which is also susceptibilities in a more integrated the world’s coral reefs by 2050. Another covered in the Threats Evaluation— commenter provided information from Disease sub-section below. Other manner. Kiessling et al. (2004) and Carpenter et commenters also emphasized the Comment 16: We received several al. (2008) and asserted that if bleaching potential for ocean warming to act comments on the capacity of reef- events become very frequent, many synergistically with other threats such building corals for acclimatization and species may be unable to maintain as nutrification as well as overfishing. adaptation to ocean warming, covering breeding populations as repeated Another commenter provided various specific characteristics of reef- bleaching causes potentially irreversible information from Ferrier-Page`s et al. building corals that may contribute to declines, perhaps mimicking conditions (2010) suggesting remarkable tolerance such capacity. Mostly, commenters that led to previous coral extinctions. In to global change, such as the potential asserted that we did not adequately contrast, some commenters disagreed to reduce bleaching vulnerability consider the ability of corals to with our conclusion of the projected through increased feeding rates. acclimatize or adapt to changing effects of ocean warming on corals and Response: In the proposed rule, we temperatures. Several comments cited coral reef ecosystems in the proposed discussed how multiple threats stress empirical evidence that corals have rule. As described above in Comment corals simultaneously or sequentially, already adapted to ocean warming, 13, many commenters pointed out whether the effects are cumulative (the thereby demonstrating the potential for several studies showing regional and sum of individual stresses) or acclimatization or adaptation. For local variability in responses of corals interactive (e.g., synergistic or example, one comment letter provided and coral reefs to ocean warming. antagonistic). The comments and information from Pandolfi et al. (2011) Response: We summarized the best supporting papers we received on these and Cahill et al. (2013) stating that more available information on the interaction topics provide supplemental recent analyses incorporating thermal

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tolerance of species indicate a wide Reefs, Other Coral Habitats, and by disease is discussed in more detail in range of outcomes including Overview of Candidate Coral the Species-specific Information and maintenance of comparable levels of Environments sections of the proposed Determinations section below. cover to 2100 and beyond. Another rule. Further, in the Threats Comments on Ocean Acidification commenter provided data from Maynard Evaluation—Disease section of this rule, (Medium-High Importance Threat, ESA et al. (2008) and Guest et al. (2012) we acknowledge diseases are of high Factor E) showing that many types of coral show importance with regard to extinction surprisingly large (∼0.5–1 °C) increases risk of corals. However, in assessing Comment 19: We received public in thermal tolerance after a single mass extinction risk over the foreseeable comments on the description of and bleaching event, due to either future, climate change-related threats future projections of ocean acidification, adaptation or acclimatization. In are highly important to all reef-building which provided information on the another comment letter, information corals. Any species-specific information complexity of ocean chemistry on provided from Jones and Berkelmans provided on disease is included in the corals, and criticism of the use of the (2010) and Baker et al. (2004) show that Species-specific Information and AR4’s worst-case scenario as the basis the acclimatization potential of corals to Determinations section later in this rule. for determining the most likely future increased temperatures is an active area Comment 18: One commenter noted scenario with regard to ocean of research, with a focus on identifying the explicit link between coral acidification. For example, one heat-resistant phenotypes. Another bleaching, disease, and the larger commenter asserted that global commenter pointed to the coral species driving environmental factor of climate projections of ocean acidification are too that occur in the Arabian Gulf as an change by citing several studies that coarse and do not take into example of species adapting to warmer show anthropogenic climate change consideration competing and extremely temperatures. weakens coral colonies and renders localized factors that affect local CO2 Response: In the proposed rule we them more susceptible to disease concentrations (e.g., local atmospheric acknowledged that there is some (Harvell et al., 1999; Harvell et al., 2002; processes, local biological processes, evidence to suggest that reef-building Knowlton, 2001). Another commenter local temperature, and upwelling from corals may have various mechanisms for provided information from Muller and deeper waters). The commenter acclimatization and adaptation to ocean van Woesik (2012), stating that emphasized that despite acknowledging warming. These topics were described exceeding environmental disease the multitude of local, regional, and in the Ocean Warming sub-section of thresholds will most likely become seasonal factors that may cause local the proposed rule, and we concluded increasingly common in rapidly CO2 concentrations to increase and pH that existing scientific information was warming oceans, leading to more to decrease, we opted instead to base inconclusive on how these processes frequent coral-disease outbreaks. The our reef-scale threat analysis on may affect individual corals’ extinction study suggested that that the expression generalized acidification predictions risk, given the projected intensity and of some coral diseases occurs when (1) from global models. Other commenters rate of ocean warming. The public environmental thresholds are exceeded also criticized our reliance on the IPCC’s comments and supporting papers have and (2) these environmental conditions AR4 report as the basis for our threat been incorporated and considered in either weaken the corals, which are then evaluation of ocean acidification to our assessment, as described in more more susceptible to infection, or corals. detail in the Threats Evaluation—Ocean increase the virulence or abundance of Response: In the proposed rule we Warming sub-section and the Species- pathogens. In other words, corals that acknowledged that numerous, complex specific Information and Determinations experience bleaching are more likely to spatial and temporal factors compound section. However, the supplemental suffer from disease outbreaks and uncertainty associated with projecting information does not alter the subsequent mortality. effects of ocean acidification on corals conclusion in the proposed rule that the Response: In the proposed rule, we in the future. We also acknowledged capacity for acclimatization and described the importance of disease as that global climate change models are adaptation of reef-building corals to a threat to corals and the potential for associated with uncertainty. We further ocean warming is inconclusive for disease to act synergistically with other acknowledge that the interpretation of corals generally at this time. threats such as ocean warming. We also future climate change threats to corals is understand that assessing the threat of complex and that effects on individual Comments on Disease (High Importance disease is highly complex, as the cause species of reef-building corals are Threat, ESA Factor C) or causes of many coral diseases difficult to determine, as described in Comment 17: One comment regarding remains either unknown or poorly more detail in the Threats Evaluation— the decline of Caribbean coral understood. Overall, the public Global Climate Change Overview populations cited land-use changes as comments we received underscored and subsection. However, we agree with well as disease outbreaks (among other supported the analysis in the SRR and commenters that ocean acidification local threats) as the causes of Caribbean the proposed rule. In addition to public will not affect all species in all locations coral decline rather than climate comments, we collected a significant uniformly over the foreseeable future, change. Some comments also provided amount of information on disease that and that different locations will such information pertaining to specific became available since the proposed experience the effects of ocean species. For example, one comment rule published. Thus, we maintain that acidification at different time scales and stated that the genetic diversity of disease is a high importance threat to at different magnitudes than others. We Acropora cervicornis in Florida may be the extinction risks of the 65 corals in provide a review of all the best available sufficient to maintain viability and this final rule. All of the supplemental information, including a review of resilience to environmental information received or otherwise AR5’s WGI (IPCC, 2013) in the Threats perturbations and disease. collected has been detailed and Evaluation—Global Climate Change Response: The proposed rule summarized in the Threats Evaluation— Overview, RCP8.5 Projections, and described how disease had a major role Disease sub-section of this final rule. Ocean Acidification sub-sections. Upon in the initial decline of Caribbean coral The extent to which the extinction risk review of the information provided in populations as described in the Coral of a particular coral species is impacted AR5’s WGI and public comments, our

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conclusion regarding the threat of ocean the proposed rule was published, in the on larvae and juvenile corals, and acidification remains unchanged from Threats Evaluation—RCP8.5 Projections interactive or synergistic effects with the proposed rule. We maintain that and Ocean Acidification sub-sections. other environmental variables. For ocean acidification is increasing in These data in our view still support the example, the commenter pointed out severity, and is likely to continue conclusion in the proposed rule that several studies that underscore the increasing in severity, within the ranges ocean acidification is increasing in potential impact of ocean acidification of reef-building corals, and is a medium- severity, and likely to continue on reef calcification rates, noting that high importance threat in assessing increasing in severity within the ranges even under the most optimistic extinction risk for the 65 corals in this of reef-building corals; however, as modeling scenario, 98 percent of reefs final rule. However, as described in described in earlier comment responses, would be chemically stressed by 2050. earlier comment responses, a key a key difference between the proposed The commenter also emphasized that difference between the proposed and and final rule is that we now more fully corals may have a limited ability to final rule is that we now more fully consider the threat moderation capacity adapt to ocean acidification based on an consider the ability of each species’ of each species’ spatial and in-situ study of two corals in Florida spatial and demographic traits to demographic traits, and of habitat Bay (Okazaki et al., 2013). moderate the impacts of threats, and we heterogeneity. Response: The comment letter and place appropriate emphasis on the non- Comment 21: We received one supporting papers support the uniform nature of global threats at the comment that identified a couple of conclusion in the proposed rule that regional and local levels which allows ocean acidification and coral reef ocean acidification is increasing in habitat heterogeneity to play a role in calcification rate studies that were not severity, and likely to continue buffering a species against vulnerability included in the SRR and proposed rule. increasing in severity, within the ranges to extinction. The commenter provided two studies: of reef-building corals, resulting in Comment 20: We received a comment One showing that coral calcification various detrimental impacts. This regarding variability in ocean increases with global warming (McNeil information also underscores the acidification on coral reefs related to et al., 2004), and another study showing complexity and uncertainty associated fluctuations in pH from localized factors that corals are already thriving in with the various specific effects of ocean such as seagrass beds. The commenter conditions similar to the ocean acidification, including interactive or provided information from Manzello et acidification conditions predicted by synergistic effects with other threats, al. (2012) indicating that local and the IPCC for 2100 (Hofmann et al., across the ranges of reef-building corals regional biochemical processes buffer 2011). as well as predicting adaptive capacity. effects of ocean acidification in Response: In the proposed rule and The information provided by the locations such as the Gulf of Mexico and supporting documents we commenter and the supporting papers South Atlantic. Manzello et al. (2012) acknowledged that some exceptional regarding the specific effects of ocean reported that the photosynthetic uptake areas exist where reef-building coral acidification on corals and coral reefs and sequestering of carbon dioxide by communities appear to be thriving have been incorporated and described seagrasses and other macroalgae and the under naturally high CO2 in more detail in the Threats positive growth response by seagrasses concentrations. As described in the Evaluation—Ocean Acidification sub- to increasing dissolved carbon dioxide comment response above to Comment section. (Palacios and Zimmerman, 2007) may 19, we agree that ocean acidification Comments on Trophic Effects of Fishing create ocean acidification refugia for will not act uniformly on all species in (Medium Importance Threat, ESA corals. Comments on specific effects of all locations over the foreseeable future. Factor A) ocean acidification on coral reefs and We provide a review of all the best reef-building corals focused on capacity information available on the threat of Comment 23: One comment provided for acclimatization of corals to ocean acidification, including these supplemental information that was not acidification, and evidence that some studies, which we received in public included in the proposed rule regarding coral species are resistant to low pH. comments, and any information we the role of herbivorous fish in terms of Response: In the proposed rule, we gathered ourselves in the Threats building and maintaining reef discussed that numerous, complex Evaluation—Ocean Acidification sub- resilience. The commenter stated that spatial and temporal factors compound section (e.g., Shamberger et al., in ‘‘overfishing also degrades coral reefs, uncertainty associated with projecting press). This supplemental information particularly by depleting key functional effects of ocean acidification on corals supports the proposed rule’s conclusion groups, such as herbivores, that reduce and coral reefs in the future, and we that the threat of ocean acidification has turf algae on reefs and maintain optimal agree with the comment that ocean already impacted corals and coral reefs conditions for coral growth and acidification will not affect all species and will become increasingly severe recruitment’’ and provided Keller et al. in all locations uniformly over the from now to 2100, with increasingly (2009) as a reference. Another foreseeable future, and that different severe consequences for corals and coral commenter also described the locations will experience the effects of reefs. However, as described in previous importance of herbivorous functional ocean acidification at different time comment responses, a key difference groups, and stated that limiting or scales and at different magnitudes than between the proposed and final rule is attempting to reduce harvest of others. In response to comments on that we now more fully consider the predatory fish may cause ecological spatial variability of ocean acidification, capacity of each species’ spatial and harm by unbalancing a healthy trophic such as lack of consideration of demographic traits, and habitat chain. localized increase in pH from adjacent heterogeneity, to buffer a species against Response: The proposed rule seagrass beds, we provide a review of vulnerability to extinction. described the importance of trophic the best available information on spatial Comment 22: We received a detailed interactions which include reducing variability in ocean acidification, comment letter with supporting papers herbivorous fish species that control including any information provided by regarding specific effects of ocean algal growth, limiting the size structure public comments as well as any acidification on reef-building corals, of fish populations, reducing species information we gathered ourselves since such as effects on reef accretion, effects richness of herbivorous fish, and

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releasing corallivores from predator the level of human impacts to corals, may be prevented by sediment control. The supplemental information including fishing pressure. preempting larval attachment. Further, provided by public comments supports Response: The issues of human the commenter identified sedimentation our conclusion in the proposed rule that demography and population trends (among other local threats) as a local healthy levels of herbivorous functional were covered explicitly in the SRR and threat with the capability of groups are essential to coral reef considered in the proposed rule. While exacerbating bleaching and disease ecosystem resilience in light of climate there may be some areas being impacts, thereby reducing the resilience change-related threats. Detailed depopulated, increased human of corals. One commenter pointed out information regarding the trophic effects population and consumption of natural that mass mortality of Acropora palmata of fishing can be found in the Threats resources are root causes for increases in at Vega Baja, Puerto Rico, was caused in Evaluation—Trophic Effects of Fishing fishing (particularly of herbivores) at part by sedimentation. Another sub-section as well as the Inadequacy of many locations around the globe commenter stated that near shore Existing Regulatory Mechanisms—Reef (Brainard et al., 2011). Data from the marine-origin sediments have almost Resilience sub-section. World Bank show human population completely been replaced by terrestrial Comment 24: One commenter stated abundance and density have increased sediments due to a lack of land use that fish landings have been stable for in all five coral reef regions since 1960 controls, resulting in near total mortality 30 years in St. Thomas, U.S. Virgin (i.e., Indian Ocean, Caribbean, Southeast of nearshore Acropora stands in the U.S. Islands, with many species increasing in Asia, Pacific, and Middle East), with the Virgin Islands. Other commenters size, indicating that overfishing is not greatest human population densities identified the negative impacts of occurring in this location or and increases in population density in sedimentation to reefs on the Hawaiian contributing to the status of the the Southeast Asia and Indian Ocean Island of Molokai, emphasizing the Caribbean species in that area. The regions. In these regions, current human issue of run-off from large rain events in commenter also pointed out numerous population densities are 4–5 times certain areas. In general, these sources of sediments and nutrients, and greater than the global average and comments emphasize the importance of coastal development projects in the U.S. probably suggest the greatest local sedimentation as a threat to the 65 coral Virgin Islands as the main contributors human-induced effects to corals and species in this final rule, with some to coral reef decline rather than coral reefs. In the areas in closest asserting that this threat is as important, overfishing. Other commenters also proximity to coral reefs, the Southeast if not more important, than the higher disagreed that overfishing was Asian, Indian Ocean and Middle East rated threat of reef fishing. contributing to coral reef decline in regions have the highest densities of Response: We acknowledge all of the Hawaii and highlighted significant people per reef area (Burke et al., 2011). public comments and information we However, these data are regional received on the threat of sedimentation increases in tourism and in-water averages. We do not dispute that human to the 65 coral species in this final rule. recreational activities as local drivers of demography within any of these regions As summarized in the proposed rule, we reef decline in that area. may be shifting to higher density in also recognize the possibility for Response: Although not explicitly metropolitan areas, resulting in a sedimentation to interact with other stated in the proposed rule, we agree decrease of human disturbance in some global and local threats and potentially that levels of fishing effort vary portions of these regions. The regional reduce the resiliency of coral reef throughout the ranges of the 65 corals trend data suggest increasing risks to ecosystems and/or impede recovery. In under consideration. We did corals and coral reefs overall (Brainard addition to public comments, we also acknowledge that exposure to this threat et al., 2011). However, because we must collected supplemental scientific varies throughout the ranges of the consider the extent to which a particular information regarding the impacts of proposed species and between the threat impacts each species throughout sedimentation to corals that became Caribbean and Indo-Pacific. In the its entire range, we still maintain that available after the proposed rule was proposed rule, we also recognized that overfishing is a medium importance published. The findings from these management and regulation of threat to all 65 coral species in this final studies and more detailed information commercial and recreational fisheries rule. regarding the evaluation of are inconsistent throughout the coral sedimentation as a threat to coral reefs Comments on Sedimentation (Low- reef world. When evaluating the current can be found in the Threats Medium Importance Threat, ESA and potential threat impacts from Evaluation—Sedimentation sub-section. Factors A and E) trophic effects of fishing, we are We also acknowledge the concern that required to assess this threat throughout Comment 26: We received some some comments expressed regarding the the entire ranges of the 65 coral species public comments on sedimentation as a importance of this threat in comparison in this final listing. We understand that threat to the 65 coral species in this to other local threats. However, for levels and impacts of overfishing differ final rule. Comments generally corals in general, we maintain that depending on the particular location underscored the importance of sedimentation is a low-medium threat to under evaluation; however, we maintain sedimentation as a considerable local the extinction risk of the 65 corals in that the trophic effects of fishing threat to corals and pointed out the this final rule. Any species-specific represent a medium importance threat potential of sedimentation to interact information we received on to the extinction risk of all 65 coral and potentially exacerbate other threats, sedimentation is included in the species in this final rule. as well as to reduce coral resilience. For Species-specific Information and Comment 25: One commenter stated example, we received a detailed Determinations section. that we failed to consider human comment asserting that prospects for demography in terms of our analysis of recovery of certain reef sites in the Comments on Nutrients (Low-Medium fishing impacts to corals. The Caribbean from acute episodes of Importance Threat, ESA Factors A and commenter noted that large swaths of hurricane damage or die-offs from E) area throughout Oceania are being bleaching and disease (brought on by Comment 27: We received limited depopulated in favor of more ocean warming) are extremely poor public comments on nutrient metropolitan countries, which reduces without sustained recruitment, which enrichment of nearshore waters (i.e.,

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eutrophication) and its impacts to coral eminent scientists and endorsed by Comments on Collection and Trade reef ecosystems. Comments generally hundreds of scientists to address the (Low Threat, ESA Factor B) underscored the importance of nutrient topic of climate change impacts on coral Comment 30: We received hundreds enrichment as a considerable local reefs; ICRS, 2012) as a source of of comments that strongly criticized our threat to corals, and emphasized the estimates of sea-level rise by the end of characterization of the trade industry as potential of nutrient enrichment to this century. However, the comment did a whole, stating that our analysis failed interact and potentially exacerbate other not expound upon the potential to use current science and/or threats, as well as reduce coral reef ramifications of these estimates. We did commercial information about the coral resiliency. For example, we received a not receive any other public comments trade. Commenters also asserted that we detailed comment letter that provided or gather new or supplemental did not adequately consider aquaculture studies regarding the impacts of nutrient information on the threat of sea-level and mariculture industries as a potential enrichment to coral species. These rise to the 65 corals in this final rule. alternative to alleviate pressures from studies, which became available after Response: Although we received only wild collection practices. For example, the proposed rule was published, one public comment on this topic, we we received a detailed comment provide evidence that nutrient collected supplemental information regarding the mariculture industry in enrichment can worsen thermal stress regarding the threat of sea-level rise to Indonesia, stating that in the last five on inshore reef communities, and that corals as a result of the IPCC’s AR5. years, the coral trade communities of management actions to reduce coastal These findings are summarized in the Indonesia have developed coral nutrient enrichment can improve the Threats Evaluation—Sea-Level Rise sub- mariculture with long-term objectives of resistance and resilience of vulnerable section. reducing the wild harvest of coral coastal coral reefs to ocean warming. species for the live coral trade. Another Another comment detailed some of the Comments on Predation (Low Threat, comment letter provided information impacts of nutrients in the U.S. Virgin ESA Factor C) from recent papers by Rhyne et al. Islands. For example, industrial effluent Comment 29: We received very few (2012) and Wood et al. (2012) that report in St. Croix allegedly impacted fisheries comments regarding the threat of declining trade in wild-harvested in the area to the point where fishermen predation to the 65 corals in this final Pacific corals and remarkable growth in struggle to sell their catch due to rule. The majority of comments we the production and trade in cultured perceived contamination. Further, a received regarding predation were corals from Pacific countries. Overall, sewage pumping station in another area specific to individual species in Guam. impacted nursery grounds for spiny many comments asserted that a shift For example, we received a detailed from wild collected corals to cultured lobsters. We received other comments comment letter that included suggested regarding the negative impacts of corals is occurring as a result of changes to individual species increasing aquaculture and mariculture nutrient enrichment in various locations vulnerability ratings to predation, as a in Florida and Hawaii from sewage operations both within the United States result of local crown-of-thorns seastar and major source countries such as outfalls and other land-based sources of (Acanthaster planci) predation levels. pollution. In general, comments Indonesia. One commenter cautioned us in terms Response: We agree with commenters emphasized the importance of nutrients of inferring predation vulnerabilities for as a threat to the 65 coral species in this that the SRR and proposed rule did not certain species from genus-level final rule, some asserting that this threat adequately describe the full scope of the information. Other comments identified is as important, if not more, than the marine ornamental trade industry and predation as a threat to corals, but higher rated threat of reef fishing. the contribution of captive culture in Response: In the proposed rule we provided no further information or terms of alleviating pressures from wild described the threat nutrient enrichment scientific references. collection. We agree that some poses to corals. The public comments Response: We acknowledge all of the significant progress has been made in and supporting papers regarding the public comments and information we terms of shifting from wild collection of impacts of nutrients to coral reef received on the threat of predation to corals to trade of aquacultured and/or ecosystems have been considered and the 65 coral species in this final rule. maricultured corals as a result of both incorporated into our assessment, as The extent to which the extinction risk U.S. domestic production and described in more detail in the Threats of a coral species is impacted by production of corals in major source Evaluation—Nutrients sub-section. We predation is discussed in more detail in countries such as Indonesia. In addition also acknowledge the concern that some the Species-specific Information and to public comments we also collected a comments expressed regarding the Determinations section, including any large amount of supplemental importance of this threat in comparison information we received from specific information on coral collection and to other local threats. However, for locations. We also agree that inferring trade. Specifically, we collected corals in general, we maintain that susceptibility to threats from genus- information about (1) the physical and nutrient enrichment is a low-medium level information is not always ecological impacts of wild collection of threat to the extinction risk of the 65 appropriate. However, that particular coral colonies and/or fragments from corals in this final rule. Any species- comment referenced a species we their natural habitats; and (2) captive specific information we received on deemed Not Warranted for listing under culture (i.e., mariculture and nutrient enrichment is included in the the ESA, and are no longer considering. aquaculture) including information on Species-specific Information and In addition to public comments, we operations and the role of home aquaria Determinations section. collected information regarding the as it relates to trade. All of the public variable effects predation has on certain comments and supporting papers have Comments on Sea-Level Rise (Low- coral species. These studies are detailed been considered and incorporated into Medium Threat, ESA Factor A) and summarized in the Threats our assessment as described in more Comment 28: We received one public Evaluation—Predation sub-section. detail in the Threats Evaluation— comment that cited the Consensus Overall, we maintain that predation is a Collection and Trade sub-section. Statement on Climate Change and Coral low level threat to the extinction risk of However, this information does not Reefs (drafted by a working group of corals in general. change our determination that the threat

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is of low importance to the extinction Therefore, while we agree CITES proposed rule and Management Report risk of corals, generally. provides some protections for corals in (NMFS, 2012b). This final rule provides Comment 31: We also received the trade industry, we maintain that the that additional explanation, as numerous comments that strongly threat from collection and trade is low summarized here. There is an emerging disagreed with our characterization and and does not dictate the listing status of body of literature regarding the concept conclusion regarding the adequacy of any individual species. In addition to of reef resilience, defined as an regulatory mechanisms within the coral public comments, we collected some ecosystem’s capacity to absorb recurrent trade industry, particularly CITES and supplemental information on regulatory shocks or disturbances and adapt to other laws in major source countries mechanisms for the global marine change without compromising its such as Indonesia. Many commenters ornamental trade industry, including ecological function or structural assert that CITES and various details regarding trade of both live and integrity (Hughes et al., 2010; Obura, regulations provide adequate dead corals and other coral reef wildlife. 2005). Recent evidence suggests that restrictions and requirements for the In light of the public comments and managing local scale disturbances for ornamental trade of coral reef species, information we received regarding the resilience will be crucial to maintaining such that trade has much less of a ornamental trade industry, the Threat complex, bio-diverse coral reef negative impact on the extinction risk of Evaluation—Collection and Trade sub- ecosystems given the predicted the 65 coral species than was portrayed section discusses the trade and its widespread impacts of climate change by the proposed rule and supporting impacts to corals in detail, including related threats (Anthony et al., 2011). documents. One commenter also information regarding the physical and Therefore, we recognize that effective described Indonesia’s development of ecological impacts as a result of the local laws and regulations as well as regulations for their mariculture collection process, advances in conservation projects and programs may industry that is helping to alleviate wild aquaculture and mariculture industries, help reduce impacts to corals and coral collection pressures. as well as issues and trends in trade of reefs from threats on an ecosystem level, Response: In the proposed rule we both live and dead coral. Any species- positively affecting the timeframe at described that there are some specific information we received on which corals may become in danger of protections afforded via CITES and collection and trade is included in the extinction by providing a protective various other national regulations in Species-specific Information and temporal buffer (i.e., resiliency) to some countries where trade of coral reef Determinations section. individual coral species in the face of species is prevalent. However, we agree climate change related threats. Some Comments on Inadequacy of Existing that our evaluation of trade regulations evidence suggests that local Regulatory Mechanisms (ESA Factor D) was incomplete. There are numerous management actions, particularly of and Conservation Efforts challenges in documenting trends in fisheries (specifically, no-take marine trade due to deficiencies of CITES Comment 32: We received several reserves) and watersheds, can delay reef import and export data, and the most comments that critiqued our evaluation loss by at least a decade under recent information is conflicting. Some of local regulatory mechanisms and ‘‘business-as-usual’’ rises in GHG reports state that 98 percent of reef- conservation efforts. Some comments emissions (Jackson et al., 2014; Kennedy building corals within the aquarium asserted that we failed to adequately et al., 2013; Marshall and Schuttenberg, trade are still wild collected, with only consider the beneficial effects of local 2006; Mumby and Steneck, 2011). two percent originating from management actions and conservation However, many scientists strongly maricultured sources (Thornhill, 2012). efforts with regard to building reef suggest that these local actions be In contrast, another report shows that resilience in the face of climate change. combined with a low-carbon economy maricultured corals accounted for For example, we received a comment to prevent further degradation of reef approximately 20 percent of the trade in letter that stated a broad consensus structures and associated ecosystems 2010 (Wood et al., 2012). Further, exists for management to increase (Kennedy et al., 2013). adequate tracking of wild and marine ecosystem resilience to climate We cannot definitively say whether maricultured corals along the supply change by reducing local anthropogenic and to what degree the presence of chain from ocean to aquarium is stressors and reduction of these regulations in a particular location is extremely difficult, yet necessary for stressors may boost the ability of currently conferring resilience benefits determining the true dimensions and species, communities, and ecosystems for any particular species. Overall, we impacts of the industry (Cohen et al., to tolerate climate-related stresses or agree that local regulatory actions and 2013). Additionally, the level of wild recover after impacts have occurred. conservation efforts to reduce threats are collection of reef-building corals may be Another commenter emphasized the imperative for resiliency of coral reef underestimated due to an importance of local management for ecosystems in the face of climate undocumented illegal trade and a increasing coral reef resiliency, change. However, for purposes of significant amount of mortality along including management of land-use evaluating the inadequacy of regulatory the supply chain from reef to aquarium changes and water quality, as well as mechanisms as well as conservation (Thornhill, 2012). There are many other utilizing coral reef restoration efforts under the ESA, we are unable to issues and discrepancies related to techniques. Overall, these comments definitively establish the current status assessing the overall impacts of the disagreed with our characterization and effectiveness of local regulation of trade and the adequacy of regulations regarding the effectiveness of local impacts from local threats for any like CITES; however, collection and regulatory mechanisms and particular species in any given location, trade was ultimately ranked as a low conservation efforts in the face of with the exception of local regulatory level threat to corals in general by the climate change related threats and urged mechanisms for Acropora palmata and BRT and in the proposed rule. Further, us to consider the concept of reef A. cervicornis, which were evaluated in no one species of coral was determined resilience. detail in the 2005 status review for those to be threatened or endangered solely Response: We recognize that certain species. Further, we maintain that due to the effects of the coral trade aspects of local management actions and global regulations to reduce impacts industry, and that is still true for the conservation efforts need more from climate change are inadequate at final determinations in this rule. explanation than was provided in the this time. For more detailed information

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about our evaluation of how local listed as threatened rather than Refuges and National Parks that include regulatory mechanisms relate to endangered or even not at all. Therefore, coral reefs. We also received a public building coral reef resilience, please we cannot solely consider whether comment letter requesting us to refer to the Threats Evaluation— regulations or conservation efforts in the consider information regarding Inadequacy of Existing Regulatory United States or any other particular Indonesia’s Coral Reef Rehabilitation Mechanisms sub-section. Likewise, for location are sufficient for reducing and Management Program as a more detailed information about our threats to corals. The importance of conservation effort. evaluation of conservation efforts please global climate change-related threats to Response: We acknowledge that the refer to the Conservation Efforts sub- the extinction risk of these corals makes Final Management Report had some section. it even more problematic to limit our minor errors and omissions. However, it Comment 33: We received some assessment of conservation efforts and should be noted that the Final comments that disagreed with our the adequacy of regulatory mechanisms Management Report was not intended to characterization of local regulatory to individual countries. For these corals, be an exhaustive document; rather, it mechanisms in general, asserting that we are required to consider the aimed to capture the breadth of existing certain local laws are sufficient for adequacy of regulatory mechanisms for regulatory mechanisms and protection of corals, thus rendering reducing GHG emissions and curbing conservation efforts that may reduce additional protection via the ESA the rate of global climate change. threat impacts to corals and coral reefs. unnecessary. For example, we heard For this final rule, we assessed Due to the immense number of from several commenters who believe regulatory mechanisms and regulatory mechanisms that exist there are adequate regulations to conservation efforts in a more species- throughout the entire ranges of the 65 prohibit the damage of reef-building specific approach. To better capture the coral species (i.e., 84 countries), the corals, such that additional protections full breadth of existing regulatory Management Report was not intended to from the ESA are redundant. We also mechanisms, in addition to the identify every individual law and received comments that disagreed with individual country descriptions in the regulation that may have an effect on our characterization of conservation Final Management Report, we re- corals or their threats in every country efforts. For example, we received a characterized and summarized the within the species’ ranges. However, comment that disagreed with our presence of existing regulatory any additional laws and regulations that conclusion regarding conservation mechanisms throughout all the were brought to our attention through efforts, asserting that coral conservation countries in the range of each individual the public comments were noted and actions already have, and will continue species. The Inadequacy of Threats considered in the analysis of to, contribute to coral species recovery. Evaluation—Existing Regulatory inadequacy of existing regulatory Examples of conservation efforts that Mechanisms sub-section provides more mechanisms presented in this final rule were not included in the Final detailed information on that range-wide under the Threats Evaluation— Management Report (FMR; NMFS, evaluation process, as well as the Inadequacy of Existing Regulatory 2012b) include ongoing coral reef Species Descriptions for the results. For Mechanisms sub-section. restoration projects, specifically in more detailed information about our Comments on Risk Analyses Florida and the wider-Caribbean, as evaluation of the inadequacy of local well as aquaculture and mariculture management actions, please refer to the Comment 35: We received many efforts both internationally (e.g., Threats Evaluations—Inadequacy of comments regarding the composition of Indonesia) and within the United States Existing Regulatory Mechanisms sub- the BRT. Some comments disagreed to try to alleviate wild collection section. For more detailed information with the selection of BRT members, pressure on coral reef ecosystems. about our evaluation of conservation asserting that because all seven Comments urged us to take these efforts efforts, please refer to the Conservation members of the BRT were Federal into consideration for evaluating the Efforts sub-section of this rule. employees, non-Federal coral biologists status of the 65 corals in this final rule. Comment 34: Several comments with expertise in the field within Response: We recognize that certain identified potential errors, omissions, specific regions (e.g., Hawaii) were locations have effective local laws, and/or inaccurate characterizations overlooked, thus casting doubt on the regulations, and programs that address within the Final Management Report qualifications of the BRT members and local threats and provide for the (NMFS, 2012b). For example, we the results of the status review. One protection and conservation of coral received a comment letter pointing out comment suggested that the BRT species. For example, it is illegal to several omissions and inaccuracies member votes should have been collect or harvest reef-building coral regarding Federal management weighted to reflect their level of species in all U.S. states, territories, and responsibilities for an extensive area of expertise in the different types of corals commonwealths. Some laws even lands and waters in the Pacific Ocean. undergoing review. Another comment prohibit harming any reef-building coral Many other comments provided stated that it would not be possible for species through activities such as boat additional laws, regulations, or certain members of the BRT to act in a groundings and impose penalties and conservation efforts that were not neutral or unbiased manner because fines for doing so. However, we must described in the Final Management they are strong proponents of evaluate whether regulatory Report or identified previously during establishing Marine Monuments, mechanisms are inadequate for corals the public engagement period during sanctuaries, and MPAs for the across their entire ranges rather than in the summer of 2012. For example, one protection of coral reef systems any one specific location. Likewise, our commenter requested our inclusion of throughout the U.S. Pacific Islands. Yet analysis of conservation efforts must Guam Public law 24–87 that ensures another comment stated there was no also include the entirety of the species’ Guam’s marine preserves are protected independent verification from experts ranges, and it must consider whether from recreational/commercial activities who did not have a stake in the Federal those efforts will result in recovering the that may prove detrimental to fragile ESA listing processes. species to the point of ameliorating ecosystems. Another commenter Response: According to agency threats throughout the species’ range to pointed out that we omitted information guidance, members of the BRT should such a degree that a species should be regarding certain National Wildlife have expertise in the particular species’

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biology, population dynamics or stated that ranking each coral species on response to threats, abundance, and ecology, or other relevant disciplines relative to the rankings of other coral other characteristics were improperly (e.g., ocean/environmental/climate species does not inform NMFS of the extrapolated to species because there are processes, analytical techniques, risk status of an individual coral numerous examples in the literature in population genetics, extinction risk, or species. Another comment stated the which ecological or physiological traits pertinent threats). Additionally, NMFS Critical Risk Threshold graphs have an are not consistent across species within must also consider team composition in inappropriate and misleading a genus. light of the Federal Advisory Committee quantitative horizontal axis, which Response: In the proposed rule, we Act (FACA). Generally, any committee suggests higher threat levels than relied on higher taxonomic level (i.e., or group established for the purpose of estimated by the BRT. A couple of genus or family) information for threats providing consensus advice or comments questioned the assignment of susceptibilities when species-specific recommendations to a Federal agency is levels of confidence in the outcomes of susceptibilities were not available. We subject to the procedural requirements the BRT voting process given the lack of acknowledge that there is intra-genus or of FACA. Biological Review Teams are information on which those outcomes intra-family variability in response to subject to FACA because their were based, noting there was not a high threats in many cases. In response to assessments constitute group advice degree of certainty between the experts. criticism of how the proposed rule and upon which NMFS may base its Response: The voting methods used supporting documents inferred species’ determinations as to whether to list by the BRT are consistent with previous characteristics based on genus-level species as endangered or threatened agency listing determinations that information, this final rule does not under the ESA. Based on the utilized similar structured decision automatically assume that genus-level requirements of FACA, the team must making techniques. This approach is information for other species in the therefore be composed of Federal typically used when quantitative genus applies to the proposed species in officials and employees, and specific modeling of extinction risk is not a that genus. Rather, a careful analysis of classes of state employees, unless viable option due to a lack of precise genus-level information is incorporated specifically exempted. As such, the quantitative population data. The BRT’s into the Species-specific Information coral BRT was composed of seven voting relied upon professional and Determination sections below for Federal scientists from NMFS’s Pacific interpretation of the best available each of the 21 genera in which the 65 Islands, Northwest, and Southeast scientific information at the time, species belong. That is, as a preface to Fisheries Science Centers and the U.S. including qualitative assessments. This the Species-specific Information and Geological Survey and National Park approach allowed the BRT to explicitly Determinations for species in a genus, Service. The members of the BRT are a address various ranges of uncertainty this final rule includes a description of diverse group of scientists with within their voting. We also emphasize the available information for other expertise in coral biology, coral ecology, that the determinations in the proposed species in the genus that are not part of coral taxonomy, physical oceanography, rule did not solely rely on information this final rule, and an analysis of the global climate change, and coral within the SRR and the voting outcomes degree of applicability of that population dynamics. Additionally, the of the BRT. As described previously in information to the species included in BRT consulted with numerous non- the proposed rule and throughout this this final rule. Further, in no case in this Federal scientists and subject matter final rule, numerous sources of final rule do we extrapolate from family- information were considered and level information. experts during the status review, and incorporated in the listing Comment 38: We received multiple had their work peer reviewed, to ensure determination process, as described in comments criticizing the definition of the best available information was explicit detail in the Risk Analyses and ‘‘foreseeable future’’ in the proposed utilized in the SRR. These subject Species-specific Information and rule and supporting documents out to matter experts are detailed in the Determinations sections. Additionally, the year 2100 because it is too far into Acknowledgements of the SRR. Last, we the ESA does not require quantitative the future. One comment stated that provided extraordinary opportunities precision when estimating extinction climate change projections beyond 50 for non-Federal scientists to provide risk and determining whether a species years have a high degree of uncertainty their expertise prior to the publication warrants listing as threatened or and may be impacted by numerous of the proposed rule, including two endangered under the ESA. Rather, the unforeseen and unpredictable scientific workshops held in the decision must be reasonable and based circumstances, and thus identifying the summer of 2012. All information solely on the best scientific and foreseeable future as out to the year received was considered in the commercial information available at the 2100 is not appropriate. Another proposed rule. time of the decision, even in light of comment stated that our use of 2100 for Comment 36: We received numerous considerable uncertainty. the foreseeable future is contrary to criticisms regarding the evaluation Comment 37: We received several previous decisions made by FWS and methods used by the BRT. Many comments that criticized how the NMFS, and there have been no comments criticized the Critical Risk proposed rule and supporting breakthroughs in climate modeling to Threshold voting method used by the documents inferred species’ justify our new position on the BRT for developing extinction risk characteristics based on genus-level reliability of long-term climate values for the 82 corals within the information (i.e., the proposed rule modeling. proposed rule. Some comments asserted assumed that information for other Response: Consistent with our that the voting process relied on species in the genus applied to the practice for all species listing subjective opinion rather than scientific proposed species in that genus). A few determinations, we established that the facts, while other comments stated that comments stated that the BRT only appropriate period of time the anonymous scoring system by the considered threats to the taxonomic corresponding to the foreseeable future BRT could not truly be anonymous. class and therefore it conducted no is a function of the particular type of Still, other comments pointed out individual species threat analysis for threats, the life-history characteristics, critical errors or flaws in the BRT’s any of the candidate coral species. Most and the specific habitat requirements for methods. For example, one comment comments stated that genus-level info the coral species under consideration.

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The timeframe established for the conduct the species-specific analyses due to its occurrence in the Caribbean. foreseeable future considered the time required under the ESA. In general, the One comment stated that the BRT’s necessary to provide for the commenters indicated that the voting determination that the entire Caribbean conservation and recovery of each process by the BRT seemed very is sufficiently limited in geographic threatened species and the ecosystems subjective, with the results coming from scale to be a factor that increases the upon which they depend. It was also a the individual scientists’ perception of extinction risk of all corals in the function of the reliability of available extinction rather than solid scientific Caribbean is at odds with genetic data. data regarding the identified threats and data. The commenter provided references extends only as far as the data allow for Response: The proposed rule and the (Baums et al., 2005b; Baums et al., making reasonable predictions about the SRR did conduct a species by species 2006a; Murdoch and Aronson, 1999; species’ response to those threats. In the analysis of extinction risk for each of the Vollmer and Palumbi, 2007) that show proposed rule, we explained that our candidate corals. However, in the that, while it is clear that regional-scale choice of the year 2100 as the proposed rule, the presentation of the processes such as bleaching and disease ‘‘foreseeable future’’ for analysis of information on which we based our are acting on all these reefs global climate change was based on determinations may have been unclear simultaneously, no two reefs or areas AR4’s use of 2100 as the end-point for because of our use of the Determination respond the same to these disturbances. most of its global climate change Tool as an organizational mechanism to Another comment asserted that no models. Similarly, most of AR5’s WGI present the enormous amount of data. In threat to Caribbean Acropora is models also use 2100 as the end-point response to criticism of the lack of imminent, and therefore endangered (some models go beyond 2100) and sufficient species-specific information listings are not supportable for these AR5’s WGI reinforces our original in the proposed rule and supporting species. rationale for defining the foreseeable documents on distribution, abundance, Response: Geographic distribution is future as the period of time from the threat susceptibilities, and other one of many factors we must evaluate to present to the year 2100. For global information, this final rule clarifies and determine a species’ status. We agree climate change threats, there is strong explains how the information relating to with commenters that an inherent support for considering the foreseeable the taxonomic, field identification, increase in extinction risk solely due to future as the period from the present to distribution, abundance, life history, occurrence in the Caribbean is not 2100 in AR5’s WGI and its cited threat susceptibilities, and management accurate; rather, the ratings in the literature (IPCC, 2013). However, we information for each of the 65 coral Determination Tool regarding basin agree that the foreseeable future for species were evaluated in reaching the occupancy were an inadvertent function purposes of other threats to the species final listing determinations. The of comparing the Caribbean basin to the and the species’ responses thereto does presentation of the information includes Indo-Pacific basin. That is, the not necessarily extend out to 2100. the information on which the proposed automatic increase in extinction risk for Therefore, in this final rule, we clarify rule was based, information submitted species occurring in the smaller, more that 2100 simply marks the outer by public comments, and information disturbed Caribbean was only relative in temporal bounds for consideration of we gathered after the proposed rule comparison to species occurring in the climate change-related threats, and does published. The information was also larger, less disturbed Indo-Pacific. In not frame our analysis across all threats analyzed in an integrated, non- light of public comments, we formulaic framework instead of in a determined that absolute range size in or our ultimate listing determinations. linear, formulaic framework as it was in both the Caribbean and Indo-pacific was Further discussion of the foreseeable the Determination Tool. The resulting inadvertently under-estimated in the future is presented in the Foreseeable information provides the basis for the 65 proposed rule. As a result, we now give Future subsections of the Threats listing determinations in this final rule. consideration to geographic distribution Evaluation and Risk Analysis sections In addition, while IUCN listings were in terms of absolute size rather than below. used by the petitioner as one criterion relative size in both the Caribbean and Comment 39: There were many for selecting coral species in the original Indo-Pacific. We still maintain that the comments on the quantity and quality of 2009 petition, and IUCN maps were Caribbean is a highly disturbed basin information used to make listing used in the 2011 SRR, no IUCN data or that has experienced loss of resilience; decisions for the candidate coral species information is used in this final rule however, the reconsideration of absolute in the proposed rule. Several comments because it does not represent the current distribution represents one piece of a stated that the present biological data do best available species-specific more holistic approach to linking each not support the proposed listings. They information. To explain more clearly the species’ characteristics to each species’ stated that the available science was changes from the proposed to the final status. The implications of occurrence insufficient and not compelling enough listings, we included an Overview of in the Caribbean and more detailed to demonstrate the need to make a Methods and Key Changes Applied in descriptions of geographic ranges and decision under the ESA. A few Final Determination Framework sub- how they may affect extinction risk are comments criticized the use of IUCN section within the Risk Analyses section now provided in more detail for all data as a surrogate for ‘‘true scientific to illustrate how all of the available species individually in the Risk data’’ on species distribution and information was considered for each Analyses and Species-specific abundance. Many comments stated that species and how it contributed to each Information and Determinations useful information was available, species’ listing status. As a result, the 65 sections below. especially on coral trade and species-specific determinations below We also explicitly incorporated mariculture, but the BRT did not use it, are based on the best available species- consideration of regional and local which led to serious errors in the SRR. specific information and improves upon variability in response to threats. We The study by Rhyne et al. (2012) was the proposed rule. have also endeavored to provide a given as an example. Other comments Comment 40: We received a couple of clearer discussion of how we assessed stated that there was little data comments disagreeing with the the vulnerability of each coral species, regarding individual species’ population characterization of the level of not just the Caribbean Acropora, to the numbers and trends, so NMFS did not extinction risk inherent for a species major threats. The evolution of the

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Determination Tool into a more inherently biased towards listing. The Tool, which was one component of the comprehensive Determination commenter criticized that the first determination framework. To better Framework is described in the Risk element in the Determination Tool was explain how the Determination Tool Analyses section of this final rule just a re-hash of the BRT’s highly assessed risk and derived listing below. subjective ranking of threats and statuses we conclude that, as some vulnerabilities. The commenter also public comments suggested, the Comments on the Determination Tool asserted that nowhere in the four Determination Tool was too linear and Comment 41: Commenters criticized elements of the Determination Tool is deterministic. We describe our final that the Determination Tool equated there a discussion of imminence or a determination framework in greater species’ characteristics to outcomes discussion of why we considered a detail in the Risk Analyses—Final without adequate rationale. For species that meets any of the four factors Determination Framework sub-section example, one commenter stated that the to be ‘‘on the brink’’ of extinction. The below, and utilize a more holistic Determination Tool suffers from a lack commenter asserted that we not only approach in considering all of the of transparency because we did not failed to adhere to the legal standard of available information for each species. provide any information regarding how endangered, but we did so on extremely As described in that section, the non- the rating values in the Determination poor evidence. Further, the commenter formulaic approach used in this final Tool were assigned, who made the criticized the results of the BRT voting rule, is more species-specific, and determinations, what their expertise as well as the Determination Tool for allowed us to address the concern that was, or on what basis the decisions were ranking each of the coral species’ in a sufficient species-specific information made. relative fashion, and as a result, asserted was not available. Several comments stated that the that our approach in determining In summary, the Final Determination Determination Tool’s decision points extinction risk for each species was Framework in this final rule is and resulting outcomes depended on flawed. composed of seven elements. The first species-specific information that was Several comments pointed out element is describing the statutory not available. For example, one additional perceived flaws in the standards for corals. The second, third, commenter asserted that there is little to Determination Tool. For example, one fourth, and fifth elements are no experimental data provided in the commenter stated that the identifying and analyzing all the proposed rule documentation to support Determination Tool dismissed the appropriate species-specific and general the ratings used in the Determination potential benefits of management characteristics that influence extinction Tool. Another commenter noted that efforts. Another commenter noted that risk for a coral species. The sixth there is almost no information on many the Determination Tool did not element is relating a species’ of the species’ abundances, geographic incorporate or consider projections of characteristics to a particular extinction ranges, trends or recruitment rates, and adaptation potential over the foreseeable risk at appropriate spatial and temporal that the ratings for these were based future (i.e., 2100). More specifically, the scales. The seventh element is explicitly solely on qualitative opinion. Similarly, commenter asserted that the stating how each species’ extinction risk another commenter used ocean Determination Tool did not sufficiently meets the statutory listing definitions as acidification as an example, stating that consider the ability of corals to migrate applied to corals, resulting in an due to the large degree of uncertainty (i.e., undergo range expansion/shift) and ultimate listing status. As a last regarding the impacts of ocean adapt to changing conditions, especially consideration, we determine if any acidification on coral species it is when local stressors are well managed. conservation efforts are abating the difficult to quantify the level of risk One commenter also suggested that the threats to the species such that it ocean acidification poses to the species. Determination Tool conflicted with the changes the individual species’ listing The commenter concluded by stating SRR (e.g., by giving too much weight to status (i.e., an endangered species’ that assigning levels of ocean distribution when the range maps that extinction risk is reduced such that it is acidification-associated risk within the the BRT relied upon were not precise). threatened or that a threatened species Determination Tool is a difficult Similarly, commenters also criticized us is not warranted). This method of proposition. Another commenter for overemphasizing the importance of implementing our Final Determination deemed the Determination Tool analysis qualitative rankings for species’ Framework for every species and results arbitrary. The commenter abundance (e.g., common, uncommon, individually is intended to be more stated that the analysis and results of rare) in the Determination Tool, stating transparent, by showing how complete the Determination Tool were based on that a coral species’ rarity does not use is made of available information to the same faulty assumptions, necessarily correspond to its reach individual listing decisions. extrapolations, assessments, and vulnerability to extinction. We believe that there is still approximations of the seven BRT Response: We acknowledge that significant value in applying a members and were based on very little, several aspects of the process by which standardized framework to each of the if any, species-specific spatial we produced our determinations in the species to ensure consistency distribution or abundance data for a proposed rule were not described or throughout the 65 individual number of the proposed species. explained clearly enough. The determinations, but now do that in a Commenters claimed the Determination Tool in the proposed rule narrative fashion in which there are no Determination Tool was flawed and was a central aspect of a larger overall recipes or formulas for endangered, equated species’ characteristics to framework for making our decisions, as threatened, and not warranted species. listing outcomes too conservatively, it organized and standardized our This approach allows for the especially for proposed endangered presentation of the risk factors, but we consideration of the system as a whole species. We received a detailed acknowledge that the larger (i.e., synergistically evaluating each comment letter that outlined several determination framework was not species’ demography, spatial criticisms of the Determination Tool and sufficiently explained in the proposed characteristics, threat susceptibilities, its four elements with regard to species rule. This lack of a clear explanation led and current and future environmental outcomes. The Determination Tool was to an overemphasis on and conditions independently of the other labeled faulty because it was deemed misunderstanding of the Determination species), leading us to species-specific

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conclusions about vulnerability to those are factors that provide additional incorporated this supplemental extinction. buffering against extinction risk. We information in our discussions in the In response to the criticism that the have incorporated that consideration in individual species-specific listing Determination Tool did not the final rule through our Final determinations in that section of this appropriately evaluate the imminence of Determination Framework and species- final rule. In light of the supplemental danger of extinction in proposing to list specific evaluations. species-specific information, and the corals as endangered, in this final rule Comments on Listing Determinations change to a more holistic and species- we more fully explain the biological specific determination framework, we Comment 43: We received numerous characteristics and distinctions between considered the ability of each species’ comments referring to the actual listing endangered and threatened corals, and distribution and abundance traits to corals not warranting listing under the determinations of the 82 candidate coral affect vulnerability to extinction in the ESA, and relate each species’ particular species in the proposed rule. Many of context of the statutory definitions of characteristics to one of those those comments referred to specific classifications. These characteristics and coral species and to specific aspects of threatened and endangered for each the distinctions between them as they those species determinations. Those species. In most cases, this relate to the three ESA classifications comments are discussed in detail in the consideration led to changes in listing are explained in the Statutory Standards Caribbean Species: Listing status from the proposed rule. These sub-section of the Risk Analyses section. Determinations, Indo-Pacific Species: species-specific assessments consider Listing Determinations, and all of the public comments and available Comments on Significant Portion of Its Reclassification of Acropora palmata information for each species and Range (SPOIR) and A. cervicornis comment response provide a detailed description of what is Comment 42: We received one sections below. The other comments and is not known for each species, comment regarding the identification of regarding listing determinations including susceptibilities to all a significant portion of its range to centered on the lack of species-specific identified threats and vulnerability to support not warranted determinations information on which the species extinction for the proposed coral species found in determinations were based. Some Comment 44: We received several Hawaii. The commenter asserted that comments were very skeptical that the letters alerting us to an extensive the species of corals proposed for listing assumptions being made from limited ongoing effort by coral expert, Dr. J.E.N. in Hawaii are abundant, relatively scientific information on individual ‘‘Charlie’’ Veron, to gather previously healthy, and relatively insulated from coral species, which the proposed rule impacts of the primary identified recognized, could justify the listing unpublished information for all reef- threats. As a result, the species will proposals. These commenters asserted building corals of the world, including presumably persist in Hawaii, despite that further studies and surveys should the 65 corals in this final rule. The more immediate threats in other be performed to gather factual and resulting report (Veron, 2014) updates portions of their ranges, ultimately relevant data on the status of the coral species-specific information on semi- preventing the species from going species, which could potentially change quantitative (i.e., survey data from 2,984 extinct. Thus, the commenter argues the assumptions used to make the individual sites) and qualitative that a significant portion of its range listing determinations. Some comments population abundance estimates (i.e., should be identified for these species, specifically stated that a much better Veron’s subjective estimates covering a rendering the species not warranted for understanding of the global distribution full range of habitats and most listing. and abundance of the species, including ecoregions the author has worked in), Response: The commenter developing better species distribution geographic distribution, principle misunderstands the function of the maps, is critical to making an informed habitat, and identification issues. SPOIR analysis. As discussed in the listing decision. Yet other comments Comments stated that given the lack of Statutory Standard sub-section below, a stated that the proposed rule did not species-specific information on SPOIR analysis is performed to ensure take into account the variability of quantitative abundances and geographic that a species that has been found not response to threats that corals can have distribution for most of our Indo-Pacific to be endangered or threatened based on based on species, location, habitat type, species, this effort proves extremely the range-wide analysis is still and other factors that define an relevant to our listing decisions within considered for listing if any portions of individual coral. Other comments this final rule. its range meet the criteria of the SPOIR suggested that NMFS was using global Response: We agree with comments Final Policy. Therefore, the function of climate predictions as a substitute a SPOIR is not to avoid a listing but to measure for species population and that information from Veron (2014) still consider a listing. In any case, as distribution information for listing supplemented the existing species- described in the Risk Analyses section purposes. specific information relied on in the below, the results of our analysis of Response: We recognize that species- proposed rule and that this information SPOIR are unchanged from the specific information was fairly limited is relevant to the determinations made proposed rule, after considering all for many of the proposed species. in this final rule. Thus, the comments and supplemental However, since the proposed rule was supplemental information received in information. At this time, no SPOIR is published, we have received or the report (Veron, 2014) was made determinable for any of the proposed collected information for all species, available to the public on NOAA’s Web species. Thus, our analysis of each including supplemental distribution site, and has been incorporated into the species at the range-wide level is and abundance information for 63 of the Species-specific Information and determinative, and no portions of the 65 species in this final rule as a result Determinations section for the 63 range require further examination. of the data collection effort by Veron species covered in the report, Veron Nevertheless, we agree with the general (2014). In addition to updating all of the (2014) does not cover non-scleractinian underlying premise of the comment, general information regarding coral reef corals in his report, and thus did not which is that if a species has significant biology, ecology, demography, and provide information for the Millepora areas of refugia or diversity of habitat, threat susceptibilities, we also species in this final rule).

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Comments on Alternatives To Listing commercial data available within the threats to these deep-sea corals or to Under the ESA applicable statutory timeframes for similar corals in the area. Additionally, Comment 45: We received several responding to petitions, as the basis for ocean acidification research cited in the comments that suggested alternatives to our final determinations. petition was conducted on mostly Comment 46: We received comments ESA listing such as Candidate tropical, reef-building corals that are that criticized our proposed Conservation Agreements (CCAs), very different from deep-sea corals; no determinations due to their assumed adding the proposed corals to the inference could be made about the inconsistency with other recent agency Species of Concern list, and extending potential effects to the status of deep-sea decisions, such as the Not Warranted the time period in which to make a corals from this information. Finally, bumphead parrotfish 12-month finding, determination to allow for the gathering there have been large swaths of fishing and the negative Alaska deep-sea corals ground closures in Alaska since 2005 of additional scientific data. One 90-day finding. Comments cited a lack and NOAA determined that these commenter suggested using CCAs, citing of adequate species-specific information closures were sufficient for protecting lack of species-specific information and and taxonomic uncertainty as deep-water corals from bottom-contact other concerns as justification. justification for the previous not fishing activities. Overall, differences Comments also asserted that because warranted and negative determinations between the Alaska deep-water corals NOAA has no authority under the ESA for bumphead parrotfish and Alaskan and the reef-building corals in this final to protect corals from climate change, corals, and claimed that the proposed rule are vast; however, we have CCAs could provide the same rule for the 68 reef-building corals complied with the requirements set conservation benefits as ESA listings. suffers from the same level of forth under the ESA in each case. Response: While we acknowledge that uncertainty. Comments thus concluded CCAs provide conservation value for that NOAA’s decision to propose 68 Comments on Caribbean Species: candidate species, no such agreements reef-building corals for listing under the Listing Determinations exist for any of the proposed species. ESA is inconsistent with previous Comment 47: We received some Therefore, we are unable to determine a agency decisions and that there is a lack comments that expressed disagreement species’ status on the basis of the of adequate species-specific information with our proposed threatened conservation provided by a CCA. to proceed with final listings. determinations for some Caribbean Further, in the Conservation Efforts Response: We respond to each species. For example, one comment section we determined that there are no petition based on the information disagreed with our proposed threatened conservation efforts currently or presented within that petition and, if we listing of Dichocoenia stokesi, citing the planned in the future that are expected conduct a status review, on the best following as justification: Large to improve the overall status of any of scientific and commercial information population numbers (even after the the 65 coral species in this final rule, available for each petitioned species at White Plague Type II epidemic), broad such that the additional protections the time. We disagree that this final rule distribution among multiple habitat provided by the ESA are not warranted. for 65 reef-building corals is types (especially hard-bottom habitats), We also considered the potential for inconsistent with our previous Not high relative abundance among all utilizing the Species of Concern Warranted 12-month finding for the corals in the region, and the presently designation, which was suggested in bumphead parrotfish. Primary threats to low prevalence of White Plague Type II. lieu of ESA listings due to a lack of bumphead parrotfish, a coral reef- Another comment stated that D. stokesi species-specific information and associated fish, were determined to be is among the most common species in taxonomic uncertainty. This designation adult harvest and juvenile habitat loss. Florida, and that population estimates can be used if we decide a species is not As a result of a thorough status review, approached 100 million colonies in warranted for listing under the ESA the bumphead parrotfish received a Not 2005, with no apparent downward because we are unable to confidently Warranted determination largely due to trend. In addition, we received assess the level of extinction risk, even its current abundance, life history, comments about the proposed qualitatively. Ultimately, based on the existing local management in the form threatened determination for Agaricia best available scientific information, we of spear fishing regulations, and lamarcki. Comments argued that due to concluded that all 65 corals within this protections for mangrove habitat. potentially larger populations not yet final rule are determinable species Overall, the differences between surveyed in deeper waters, the under the ESA. We also concluded that bumphead parrotfish and the reef- threatened status for A. lamarcki is not we have enough information to building corals in this final rule are vast; warranted. Many comments disagreed qualitatively assess the level of however, we have complied with the with the proposed endangered extinction risk and make listing requirements set forth under the ESA in determinations for the Orbicella determinations for most of the 65 each case. (formerly Montastraea) annularis species in this final rule with some Likewise, we disagree that this final complex (i.e., O. annularis, O. faveolata, degree of confidence. The species that rule is inconsistent with the negative and O. franksi). One comment provided are determined to be not warranted for 90-day finding for 44 Alaska deep-sea information from van Woesik et al. listing due to a lack of sufficient corals. The Alaska deep-sea coral (2012) as justification for listing O. information to assess their status are species are non-reef building and annularis complex as threatened rather clearly described as such in the exhibit many different characteristics than endangered. Other comments individual species determinations. than shallow-water tropical corals, submitted a technical report (Miller et Those species may be considered for which have been comparatively well al., 2013) from the Nova Southeastern inclusion on the Species of Concern list researched. The Alaska corals were University on population abundance after this listing rule becomes final. petitioned due to climate change related estimates and trends for the Caribbean Extending the time period in which to threats, as well as physical threats from coral species in the Florida Keys, in make final species determinations in commercial fisheries. NOAA considered opposition to all proposed endangered order to collect more scientific data is these factors, but found that there are no listing determinations, including the not permissible under the ESA. We are empirical studies that have shown proposed endangered determinations for required to use the best scientific and harmful effects of climate change related the Orbicella species as well as

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Dendrogyra cylindrus and annularis, O. faveolata, O. franksi, D. that provided species-specific Mycetophyllia ferox. Miller et al. (2013) cylindrus, and M. ferox as endangered information for each of the proposed provided recommended changes to the species. Our final determination for endangered species (e.g., only two proposed listing statuses for each of the these species is to list them as percent, 5.9 percent and 9.4 percent of proposed Caribbean species using their threatened species. We have determined the references used in the SRR provided population and distribution estimates as D. stokesi and A. lamarcki do not species-specific information for support. We received other comment warrant listing. Acropora rudis, Acropora lokani, and Acropora jacquelineae, respectively). letters that also noted the large Comments on Indo-Pacific Species: We also received comments regarding population abundances of several of the Listing Determinations Caribbean species, despite some local the proposed endangered declines (i.e., O. annularis and O. Comment 48: We received several determinations for various Acropora faveolata). One comment also noted that comments regarding our proposed species, particularly A. lokani and A. for five of the Caribbean species (i.e., O. threatened and endangered jacquelineae. For example, one franksi, D. cylindrus, M. ferox, D. determinations for various Indo-Pacific comment emphasized the lack of stokesi, and A. lamarcki) there is a species. Several comments disagreed adequate data for the proposed complete lack of population data to with our proposed threatened endangered determination of A. support ESA listings. We also received determinations for the Hawaiian jacquelineae, citing questionable information regarding the ecology of O. Montipora clades (M. dilitata/flabellata/ taxonomic status and lack of density annularis and O. faveolata in opposition turgescens and M. patula/verrilli). As estimates and distribution information. to their proposed endangered described in more detail below, Likewise, another comment criticized determinations, but supporting comments disagreed with the status of the proposed endangered determination threatened listings. One comment these clades and suggested they be for A. lokani, stating that there is argued that the total population number assessed individually rather than virtually no published information estimates of these two species are very lumped into groups (see Comment 49 available for this species. Another large and that, in light of their broad below for more details). Taxonomic comment letter recommended depth ranges and multi-habitat uncertainty as it relates to the Genus threatened designations for A. distributions, these species are Montipora and the decision to lump jacquelineae, A. lokani, and A. rudis relatively resistant (in ecologic time) to these two groups of species is addressed rather than endangered, based on van in more detail in the response to extinction. Accordingly, the comment Woesik et al. (2012), and stated that comments on taxonomic uncertainty asserted that these species’ potential Euphyllia paradivisa absolutely does (Comment 3 above). Comments also listing is contrary to their ecology, not warrant endangered status. We asserted that the Montipora clades not especially in light of their remaining received other comments in only have significantly large geographic substantial population numbers both in disagreement with our proposed ranges, but also include some of the Florida and throughout their range. endangered determinations, but they most common coral species in Hawaii, did not include any other substantive Response: Since the proposed rule thus rendering these clades not information or data to consider. was published, we received and warranted for threatened listing. We Response: We recognize that species- collected supplemental information for received many other comments that specific information was limited for all the Caribbean species, including disagreed with the proposed threatened many of the Indo-Pacific species. Since updated distribution and abundance determinations for a number of the the proposed rule was published, information. Therefore, we updated and Indo-Pacific coral species, but we did however, we have received or collected expanded our individual species- not receive any additional substantive supplemental information for several specific descriptions in the Species- information or data for consideration of species, including updated distribution specific Information and Determinations those arguments. and abundance information for 63 of the section for all 65 reef-building corals One commenter provided information 65 species in this final rule as a result within this final rule. These species- regarding the proposed endangered of the data collection effort by Veron specific assessments consider the public status of Pocillopora elegans in the (2014). As a result, we substantially comments and available information for Eastern Pacific. Evidence from updated and expanded our individual each species, and explain what is and is southwestern Nicaragua suggests that P. species-specific descriptions in the not known for each species, including elegans has undergone extensive Species-specific Information and susceptibilities to the identified threats mortality, with only a few fragmented Determinations section for all 65 reef- and overall vulnerability to extinction. and small colonies persisting. The data building corals within this final rule. Further, as described in earlier comment provided, while limited, supports a These species-specific assessments responses, we now more fully consider wider body of evidence suggesting consider all of the public comments and the ability of abundance, distribution particular vulnerability of P. elegans in available information for each species, and habitat heterogeneity to affect the Eastern Pacific Ocean. However, as and provide a detailed description of vulnerability to extinction in the context described above in Comments on what is and is not known for each of the statutory definitions of threatened Taxonomic Uncertainty in Reef-building species, including vulnerabilities to all and endangered as applied to corals. Corals, new information on Pocillopora identified threats. The reconsiderations of the spatial and species has resulted in our Comment 49: We received some demographic factors contributed to determination that P. elegans is not comments that provided species- changes in all the Caribbean species’ determinable under the ESA. specific information for various Indo- statuses in this final rule. Thus, as The main argument against our Pacific species that is being applied in described in detail in the Species- proposed endangered determinations for this final rule. The species-specific specific Information and Determinations Indo-Pacific species is a lack of information we received predominantly section, based on the public comments, adequate species-specific information to relates to relative abundance and best available information, and the Final support an endangered status. For geographic distributions. We Determination Framework, we are example, one comment letter noted the specifically received comments on revising our proposal to list O. percentage of references used in the SRR abundance for the following Indo-

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Pacific species: Acropora aspera, Porites Determinations section, based on the endangered. Most comments agreed nigrescens, Acropora diversa, and Final Determination Framework and with the current status of threatened for Isopora cuneata. We specifically supplemental information, we are the Caribbean acroporid species. Many received comments on distribution for maintaining our proposals to list comments cited increasing abundances, the following Indo-Pacific species: Acropora globiceps, Acropora recovering populations, and significant Alveopora allingi, Acropora palmerae, pharaonis, Acropora retusa, Acropora advances in active restoration projects Acropora paniculata, Acropora speciosa, Acropora tenella, Isopora as justification for not reclassifying jacquelineae, Acropora rudis, Euphyllia crateriformis, Montipora australiensis, them as endangered. One comment paradivisa, Acanthastrea brevis, Pavona diffluens, Porites napopora, and opposed the proposed reclassification, Acanthastrea ishigakiensis, Seriatopora aculeata as threatened in citing population numbers (Miller et al., Acanthastrea regularis, Acropora this final rule. Five Indo-Pacific coral 2013), genetic diversity (Hemond and globiceps, Acropora lokani, Acropora species determinations changed from Vollmer, 2010), forward-looking striata, Alveopora fenestrata, Alveopora endangered in the proposed rule to population models and extinction verilliana, Astreopora cucullata, threatened in the final rule: Acropora models based on paleontological data Barabattoia laddi, Euphyllia jacquelineae, Acropora lokani, (van Woesik et al., 2012), and a better paraancora, Millepora tuberosa, Pavona Acropora rudis, Anacropora spinosa, understanding of the causes of and diffluens, Pocillopora danae, Acropora and Euphyllia paradivisa. Forty Indo- resistance to mortality (Kline and verweyi, and the Montipora clades that Pacific coral species’ determinations Vollmer, 2011; Vollmer and Kline, 2008) are discussed in more detail below. We changed from threatened in the as justification. Comments also stated received several detailed comment proposed rule to not warranted in the that there has been no significant letters that provided species-specific final rule: Acanthastrea brevis, change in the population status of the information regarding the Hawaiian Acanthastrea hemprichii, Acanthastrea acroporids since their initial listing in Montipora clades (i.e., Montipora ishigakiensis, Acanthastrea regularis, 2006, and populations are relatively dilatata/flabellata/turgescens and Acropora aculeus, Acropora acuminata, stable and recovering in some areas. Montipora patula/verrilli). Several of the Acropora aspera, Acropora dendrum, One commenter also emphasized that A. comments provided references to Acropora donei, Acropora horrida, cervicornis in particular does not journal articles or other reports as new Acropora listeri, Acropora microclados, warrant endangered listing status due to species-specific information. Some of Acropora palmerae, Acropora its presence throughout its entire those references were already available paniculata, Acropora polystoma, biogeographical range, population to NMFS and some constituted Acropora striata, Acropora vaughani, expansion northward in south Florida, supplemental information we did not Acropora verweyi, Alveopora allingi, and its ability to still reproduce consider in the proposed rule. We Alveopora fenestrata, Alveopora sexually. One commenter asserted that received three comments specific to verrilliana, Anacropora puertogalerae, reclassifying the Caribbean Acropora genetics of Indo-Pacific species Astreopora cucullata, Barabattoia laddi, species to endangered is not warranted specifically referring to Pavona species Caulastrea echinulata, Euphyllia because the threats to these species are at mesophotic depths and to Pocillopora cristata, Euphyllia paraancora, Isopora not imminent. Additionally, many species. Species-specific comments cuneata, Millepora tuberosa, Montipora comments cited the growing number of regarding taxonomy were specific to angulata, Montipora calcarea, successful restoration projects Acropora acuminata, Acropora Montipora caliculata, Montipora throughout southeast Florida and the paniculata, and Acropora polystoma. dilatata/flabellata/turgescens, Caribbean (Hollarsmith et al., 2012; Comments with species-specific Montipora lobulata, Montipora patula/ Johnson et al., 2011; Young et al., 2012) information on threat vulnerabilities verrilli, Pachyseris rugosa, Pectinia that continue to aid in conservation of applied to Acropora aculeus, Acropora alcicornis, Physogyra lichtensteini, acroporids and help recover genetically aspera, Acropora paniculata, Acropora Porites horizontalata, and Porites viable populations. Overall, comments polystoma, Montipora patula, nigrescens. Finally, Millepora foveolata suggest the Caribbean acroporids should changed from endangered in the Montipora flabellata, Pocillopora remain threatened under the ESA, and proposed rule to not warranted in the elegans, Porites horizontalata, and do not warrant reclassification to final rule. endangered status. However, we did Seriatopora aculeata. Last, as described in Comment 2, Response: Overall, most of the three coral species determinations receive one comment letter in support of supplemental information we received changed from endangered or threatened the reclassifications for the Caribbean for the Indo-Pacific species was specific in the proposed rule to not determinable acroporids. to certain geographic locations; in the final rule: Pocillopora elegans Response: As described previously, however, we must evaluate the status of (eastern Pacific) warranted listing as we have revised and provided a clearer the species throughout the entirety of endangered in the proposed rule but explanation of our decision-making their ranges. As described in earlier was considered not determinable in the framework to further strengthen our comment responses, we now more fully final rule, and Pocillopora danae and final listing determinations. As with all consider the ability of spatial and Pocillopora elegans (Indo-Pacific) other species in this final rule, we demographic traits, as well as the warranted listing as threatened in the updated all of the general information heterogeneous habitats occupied by all proposed rule but were considered not regarding coral reef biology, ecology, of the Indo-Pacific species, to affect determinable in the final rule. demography, and threat susceptibilities vulnerability to extinction in the context relevant to the Caribbean acroporids, of the statutory definitions of threatened Comments on Reclassification of and thus we substantially updated and and endangered for each species. For Acropora palmata and Acropora expanded our individual species- many of the Indo-Pacific species, their cervicornis specific descriptions for these species in geographic ranges include waters Comment 50: Several comments the Species-specific Information and between the east coast of Africa and disagreed with our proposal to reclassify Determinations section. Further, as French Polynesia. As described in detail the Caribbean species A. cervicornis and previously described in earlier comment in the Species-specific Information and A. palmata from threatened to responses, we more fully consider in

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this final rule the ability of spatial and and commercial data available, after exemptions from Section 9 take demographic traits, as well as habitat conducting a status review and taking prohibitions for specific activities that heterogeneity, to affect vulnerability of conservation measures into account. should be included in a 4(d) rule issued the Caribbean acroporids to extinction Therefore, comments relevant to the for threatened species listed in this final in the context of the statutory proposed listing include those rule. Two comments recommended that definitions of threatened and comments that provide additional lawful emissions of GHG should be endangered for corals. substantive information regarding included as an exception in any future We also carefully considered the whether a species is in danger of 4(d) rule. Two other comments said the significant progress of active restoration extinction or likely to become so in the opposite, stating that NMFS should not projects in the state of Florida and the foreseeable future (e.g., the biology, consider GHG emissions in the context wider-Caribbean. We agree that these status, and/or threats to the species, of the ESA. efforts confer conservation and potential evaluation methodologies, effectiveness Response: The comments described recovery benefits for the species; of conservation measures, accuracy and above did not provide substantive however, these efforts, to date, are very comprehensiveness of best available information to help inform the final limited in scale compared to the species information, etc.). We are unable to listing determinations for the 65 coral ranges and should not be considered a consider other types of comments in a species. NMFS is not required to issue panacea for conserving and recovering listing determination (e.g., socio- a 4(d) rule for threatened species in the Caribbean acroporids. The economic or policy impacts). However, conjunction with a final ESA listing. We Conservation Efforts section of this rule after we implement the final listings, we will do so only if we determine it is provides more information on active will work with our stakeholders and necessary and advisable for the coral reef restoration efforts. As affected entities to reduce the impact of conservation of threatened species. If we described in detail in the Species- the listings while still providing for the make that finding for threatened species specific Information and Determinations conservation of the listed corals. listed in this final rule, issuance of a section, based on the Final 4(d) rule is a separate rule-making Determination Framework and Comments on Critical Habitat process that will include specific supplemental information, we are Comment 52: We received three opportunities for public input. As such, changing our proposal to reclassify A. comments related to critical habitat. the comments above are noted but not palmata and A. cervicornis as One commenter offered to provide responded to further in this final rule. endangered species. Acropora palmata information to assist in the economic Comments on Identification of Those and A. cervicornis will remain listed as analysis required for critical habitat Activities That Would Constitute a threatened species. designation. A second commenter proposed the use of NOAA benthic Violation of Section 9 of the ESA Comments on Effects of Listing habitat maps to define areas of critical Comment 54: We received numerous Comment 51: We received several habitat for listed corals and requested comments regarding concerns over the comments that described potential reconsideration of designated critical definition of ‘‘take’’ for corals under the negative effects that could result from habitat for Acropora palmata and ESA. Comments questioned how we ESA coral listings. These include Acropora cervicornis. A third would define ‘‘take’’ if corals are listed, regulatory burdens in the form of permit commenter requested to be consulted considering their unique biological and applications and other various during critical habitat designation to ecological characteristics (i.e., corals are paperwork, consultations and biological ensure the operation of their facilities colonial and clonal organisms). One opinions, postponement of in-water would not be affected. commenter pointed out a lack of maintenance activities, and increased Response: The comments summarized certainty regarding the threshold of costs associated with harbor above do not provide substantive ‘‘take’’ for coral larvae. Another improvement projects. We also received information to help inform the final commenter thought it was unclear how numerous comments expressing species determinations. NMFS is people would know if they are ‘‘taking’’ concern about impacts to cultural required to designate critical habitat at a listed coral and expressed concern practices as a result of listing, including the time of final rule publication, unless about the ability to conduct cultural native artists’ livelihoods, reef access by we determine that critical habitat is practices. A third commenter stated indigenous peoples, fishing, lime undeterminable at that time. Below, we that, in the example of corals, the stated production, customary navigation and discuss our determination that critical goals of the ESA are at odds with the seafaring, and specifically native habitat is not currently determinable for best plan for the recovery of any coral Hawaiian recreational and cultural the species being newly listed through species. practices, and the cultural needs and this final rule. Designation of critical Response: We agree that defining practices of American Samoa. One habitat will occur via a separate rule- ‘‘take’’ of corals under the ESA is both comment expressed concern that making process once this final rule is unique and challenging, because of the reclassifying A. palmata and A. published, which will include biology of reef-building corals. As cervicornis from threatened to opportunities for public participation described below under Corals and Coral endangered will impede ongoing and input. As such, the comments Reefs—Individual Delineation, these restoration and recovery efforts. We described above are noted but are not species are both colonial (i.e., capable of received one comment encouraging responded to further in this final rule. creating colonies from multiple NMFS to make sure we have adequate genetically-identical polyps) and clonal staff to carry out the additional Comments on ESA Section 9 Take (i.e., capable of asexual reproduction to workload associated with ESA Section 7 Prohibitions create genetic duplicates). The ESA take consultations for any coral species that Comment 53: We received 12 prohibitions only apply to endangered are listed in this final rule. comments specific to ESA 4(d) rule- species immediately upon listing. No Response: The ESA explicitly restricts making, which is discussed in the species in this final rule are being listed the factors that can be considered in Section 9 Take Prohibitions section of as endangered; therefore, we do not listing decisions. Listing decisions can the proposed rule. Eight of these define activities that may result in take be based solely on the best scientific comments requested or suggested in this final rule, because take is not

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automatically prohibited for threatened explanations to note the comments were Turbinaria reniformis’ tolerance to species. Should we deem it necessary received and explain why they are not threats associated with climate change. and advisable that extending any of the considered relevant to the content of the Response: A Not Warranted finding is ESA section 9 prohibitions, including proposed rule. a final decision for which public take prohibitions, is necessary for the Comment 56: We received several comments are not solicited. Therefore, conservation of any of the newly-list comments regarding concerns over comments on the not warranted findings threatened coral, we will do so in a potential economic impacts as a result are noted but not considered relevant to subsequent rule-making. of listing coral species from various the content of the proposed rule and are concerned parties. In addition, we not responded to directly in this final Comments on Policies on Role of Peer received many comments criticizing the rule. We do note, however, that species Review proposed rule as an inappropriate use of determinations are based on more than Comment 55: We received two the ESA to protect corals in the face of just geographic range or existing threats comments that criticized NMFS for not global climate change. Some comments alone and not warranted determinations conducting peer review on the proposed emphasized that the ESA is not were reached by considering all rule. One commenter stated the designed to regulate GHGs and thus available information on species following: ‘‘The Department of ESA listings are not a prudent use of abundance, range, depth distribution, Commerce issued guidelines to comply time and resources. Comments also and threat vulnerabilities including with the OMB mandate, publishing the cited impacts to cultural practices susceptibility and exposure, as is final Guidelines for Ensuring and related to marine resource use in described in more detail in the not Maximizing the Quality, Objectivity, opposition of ESA coral listings. warranted findings. Utility, and Integrity of Disseminated Response: Due to the statutory As also described in the proposed Information in October 2002. As part of requirements of the ESA, comments rule, a threatened coral is likely to the NOAA guidelines, the agency must relevant to the proposed listing include become an endangered coral within the apply a higher standard to ‘influential those comments that provide additional foreseeable future throughout all or a scientific information’ (‘ISI’), which is substantive information regarding any significant portion of its range. For defined as scientific information the facet of the proposed rule (e.g., the threatened species, there is a temporal agency reasonably can determine will biology, status, and/or threats to the delay in extinction risk afforded by have or does have a clear and species, evaluation methodologies, some characteristics of the species, such substantial impact on important public accuracy and comprehensiveness of best as broader distribution, larger policies or private sector decisions.’ Id. available information, etc.). Comments populations, lower vulnerability to the ISI is subject to the more stringent not relevant to this rule making are most important threats, and better information standards in the OMB’s those comments that are not related to management. Threatened species are Final Information Quality Bulletin for the content of the proposed rule and/or less vulnerable than endangered Peer Review (‘‘OMB Peer Review comments that we are legally unable to species, but still have characteristics Bulletin’’), which requires peer review consider in a listing determination (e.g., that are likely to put them at elevated by qualified specialists in the relevant economic impacts). While we are extinction risk within the foreseeable field (70 F.R. 2664; January 14, 2005).’’ required to review and consider all future. For each of the 65 species under Response: The proposed rule itself comments, comments on issues outside consideration, we explain how a was not peer reviewed. However, the the scope of the proposed rule, such as species’ characteristics and its ability to supporting documents that formed the the comments described above, were provide buffering capacity to the basis for the determinations in the noted, but are generally not responded identified threats influences its proposed rule (e.g., the SRR, FMR) were to in this final rule. extinction risk over the foreseeable independently peer reviewed by subject Comment 57: Several commenters future. Some of the 65 species in this matter experts. In addition, much of the provided general support for the final rule meet the definition of information we received as a result of proposed listings but did not provide threatened, as explained in the species the public engagement and public substantive information or specific sections below. comment periods and incorporated into comments on the content of the Basis of Listing Determinations this final rule was independently peer proposed rule. reviewed. During the public comment Response: General support for the The following sections summarize all period and subsequent 6-month proposed action does not constitute of the best available information on reef- extension solicitation, we received submission of substantive information building corals in general, which critical review of the information on regarding any facet of the proposed rule. provides the baseline context and which the proposed rule was based from Therefore, these comments were noted foundation for our species-specific several coral reef experts. As a result, but are not responded to in this final listing determinations. While this the information used to form the basis rule. general information illustrates that the of our final listing determinations Comment 58: We received three most important threats are currently represents the best available scientific comments pertaining directly to one or increasing in severity, and likely to and commercial information to date on more of the 16 Not Warranted findings continue increasing further in the the 65 reef-building coral species within that were issued simultaneously with foreseeable future, it also illustrates that this final rule, and that we have the proposed rule. One commenter the impacts from these threats, both complied with all applicable policies questioned why some Caribbean species currently and over the foreseeable and guidance on peer review. were determined to be Not Warranted future, are difficult to interpret and do while others are proposed because not necessarily correlate to increased Comments Outside of the Scope of the threats to all species appear to be the vulnerability to extinction due to the Proposed Rule same. Another commenter stated that biological and physical variability and We received numerous public Porites pukoensis should have been complexity of corals and their habitat. comments in response to the proposed proposed for listing based solely on the Accordingly, our Final Determination rule that are outside the scope of this fact that it is endemic to Hawaii. A third Framework and species determinations rulemaking. Below are brief commenter provided information on are based upon an analysis of the best

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available species-specific information typical NMFS’ ESA listing if numerous polyps die, or if the colony evaluated within a worsening future determinations (i.e., vertebrates). is broken apart or otherwise damaged. environment. As summarized in the proposed rule, The biology of such clonal, colonial In addition to the comments we corals are marine invertebrates in the species creates ambiguity with regard to received on the proposed rule that phylum Cnidaria that occur as polyps, delineation of the individual in reef- include new or supplemental usually forming colonies of many clonal building corals, specifically: (1) Polyps information, we have continued to polyps on a calcium carbonate skeleton. versus colonies; (2) sexually-produced collect information that has either The Cnidaria include true stony corals versus asexually-produced colonies; and emerged since the publication of the (class Anthozoa, order Scleractinia), the (3) difficulty determining colony proposed rule or that was published at blue coral (class Anthozoa, order boundaries. Each source of ambiguity is the time of the proposed rule, but had Helioporacea), and fire corals (class addressed below, leading to a been inadvertently overlooked. This Hydrozoa, order Milleporina). All 68 conclusion regarding the delineation of latter category also includes literature proposed species are reef-building the ‘‘individual’’ for the species covered cited in the SRR or SIR, but that was corals, because they secrete massive by this final rule, which was not further examined to provide relevant calcium carbonate skeletons that form specifically defined in the proposed information. Therefore, we consider the physical structure of coral reefs. rule. Though not specifically defined, ‘‘supplemental information’’ to be that Reef-building coral species collectively we applied this same concept of the which was not considered at the time of produce coral reefs over time in high- individual in the proposed rule. the proposed rule that expands upon the growth conditions, but these species The polyp could be considered as the themes in the proposed rule, but does also occur in non-reef habitats (i.e., they smallest unit of the individual for reef- not fundamentally change a finding are reef-building, but not reef- building corals. Each polyp in a coral from the proposed rule. ‘‘New dependent). There are approximately colony consists of a column of tissue information’’ is considered to be that 800 species of reef-building corals in the with a mouth and tentacles on the upper which is novel and results in a change world. side, growing in a cup-like skeletal Most corals form complex colonies to a finding in the proposed rule. To structure (the corallite) made of calcium made up of a tissue layer of polyps (a distinguish between the information on carbonate that the polyp produces column with mouth and tentacles on the which the proposed rule was based from through calcification. The polyps are the upper side) growing on top of a calcium new or supplemental information, we building blocks of the colony, and most carbonate skeleton, which the polyps colony growth occurs by increasing the will only cite the primary literature for produce through the process of number of polyps and supporting new or supplemental information. For calcification. Millepora fire corals are skeleton. Polyps carry out the biological clarity, we will distinguish whether the also reef-building species, but unlike the functions of feeding, calcification, and information was identified via public stony corals, they have near- reproduction. However, because the comment or if we gathered it ourselves. microscopic polyps containing tentacles polyps within a colony are modular All the general information on reef- with stinging cells. units, and connected to one another building corals, which provides the Individual Delineation physiologically (i.e., via nerve net and appropriate context for our species- gastrovascular cavity, and are the same specific determinations, is provided in Comment 5 identified the lack of sex), single polyps within a colony are the Corals and Coral Reefs and Threats clarity on and complexity of the not considered to be individuals for Evaluation sections. The Risk Analyses delineation of the ‘‘individual’’ with purposes of this final rule. section follows and describes our respect to corals and its influence in Alternatively, only colonies methods and final determination estimating population abundance. We originating from sexually-produced framework for making our agree that this is a complex issue and larvae could be considered as the determinations. Last, we provide the did not provide sufficient details on individual for reef-building corals. individual listing determinations in the how we identified what an individual is Colonies are founded by either sexually- Species-specific Information and and how the consideration of this issue produced larvae that settle and become Determinations section, which are based factored into our estimates of the primary polyp of a colony, or on all of the best available information abundances for each of the proposed asexually-produced fragments of pre- for each coral species. species in the proposed rule. Thus, in existing colonies that break off to form Corals and Coral Reefs this final rule, we provide details on a new colony. Fragments from the same how we considered individual colony can fuse back together into the This section provides a summary of delineation in the proposed rule and same colony if they are close enough to the best available information on the this final rule. grow together. Fragmentation in biology and habitat of reef-building Reef-building corals are clonal branching species may lead to a large corals as it pertains to this final rule. organisms. A single larva will develop number of asexually-produced, First, we briefly summarize the into a discrete unit (the primary polyp) genetically identical colonies, information from the proposed rule, that then produces modular units (i.e., commonly resulting in a population which is based on the SRR and SIR. We genetically-identical copies of the made up of more asexually-produced also address all relevant comments primary polyp) of itself, which are colonies than sexually-produced received pertaining to the biology and connected seamlessly through tissue colonies (Hughes, 1984). Sexually- habitats of reef-building corals. Further, and skeleton. These modular units may produced colonies are important to the we provide supplemental information be solitary (e.g., fungiid corals) or population by increasing the genetic relevant to biology and habitat of corals colonial. Most reef-building coral diversity of the population, and colonies that we gathered during the period species are colonial, including all originating from asexually-produced between the proposed and this final species covered in this final rule. fragments do not contribute to the rule. This information provides part of Colony growth is achieved mainly effective population (i.e., group of the context in which we evaluate the through the addition of more polyps, genetically unique individuals). Asexual species’ status and illustrates the unique and colony growth is indeterminate. reproduction, though it does not create nature of this evaluation compared to The colony can continue to exist even new genetic individuals, is likely the

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more critical mode for some species, identified in the field. We acknowledge the Caribbean; Acropora Biological especially branching species, allowing that there are limitations with this Review Team, 2005). The best available them to grow, occupy space, and persist definition of the individual, including information indicates that, while several between relatively rare events of sexual usually-unknown proportions of of the candidate species have hybrid reproduction. Sexually- and asexually- genetically-distinct individuals in a histories, there is no evidence to suggest produced colonies often cannot be population and the difficulty with the any of them are ‘‘hybrid species’’ (that distinguished from one another in the determination of physiological colony is, all individuals of a species being F1 field, but are identifiable as an boundaries. But defining the individual hybrids); thus, they were all considered individual, in most cases. Thus, we use this way is the most supportable for this to meet the definition of a ‘‘species.’’ the concept of the ‘‘physiological final rule based on the best available Studies elucidating complex colony’’ as the entity that can be science. While we did not specifically taxonomic histories were available for considered an individual. The name the individual as the several of the genera addressed in the physiological colony for reef-building physiological colony in the proposed status review, and we were able to colonial species is defined here as any rule, it is how we considered the incorporate those into our species colony of the species, whether sexually individual in the proposed rule because determinations. Thus, while we made or asexually produced. the majority of the information on species determinations for most of the A physiological colony is generally abundance is based on the physiological 82 candidate coral species on the autonomous from other colonies of the colony which can be readily identified nominal species included in the same species. However, colony and counted in field surveys. Thus, in petition, we made alternate morphology, partial colony mortality, our species determinations we use the determinations on the proper taxonomic and other colony growth characteristics physiological colony to inform how we classification for the candidate species (e.g., formation of stands or thickets) can estimate abundance of a coral species Montipora dilatata and M. flabellata; complicate the delineation of because that is how field surveys Montipora patula and Porites pukoensis physiological colonies from one another estimate coral abundance. Using the based on genetic studies. We decided to in the field. For example, the overall physiological colony to estimate subsume a nominal species (morpho- colony morphology of many encrusting abundance in the final rule does not species) into a larger clade whenever species (e.g., some Montipora species) is change how we estimated abundance in genetic studies failed to distinguish largely dictated by the underlying the proposed rule, in which we also between them (e.g., Montipora dilatata, substrate. In those cases, colony shape relied on information that uses the M. flabellata, and M. turgescens (not may not distinguish colonies from one physiological colony to report petitioned) and Porites Clade 1 forma another, and boundaries between abundance estimates. If we have pukoensis). Comment 3 objected to the separate encrusting colonies that have information on the effective population lumping of the Montipora species based grown together may be difficult or size (i.e., proportion of clonality) for a solely on one study. However, because impossible to make out visually. Partial species, that information is also the commenter did not provide any mortality of colonies, especially larger considered. contrary information and we did not colonies, can also mask the boundaries find any new or supplemental between colonies, because the algae- Taxonomic Uncertainty in Reef-Building information suggesting that subsuming encrusted coral skeleton of a partially Corals the Montipora species into a larger clade dead colony may appear to delineate To determine if the proposed corals is incorrect, we are maintaining our two or more colonies. In addition, many meet the ESA definition of a species, we determination that M. dilitata/M. reef-building coral species occur in had to address issues related to the flabellata/M. turgescens and M. patula/ stands or thickets that may be tens of taxonomic uncertainty in corals (e.g., M. verrilli are considered species under meters or more in diameter (e.g., some reliance on morphological features the ESA. Acropora species), possibly consisting rather than genetic and genomic science In the proposed rule, Pocillopora of multiple colonies or only one large to delineate species) and corals’ elegans was split into two separate colony, also masking the boundaries evolutionary history of reticulate species because the two geographically- between colonies. In each of these processes (i.e., individual lineages distant populations have different instances, the actual number of showing repeated cycles of divergence modes of reproduction. Additionally, genetically-distinct individuals can only and convergence via hybridization). To the proposed rule examined the listing be determined through genetic analysis. address taxonomic uncertainty related status of P. danae. After consideration Those techniques have not been to species delineation, except as of the information on taxonomic established for all coral species and are described below where genetic uncertainty, including from the not feasible to conduct for every reef information was available, the proposed proposed rule and supporting assessment. Therefore, most reef rule considered the nominal species documents, Comment 2, and new assessments for coral abundance also designation as listed in the petition, information, we have determined that use the concept of the physiological acknowledging that future research may these three Pocillopora species (P. colony as the unit for enumerating result in taxonomic reclassification of elegans (Eastern Pacific), P. elegans species. some of the candidate species. (Indo-Pacific), and P. danae), are not Despite the challenges in individual Additionally, to address complex listable entities under the ESA. As delineation of clonal, colonial reef- reticulate processes in corals, the BRT explained in the response to Comment building corals, this final rule considers attempted to distinguish between a 2, new information on the three the ‘‘individual’’ for each of the ‘‘good species’’ that has a hybrid proposed Pocillopora species proposed proposed species to be the physiological history—meaning it may display genetic for listing indicates an increasing level colony, as defined above. That is, signatures of interbreeding and back- of taxonomic uncertainty to the point polyps are not considered individuals, crossing in its evolutionary history— that these three species are not listable but sexually- and asexually-produced and a ‘‘hybrid species’’ that is composed entities under the ESA at this time. colonies are considered individuals entirely of hybrid individuals (as in the Thus, this final rule considers 65 of the because they are a type of physiological case of Acropora prolifera, discussed in 68 species included in the proposed colony and are the unit that can be the status review of acroporid corals in rule. However, even though these

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remaining 65 species are determinable morphological plasticity, different other factors prior to settlement and under the ESA, some uncertainty methods) is provided by massive Porites metamorphosis. Such mortality cannot regarding taxonomy and certain species species: Many species occur together in be directly observed, but is inferred identification remains. These the same habitats and locations, from the large amount of eggs and sperm uncertainties are addressed for each morphological plasticity is high for both spawned versus the much smaller species in the Species-specific colony shape and corallite structure, number of recruits observed later. Coral Information and Determinations and experts disagree about how to larvae are relatively poor swimmers; sections. distinguish the species (Forsman et al., therefore, their dispersal distances In addition to these specific examples 2009; Veron, 2000). largely depend on the duration of the of species delineation, Comment 1 Coral species identification is based pelagic phase and the speed and stated that taxonomic uncertainties on the assumption that the taxonomy is direction of water currents transporting associated with many reef-building correct. The high biodiversity, high the larvae. The documented maximum coral species are problematic for the morphological plasticity, and different larval life span is 244 days (Montastraea ESA listing determination process. We methodologies create species magnistellata), suggesting that the acknowledge the clear delineation identification problems even when the potential for long-term dispersal of coral among individuals that characterizes taxonomy is correct. But if the larvae, at least for some species, may be vertebrate species is often absent in reef- taxonomy is not correct, the species substantially greater than previously building coral species. This final rule identification problems described here understood and may partially explain addresses that ambiguity with the are irrelevant because species with a the large geographic ranges of many general introductions in this sub- high level of taxonomic uncertainty species. section, then by providing species- (e.g., the Pocillopora species in this final The spatial and temporal patterns of specific information for each species. rule) are not listable entities under the coral recruitment have been studied Therefore, the level of taxonomic ESA. Both the species delineation and extensively. Biological and physical uncertainty is addressed for each of the species identification problems are factors that have been shown to affect species in this final rule in the Species- highly species-specific, and are spatial and temporal patterns of coral specific Information and Determinations addressed for each species in the recruitment include substrate sub-sections below. Species-specific Information and availability and community structure, Determinations section. grazing pressure, fecundity, mode and Species Identification timing of reproduction, behavior of Reproductive Life History of Reef- We received several comments related larvae, hurricane disturbance, physical Building Corals to the difficulty in coral species oceanography, the structure of identification (see Comment 1). In the As summarized in the proposed rule, established coral assemblages, and proposed rule we acknowledged the corals use a number of diverse chemical cues. Additionally, factors difficulty in identification and how that reproductive strategies that have been other than dispersal may influence affected the ability to accurately infer researched extensively; however, many recruitment, and several other factors abundances for individual species (see individual species’ reproductive modes may influence reproductive success and proposed rule Distribution and remain poorly described. Most coral reproductive isolation, including Abundance section). However, we did species use both sexual and asexual external cues, genetic precision, and not discuss the species identification propagation. Sexual reproduction in conspecific signaling. uncertainty on a species by species corals is primarily through In general, on proper stimulation, basis. In this sub-section, we more fully gametogenesis (i.e., development of eggs coral larvae settle and metamorphose on describe the challenge of species and sperm within the polyps near the appropriate substrates. Some evidence identification. In the Species-specific base). Some coral species have separate indicates that chemical cues from Information and Determinations section, sexes (gonochoric), while others are crustose coralline algae, microbial films, we address the identification hermaphroditic. Strategies for and/or other reef organisms or acoustic uncertainty for each species, and fertilization are either by ‘‘brooding’’ or cues from reef environments stimulate determine if that uncertainly affects the ‘‘broadcast spawning’’ (i.e., internal or settlement behaviors. Calcification reliability of the distribution and external fertilization, respectively). begins with the forming of the basal abundance information described for Asexual reproduction in coral species plate. Buds formed on the initial each species, based on expert analysis most commonly involves fragmentation, corallite develop into daughter (Fenner, 2014b). where colony pieces or fragments are corallites. Once larvae are able to settle In this final rule ‘‘species dislodged from larger colonies to onto appropriate hard substrate, identification’’ refers to the assignment establish new colonies, although the metabolic energy is diverted to colony of a given individual to a species based budding of new polyps within a colony growth and maintenance. Because on its appearance in the field or lab. In can also be considered asexual newly settled corals barely protrude contrast, ‘‘species delineation’’ refers to reproduction. In many species of above the substrate, juveniles need to the definition of reef-building corals as branching corals, fragmentation is a reach a certain size to limit damage or distinct species based on their scientific common and sometimes dominant mortality from threats such as grazing, classification or taxonomy (covered in means of propagation. sediment burial, and algal overgrowth. the previous sub-section). Many reef- Depending on the mode of In some species, it appears that there is building coral species are difficult to fertilization, coral larvae (called virtually no limit to colony size beyond identify for many reasons, including: (1) planulae) undergo development either structural integrity of the colony The high biodiversity of reef-building mostly within the mother colony skeleton, as polyps apparently can bud corals; (2) the high morphological (brooders) or outside of the mother indefinitely. plasticity in many reef-building coral colony, adrift in the ocean (broadcast Comment 4 identified the lack of species; and (3) the different methods spawners). In either mode of larval information on coral population used for species identification. An development, larvae presumably dynamics and connectivity; however, it example of all three factors working experience considerable mortality (up to did not provide any supplemental together (high biodiversity, 90 percent or more) from predation or information, other than for Acropora

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cervicornis, which will be considered in colonies can exhibit partial mortality in individual extinction risk assessments that species’ determination. Therefore, which a subset of the polyps in a colony for those species in the Species-specific the section above is a summary of the dies, but the colony persists. Colonial Information and Determinations section. information on coral reproductive life species present a special challenge in Unlike quantitative abundance data, history from the proposed rule as it determining the appropriate unit to qualitative abundance characterizations contributes to the extinction risk evaluate for status. In addition, new (e.g., rare, common), were available for analyses for the proposed corals. In our coral colonies, particularly in branching all species (Veron, 2000), and were species determinations, we consider life species, can be added to a population by considered in the proposed rule’s history characteristics that may fragmentation (breakage from an individual species extinction risk contribute to extinction risk. For existing colony of a branch that evaluations. These estimates are the example, species with high recruitment reattaches to the substrate and grows) as subjective opinion of the author and are rates or fast growth rates may have the well as by sexual reproduction (see meant to indicate relative abundance ability to more quickly recover from above, and Fig. 2.2.1 in SRR). between the categories. That is, a rare disturbances. Additionally, long-lived Fragmentation results in multiple, species has fewer individuals as species with large colony size can genetically identical colonies (ramets) compared to an uncommon one, and an sustain partial mortality (fission) and while sexual reproduction results in the uncommon species has fewer still have potential for persistence and creation of new genetically distinct individuals than a common one. These regrowth. However, detailed life history individuals (genotypes or genets). estimates are also meant to describe the information is not available for all of the In the proposed rule, quantitative author’s opinion of the qualitative species considered in this final rule, abundance estimates were available for abundance of the species throughout its though it is used when available. only a few of the candidate species. In range, and not necessarily an estimate of the Indo-Pacific, many reports and long- the abundance at an individual location. Distribution and Abundance of Reef- term monitoring programs describe Since the proposed rule was published, Building Corals coral percent cover only to genus level semi-quantitative (i.e., survey data from The proposed corals are distributed because of the substantial diversity 2,984 individual sites) and updated throughout the wider-Caribbean (i.e., within many genera and difficulties in non-quantitative (i.e., the author’s the tropical and sub-tropical waters of field identification among congeneric subjective estimates covering a full the Caribbean Sea, western Atlantic species. In the Caribbean, most of the range of habitats and most ecoregions Ocean, and Gulf of Mexico; herein candidate species are either too few in the author has worked in) abundance referred to collectively as ‘‘Caribbean’’), numbers to document meaningful estimates were provided for 63 of the 65 the Indo-Pacific biogeographic region trends in abundance from literature corals covered in this final rule (Veron, (i.e., the tropical and sub-tropical waters reports (e.g., Dendrogyra cylindrus), or 2014). In addition to the semi- of the Indian Ocean, the western and commonly identified only to genus quantitative and non-quantitative central Pacific Ocean, and the seas (Mycetophyllia and Agaricia spp.), or estimates, Veron (2014) provided connecting the two in the general area potentially misidentified as another occupancy of each species within the of Indonesia), and the tropical and sub- species. At the time of the proposed approximately 150 ecoregions he has tropical waters of the eastern Pacific rule, the only comprehensive defined. An ecoregion is defined as an Ocean. In our species determinations, abundance data in the Caribbean were area that is internally cohesive (i.e., spatial and demographic traits inform for the three Orbicella species, partially areas with similar habitats share similar our evaluation of a species’ current because they historically made up a species complements), but externally status and its capacity to respond to predominant part of live coral cover. distinct from neighboring regions changing conditions over the Even for these species, the time series (http://coral.aims.gov.au/). Ecoregions foreseeable future. One important data are often of very short duration are widely used in biogeography demographic trait is absolute (they were not separated as sibling because they incorporate a substantial abundance, which is a function of local species until the early 1990s and many amount of background knowledge, are a density (either quantitative or surveys continue to report them as good platform for statistical analysis, qualitative) and range size. Absolute ‘‘Orbicella annularis complex’’) and and allow the pooling and comparison abundance is more informative than a cover a very limited portion of the of different datasets from the same relative description of abundance for species range (e.g., the time series only ecoregion. Ecoregions are not equal in corals such as ‘‘rare,’’ because even a monitors a sub-section of a single size and thus occupancy in the same coral species described as ‘‘rare’’ may national park). In general, the available number of ecoregions by two different still have millions of individual quantitative abundance data were so species does not indicate the same range colonies or more (i.e., few individuals limited or compromised due to factors size. Rather, the number of ecoregions per unit area spread across a very large such as small survey sample sizes, lack occupied is a good indication of the area). Similarly, the spatial trait of of species-specific data, etc., that they diversity of habitats and geographic geographic distributions are not were considerably less informative for distribution in which a species may be considered on a relative scale (i.e., evaluating the risk to species than other found. These data are included in the narrow, moderate, wide as we did in the data, and were therefore generally not individual extinction risk assessments proposed rule), but rather considered on included as part of the individual for those species in the Species-specific an absolute scale, which for even the species extinction risk evaluations. Information and Determinations section. smallest species distribution Comment 47 provided quantitative As previously described in the encompasses millions of square miles. abundance estimates from Florida for all Individual Delineation section, clonal, As described in the Individual of the proposed corals in the Caribbean. colonial organisms, such as corals, are Delineation sub-section, determining In addition, we gathered supplemental vastly different in their biology and abundance of the proposed corals information providing quantitative ecology than vertebrates, which are presents a unique challenge because abundance estimates and distribution typically the focus of ESA status corals are clonal, colonial invertebrates, for individual species in the Caribbean reviews. Therefore, concepts and terms and colony growth occurs by the and Indo-Pacific. These data are that are typically applied to vertebrates addition of new polyps. In addition, included and described in the have very distinct meanings when

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applied to corals. A ‘rare’ coral may still upper fore-reefs or upper slopes and wide indistinct crests. In addition, have millions of colonies as compared (approximately 5–10 to 10–20 m depth), barrier reefs typically have immense to a ‘rare’ vertebrate, which may only mid-slopes that often occur as terraces back-reefs consisting of reef flats have hundreds of individuals. or shelves (approximately 10–20 to 20– abutting the reef crest, and large lagoons 30 m depth), and deep fore-reefs, lower that may vary from clear and sandy near Coral Habitats slopes, or walls (approximately 30–40 m the reef to turbid and muddy near land, As summarized in the Coral Reefs, depth) that transition to mesophotic and include various features such as Other Coral Habitats, and Overview of areas (greater than 30–40 m depth). The patch reefs and islands (Maxwell, 1968). Candidate Coral Environments section reef crest (approximately 0 to 5–10 m Atolls occur in oceanic waters far from of the proposed rule, a ‘‘coral reef’’ is a depth) forms the boundary between the land, and may be hundreds of complex three-dimensional structure reef slope and back-reef, and generally kilometers across. Their reef slopes occurring from the surface to includes a consolidated ridge or rim often form vertical walls dropping into approximately 30 to 40 meters of depth where the waves break, and a lower reef abyssal waters, and their back-reefs resulting from the skeletal growth of crest on the seaward side of the algal consist of large, clear lagoons (Veron, reef-building corals that provides ridge often made of up of buttresses and 2000; Wells, 1951). Environmental habitat, food, and shelter for numerous surge channels (i.e., spur-and-groove conditions vary greatly between the marine species. As such, coral reefs structures). The back-reef lies between habitat types found on the reefs slopes, foster exceptionally high biodiversity the reef crest and land (or middle of the reef crests, and back-reefs of the world’s and provide the following essential lagoon, in the case of atolls). The back- coral reefs. In addition, much variability functional roles: Primary production reef generally includes reef flats also occurs within each habitat type. For and recycling of nutrients in relatively (approximately 0 to 1–5 m depth) and example, Maxwell (1968) describes six nutrient poor (oligotrophic) seas, lagoons (approximately 1–5 to over 30 geomorphological types of reef crests, calcium carbonate deposition yielding m depth), interlaced with tide pools, and how the different environmental reef construction, sand production, channels, patch reefs, and other conditions provide ‘‘coral zones’’ modification of near-field or local water features. The characteristics of these unique to each type of reef crest. The circulation patterns, and habitat for habitat types vary greatly by reef physical diversity of coral reef habitat is secondary production, including categories, locations, latitudes, illustrated by Kuchler (1986), who notes fisheries. These functional roles yield frequency of disturbance, etc., and there that the scientific literature on the GBR important ecosystem services in is also much habitat variability within alone used over 20 terms for the reef addition to direct economic benefits to each habitat type, together constituting slope or its habitats, over 50 terms for human societies such as traditional and the habitat heterogeneity of coral reefs, the reef crest or its habitats, and over cultural uses, food security, tourism, as described further below. 100 terms for the reef flat and lagoon and potential biomedical compounds. and their habitats. Coral reefs protect shorelines, coastal Fringing reefs occur adjacent to In conclusion, five main points are ecosystems, and coastal inhabitants coastlines, and subsequently the important regarding coral habitat on from high seas, severe storm surge, and habitats associated with their reef slopes coral reefs (as opposed to non-reefal and tsunamis. and back-reefs may be quite different mesophotic habitats) for this final rule: The three broad categories of coral than on barrier reefs or atolls. The reef (1) Regardless of reef category, reefs reefs are fringing reefs, barrier reefs, and slopes of many fringing reefs that are generally consist of reef slopes, reef atolls. Fringing reefs are mostly close to protected from strong wave action (e.g., crests, and back-reefs, each of which coastlines, and usually have a high on leeward sides of islands) consist of have distinct habitats, but those habitats component of non-carbonate sediment. unconsolidated material sloping gently can be highly variable between reef Barrier reefs are offshore and are towards deeper water, while those of types and locations; (2) spatial composed of wave-resistant fringing reefs in more exposed areas variability in coral habitat conditions is consolidated limestone. Atolls are (e.g. windward sides of islands) are very high between habitat types, as well usually a wall of reefs partially or usually more consolidated. On many as within the habitat types described completely enclosing a central lagoon. fringing reefs, even on the reef slope, above (i.e., deep fore-reefs, walls, mid- There are not sharp differences that natural turbidity and sedimentation may slopes, upper reef slopes, lower reef clearly mark boundaries between reef be high due to proximity to land. crests, algal ridges, reef flats, and types. For example, fringing reefs Fringing reefs typically have narrow lagoons), producing highly variable gradually become barrier reefs with back-reefs consisting of a reef flat environmental conditions across both increasing distance from shore. Also, abutting the reef crest, and possibly tide large and small spatial scales at any the shape of both barrier reefs and atolls pools, channels, or small lagoons given point in time; (3) temporal is largely determined by the bathymetry between the reef flat and shore (Goreau, variability in coral habitat conditions is of the substratum, producing many 1959; Veron, 2000). Barrier reefs also very high, both cyclically (e.g., from irregularly shaped reefs that are typically form tens to hundreds of tidal, seasonal, annual, and decadal intermediary between the two types. kilometers from coastlines, their reef cycles) and episodically (e.g., storms, Isolated reefs that do not fit any of these slopes are composed of consolidated temperature anomalies, etc.); (4) descriptions are referred to as platform limestone that may plunge steeply to together this spatial and temporal reefs (Veron, 2000). deeper water, and natural turbidity and variability in environmental conditions Despite the differences between the sedimentation are very low due to across multiple scales produces the very reef categories, most fringing reefs, distance from land. Thus the high habitat heterogeneity of coral reefs; barrier reefs, atolls, and platform reefs characteristics of their reef slope and (5) while most coral species in this consist of a reef slope, a reef crest, and habitats can be quite different than on final rule are more common in certain a back-reef, which in turn are typically fringing reefs. Barrier reefs are exposed reef habitat types, they are typically characterized by distinctive habitats. to very strong wave action, and their found in many different habitat types. The reef slope is the seaward side of the reef crests can vary from high, Reef-building corals have specific coral reef between the reef crest and the consolidated algal ridges to habitat requirements, including hard deep ocean, and generally includes unconsolidated shingle ramparts to low substrate, narrow mean temperature

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range, adequate light, and adequate (Blakeway et al., 2013; Browne et al., corals (Bridge et al., 2012a; Bridge and water flow. These habitat requirements 2012), very warm (Riegl and Purkis, Guinotte, 2013; Bridge et al., 2012b). As most commonly occur on the shallow 2012; Riegl et al., 2011), or cold because noted in one of these recent papers, tropical and subtropical coral reefs of high latitude (Dalton and Roff, 2013; several coral species (including described above, but also occur in non- Lybolt et al., 2011) or upwelling Acropora aculeus, A. jacquelineae, and reefal and mesophotic areas. All of the (Alvarado et al., 2011; Manzello et al., A. tenella) are common and proposed species require hard 2008), and other environments (Couce et geographically widespread in deeper substrates. Thus, in this final rule, ‘‘non- al., 2012; Done, 1982; Perry and waters (30–60 m; Bridge et al., 2013b). reefal habitats’’ refers to hard substrates Larcombe, 2003). Some coral species Other recent studies in Curac¸ao where reef-building corals can grow, can also live on soft substrates, such as (Bongaerts et al., 2013), Bermuda (Locke including marginal habitats where Manicina areolata in the Caribbean, et al., 2013), and Hawaii (Luck et al., conditions prevent reef development staghorns (Acropora) that must begin on 2013) reveal extensive mesophotic (e.g., turbid or high-latitude or hard substrate but can then grow over habitats and reef-building coral upwelling-influenced areas) and soft substrates, and Catalaphyllia communities. These studies expand the recently available habitat (e.g., lava jardini, which is common in some soft known potential habitats for reef- flows). The term ‘‘mesophotic habitats’’ substrates in Australia. Such habitat is building corals, but species diversity refers to hard substrates deeper than 30 not necessarily indicative of low- and abundances have not been well- m. Coral reefs, non-reefal areas, and diversity coral assemblages, as shown documented due to the relative mesophotic areas are not necessarily by turbid sites, which have been inaccessibility of these habitats to sharply delineated from one another, documented to support over 160 species divers. thus one may gradually blend into of reef-building corals (Perry and In summary, the magnitude of another. We anticipate the total area of Larcombe, 2003), and fresh lava flows, habitats potentially supporting reef- non-reefal and mesophotic habitats is which have been documented to building coral species is extremely greater than the total area of shallow support fully recovered coral large, and much larger than the 0.2 coral reef habitats within the ranges of communities only 20 years after the percent of the marine environment the corals in this final rule. flow (Grigg and Maragos, 1974). provided in the SRR. Globally, some Comments 6 and 7 suggested that we Marginal habitats expands the diversity reef-building corals can occur in did not consider non-reefal habitats and of environmental conditions that can shallow coral reef, non-reefal, and/or mesophotic habitats adequately in our support some reef-building corals and mesophotic habitats. These three types proposed rule. However, these therefore may provide refugia from of general habitats combined provide comments did not provide any new or some threats affecting shallow coral reef the overall physical environment of supplemental information on how to habitat, as described in the Spatial and many species, and supplemental interpret the importance of these Temporal Refugia sub-section below. information on non-reefal and habitats in our extinction risk analysis. mesophotic habitats indicates that their Comment 7 includes two studies that Since 2012, research on mesophotic magnitude is larger than previously provide supplemental information on habitats has demonstrated that many understood. the extent of mesophotic reefs. In reef-building corals have greater depth Inter-Basin Comparisons addition to the public comment distributions than previously reported. received on the diversity and Twenty-two of the proposed species As described in the proposed rule, the complexity of coral reef habitats, have been reported from mesophotic Caribbean and Indo-Pacific basins supplemental information has become depths (i.e., 30 m or more) and several contrast greatly both in size and in available on non-reefal and mesophotic more reported at 25 m. For other condition. The Caribbean basin is habitats since the publication of the species, their biogeographic ranges may geographically small and partially proposed rule. The following sub- be underestimated due to lack of enclosed, has high levels of sections on non-reefal and mesophotic mesophotic exploration. These studies connectivity, and has relatively high habitats are intended to illustrate the demonstrate that some species in human population densities. The wider- diversity of reef-building coral habitats, shallow coral reef habitats readily Caribbean occupies five million square but are not intended to provide an extend to mesophotic depths if water km of water and has approximately exhaustive list of them. clarity and temperatures remain 55,000 km of coastline, including Non-reefal habitats include marginal favorable (Kahng et al., 2014). For approximately 5,000 islands. Shallow habitats (Perry and Larcombe, 2003), as example, investigations in American coral reefs occupy approximately 25,000 well as newly available natural habitats Samoa (Bare et al., 2010), the Hawaiian square km (including ≈2,000 square km such as the hard substrates created by Archipelago (Kahng et al., 2010; Rooney within U.S. waters), or about 10 percent lava flows (Grigg and Maragos, 1974), et al., 2010), and the Mariana of the total shallow coral reefs of the tsunamis (scoured bedrock or Archipelago (Rooney et al., 2012), have world. The amount of non-reefal and transported boulders (Goto et al., 2010)), revealed extensive mesophotic coral reef mesophotic habitat that could or other episodic processes. Non-reefal ecosystems. While classically potentially be occupied by corals in the habitats are defined as areas where considered to be limited to 100 m, Caribbean is unknown, but is environmental conditions prevent reef mesophotic reefs have been observed as potentially greater than the area of formation but reef-building corals are deep as 130 m in some of these areas, shallow coral reefs in the Caribbean. present. Marginal habitats are much including at depths in excess of 150 m The Caribbean region has experienced more common than newly-available in the Au‘au Channel of Hawaii (Blyth- numerous disturbances to coral reef natural habitats. Marginal habitats are Skyrme et al., 2013). Likewise, systems throughout recorded human very diverse, as they occur where investigations on Australia’s GBR found history. Fishing has affected Caribbean seawater temperatures or light levels are extensive mesophotic habitats both reefs since before European contact, and sub-optimal (i.e., inadequate for high along the continental shelf-edge and on continues to be a threat. Beginning in skeletal growth but still allowing reef- submerged reefs inside the lagoon of the the early 1980s, a series of basin-scale building corals to survive), and thus GBR, both of which support previously disturbances has led to altered include environments that are turbid unknown communities of reef-building community states, and a loss of

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resilience (i.e., inability of corals and than the 10 percent reported earlier. The While the reef communities in the coral communities to recover after a earlier reports were based on less Caribbean may have poor resilience, the disturbance event). Massive, Caribbean- thorough sampling of the available data, reefs in the central Pacific (e.g., wide mortality events from disease and were also dominated by data from American Samoa, Moorea, Fiji, Palau, conditions of both the keystone grazing the Florida Keys, U.S. Virgin Islands, and the Northwestern Hawaiian Islands) urchin Diadema antillarum and the and Jamaica, which may not be appear to remain much more resilient dominant branching coral species representative of the entire Caribbean despite major bleaching events from Acropora palmata and Acropora (Jackson et al. 2014). ocean warming, hurricanes, and crown- cervicornis precipitated widespread and In conclusion, the supplemental of-thorns seastar predation outbreaks. dramatic changes in reef community information regarding live coral cover That is, even though the reefs have structure. None of the three important does not dispute that there has been a experienced significant impacts, corals keystone species (Acropora palmata, long-term overall decline in live coral have been able to recover, as described Acropora cervicornis, and Diadema cover in the Caribbean and that those below. Several factors likely result in antillarum) have shown much recovery declines are likely ongoing and likely to greater resilience in the Indo-Pacific over decadal time scales. In addition, continue in the future as a result of a than in the Caribbean: (1) The Indo- continuing coral mortality from periodic multitude of global and local threats at Pacific is more than 10-fold larger than acute events such as hurricanes, disease all spatial scales. These wide-scale the Caribbean, including many remote outbreaks, and bleaching events from changes in coral populations and areas; (2) the Indo-Pacific has ocean warming have added to the poor communities have affected habitat approximately 10-fold greater diversity state of Caribbean coral populations and complexity and may have already of reef-building coral species than the yielded a remnant coral community reduced overall reef fish abundances. Caribbean; (3) broad-scale Caribbean with increased dominance by weedy These trends are expected to continue. reef degradation likely began earlier brooding species, decreased overall However, as the above information than in the Indo-Pacific; (4) iron coral cover, and increased macroalgal illustrates, live coral cover trends are enrichment in the Caribbean may cover. Additionally, iron enrichment in highly variable both spatially and predispose it to algal growth versus lack the Caribbean may predispose the basin temporally, producing patterns on small of broad-scale iron enrichment in the to algal growth. Further, coral growth scales that may not be indicative of Indo-Pacific; (5) there is greater coral rates in the Caribbean have been conditions throughout the basin. cover on mesophotic reefs in the Indo- declining over decades. Pacific than in the Caribbean; and (6) Ocean basin size and diversity of Caribbean-wide meta-analyses suggest there is greater resilience to algal phase habitats (e.g., reef-flats, forereef, that the current combination of shifts in the Indo-Pacific than in the mesophotic, non-reefal), as well as some disturbances, stressful environmental Caribbean. factors such as elevated ocean vast expanses of ocean area with only Even given the relatively higher temperatures, nutrients and sediment very local, spatially-limited, direct resilience in the Indo-Pacific as loads, and reduced observed coral human influences, have provided compared to the Caribbean, one meta- reproduction and recruitment have substantial buffering of Indo-Pacific analysis of overall coral status yielded a loss of resilience, even to corals from many of the threats and throughout the Indo-Pacific indicates natural disturbances such as hurricanes. declines manifest across the Caribbean. that substantial loss of coral cover (i.e., Coral cover (percentage of reef The Indo-Pacific (Indian and Pacific lower densities throughout the range, substrate occupied by live coral) across Oceans) is enormous and hosts much but not range contraction) has already the region has declined from greater coral diversity than the ∼ occurred in most subregions. As of approximately 50 percent in the 1970s Caribbean region ( 700 coral species 2002–2003, the Indo-Pacific had an to approximately 10 percent in the early compared with 65 coral species). The overall average of approximately 20 2000s (i.e., lower densities throughout Indo-Pacific region encompasses the percent live coral cover, down from the range, not range contraction), with tropical and sub-tropical waters of the approximately 50 percent since the concurrent changes between subregions Indian Ocean, the western and central 1970s. However, supplemental in overall benthic composition and Pacific Ocean, and the seas connecting information refines this estimate. Data variation in dominant species. However, the two in the general area of Indonesia. from 154 surveys of reefs across the supplemental information suggests that This vast region occupies at least 60 Pacific performed between 1980 and this estimate of coral cover decline in million square km of water (more than 1982 had mean live coral cover of 42.5 the Caribbean is an oversimplification. ten times larger than the Caribbean), and percent (Bruno and Selig, 2007). Coral In the Caribbean, quantitative surveys of includes 50,000 islands and over 40,000 cover in the Indian Ocean declined from a few dozen sites from before the early km of continental coastline, spanning approximately 40 percent prior to the 1980s suggest the regional mean for approximately 180 degrees of longitude 1998 bleaching event to approximately coral cover was 30–40 percent around and 60 degrees of latitude. There are 22 percent; subsequently, mean coral 1980 (Gardner et al., 2003; Schutte et approximately 240,000 square km of cover increased to approximately 30 al., 2010). Supplemental information shallow coral reefs in this vast region, percent by 2005 (Ateweberhan et al., based on more complete sampling effort which is more than 90 percent of the 2011) Live coral cover likely had (i.e., meta-analysis of 35,000 total coral reefs of the world. In already declined in all regions before quantitative reef surveys from 1969 to addition, the Indo-Pacific includes 1980, but region-wide quantitative data 2012) indicates higher levels of abundant non-reefal habitat, as well as is generally lacking. For example, local ‘‘current’’ percent live coral cover in the vast but scarcely known mesophotic surveys before 1980 from several parts Caribbean than described in the areas that provide coral habitat. The of the Indo-Pacific documented live proposed rule. For example, a recent amount of non-reefal and mesophotic coral cover of 50 to 70 percent (Gomez study found that average coral cover habitat that could potentially be et al., 1981). throughout the wider-Caribbean occupied by corals in the Indo-Pacific is Unlike the Caribbean, no recent declined by 66 percent from an overall unknown, but is likely greater than the region-wide reports of current, overall average of 41 percent between 1969– area of shallow coral reefs in the Indo- live coral cover are available for the 1983 to 14 percent today, slightly higher Pacific (NMFS, 2012b; SIR Section 4.3). Indo-Pacific as a whole. However,

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recent reports from parts of the region led to different results in studies detailed description of the eastern have found current live coral cover measuring changes in live coral cover Pacific is not necessary. higher than the 20 percent for the region over time. For example, one study Spatial and Temporal Refugia reported earlier, and stable or increasing (Bellwood et al., 2004) reported live coral cover. For example, approximately 50 percent declines in Comment 7 suggested that certain monitoring data collected annually from live coral cover on GBR over the last habitats (e.g., mesophotic) may provide 47 sites on the GBR from 1995 to 2009 several decades, but another study refugia for shallow water corals. averaged 29 percent live coral cover. disagreed (Sweatman et al., 2011), Therefore, we provide the following More importantly, this study found no making the case for considerably discussion of temporal and spatial evidence of consistent, system-wide smaller declines, using a different refugia. Some of these concepts were decline in coral cover since 1995. method. Both studies provided detailed discussed in the Threats Evaluation Instead, fluctuations in coral cover at support for their methods and findings section of the proposed rule as they sub-regional scales (10–100 km), driven (Hughes et al., 2011; Sweatman and relate to exposure of corals to the mostly by changes in fast-growing Syms, 2011). Studies supporting both various threats and how exposure Acroporidae, occurred as a result of results have since been published influences extinction risk. The above localized disturbance events and (De’ath et al., 2012; Osborne et al., information on coral habitats illustrates subsequent recovery (Osborne et al., 2011), and such disagreements illustrate the enormous heterogeneity of the 2011). However, another recent study the complexity of determining trends in environments that many of these species based on 2,258 surveys of 214 GBR reefs live coral cover. inhabit. Each species occurs in a patchwork of variable habitat conditions over 1985–2012, showed declines in In conclusion, the supplemental at any given point in time, with certain live coral cover from 28 percent to 14 information regarding live coral cover combinations of variables at certain percent, a loss of half of the initial coral does not dispute that there has been a locations producing favorable cover. In the Philippines, a study of 317 long-term overall decline in live coral conditions that may provide refugia sites from 1981 to 2010 averaged 36 cover in both the Caribbean and Indo- from threats such as ocean warming. percent live coral cover, and showed an Pacific, and that those declines are Habitat conditions are highly variable overall increase from 29 percent in 1981 likely ongoing and likely to continue in over time in different ways, including to 37 percent in 2010 (Magdaong et al., the future due to a multitude of global cyclically (e.g., from tidal, seasonal, 2013). A study of 366 sites from 1977 to and local threats at all spatial scales. 2005 in the Indian Ocean documented annual, and decadal cycles), Further, both basins have experienced episodically (e.g., storms, temperature large initial decline from approximately conditions leading to coral mortality 35 percent live coral cover to anomalies, etc.), and linearly (e.g., and prevention of full recovery; gradual thermal regime changes, which approximately 15 percent at most sites however, the Caribbean has been more following the 1998 bleaching event, will both degrade and improve habitat, greatly impacted. While basin-wide depending on location and initial followed by partial recovery to averages are useful for large-scale approximately 25 percent, and then conditions). The dynamic nature of reef- comparisons, they do not describe building coral habitats may provide stability of live coral cover conditions at finer, regional scales. For (Ateweberhan et al., 2011). Likewise, a refugia for some corals from some example, decreases in overall live coral study in Western Australia from 2005 to threats, both spatially and temporally cover have occurred since 2002 in some 2009, following the 2005 bleaching (Fine et al., 2013; McClanahan et al., areas, such as on the GBR, while event, documented declines to 10 2011; Riegl and Piller, 2003). increases have occurred in other areas, percent live coral cover as a result of the Some habitats have natural features such as in American Samoa. As the event and then subsequent recovery to that reduce stress from extremely high supplemental information further 30 percent (Ceccarelli et al., 2011). A temperatures or light levels (i.e., the illustrates, live coral cover trends are study in the Andaman Islands from most common causes of coral highly variable both spatially and 2010 to 2012 following the 2010 bleaching), which may provide spatial temporally, producing patterns on small bleaching also documented substantial refugia for some reef-building coral recovery of live coral cover (Marimuthu scales that can be easily taken out of species from ocean warming and other et al., 2012; Osborne et al., 2011). context. Live coral cover trends are threats. Deeper water may be cooler These recent studies illustrate the complex, dynamic, and highly variable depending on the amount of mixing, dynamic nature of live coral cover, across space and time. Thus their and is exposed to less light (i.e., especially recovery from the 1998 interpretation requires the appropriate irradiance). Mesophotic habitats are bleaching event. It is likely that the spatial-temporal context (i.e., entire very extensive, and recent investigations overall basin-wide live coral cover in range or each species now and through provide evidence that mesophotic both the Caribbean and the Indo-Pacific foreseeable future), and an habitat functions as refugia for some has declined over decadal and centurial understanding of the various physical, reef-building corals. A review of time scales, but with fluctuations on biological, and ecological processes at mesophotic habitat on Australia’s GBR shorter time scales and within smaller work within coral communities and concluded that reef-building corals in geographic scales. This is significant coral reef ecosystems. mesophotic habitat are less likely to be because coral decline doesn’t occur in In the proposed rule, we provided a affected by warming-induced bleaching every location at every time scale. summary of conditions in the eastern events than their counterparts on nearby Rather, there are periods of decline and Pacific to illustrate the contrast to the shallow reefs (Bridge et al., 2012a). recovery over shorter time periods in conditions in Indo-Pacific and Mesophotic habitat may also be various locations throughout the larger Caribbean. This description was important for recovery of corals basins. This has broad implications relevant because the range of one of our disturbed coral reefs by providing when analyzing the temporal and candidate species, Pocillopora elegans sources of propagules to recolonize spatial elements of a coral species’ (eastern Pacific), was restricted to the shallow reefs following disturbances extinction risk. eastern Pacific. Because we are no (Bridge and Guinotte, 2013). A 37-year Disagreements over the methods of longer considering the three proposed record from the eastern Pacific across how to measure live coral cover have Pocillopora species in this final rule, a the two most severe El Nin˜ o events on

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record (1982–83 and 1997–98) shows ocean warming and acidification and expansion into temperate areas how an exceptionally thermally- increase over the twenty-first century. (Woodroffe et al., 2010). Predicted sensitive reef-building fire coral, Aside from mesophotic and marginal ocean warming in the twenty-first Millepora intricata, twice survived habitats, other types of habitats may century is expected to result in a similar catastrophic bleaching in a deeper water provide refuge for reef-building corals pattern of poleward expansion, thus refuge (>11 m depth). During both from ocean warming and other threats. newly-colonized areas may provide events, M. intricata was extirpated Some of these have long been known to temporary refugia for some species (van across its range in shallow water but reduce thermal stress, such as those Hooidonk et al., 2013b). For example, showed recovery within several years, habitats with highly-fluctuating models suggest that such expansion of while two other fire corals without conditions, strong currents from wind or reef-building corals could occur at the deep-water populations were driven to tides, and shading from frequent cloud rate of 1–4 km per year in Japan (Yara regional extinction (Smith et al., in cover or complex bathymetry, as et al., 2011). As temperatures increase to press). described in the proposed rule and the optimal range for reef-building The refuge value of mesophotic supporting documents. Supplemental corals in these northerly and southerly habitats is limited, however. Only about information suggests other areas, however, the simultaneous one-quarter of all reef-building coral oceanographic features may also increase in ocean acidification may species occur at mesophotic depths provide refuge from ocean warming negate the suitability of these areas (van (Bongaerts et al., 2012) and only 22 of both currently and the foreseeable Hooidonk et al., 2014; Yara et al., 2012). our proposed species. Also, there is future, such as: (1) Large-scale While it may appear that there is no limited connectivity between upwelling in both the Pacific long-term, large-scale refugia from both mesophotic and shallow coral habitats, (Karnauskas and Cohen, 2012) and ocean warming and ocean acidification at least for some species, suggesting that Caribbean (Bayraktarov et al., 2012); (2) (van Hooidonk et al., 2014), on a finer the actual likelihood of mesophotic the similar but smaller-scale regional and/or reef-scale, there is still corals repopulating shallow reef habitats phenomenon of internal tidal bores that a large amount of refugia in the form of is low for those species. For example, transport cooler, deeper water to heterogeneous habitat, including genetic connectivity between warmer, shallower areas (Storlazzi et al., mesophotic, non-reefal, and marginal mesophotic and shallow populations is 2013); (3) and the wakes of relatively habitats, that provide a buffer to corals high in Seriatopora hystrix on the GBR cool water left by the passage of tropical from threats into the foreseeable future. cyclones (Carrigan, 2012). Most of the (van Oppen et al., 2011) and Millepora refugia described above are with regard Corals and Coral Reefs Conclusion intricata in the eastern Pacific (Smith et to ocean warming, but some of these The above general information on al., in press), but low for Montastraea habitat types provide refugia potential reef-building coral biology and habitat cavernosa in the Caribbean (Brazeau et from ocean acidification, such as highly- leads to several important overall points al., 2013). fluctuating habitats which limit pH that apply both currently and over the Marginal habitats are also extensive, minima via tidal flux (Shaw et al., foreseeable future. With regard to reef- and recent investigations provide 2012), and from disease and building coral biology, first, evidence that marginal habitat also sedimentation, such as high-energy delineations between individual functions as refugia for some reef- habitats which provide flushing that colonies of the same species, and building corals. Marginal habitats reduces conditions conducive to disease between species, can be highly include turbid (Blakeway et al., 2013; and removes sediment. Seagrass beds uncertain, creating ambiguity with Browne et al., 2012), very warm (Riegl provide beneficial changes in ocean regard to the status of species—specific and Purkis, 2012; Riegl et al., 2011), chemistry to seawater on adjacent reefs, sources of uncertainty include unclear cold (Dalton and Roff, 2013; Lybolt et providing local refugia to ocean individual delineations, taxonomic al., 2011), soft substrate, and other acidification (Manzello et al., 2012). uncertainty, and species identification environments (Couce et al., 2012; Done, Depth also provides some refugia uncertainty. Thus, in our species 1982; Perry and Larcombe, 2003) with potential from disease, as most studies determinations we use the physiological sub-optimal coral growth conditions. A show a negative correlation between colony to inform how we estimate study of future coral habitat suitability depth and coral disease incidence. abundance of a coral species because under ocean warming and acidification However, some studies show no such that is how field surveys estimate coral suggests that marginal habitats may correlation, and disease incidence can abundance. Using the physiological provide important refugia for some reef- be comparable between mesophotic and colony to estimate abundance in the building corals (Couce et al., 2013b), shallow depths (Brandt et al., 2012). final rule does not change how we though not all coral species can survive Thermal regime changes from ocean estimated abundance in the proposed in these habitats. The study found that warming will have opposite effects on rule, in which we also relied on the IPCC AR4’s higher emission habitat, depending on location: In information that uses the physiological scenarios are all likely to result in: (1) locations already near the thermal colony to report abundance estimates. If Range expansion at the high-latitude maxima of reef-building corals, warming we have new or supplemental boundaries; (2) no decreased suitability will degrade habitat, but in locations information on the effective population in currently marginal eastern Equatorial currently too cool for these species, size (e.g., proportion of clonality) for a Pacific locations as well as in the warming will improve habitat, if other species, that information is also Atlantic generally; and (3) severe habitat features conducive to reef considered. Second, while corals can temperature-driven impacts in the growth are also present, such as hard reproduce both sexually and asexually, western Equatorial Pacific (Coral substrate and appropriate light and abundance estimates are based solely on Triangle) and surrounding regions. water chemistry conditions. Geological the physical number of coral colonies These findings led to the conclusion evidence from past global warming that does not recognize mode of that marginal habitat is likely to periods shows a pattern of poleward reproduction. Dispersal and recruitment function as a patchwork of refuge expansion of some reef-building coral patterns are highly variable across space habitats for some reef-building corals in ranges, coupled with decline in and time, leading to complex and poorly both the Indo-Pacific and Atlantic as equatorial areas (Kiessling et al., 2012) understood population dynamics and

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connectivity. In our species same reef survive and acclimatize, the candidate species’ extinction risk determinations, we consider life history potentially leading to adaptation. The over the foreseeable future. characteristics that may contribute to magnitude and diversity of reef-building The proposed rule qualitatively extinction risk. For example, species coral habitats creates high physical ranked each threat as high, medium, with high recruitment rates or fast heterogeneity across the ranges of these low, or negligible (or combinations of growth rates may have the ability to species, providing habitat refugia from two; e.g., ‘‘low-medium’’) importance in more quickly recover from disturbances. threats. Some of these refuge habitats terms of their contribution to extinction Additionally, long-lived species with may already be occupied by the species; risk of all coral species across their large colony size can sustain partial others could become occupied as their ranges. These qualitative rankings mortality (fission) and still have suitability changes, assuming the considered: (1) The severity of the potential for persistence and regrowth. species are able to reproduce and threat; (2) the geographic scope of the Third, all species considered in this successfully recruit into these areas. The threat; (3) the level of certainty that final rule occur in multiple habitat types habitat heterogeneity and refugia lead to corals in general (given the paucity of and have considerable distributions that variable micro-climates at a reef scale species-level information) are affected encompass at least thousands of islands that leads to variable responses by reef- by each threat; (4) the projections of and multiple habitat types, which building corals to threats, both spatially potential changes in the threat; and (5) influences absolute abundances—the and over time, which adds complexity the impacts of the threat on each absolute distributions and absolute to assessing the status of species in a species. Global climate change directly abundances of these species are key worsening environment. influences two of the three highest components of their vulnerability to ranked threats, ocean warming and Overall, in our species extinction. Therefore, in our species ocean acidification, and indirectly determinations, we recognize that the determinations, the spatial and (through ocean warming) influences the exposure and response of a coral species demographic traits of absolute remaining highest ranked threat, to global threats varies spatially and abundance and absolute distribution disease. temporally based on variability in the inform our evaluation of a species’ We identified nine threats (see Table species’ habitat and distribution. All current status and its capacity to 1) as posing either current or future respond to changing conditions over the species considered in this final rule extinction risk to the proposed corals. foreseeable future. occur in multiple habitat types, or reef However, the SRR identified 19 threats Additionally, because of variability environments, and have distributions that affect corals. The ten threats not between species, some generalities that encompass diverse physical included in Table 1 did not rank highly cannot be assumed to apply equally to environmental conditions that influence in their contribution to extinction risk, each species. Therefore, in our species how that species responds to global although they do adversely affect the determinations we consider the threats. As such, the concept of species. Ocean warming, ocean complex nature of coral biology and heterogeneous habitat influences acidification, and disease are assume that for all species, responses to extinction risk for all species in this overarching threats of high or medium- threats will be variable between final rule because each species high importance when evaluating the individual coral colonies and even experiences a wide variety of conditions extinction risk of the proposed species. between different portions of the same throughout its range which allows for These impacts are currently occurring, colony. The best available species- variable responses to global and local and are expected to worsen, posing specific information for each of the 65 threats. increasingly severe effects on the species is provided in the Species- Threats Evaluation species considered in this final rule. specific Information and Determinations Other threats are of medium or medium- sub-sections below. Section 4(a)(1) of the ESA and NMFS’ low importance when evaluating With regard to reef-building coral implementing regulations (50 CFR 424) extinction risk because their effects are habitat, first, the heterogeneity of reef- state that the agency must determine largely indirect and/or local to regional building coral habitat varies greatly both whether a species is endangered or in spatial scale. These include trophic spatially and temporally. That is, the threatened because of any one or a effects of fishing, sea-level rise, and habitat of a given species varies combination of five factors: (A) Present water quality issues related to spatially (i.e., even the smallest ranges or threatened destruction, modification, sedimentation and nutrients. The of the species included in this final rule or curtailment of habitat or range; (B) remaining threats can be locally acute, encompass thousands of islands and overutilization for commercial, but because they affect limited multiple habitat types) and temporally recreational, scientific, or educational geographic areas, they are of low (i.e., varies over time in response to purposes; (C) disease or predation; (D) importance when evaluating extinction disturbances and recoveries). Second, inadequacy of existing regulatory risk. Examples in this category are some habitat types are understudied mechanisms; or (E) other natural or predation or collection for the (e.g., mesophotic and marginal) so data manmade factors affecting its continued ornamental trade industry. These threats about their contribution to the existence. In the proposed rule, our are more significant to certain species, distribution and abundance of evaluation of the five factors was such as those with naturally low individual coral species are limited, as informed by the SRR and SIR for factors abundance and/or those at severely well as the possibility of refugia from A–C and E; and the Final Management depleted population levels. However, particular threats being underestimated. Report for factor D. We identified factors none of the species in this final rule can Third, a diversity of habitats likely acting directly as stressors to the 82 be characterized as such. helps some species capacity to coral species (e.g., sedimentation and Table 1. The nine most important acclimatize and adapt to changing elevated ocean temperatures) as distinct threats contributing to extinction risk conditions, especially extreme habitats. from the sources responsible for those for corals in general and ordered For example, while some colonies die factors (e.g., land management practices according to importance. The threat is during the stressful conditions common and climate change) and qualitatively paired with its corresponding ESA to extreme habitats, other colonies at the evaluated the impact each threat has on section 4 factor in the last column.

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Threat Importance Section 4 factor

Ocean Warming ...... High ...... E. Disease ...... High ...... C. Ocean Acidification ...... Medium-High ...... E. Trophic Effects of Fishing ...... Medium ...... A. Sedimentation ...... Low-Medium ...... A and E. Nutrients ...... Low-Medium ...... A and E. Sea-Level Rise ...... Low-Medium ...... A. Predation ...... Low ...... C. Collection and Trade ...... Low ...... B.

Some comments (e.g., Comment 26) species’ likely response. As described the climate-related impacts to coral reefs suggested that local threats, such as below, the more vulnerable a coral may be substantial within that sedimentation, are more important species is to the high importance threats timeframe, our conclusion that 2100 is locally to species’ extinction risk than (i.e., ocean warming, diseases, ocean the appropriate timeframe for purposes the higher rated threats. In the proposed acidification), the more likely the of analyzing climate change-related rule, we acknowledged that some of the species is at risk of extinction, either threats remains unchanged. local threats have been the cause of now or within the foreseeable future. Nine Most Important Threats to Reef- mass coral mortality in particular The threats related to global climate Building Corals locations. Further, supplemental change (e.g., bleaching from ocean information provides evidence that local warming, ocean acidification) pose the As described above and shown in threats, such as overfishing and disease, greatest potential extinction risk to Table 1, we considered nine threats to have actually been more significant corals and have been evaluated with be the most important to the current or drivers of past coral reef species decline, sufficient certainty out to the year 2100. expected future extinction risk of reef- particularly in the Caribbean (Jackson et Comment 38 provides a summary of building corals: Ocean warming, al., 2014). However, we must evaluate the comments we received on the disease, ocean acidification, trophic all threats that pose an extinction risk to determination of foreseeable future in effects of reef fishing, sedimentation, the proposed species over the the proposed rule and supporting nutrients, sea-level rise, predation, and foreseeable future. Given the predicted documents as extending out to the year collection and trade. Vulnerability of a impacts of climate-related threats over 2100. Many comments criticized the use coral species to a threat is a function of the foreseeable future, we maintain the of 2100 because they considered it to be susceptibility and exposure, considered relative importance ranking of the too far into the future. We do not agree at the appropriate spatial and temporal threats to reef-building corals generally. that 2100 is too far in the future to be scales. In this finding, the spatial scale However, we acknowledge that lower considered foreseeable as it pertains to is the current range of the species, and importance threats also pose significant projections regarding climate-change the temporal scale is from now through risk to individual species in certain related threats. As described in detail in the foreseeable future. Susceptibility locations. the Global Climate Change—General refers to the response of coral colonies Overview section, the IPCC Fifth to the adverse conditions produced by Foreseeable Future Assessment Report (AR5), Climate the threat. Susceptibility of a coral In the proposed rule, we established Change 2013: The Physical Science species to a threat is primarily a that the appropriate period of time Basis (IPCC, 2013), commonly referred function of biological processes and corresponding to the foreseeable future to as the Working Group I Report (WGI), characteristics, and can vary greatly is a function of the particular types of is a continuation of AR4. Most of AR5 between and within taxa. Susceptibility threats, the life-history characteristics, WGI’s models also use 2100 as the end- depends on direct effects of the threat and the specific habitat requirements for point (some models go beyond 2100) on the species, and it also depends on the coral species under consideration. and the supplemental information the cumulative (i.e., additive) and The timeframe corresponding to the included in AR5 reinforces our original interactive (i.e., synergistic or foreseeable future takes into account the basis for defining the foreseeable future antagonistic) effects of multiple threats time necessary to provide for the as the period of time from the present acting simultaneously on the species. conservation and recovery of each to the year 2100 (IPCC, 2013). That is, Exposure refers to the degree to which threatened species (e.g., recruitment the foreseeable future is not defined as the species is likely to be subjected to rate, growth rate, etc.) and the the year 2100, but rather as the time the threats throughout its range, so the ecosystems upon which they depend, period from the present to the year overall vulnerability of a coral species to but is also a function of the reliability 2100, with increasing uncertainty in threats depends on the proportion of of available data regarding the identified climate change projections over that colonies that are exposed to the threats. threats and extends only as far as the time period. So while precise conditions Thus, the exposure of a species to data allow for making reasonable during the year 2100 are not reasonably threats, on a range-wide scale, is a predictions about the species’ response foreseeable, the general trend in function of physical processes and to those threats. As is discussed further conditions during the period of time characteristics that affect the frequency in the Foreseeable Future and Current from now to 2100 including the period or degree to which individual colonies and Future Environmental Conditions 2081 to 2100 is reasonably foreseeable experience the threats and the ability of subsections of the Risk Analysis section as a whole, although less so through its spatial and demographic traits to below, the period of time over which time. Because the time period of the affect its overall vulnerability. A species individual threats and responses may be present to the year 2100 is strongly may not necessarily be highly projected varies according to the nature supported as a reasonably foreseeable vulnerable to a threat even when it is of the threat and the type of information timeframe in the climate science highly susceptible to the threat, if available about that threat and the projections in AR5’s WGI, and because exposure is low over the appropriate

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spatial and temporal scales. strength of the climate’s response to per square meter, W/m2) quantifies Consideration of the appropriate spatial GHG concentrations; and (3) large energy fluxes caused by changes in and temporal scales is particularly natural variations. The warming rate these drivers relative to the year 1750. important, because of potential high slow-down (or ‘‘hiatus’’ discussed in the Increasing RF leads to surface warming, variability in some threats over the large Threats Evaluation—Ocean Warming and decreasing RF leads to surface spatial scales. The nine most important section) since 1998 is an example of a cooling. The concentration of CO2 in the threats are summarized below, large natural variation that was not atmosphere is the dominant including general descriptions of predicted by the models at that time. anthropogenic driver. Higher susceptibility and exposure. Species- However, AR4’s projections are built on atmospheric CO2 results in: Ocean specific threat susceptibilities are scientifically sound principles, and they warming via the greenhouse effect, described in the Species-specific fairly simulate many large-scale aspects ocean acidification via oceanic uptake Information and Determinations section. of present-day conditions, and thereby of CO2, and rising sea levels via ice provided the best available information melting and thermal expansion. Patterns Global Climate Change—General on climate change at the time the in solar activity and major volcanic Overview proposed rule was published. Overall eruptions are the two dominant natural Several of the most important threats uncertainty is not necessarily any drivers. Solar activity can either contributing to the extinction risk of greater in AR5 than in AR4, but rather increase or decrease RF, whereas major corals are related to global climate the uncertainty is understood better and volcanic eruptions only decrease RF. change. The main concerns regarding expressed more clearly in AR5’s WGI Current total RF relative to 1750 is impacts of global climate change on (IPCC, 2007; IPCC, 2013; Knutti and Jan positive, and has led to an uptake of coral reefs generally, and on the Sedla´cek, 2012). AR5’s WGI represents energy by the climate system. The proposed corals in particular, are the the largest synthesis of global climate largest contribution to current total RF magnitude and the rapid pace of change change physical science ever compiled, is the increasing atmospheric in GHG concentrations (e.g., carbon and a substantial advance from AR4. concentration of CO2 since 1750, most dioxide (CO2) and methane) and WGI is divided into four sections that of which has been anthropogenic CO2 atmospheric warming since the examine observations, drivers, emitted since 1860, and the mean rate Industrial Revolution in the mid-19th understanding, and projections of of increase in CO2 is unprecedented in century. These changes are increasing changes to the global climate system. the past 20,000 years. Current CO2 the warming of the global climate The primary results of these four levels (∼400 ppm) will result in system and altering the carbonate sections relevant to this rule are continued warming even if chemistry of the ocean (ocean summarized below; then a summary of anthropogenic emissions went to zero acidification), which affects a number of the potential impacts to corals resulting now (this is referred to as biological processes in corals, including from the IPCC climate change scenario ‘‘commitment’’ to future warming from secretion of their skeletons. The that we consider to be the most the CO2 build-up already in the description and analysis of global impactful to corals is provided in the atmosphere), but reducing emissions climate change in the proposed rule and RCP8.5 Projections section below, with now would strongly influence the levels supporting documents were based a focus on ocean warming and of future warming (IPCC, 2013). largely on the IPCC AR4, The Physical acidification, two of the most important The third section of WGI describes Science Basis (IPCC, 2007) and threats to corals. past climate patterns to understand the supporting literature. Supplemental The first section of WGI considers changes in the climate system. It is information gathered during the public observations of changes in the climate ‘‘extremely likely’’ that human activities engagement period shows that global system, which refers to description of caused more than half of the observed temperatures continue to increase and past climate patterns, and the certainty increase in global average surface that temperature patterns differ associated with the same. The overall temperature from 1951 to 2010. regionally. conclusion of this section is that Anthropogenic GHGs have ‘‘very likely’’ As summarized in Comment 11, we warming of the climate system is made a substantial contribution to received many comments on our unequivocal and since the 1950s, many upper-ocean warming (above 700 m) analysis of global climate change in the of the observed changes are observed since the 1970s. It is also ‘‘very proposed rule. Some commenters unprecedented over decades to likely’’ that oceanic uptake of asserted that we did not adequately millennia. With regard to ocean anthropogenic CO2 has reduced surface portray the level of uncertainty warming, it is ‘‘virtually certain’’ that water pH. The anthropogenic ocean associated with the available climate the upper ocean (0–700 m) warmed warming observed since the 1970s has change models. Others provided from 1971 to 2010. With regard to ocean contributed to global sea-level rise over information that global GHG emissions acidification, it is ‘‘very likely’’ that the this period through ice melting and and global temperatures continue to rise pH of surface ocean waters has thermal expansion (IPCC, 2013). unabated. Additionally, significant decreased as a result of ocean uptake of The fourth section of WGI uses supplemental information has become anthropogenic CO2 from the projected changes in the climate system available on global climate change since atmosphere. With regard to sea-level to model potential patterns of future the proposed rule, specifically, AR5’s rise, it is ‘‘virtually certain’’ that the climate. WGI uses a new set of four WGI (IPCC, 2013), and its companion global mean sea level rose by 19 cm representative concentration pathways report, Climate Change 2014: Impacts, from 1901 to 2010 (IPCC, 2013). (RCP) that provide a standard Adaptation, and Vulnerability, The second section of WGI considers framework for consistently modeling commonly referred to as the Working drivers of changes in the climate system, future climate change. These replace the Group II Report (WGII; IPCC, 2014). which refers to explanations of factors old Special Report on Emissions The IPCC has summarized the major forcing climate patterns. Natural and Scenarios (SRES) system used in prior sources of uncertainty associated with anthropogenic substances and processes assessments. The new RCPs are named AR5’s WGI projections of global climate that alter the Earth’s energy budget are according to increases in radiative change as: (1) The projected rate of drivers of climate change. In AR5, forcing (RF) relative to the 1986–2005 increase for GHG concentrations; (2) radiative forcing (RF, measured in watts average by the year 2100 of 2.6, 4.5, 6.0,

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and 8.5 W/m2, RCP2.6, RCP4.5, RCP6.0, warming and ocean acidification, in our time period to approximately +/¥0.7 °C and RCP8.5. The four new pathways assessment of extinction risk for the by 2060 (IPCC, 2013; WGI Figure 11.19). have atmospheric CO2 equivalents of corals in the final rule. RCP8.5 is the Projected changes in annual mean ocean 421 (RCP2.6), 538 (RCP4.5), 670 scenario with the highest GHG temperature between 60 °N and 60 °S (RCP6.0), and 936 ppm (RCP 8.5) in emissions rate and subsequent future latitude in 2081–2100 are shown in WGI 2100, and follow very different GHG levels; thus it would be the most Figure 12.12. Under RCP8.5, annual trajectories to reach those endpoints. impactful to corals through ocean mean surface ocean temperature The purpose of the RCPs was to warming and ocean acidification. between 60 °N and 60 °S latitude is explicitly explore the impact of different However, should another of the IPCC projected to increase by approximately climate policies in addition to the no- RCPs ultimately be realized, the 3.5 °C by 2081–2100 compared to the climate-policy scenarios explored in the negative impacts to corals would be 1986–2005 average (IPCC, 2013; WGI earlier scenarios (Van Vuuren et al., lower. Figure 12.12). A different graph using 2011). The four new pathways were As described above, we received and the same data shows global annual collected significant supplemental developed with the intent of providing mean surface ocean temperature is information regarding our consideration a wide range of total climate forcing to projected to increase by approximately of global climate change in the proposed guide policy discussions and 3.5 °C by 2081–2100 compared to the specifically include one mitigation rule. Additional observations, data, and 1986–2005 average, with 5 to 95 percent pathway leading to a very low forcing testing have produced better models and range of +/¥1–1.5 °C (IPCC, 2013; level (RCP2.6), two stabilization a greater understanding of the Figure AI.SM8.5.4). Thus, RCP8.5 pathways (RCP4.5 and RCP6), and one uncertainty inherent in climate change pathway with continued high GHG projections. Annual GHG emission rates projects that global annual mean ocean continue to climb to record levels, and surface temperatures will increase by emissions (RCP8.5). ° The RCP method more strongly the last decade has been the warmest on approximately 0.4–1 C by 2030, ° represents the physical processes record, underscoring the proposed rule’s approximately 0.7–2 C by 2060, and ° underlying climate change, and various conclusions about climate change approximately 2–5 C by 2081–2100 factors affecting GHG emissions threats to reef-building corals. We (IPCC, 2013). globally, than previous methods. WGI conclude that the supplemental Projected changes in Indo-Pacific adjusts the likely global surface information supports the central annual median ocean surface warming that would result from a premise of the proposed rule that global temperatures (i.e., WGI’s West Indian doubling of atmospheric CO2 to climate change-related threats have Ocean, North Indian Ocean, Southeast 1.5–4.5 °C (compared to AR4’s estimate already caused widespread impacts to Asia, North Australia, and Pacific of 2.0–4.5 °C), due to improved corals and coral reefs and these impacts Islands regions), and Caribbean annual understanding of the climate system, the will become increasingly severe from median land and ocean combined extended temperature record in the now to 2100, with correspondingly surface temperatures, compared to the atmosphere and ocean, and new severe consequences for corals and coral 1986–2005 average are shown in the estimates of radiative forcing to GHG reefs. However, we acknowledge that figures in WGI’s Annex I’s concentrations. Taken together, the four the interpretation of future climate Supplementary Material for RCP8.5 for new pathways project wide ranges of change threats to corals and coral reefs these six WGI regions, which together increases in ocean warming, ocean is associated with complexity and cover the ranges of the species included acidification, and sea level rise globally uncertainty, and that precise effects on in this final rule. The figures include throughout the 21st century with individual species of reef-building graphs in the upper right showing the conditions seen in RCP 2.6–6.0 corals are difficult to determine. projected median temperature increase requiring significant changes in Species-specific threat susceptibilities to 2100 under RCP8.5, the 25 to 75 anthropogenic GHG emissions (IPCC, of each of the 65 species in this final percent range, and the 5 to 95 percent 2013). rule to the threats resulting from global range. The figures also includes maps of The proposed rule and supporting climate change are described in the each region showing projected changes documents assumed that AR4’s highest- Species-specific Information and spatially under RCP8.5 for the time emission scenario A1FI was the most Determinations section below. likely to occur for two reasons: (1) periods 2016–2035, 2046–2065, and Recent annual GHG emission growth RCP8.5 Projections 2081–2100, and for the 25 percent, 50 rates had exceeded the GHG emission Because we have determined that percent, and 75 percent projections growth rates in A1F1 (except 2009 when RCP8.5 is the most impactful pathway under RCP8.5 for each of these time the global recession slowed growth); to corals, we provide a summary of periods. For the Caribbean, the range of and (2) there were no indications that RCP8.5’s projections over the projections spanned by the 25, 50, and major reductions in GHG emissions foreseeable future for ocean warming 75 percent range maps are: For 2016– ° would occur in the near to mid-term and ocean acidification (IPCC, 2013). 2035, increases of 0.5–1.0 C; for 2046– ° future (decades) through national or Where possible, projections are 2065, increases of 1.0–3.0 C; and for international policies or major changes provided for the near-term (to mid- 2081–2100, increases of 2.0–4.0 °C. in the global fossil fuel economy century) and long-term (to 2100), and Spatial variability in the projections (Brainard et al., 2011). Recent annual globally and regionally (Indo-Pacific consists mostly of larger increases in the GHG emission growth rates (except and Caribbean). Implications for coral Greater Antilles and Jamaica, and lower 2009) exceed the GHG emission growth reefs are also described. increases in the Lesser Antilles and the rates in RCP8.5 (Le Que´re´ et al., 2013). Ocean Warming. Under RCP8.5, Bahamas (Figure AI.SM8.5.44). The While the President’s Climate Action annual averaged, globally averaged, percent ranges in the projections Plan and intensified international surface ocean temperature is projected described above are from the maps and climate negotiations may change global to increase by approximately 0.7 °C by are for the 25 to 75 percent range, emissions trajectories, we make the 2030 and 1.4 °C by 2060 compared to however range of projections within the conservative assumption to evaluate the 1986–2005 average, with the 10 to 5 to 95 percent range are considerably RCP8.5, and its projections for ocean 90 percent range increasing over that greater, as shown in the bar-and-whisker

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graph in the upper right of each figure reduction of 0.31 (statistical range of Implications for Coral Reef (IPCC, 2013). 0.30 to 0.32) by 2100 (IPCC, 2013; WGI Ecosystems. AR5’s WGII Report For the Indo-Pacific (WGI’s West Figure 6.28a). Projected changes in describes the effects of WGI’s climate Indian Ocean, North Indian Ocean, global surface pH in the 2090s change projections on the world’s Southeast Asia, North Australia, and compared to the 1990s under RCP8.5 are ecosystems, including coral reefs. The Pacific Islands regions), the range of shown in the map in WGI Figure 6.28b. report includes a description of projections spanned by the 25, 50, and In the tropical Indo-Pacific, decreases of ‘‘Projected Impacts’’ on coral reefs of all 75 percent range maps are: For 2016– 0.25 to 0.40 are projected, with the four WGI pathways combined, and a 2035, increases of 0.0–1.0 °C; for 2046– lower decreases in the central and general overview of projected impacts to 2065, increases of 1.0–3.0 °C; and for eastern Pacific, and the higher decreases coral reefs. While this information does 2081–2100, increases of 2.0–5.0 °C. in the GBR area and the northern not specifically describe projected Spatial variability in the projections Philippines, while most of the impacts of RCP8.5 to coral reefs by consists mostly of larger increases in the Caribbean is projected to decrease in pH 2100, it strongly suggests that the Red Sea, Persian Gulf, and the Coral by 0.30 to 0.35. The pH reductions projected impacts of ocean warming and Triangle, and lower increases in the associated with RCP8.5 are projected to ocean acidification will increase (IPCC, central and eastern Indian Ocean and result in declining aragonite saturation 2014). Likewise, the recent U.S. south-central Pacific (Figures states, as shown in WGI Figure 6.29. National Climate Assessment (NCA) AI.SM8.5.92, 116, 124, 132, and 140). Projected median surface aragonite report describes the effects of projected The percent ranges in the projections saturation states of the world’s oceans climate change on United States described above are from the maps and are shown for 2050 and 2100 in Figure ecosystems, including coral reefs. are for the 25 to 75 percent range, 6.29d and f respectively, and by depth Chapter 24 of the report includes a brief however range of projections within the for the Atlantic and Pacific Oceans in and general description of projected 5 to 95 percent range are considerably 2100 in Figure 6.29c and e respectively. climate change without specifically greater, as shown in the bar-and-whisker Surface aragonite saturation states in the examining any particular pathway graph in the upper right of each figure tropical Indo-Pacific and Caribbean are (Doney et al., 2014). As with WGII, (IPCC, 2013). projected to decline from current levels while the NCA report does not To summarize ocean warming of over 3, to less than 2.5 by 2100, with specifically describe projected impacts projections, RCP8.5 projects annual similar spatial patterns as for pH of RCP8.5 to coral reefs by 2100, it median ocean surface temperature reductions (IPCC, 2013; WGI Figure strongly suggests that the projected increases for the Indo-Pacific, and 6.29). Statistical range is not provided impacts of ocean warming and ocean annual median land and ocean for aragonite saturation state, but we acidification will increase on United combined surface temperature increases assume it to be similar to that associated States coral reefs. for the Caribbean. Projected median with pH projections. As shown in temperatures, and associated 25 to 75 Recent papers specifically address Figures 6.28 and 6.29, spatial variability percent range and 5 to 95 percent range, future changes in Indo-Pacific and is projected under RCP8.5 for both pH are provided for the time periods of Caribbean coral reef ecosystems and aragonite saturation state reductions 2016–2035, 2046–2065, and 2081–2100. resulting from RCP8.5’s projections of over the foreseeable future within the We interpret these projections as combined ocean warming and ocean ranges of the species included in this follows: (1) Global annual median ocean acidification, including Couce et al. final rule (IPCC, 2013). surface temperatures are likely to rise (2013a) and van Hooidonk et al. (2014). approximately 2–5 °C by 2081–2100, We interpret RCP8.5’s ocean Couce et al. (2013a) uses RCP8.5’s ocean exacerbating the impacts of ocean acidification projections as follows: (1) warming and ocean acidification warming on reef-building corals; (2) Mean surface pH in the tropics is projections to develop predictions of these global mean projections are not projected to decline by approximately ‘‘average change in suitability’’ of coral necessarily representative of ocean 0.31 to approximately 7.75 by 2100, reef habitat by 2070, concluding that surface temperature conditions with a subsequent large decline in declines in conditions will be driven throughout the ranges and habitats of aragonite saturation state in surface primarily by ocean warming, and vary the species in this final rule through the tropical waters, exacerbating the spatially within the ranges of the foreseeable future, due to spatial impacts of ocean acidification on reef- species included in this final rule. variability and statistical range of the building corals; (2) surface pH and Couce et al. (2013) predicts marked RCP8.5 ocean warming projections aragonite saturation state conditions declines in environmental suitability for described above for the Indo-Pacific and throughout the ranges of the species in shallow coral reef habitats across the Caribbean regions; and (3) ocean surface this final rule through the foreseeable equatorial western Pacific and adjacent temperature conditions in the future are not necessarily represented by areas (e.g., Coral Triangle) by 2070, and foreseeable future within the ranges of these mean projections, due to the generally less favorable conditions the species in this final rule are spatial variability within the Indo- elsewhere on Indo-Pacific and assumed to vary spatially at the coarse Pacific and Caribbean regions, and the Caribbean coral reefs. Some coral reef spatial scales shown in WGI for the statistical range of the RCP8.5 ocean areas show little or no change in Indo-Pacific and Caribbean regions, and acidification projections; and (3) surface environmental suitability by 2070, more so at finer spatial scales, and to pH and aragonite saturation state including portions of the western Indian fall within the statistical ranges conditions in the foreseeable future and central Pacific Oceans, likely projected for the Indo-Pacific and within the ranges of the species in this because seawater temperatures are Caribbean regions. final rule are assumed to vary spatially moderated by physical factors such as Ocean Acidification. Under RCP8.5, at the coarse spatial scales shown in higher latitudes or upwelling but mean surface pH in the tropics (20 °N WGI for the Indo-Pacific and Caribbean aragonite saturation states are suitable to 20 °S) is projected to decline from the regions, and more so at finer spatial (Couce et al., 2013a; Fig. 1e). Many current pH of approximately 8.05 to scales, and to fall within the statistical species included in this final rule occur approximately 7.95 by 2050, and to ranges projected for the Indo-Pacific and in areas of the western Indian and approximately 7.75 by 2100, or a Caribbean regions. central Pacific Oceans predicted to have

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little or no change in environmental future conditions; and (4) neither paper species. The primary observable coral suitability by 2070. Notably, the paper analyzed the impacts of future climate response to ocean warming is bleaching concluded the detrimental effect of change on individual coral species. of adult coral colonies, wherein corals higher ocean warming appears to In conclusion, RCP8.5 projects expel their symbiotic zooxanthellae in strongly outweigh the impacts of lower impacts to global coral reef ecosystems response to stress. For many corals, an aragonite saturation states for tropical over the foreseeable future from the episodic increase of only 1 °C–2 °C shallow water coral reefs (Couce et al., combined effects of increased ocean above the normal local seasonal 2013a). temperature and ocean acidification, the maximum ocean temperature can van Hooidonk et al. (2014) also effects of which are likley to be induce bleaching. Corals can withstand applies RCP8.5’s ocean warming and compounded by increasing coral mild to moderate bleaching; however, ocean acidification projections to disease, trophic effects of fishing, land- severe, repeated, or prolonged bleaching predict ‘‘when severe coral bleaching based sources of pollution, and other can lead to colony death. Coral events start to occur annually, and of threats to corals. However, projecting bleaching patterns are complex, with changes in aragonite saturation state’’ species-specific responses to global several species exhibiting seasonal over the 21st century. The paper threats is complicated by several cycles in symbiotic dinoflagellate concludes that 90 percent of all coral physical and biological factors: (1) density. Thermal stress has led to reefs are projected to experience severe Global projections of changes to ocean bleaching and associated mass mortality bleaching annually by 2055, that five temperatures and acidification over the in many coral species during the past 25 percent declines in calcification are foreseeable future are associated with years. In addition to coral bleaching, projected for all reef locations by 2034, three major sources of uncertainty (GHG other effects of ocean warming with the predicted changes in emissions assumptions, strength of the detrimentally affect virtually every life- conditions varing spatially across the climate’s response to GHG history stage in reef-building corals. geographic ranges of the species concentrations, and large natural Impaired fertilization, developmental included in this final rule. These variations); (2) there is spatial variability abnormalities, mortality, impaired authors predicted that the most rapid in projected environmental conditions settlement success, and impaired increases in ocean warming will occur across the ranges of the species in this calcification of early life phases have all in the western equatorial Pacific, the final rule at any given point in time; and been documented. In the proposed rule, slowest in the Indian Ocean, eastern (3) species-specific responses depend on we relied heavily on AR4 in evaluating Pacific Ocean, and high latitude areas, many biological characteristics, extinction risk from ocean warming and intermediate elsewhere (van including, at a minimum, distribution, because it contained the most Hooidonk et al., 2014; Fig 1a). The most abundance, life history, susceptibility to thoroughly documented and reviewed rapid declines in aragonite saturation threats, and capacity for acclimatization. assessments of future climate and state are predicted for the same general The available species-specific represented the best available scientific areas as the slowest warming, the information on how species in this final information on potential future changes slowest declines in aragonite saturation rule respond to climage change is in the earth’s climate system. Emission state in roughly the same areas as the limited. Therefore, analysis of the rates in recent years have met or most rapid warming, and intermediate biological characteristics on a case-by- exceeded levels predicted by AR4’s elsewhere in the Indo-Pacific and in the case basis is emphasized in considering worst-case scenarios, resulting in all Caribbean (van Hooidonk et al., 2014; a species’ vulnerability to extinction. scenarios underestimating the projected Fig 1d). One of the paper’s conclusions Ocean Warming (High Importance climate condition. is that there are no real refugia for coral Threat, ESA Factor E) reefs to the combined threats of higher Exposure of colonies of a species to ocean warming and lower aragonite Ocean warming is considered under ocean warming can vary greatly across saturation states (van Hooidonk et al., ESA Factor E—other natural or its range, depending on colony location 2014). manmade factors affecting the (e.g., latitude, depth, bathymetry, Several points to consider when continued existence of the species— habitat type, etc.) and physical interpreting Couce et al. (2013a) and because the effect of the threat results processes that affect seawater van Hooidonk et al. (2014) are: (1) The from human activity and affects temperature and its effects on coral different results and conclusions are individuals of the species directly, and colonies (e.g., winds, currents, likely due to the different methods, and not their habitats. In the proposed rule, upwelling shading, tides, etc.). Colony illustrate the sensitivity and variability we described the threat from ocean location can moderate exposure of in predicting the impacts of projected warming as follows. Mean seawater colonies of the species to ocean changes in climate on coral reefs; (2) temperatures in reef-building coral warming by latitude or depth, because both papers used very coarse spatial habitat in both the Caribbean and Indo- colonies in higher latitudes and/or scales (1° × 1° cells, or >10,000 km2 at Pacific have increased during the past deeper areas are usually less affected by the Equator), thus each cell can include few decades, and are predicted to warming events. Deeper areas are many different reefs that collectively continue to rise between now and 2100. generally less affected typically because represent diverse coral communities As also described in the proposed rule, lower irradiance reduces the likelihood and habitats, which in turn can affect the frequency of warm-season of warming-induced bleaching. Also, the local spatial and temporal patterns temperature extremes (warming events) some locations are blocked from warm of coral responses to ocean warming and in reef-building coral habitat in both the currents by bathymetric features, and acidification; (3) both papers predict Caribbean and Indo-Pacific has some habitat types reduce the effects of high spatial variability in future increased during the past two decades, warm water, such as highly fluctuating conditions across coral reefs, and both and it is also predicted to increase environments. Physical processes can show the western equatorial Pacific as between now and 2100. moderate exposure of colonies of the having the most degraded future Ocean warming is one of the most species to ocean warming in many conditions, and parts of the Indian important threats posing extinction risks ways, including processes that increase Ocean, central Pacific, and some to the proposed coral species; however, mixing (e.g., wind, currents, tides), outlying areas as having less degraded individual susceptibility varies among reduce seawater temperature (e.g.,

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upwelling, runoff), or increase shading decreased vertical mixing of both heat mean surface air temperature warming (e.g. turbidity, cloud cover). Exposure of and nutrients, leaving surface waters has occurred since 1998, which AR5’s colonies of a species to ocean warming warmer and nutrient-poor. While the WGI refers to as a ‘‘hiatus.’’ Despite this will likely vary annually and decadally, implications for corals and coral reefs of slowdown in warming, the period since while increasing over time, because: (1) these increases in warming-induced 1998 is the warmest recorded and ‘‘Each Numerous annual and decadal stratification have not been well of the last three decades has been processes that affect seawater studied, it is likely that these changes successively warmer at the Earth’s temperatures will continue to occur in will both exacerbate the temperature surface than any preceding decade since the future (e.g., inter-decadal variability effects described above (e.g., increase 1850.’’ in seawater temperatures and upwelling bleaching and decrease recovery) and The slow-down in global mean related to El-Nin˜ o Southern Oscillation); decrease the overall net productivity of surface warming since 1998 is not fully and (2) ocean warming is predicted to coral reef ecosystems (e.g., fewer explained by AR4 or AR5 WGI’s models, substantially increase by 2100. nutrients) throughout the tropics and but is consistent with the substantial Multiple threats stress corals subtropics. decadal and interannual variability seen simultaneously or sequentially, whether Overall, there is ample evidence that in the instrumental record and may the effects are cumulative (the sum of climate change (including that which is result, in part, from the selection of individual stresses) or interactive (e.g., already committed to occur from past beginning and end dates for such synergistic or antagonistic). Ocean GHG emissions and that which is analyses. Possible factors in the slow- warming is likely to interact with many reasonably certain to result from down may include the following: Heat other threats, especially considering the continuing and future emissions) will absorption by the deep ocean (Guemas long-term consequences of repeated follow a trajectory that will have a major et al., 2013; Levitus et al., 2012) thermal stress, and that ocean warming impact on corals. There has been a facilitated by stronger than normal trade is expected to continue to increase over recent research emphasis on the winds (England et al., 2014), volcanic the foreseeable future. Increased processes of acclimatization and eruptions over the last decade (Santer et seawater temperature can lower adaptation in corals, but in the proposed al., 2014), La Nin˜ a-like decadal cooling resistance to coral diseases and reduce rule we determined that, taken together, that produces multi-year periods of coral health and survivorship. Coral the body of research was inconclusive slower warming than the long-term disease outbreaks often have either as to how these processes may affect anthropogenic forced warming trend accompanied or immediately followed individual corals’ extinction risk, given (Benestad, 2012; Easterling and Wehner, bleaching events, and also follow the projected intensity and rate of ocean 2009; Kosaka and Xie, 2013), inherent seasonal patterns of high seawater warming. As detailed in Comments 12– variability within the climate system temperatures. The effects of greater 16, we received numerous comments that cannot currently be modeled, and ocean warming (e.g., increased related to ocean warming threats to potentially other factors (IPCC, 2013). bleaching, which kills or weakens corals that focused on the following As explained above, the major sources colonies) are expected to interact with aspects: (1) General future projections of of uncertainty in climate change the effects of higher storm intensity ocean warming levels; (2) accounting for projections such as AR4 or AR5’s WGI (e.g., increased breakage of dead or spatial variability; (3) the future decline are: (1) The projected rate of increase for weakened colonies), resulting in an of coral reefs because of increasing GHG GHG concentrations; (2) strength of the increased rate of coral declines. emissions; (4) the possibility of wide climate’s response to GHG Likewise, ocean acidification and ranging responses by coral reef concentrations; and (3) large natural nutrients may reduce thermal ecosystems; (5) the specific effects of variations. The slow-down in warming thresholds to bleaching, increase ocean warming on reef-building corals; since 1998 is an example of a large mortality, and slow recovery. and (6) the capacity of reef-building natural variation that could not be There is also mounting evidence that corals for acclimatization and predicted, at least by the models at that warming ocean temperatures can have adaptation to ocean warming. time. direct impacts on early life stages of With regard to the future projections Comment 12 identified several corals, including abnormal embryonic of global climate change, the proposed sources of spatial variability in ocean development at 32 °C and complete rule and supporting documents warming and requested our fertilization failure at 34 °C for one assumed that AR4’s highest-emission consideration of additional information. Indo-Pacific Acropora species. In scenario A1FI was the most likely. As The proposed rule acknowledged both addition to abnormal embryonic discussed in Global Climate Change— spatial and temporal variability in ocean development, symbiosis establishment, General Overview, we assume that for warming and considered the effect that larval survivorship, and settlement corals RCP8.5 is the most impactful variability would have on the proposed success have been shown to be impaired pathway for present to the year 2100. corals. However, we acknowledge that in Caribbean brooding and broadcasting Ocean warming projections and supplemental information has since coral species at temperatures as low as implications for coral reefs are become available, and we consider it 30 °C–32 °C. Further, the rate of larval described above in the RCP8.5 here. Regional and local variability in development for spawning species is Projections section. ocean warming conditions may lead to appreciably accelerated at warmer Comment 12 also criticized our lack warming-induced bleaching that is more temperatures, which suggests that total of consideration of the post-1998 hiatus or less severe regionally or locally than dispersal distances could also be in global warming. The proposed rule globally. A hot spot of ocean warming reduced, potentially decreasing the did not consider this phenomenon as occurs in the equatorial western Pacific likelihood of successful settlement and the issue was only emerging during the where regional warming is higher than the replenishment of extirpated areas. time the proposed rule was drafted. overall warming in the Indo-Pacific, Finally, warming will continue However, because supplemental exposing corals and coral reefs in this causing increased stratification of the information has become available since area to a higher risk of warming-induced upper ocean because water density that time, we consider it here. Despite bleaching. The hot spot overlaps the decreases with increasing temperature. unprecedented levels of GHG emissions Coral Triangle (Couce et al., 2013b; Increased stratification results in in recent years, a slow-down in global Lough, 2012; Teneva et al., 2012; van

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Hooidonk et al., 2013b). Several other the potential for mesophotic habitat to ecological functions (Hughes et al., areas in the Indo-Pacific have been provide refugia from ocean warming 2012; Pandolfi et al., 2011). Many identified as having lower than average (Bridge et al., 2013a; Smith et al., in factors contribute to the heterogeneous warming, including the western Indian press), although it does not always do so responses of coral reefs to climate Ocean, Thailand, the southern GBR, (Neal et al., 2013). Marginal habitats, change threats, including complexity central French Polynesia, and the such as high latitude sites, upwelling associated with coral reef habitat, as eastern equatorial Pacific, potentially regions, and turbid areas like the GBR well as the biology of reef-building coral resulting in relatively lower risk of inner shelf, also may provide refugia species themselves. As described in the warming-induced coral bleaching in from ocean warming for some species in Corals and Coral Reefs section, the these areas (Couce et al., 2013b; van some conditions (Browne et al., 2012; exceptional complexity, extent, and Hooidonk et al., 2013b). Spatial Couce et al., 2013b; Dalton and Roff, diversity of coral reef habitat increases variability in ocean warming is lower in 2013), but not others (Lybolt et al., the uncertainty associated with coarse the much smaller Caribbean, and there 2011). Taken together, mesophotic and modeling of reef responses to climate are fewer areas there with lower than marginal habitats may represent a change threats. Likewise, many aspects average warming (Buddemeier et al., network of refugia from ocean warming of reef-building coral biology contribute 2011). The regional and local for some species. to complex responses to ocean warming, heterogeneity in ocean warming likely Comment 14 emphasized both that including species-level processes such results in high variability in coral coral reefs are likely to decline sharply as capacity for acclimatization and responses across spatial scales (Selig et in the future because of increasing GHG adaptation (Palumbi et al., 2014), the al., 2010). emissions (e.g., Carpenter et al., 2008; potential for range expansion (Yamano There are several types of temporal Donner, 2009; Frieler et al., 2012; et al., 2011; Yara et al., 2011), and variability in ocean warming on coral Kiessling and Baron-Szabo, 2004) and community-level processes such as reefs. First, the rate of ocean warming that a wide range of responses by coral changes in competition and predation itself changes over time. For example, reef ecosystems are possible. Studies (Cahill et al., 2013; Hughes et al., 2012). ocean warming has increased in the provided by commenters, and others on These different processes occur Indo-Pacific since 1950, but at different recent modeling results (Frieler et al., simultaneously, and contribute to rates at different times (Lough, 2012). 2012; van Hooidonk and Huber, 2012; highly-variable, complex, and uncertain Second, different periods of ocean van Hooidonk et al., 2013b) and responses of reef-building coral species warming can result in variability in scientific opinion statements (Birkeland and in turn coral reefs to climate warming-induced bleaching at the same et al., 2013; ICRS, 2012) suggest changes threats like ocean warming. location. For example, a study in disastrous effects of ocean warming, in Moreover, management of local threats Thailand showed significant differences combination with other threats, on coral can increase resilience of coral reefs to in the susceptibility of coral taxa to reef ecosystems. For example, even in ocean warming and other global climate bleaching events between the years 1998 AR5 WGI’s best-case pathway (RCP2.6) change threats (Jackson et al., 2014; and 2010 and among coral species at the where CO2 equivalent concentrations Pandolfi et al., 2011), as described same site (Sutthacheep et al., 2013). peak at 455 ppm, one model suggests further in the Threats Evaluation— Spatial variability in ocean warming that 95 percent of coral reefs will Inadequacy of Existing Regulatory between sites also results in temporal experience annual bleaching conditions Mechanisms section. variability in ocean warming impacts, as by the end of the century (van Hooidonk the different areas are subsequently et al. 2013b). Another model suggests Comment 15 focused on the specific affected at different rates into the future that preserving more than 10 percent of effects of ocean warming on reef- (van Hooidonk et al., 2013b). For coral reefs worldwide would require building corals. The proposed rule example, a recent study found that limiting warming to less than 1.5 °C described the known specific effects of Australian subtropical reef-building above pre-industrial levels. Even ocean warming as well as the threats coral communities are affected by ocean assuming high adaptive capacity of that act simultaneously or sequentially, warming more slowly than tropical reef- corals and the more optimistic AR5 and whether the effects are cumulative building coral communities, resulting in pathways, the model suggests that one- (the sum of individual stresses) or slower rates of changes in the third of the world’s coral reefs are interactive (e.g., synergistic or subtropical than tropical communities projected to be subject to long-term antagonistic). The rapidly growing (Dalton and Roff, 2013). These studies degradation (Frieler et al., 2012). In literature on synergistic effects of ocean underscore the temporal variability of addition, the combined effects of ocean warming-induced bleaching with other ocean warming and warming-induced warming and ocean acidification would threats demonstrates that bleaching is bleaching across the ranges of reef- produce even more severe impacts on exacerbated by nutrients (Cunning and building coral species, complicating the coral reefs globally (van Hooidonk et al., Baker, 2013; Vega Thurber et al., 2013; interpretation of the effects of ocean 2013a; Yara et al., 2012). Wiedenmann et al., 2013), disease is warming on any given coral species These and other studies predict the exacerbated by warm temperatures and across its range and over time. irreversible disappearance of coral reefs bleaching (Ban et al., 2013; Bruno et al., Mesophotic and marginal habitats on a global scale in the next few 2007; Muller and van Woesik, 2012; serving as refugia from ocean warming decades. However, other recent studies Rogers and Muller, 2012), ocean are relatively new and potentially suggest that coral reef degradation warming and acidification may impact important considerations for the resulting from global climate change corals in opposite but converging ways vulnerability of coral species to ocean threats alone is likely to be a more (van Hooidonk et al., 2013a; Yara et al., warming. Mesophotic habitats continue spatially, temporally, and taxonomically 2012), and bleaching is exacerbated by to be explored, with new surveys heterogeneous process. These studies a variety of physical factors (Yee and finding larger habitat areas and greater indicate that coral reef ecosystems, Barron, 2010) or can be reduced by depth distributions for some reef- rather than disappear entirely as a result biological factors (Connolly et al., 2012; building corals (Blyth-Skyrme et al., of future impacts, will likely persist, but Fabricius et al., 2013). Other 2013; Bridge and Guinotte, 2012). with unpredictable changes in the information on species-specifics effects Supplemental information demonstrates composition of coral species and of ocean warming is provided in the

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Species-specific Information and since the Industrial Revolution because affects various coral life history events Determinations section below. observed bleaching responses are lower by, among other processes, causing Comment 15 focused on the potential than predicted by the warm temperature adult mortality, reducing sexual and capacity of reef-building corals for anomalies (Logan et al., 2013). A recent asexual reproductive success, and acclimatization and adaptation to ocean study of fast-growing, shallow water impairing colony growth. A diseased warming and provided several new coral species demonstrated that state results from a complex interplay of studies (Cahill et al., 2013; Guest et al., acclimatization and adaptive responses factors including the cause or agent 2012; Jones and Berkelmans, 2010) and allowed them to inhabit reef areas with (e.g., pathogen, environmental toxicant), some that we considered in the water temperatures far above their the host, and the environment. All coral proposed rule (Baker et al., 2004; expected tolerances (Palumbi et al., disease impacts are presumed to be Maynard et al., 2008; Pandolfi et al., 2014). Similar to the mechanisms of attributable to infectious diseases or to 2011). Identified mechanisms include coral acclimatization and adaptation poorly-described genetic defects. Coral symbiont shuffling (Baker, 2012; described above, there is a rapidly disease often produces acute tissue loss. Cunning et al., 2013; Ortiz et al., 2013; growing body of literature on the Other manifestations of disease in the Silverstein et al., 2012), symbiont responses of corals to ocean warming broader sense, such as coral bleaching shading by host pigments or tissue (Ateweberhan et al., 2013; Baker et al., from ocean warming, are incorporated (Mayfield et al., 2013; Smith et al., 2013; Bellantuono et al., 2012; Castillo under other factors (e.g., manmade 2013a), host genotype expression et al., 2012; Coles and Riegl, 2013; Penin factors such as ocean warming as a (Baums et al., 2013; Granados-Cifuentes et al., 2013). These studies help explain result of climate change). et al., 2013; Meyer et al., 2011), and host the capacity for reef-building corals to Coral diseases are a common and protein expression (Barshis et al., 2013; acclimatize and adapt to ocean warming significant threat affecting most or all Voolstra et al., 2011). As described in and warming-induced bleaching and coral species and regions to some the Corals and Coral Reefs section, the suggest some limited capacity. However, degree, although the scientific dynamic association of host coral and any such capacity is highly dependent understanding of individual disease symbiotic zooxanthellae and microbes on species, location, habitat type, and causes in corals remains very poor. The provides potential for acclimatization or many other factors. Available species- incidence of coral disease appears to be adaptation of some reef-building coral specific information on vulnerability to expanding geographically in the Indo- species to environmental changes. ocean warming and warming-induced Pacific, and there is evidence that corals Many recent studies provide evidence bleaching, including evidence of with massive morphology species are that certain reef-building coral acclimatization or adaptation, is not recovering from disease events in communities have acclimated or provided in the Species-specific certain locations. The prevalence of adapted to ocean warming, at least to Information and Determination sections disease is highly variable between sites some degree. The bleaching and below. and species. Increased prevalence and mortality of some colonies of a coral After considering this supplemental severity of diseases is correlated with species on a reef, followed by the information in addition to that which increased water temperatures, which recovery of hardier colonies, is the was available for the proposed rule, our may correspond to increased virulence process by which acclimatization and conclusion regarding ocean warming of pathogens, decreased resistance of adaptation of a species to ocean remains unchanged from the proposed hosts, or both. Moreover, the expanding warming occurs. Examples of bleaching, rule, in that we consider ocean warming coral disease threat may result from mortality, and recovery provide to be of high importance in contributing opportunistic pathogens that become information about the capacity for to extinction risk for the 65 corals in damaging only in situations where the acclimatization and adaptation. Several this final rule. However, we host integrity is compromised by such examples were provided in the acknowledge that the interpretation of physiological stress or immune proposed rule and supporting future ocean warming and warming- suppression. Overall, there is mounting documents (Diaz-Pulido et al., 2009; induced impacts to corals and coral evidence that warming temperatures Hueerkamp et al., 2001; Kayanne et al., reefs is associated with complexity and and coral bleaching responses are linked 2002). More recently, many relevant uncertainty, and that precise effects on (albeit with mixed correlations) with studies have become available on the individual species of reef-building increased coral disease prevalence and effects of the 1998 bleaching event. For corals are especially difficult to mortality. Complex aspects of example, in comparisons of 1998 and determine. The impact of ocean temperature regimes, including winter 2010 bleaching events and recovery in warming may be mediated by several and summer extremes, may influence southeast Asia, some coral species factors and the extent to which the disease outbreaks. Bleaching and coral demonstrated more resistance to extinction risk of a coral species is abundance seem to increase the bleaching in 2010, suggesting impacted by ocean warming depends on susceptibility of corals to disease acclimatization or adaptation to thermal its particular level of susceptibility, contraction. Further, most recent stress (Sutthacheep et al., 2013). In a combined with its spatial and research shows strong correlations study on an isolated reef in Australia, demographic characteristics in the between elevated human population recovery of coral cover occurred within context of worsening environmental density in close proximity to coral reefs 12 years of the 1998 bleaching event conditions out to 2100, which is and disease prevalence in corals. (Gilmour et al., 2013). In contrast, discussed in detail for each species in Although disease causes in corals studies in the U.S. Virgin Islands and the Species-specific Information and remain poorly understood, some general Florida demonstrated little if any Determinations section. patterns of biological susceptibility are recovery in the 10 to 12 years following beginning to emerge. There appear to be the 1998 bleaching event (Rogers and Disease (High Importance Threat, ESA predictable patterns of immune capacity Muller, 2012; Ruzicka et al., 2013). Factor C) across coral families, corresponding A recent analysis comparing observed Disease is considered under ESA with trade-offs with their life history versus predicted coral bleaching events Factor C—disease or predation. In the traits, such as reproductive output and suggests that corals may have already proposed rule we described the threat of growth rate. Both Acroporidae and responded adaptively to some warming disease as follows. Disease adversely Pocilloporidae have low immunity to

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disease. However, both of these families Burge et al. (2014) summarized the from one of these studies suggest the have intermediate to high reproductive current understanding of interactions hypothesized relationship between outputs. Both Faviidae and Mussidae among coral disease, elevated bleaching and disease events may be are intermediate to high in terms of temperature, and bleaching. This weaker than previously thought, and disease immunity and reproductive supplemental information provides more likely to be driven by common output. Finally, while Poritidae has high further insight of coral disease impacts responses to environmental stressors, immunity to disease, it has a low at the individual level and the local rather than directly facilitating one reproductive output. aggregation level, and provides future another. The effects of coral disease depend on predictions for the role of coral disease Ateweberhan et al. (2013) reviewed exposure of the species to the threat, at the population level. and summarized interactions between which varies spatially across the range At the individual level, recent studies important threats to corals. They note of the species and temporally over time. examine both underlying factors and that disease can interact not only with Exposure to coral disease is moderated mechanistic explanations for the ocean warming and bleaching events, by distance of some coral habitats from contraction and expansion of coral but may also be exacerbated by the primary causes of most disease disease. For example, one study sedimentation, nutrients, overfishing, outbreaks, such as stressors resulting investigated microbial community and destructive practices on coral reefs. from sedimentation and nutrient over- dynamics in the mucus layer of corals From a broad, population-wide enrichment. Exposure to coral disease to understand how the surface microbial perspective, Yakob and Mumby (2011) can also be moderated by depth of many community responds to changes in provide an important alternative context habitats, with deep habitats generally environmental conditions and under in which to demonstrate that high being less affected by disease outbreaks what circumstances it becomes population turnover within novel associated with stressors resulting from vulnerable to overgrowth by pathogens. ecosystems (those that are different from ocean warming. Disease exposure in They found that a transient thermal the past and created by climate change) remote areas and deep habitats appears anomaly can cause the microbial may enhance coral resistance to disease. to be low but gradually increasing. community to shift from a stable state They emphasize the need to move away Exposure to coral disease will increase dominated by antibiotic microbes to a from future projections based on as factors that increase disease stable state dominated by pathogens. historical trends and start to account for outbreaks (e.g., warming events) expand Beneficial microbes may not be able to novel behavior of ecosystems under over time. resume dominance after a temperature climate change. As explained above, disease may be disturbance until the environment After considering this supplemental caused by threats such as ocean becomes considerably more favorable information in addition to that which warming and bleaching, nutrients, and for them (Mao-Jones et al., 2010). was available for the proposed rule, our toxins. However, interactive effects Another study conducted a meta- conclusion regarding disease remains between independently-arising disease analysis to determine whether the unchanged from the proposed rule, in and other threats are also important, presence of particular microbial taxa that we consider coral disease to be of because diseased colonies are more correlates with the state of coral health high importance in contributing to susceptible to the effects of some other and found distinct differences in the extinction risk for the 65 corals in this threats. For example, diseased or microbial taxa present in diseased and final rule. The impact of disease may be recovering colonies may become more healthy corals (Mouchka et al., 2010). A mediated by several factors and the quickly stressed than healthy colonies third study investigated three variables extent to which the extinction risk of a by land-based sources of pollution commonly associated with immunity in coral species is impacted by disease (sedimentation, nutrients, and toxins), hard and soft corals spanning ten depends on its particular level of may more quickly succumb to families on the GBR. They found that all susceptibility, combined with its spatial predators, and may more easily break three variables (phenlyoxidase activity, and demographic characteristics in the during storms or as a result of other size of melanin containing granular context of worsening environmental physical impacts. cells, and fluorescent protein conditions out to 2100, which is Comments 17 and 18 discussed the concentrations) were significant discussed in detail for each species in importance of disease as a threat to predictors of susceptibility (Palmer et the Species-specific Information and corals and provided a few scientific al., 2010). Many other studies have Determinations section. studies (Harvell et al., 1999; Harvell et focused on bacterial or eukaryotic al., 2002; Muller and van Woesik, 2012; Ocean Acidification (Medium-High pathogens as the source of coral disease; Importance Threat, ESA Factor E) Rogers and Muller, 2012) to emphasize however, a more recent study examined this importance. Muller and van Woesik the role of viruses and determined that Ocean acidification is considered (2012) examined spatial epidemiology a specific group of viruses is associated under ESA Factor E—other natural or in the Caribbean to test if pathogens are with diseased Caribbean corals (Soffer et manmade factors affecting the contagious and spread from infected to al., 2013). continued existence of the species— susceptible hosts. They found no Several studies provide further because the effect is a result of human evidence of clustering for these diseases, evidence of disease outbreaks that were activity and affects individuals of the so they did not follow a contagious significantly correlated with bleaching coral species more so than their disease model. They suggest the events. The bleaching occurred first, habitats. In the proposed rule we expression of coral disease is a two-step then several months to a year later, there described that ocean acidification is a model: Environmental thresholds are were significant increases in disease result of global climate change caused exceeded, then those conditions either prevalence in bleached areas (Ban et al., by increased GHG accumulation in the weaken the coral or increase the 2013; Brandt and McManus, 2009; atmosphere. Reef-building corals virulence of the pathogen (Muller and Bruno et al., 2007; Croquer et al., 2006; produce skeletons made of the aragonite van Woesik, 2012). Croquer and Weil, 2009; Miller et al., form of calcium carbonate; thus, We also gathered supplemental 2009). The specific interactions between reductions in aragonite saturation state information on the threat of disease the two phenomena varied among caused by ocean acidification pose a since the proposed rule was published. disease-bleaching combinations. Results major threat to these species and other

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marine calcifiers. Ocean acidification ocean acidification on corals and their exposure to ocean acidification. The has the potential to cause substantial responses. Corals are able to regulate pH spatial variability in seawater pH occurs reduction in coral calcification and reef within their tissues, maintaining higher from reef to global scales, driven by cementation. Further, ocean pH values in their tissues than the pH numerous physical and biological acidification adversely affects adult of surrounding waters. This is an characteristics and processes, including: growth rates and fecundity, fertilization, important mechanism in naturally Seawater temperature; proximity to pelagic planula settlement, polyp highly-fluctuating environments (e.g., land-based runoff and seeps; proximity development, and juvenile growth. The many backreef pools have diurnally to sources of oceanic CO2; salinity; impacts of ocean acidification can lead fluctuating pH) and suggests that corals nutrients; photosynthesis; and to increased colony breakage and have some adaptive capacity to respiration. In cooler waters, CO2 fragmentation and mortality. Based on acidification. However, as with ocean absorption is higher, driving pH and observations in areas with naturally low warming, there is high uncertainty as to aragonite saturation state lower, thus pH, the effects of increasing ocean whether corals will be able to adapt relatively cool coral habitats are more acidification may also include potential quickly enough to the projected changes susceptible to acidification, such as reductions in coral size, cover, diversity, in aragonite saturation state. those at higher latitudes, in upwelling and structural complexity. In addition to the direct effects on areas, and in deeper environments. On As CO2 concentrations increase in the coral calcification and growth, ocean coral reefs, wave and wind-induced atmosphere, more CO2 is absorbed by acidification may also affect coral mixing typically maintain roughly the oceans, causing lower pH and recruitment, reef cementation, and other similar temperatures in the shallow reduced availability of carbonate ions, important reef-building species like photic zone preferred by most reef- which in turn results in lower aragonite crustose coralline algae. Studies suggest building corals, thus the deeper saturation state in seawater. Because of that the low pH associated with ocean environments that are more susceptible the increase in CO2 and other GHGs in acidification may impact coral larvae in to acidification are generally below this the atmosphere since the Industrial several ways, including reduced photic zone. Revolution, ocean acidification has survival and recruitment. Ocean Land-based runoff decreases salinity already occurred throughout the world’s acidification may influence settlement and increases nutrients, both of which oceans, including in the Caribbean and of coral larvae on coral reefs more by can raise pH. Local sources of oceanic Indo-Pacific, and is predicted to indirect alterations of the benthic CO2 like upwelling and volcanic seeps considerably increase between now and community, which provides settlement lower pH. Photosynthesis in algae and 2100, as described above in the RCP8.5 cues, than by direct physiological seagrass beds draws down CO2, raising Projections section. Along with ocean disruption. A major potential impact pH. High variability over various time- warming and disease, we considered from ocean acidification is a reduction scales is produced by numerous ocean acidification to be one of the most in the structural stability of corals and processes, including diurnal cycles of important threats posing extinction risks reefs, which results both from increases photosynthesis and respiration, seasonal to coral species between now and the in bioerosion and decreases in reef variability in seawater temperatures, year 2100; however, individual cementation. As atmospheric CO2 rises and decadal cycles in upwelling. susceptibility varies among the globally, reef-building corals are Temporal variability in pH can be very proposed species. expected to calcify more slowly and high diurnally in highly-fluctuating or Numerous laboratory and field become more fragile. Declining growth semi-enclosed habitats such as reef flats experiments have shown a relationship rates of crustose coralline algae may and back-reef pools, due to high between elevated CO2 and decreased facilitate increased bioerosion of coral photosynthesis during the day (pH goes calcification rates in some corals and reefs from ocean acidification. Studies up) and high respiration during the other calcium carbonate secreting demonstrate that ocean acidification night (pH goes down). In fact, pH organisms. However, because only a few will likely have a great impact on corals fluctuations during one 24-hr period in species have been tested for such and reef communities by affecting such reef-building coral habitats can effects, it is uncertain how most will community composition and dynamics, exceed the magnitude of change fare in increasingly acidified oceans. In exacerbating the effects of disease and expected by 2100 in open ocean addition to laboratory studies, recent other stressors (e.g., temperature), subtropical and tropical waters. As with field studies have demonstrated a contributing to habitat loss, and spatial variability in exposure to ocean decline in linear growth rates of some affecting symbiont function. Some warming, temporal variability in coral species, suggesting that ocean studies have found that an atmospheric exposure to ocean acidification is a acidification is already significantly CO2-level twice as high as pre-industrial combination of high variability over reducing growth of corals on reefs. levels will start to dissolve coral reefs; short time-scales together with long- However, this has not been widely this level could be reached as early as term increases. While exposure of the demonstrated across coral species and the middle of this century. Further, the proposed coral species to ocean reef locations, suggesting species- rate of acidification may be an order of acidification varies greatly both specific effects and localized variability magnitude faster than what occurred 55 spatially and temporally, it is expected in aragonite saturation state. A potential million years ago during the Paleocene- to increase for all species across their secondary effect is that ocean Eocene Thermal Maximum (i.e., the ranges between now and 2100. acidification may reduce the threshold period in which global temperatures Ocean acidification likely interacts at which bleaching occurs. Overall, the rose 5 to 9 °C, providing a context in with other threats, especially best available information demonstrates which to understand climate change). considering that ocean acidification is that most corals exhibit declining While CO2 levels in the surface waters expected to continue to increase over calcification rates with rising CO2 of the ocean are generally in equilibrium the foreseeable future. For example, concentrations, declining pH, and with the lower atmosphere, there can be ocean acidification may reduce the declining aragonite saturation state, considerable variability in seawater pH threshold at which bleaching occurs, although the rate and mode of decline across reef-building coral habitats, increasing the threat posed by ocean can vary among species. Recent studies resulting in colonies of a species warming. One of the key impacts of also discuss the physiological effects of experiencing high spatial variability in ocean acidification is reduced

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calcification, resulting in reduced in seawater around coral reefs (Shaw et synergistic effects (Ateweberhan et al., skeletal growth and skeletal density, al., 2013). On larger scales, a recent 2013; Dove et al., 2013; Kroeker et al., which may lead to numerous interactive study demonstrated that some coastal 2013), but not all (Wall et al., 2013). effects with other threats. Reduced areas of the Gulf of Mexico and South However, impacts of ocean acidification skeletal growth compromises the ability Atlantic were buffered against ocean are more rapid in cool water, such as in of coral colonies to compete for space acidification because of the input of mesophotic habitat (Cerrano et al., 2013) against algae, which grows more quickly fresh, alkaline surface waters carrying and temperate areas (Yara et al., 2012). as nutrient over-enrichment increases, dissolved inorganic carbon (Wang et al., especially if not held in check by 2013). Variability in ocean acidification Several other recent papers also herbivores. Reduced skeletal density at basin and global scales is influenced provide information on the impacts of weakens coral skeletons, resulting in largely by upwelling and latitude, with ocean acidification on reef-building greater colony breakage from natural more acidification in areas of high corals. A study of the effects of ocean and human-induced physical damage. upwelling and lower temperatures. The acidification on primary polyps with As discussed in Comments 18–21, we interaction of ocean acidification with and without zooxanthellae found that received numerous comments related to ocean warming produces basin-level polyps with zooxanthellae had higher the threat to corals from ocean patterns of higher and lower habitat tolerance to ocean acidification, acidification including: (1) The suitability for reef-building corals suggesting that coral species that overview and future projections of (Couce et al., 2013b; van Hooidonk et acquire symbionts from the ocean acidification; (2) variability in al., 2013a; Yara et al., 2012). environment will be more vulnerable to ocean acidification; and (3) specific Comments 19 and 20 underscore ocean acidification than corals that effects of ocean acidification on reef- specific effects to corals from ocean maternally acquire symbionts (i.e., building corals. acidification identified in the proposed brooding species; Ohki et al., 2013). A Comment 17 stated that we rule, including: (1) Effects on reef study of Porites corals at a field site with oversimplified the complexity and accretion; (2) effects on larvae and naturally low pH found that the corals variability in the future projections of juvenile corals; (3) interactive effects were not able to acclimatize enough to ocean acidification, and criticized our with other environmental variables; and prevent the impacts of local ocean reliance on AR4 as the basis for our (4) miscellaneous effects. Recent acidification on their skeletal growth threat evaluation. In the proposed rule, research identifies impacts of ocean and development, despite spending we acknowledged the uncertainty acidification on reef accretion due to their entire lifespan in low pH seawater associated with projections of ocean reduced coral calcification (Chan and (Crook et al., 2013). A study of the acidification from global climate Connolly, 2013) and impacts on effects of ocean acidification on change. However, while there are many crustose coralline algae (Doropoulos and sources of uncertainty in climate change Diaz-Pulido, 2013). Recent research has different coral species in different projections, and likewise for ocean also found that impacts of ocean environments found that effects were acidification, the ocean acidification acidification on brooded larvae of highly species-dependent, and projections in AR4 and AR5’s WGI Pocillopora damicornis were higher furthermore, that effects within a represent the best available information. when the larvae were released earlier species depended on the environment The proposed rule and supporting (Cumbo et al., 2013) and that (Kroeker et al., 2013). documents assumed that AR4’s highest- nutritionally replete juvenile corals After considering this supplemental emission scenario A1F1 was the most were less susceptible to ocean information in addition to that which likely to occur. Now that AR5’s WGI is acidification than nutritionally deprived was available for the proposed rule, our available, we consider the most juveniles (Drenkard et al., 2013). conclusion regarding ocean acidification impactful pathway to coral is WGI’s Many recent studies have investigated remains unchanged from the proposed RCP8.5, which includes ocean the interactive effects of ocean rule, in that we consider ocean acidification projections. These acidification with other environmental acidification to be of medium-high projections are described above in the variables. The opposing effects of ocean importance in contributing to extinction RCP8.5 Projections section, along with warming and ocean acidification were risk for the 65 corals in this final rule. two independent analyses of the effects discussed in a study that demonstrated However, we acknowledge that the of ocean acidification projections in low light conditions can exacerbate interpretation of future ocean RCP8.5 on coral reefs in the 21st ocean acidification effects. Low-light acidification and acidification-induced century. As noted in the RCP8.5 conditions can provide a refuge for reef- impacts to corals and coral reefs is Projections section, there is uncertainty building corals from thermal and light associated with complexity and in these ocean acidification projections stress, but this study suggests that lower for coral reefs. light availability will potentially uncertainty and that the effects on Comment 18 specifically cites increase the susceptibility of key coral individual species of reef-building Manzello et al. (2012) and Palacios and species to ocean acidification (Suggett et corals are especially difficult to Zimmerman (2012; 2007) to illustrate al., 2013). Another study predicts that determine. The impact of ocean that variability in ocean acidification on increasing storms predicted by climate acidification may be mediated by coral reefs can be buffered by local and change, together with ocean several factors and the extent to which regional biogeochemical processes acidification, are likely to increase the extinction risk of a coral species is within seagrass beds. Additionally, collapse of table corals (Madin et al., impacted by ocean acidification biogeochemical processes within coral 2012). Salinity extremes on a nearshore depends on its particular level of reef communities (Andersson et al., coral community did not affect the susceptibility, combined with its spatial 2013) may buffer the effects of sensitivity of reef-building corals to and demographic characteristics in the decreasing pH. Other scientific studies ocean acidification (Okazaki et al., context of worsening environmental identify mechanisms that can exacerbate 2013). Finally, several studies have conditions out to 2100, which is changes in seawater pH around coral investigated the simultaneous effects of discussed in detail for each species in reefs from ocean acidification, such as ocean warming and ocean acidification, the Species-specific Information and diurnal variability that can amplify CO2 most of which have found harmful Determinations section.

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Trophic Effects of Fishing (Medium attachment. Additionally, macroalgae from one coral colony to another as they Importance Threat, ESA Factor A) can suppress the successful colonization transit and consume from each coral Trophic effects of fishing are of the substrate by corals through colony. With increasing abundance, considered under ESA Factor A—the occupation of the available space, they transmit disease to higher present or threatened destruction, shading, abrasion, chemical poisoning, proportions of the corals within the modification, or curtailment of its and infection with bacterial disease. population. habitat or range—because the main Overfishing can have further impacts Comments 21–23 focused on the effect of concern is to limit availability on coral mortality via trophic cascades. following aspects of the trophic effects of habitat for corals. In the proposed In general larger fish are targeted, of reef fishing: (1) The importance of the rule we described the threat of the resulting in fish populations of small threat to coral reefs; (2) higher individuals. For parrotfishes, the effect importance localized threats; and (3) trophic effects of reef fishing as follows. of grazing by individuals greater than 20 consideration of human demography. Fishing, particularly overfishing, can cm in length is substantially greater Comment 21 highlighted Keller et al. have large scale, long-term ecosystem- than that by smaller fish. Up to 75 (2009), which provides additional level effects that can change ecosystem individual parrotfishes with lengths of support for the importance herbivores structure from coral-dominated reefs to about 15 cm are necessary to have the play in the maintenance of recruitment algal-dominated reefs (‘‘phase shifts’’). same reduction in algae and promotion habitat. Further, recent information Even fishing pressure that doesn’t rise to of coral recruitment as a single shows that one of the most detrimental the level of overfishing potentially can individual 35 cm in length. Species effects of unsustainable fishing pressure alter trophic interactions that are richness of the herbivorous fish is the alteration of trophic interactions important in structuring coral reef population is also very beneficial to that are particularly important in ecosystems. These trophic interactions maintaining available substrate structuring coral reef ecosystems include reducing population abundance potentially leading to enhanced coral (Jackson et al., 2012; Jackson et al., of herbivorous fish species that control populations. Because of differences in 2014; Ruppert et al., 2013). These algal growth, limiting the size structure their feeding behaviors, several species trophic interactions include reducing of fish populations, reducing species of herbivorous fishes with population abundance of herbivorous richness of herbivorous fish, and complementary feeding behaviors can fish species that control algal growth, releasing corallivores from predator have a substantially greater positive limiting the size structure of fish control. Thus, an important aspect of effect than a similar biomass of a single populations, reducing species richness maintaining resilience in coral reef species on reducing the standing stock of herbivorous fish, and releasing ecosystems is to sustain populations of of macroalgae, of increasing the cover of corallivores from predator control. herbivores, especially the larger scarine crustose coralline algae, and increasing Thus, an important aspect of herbivorous wrasses such as parrotfish. live coral cover. maintaining resilience in coral reef On topographically complex reefs, Exposure to the trophic effects of ecosystems is to sustain functional population densities can average well fishing in the Caribbean may be populations of herbivores, especially the over a million herbivorous fishes per moderated by distance of some coral larger parrotfish and other key 2 km , and standing stocks can reach 45 habitats from fishing effort. Exposure to functional herbivorous fish (Hughes et metric tons per km2. In the Caribbean, the trophic effects of fishing in the Indo- al., 2010; Jackson et al., 2012; Jackson et parrotfishes can graze at rates of more Pacific is likely more moderated by al., 2014; Kennedy et al., 2013). Further, than 150,000 bites per square meter per distance than in the Caribbean, due to Jackson et al. (2014) considers day, and thereby remove up to 90–100 a greater proportion of reef-building overfishing (associated with high percent of the daily primary production coral habitats located in remote areas human densities) to be one of the major (e.g., algae). Under these conditions of away from fishing effort. Exposure to causes of the region-wide decline in topographic complexity with substantial the trophic effects of reef fishing may Caribbean corals while acknowledging populations of herbivorous fishes, as also moderated by depth of many that climate threats are likely to be long as the cover of living coral is high habitats in both regions, but again more major sources of mortality in the future. and resistant to mortality from so in the Indo-Pacific than in the In addition to direct overfishing of environmental changes, it is very Caribbean. Deep habitats are generally primary consumers such as parrotfish, unlikely that the algae will take over less affected by the trophic effects of recent studies found that overfishing of and dominate the substrate. However, if fishing, especially in the Indo-Pacific. top reef predators such as sharks and herbivorous fish populations, Exposure to the trophic effects of fishing other predatory fish, such as large particularly large-bodied parrotfish, are will increase as the human population groupers in the Caribbean, can have an heavily fished and a major mortality of increases over time. impact that cascades down the food coral colonies occurs, then algae can The trophic effects of fishing are chain, potentially contributing to grow rapidly and prevent the recovery likely to interact with many other mesopredator release, and ultimately of the coral population. The ecosystem threats, especially considering that altering the numbers of primary can then collapse into an alternative fishing impacts are likely to increase consumers available to control algal stable state, a persistent phase shift in within the ranges of many of the growth (Jackson et al., 2012; Jackson et which algae replace corals as the proposed corals over the foreseeable al., 2014; Ruppert et al., 2013). dominant reef species. Although algae future. For example, when carnivorous After considering this supplemental can have negative effects on adult coral fishes are overfished, corallivore information in addition to that which colonies (e.g., overgrowth, bleaching populations may increase, resulting in was available for the proposed rule, our from toxic compounds), the ecosystem- greater predation on corals. Further, conclusion regarding the trophic effects level effects of algae are primarily from overfishing appears to increase the of fishing remains unchanged from the inhibited coral recruitment. frequency of coral disease. Fishing proposed rule. Trophic effects of fishing Filamentous algae can prevent the activity usually targets the larger apex are a medium importance threat in colonization of the substrate by planula predators. When predators are removed, assessing global extinction risk for the larvae by creating sediment traps that corallivorous butterfly fishes become 65 corals in this final rule. Because the obstruct access to a hard substrate for more abundant and can transmit disease main effect of trophic effects of reef

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fishing is habitat alteration, there are no that sedimentation poses to the corals stressors including disease and climate species-specific levels of exposure and under consideration, human activity has factors such as bleaching susceptibility susceptibility. However, the extent to resulted in quantifiable increases in and reduced calcification (Ateweberhan which an individual species’ sediment inputs in some reef areas. et al., 2013; Suggett et al., 2013). MPAs recruitment is affected is discussed in Continued increases in coastal human provide little protection against indirect more detail in the Species-specific populations combined with poor land stressors like sedimentation from Information and Determinations section, use and nearshore development upland activities (Halpern et al., 2013). when species-specific information is practices will likely increase sediment The effects of sedimentation can be available. delivery to reef systems. Nearshore variable for different coral species and sediment levels will also likely increase may depend on other environmental Sedimentation (Low-Medium with sea-level rise. Greater inundation conditions (Blakeway et al., 2013; Importance Threat, ESA Factors A and of reef flats can erode soil at the Suggett et al., 2013). E) shoreline and resuspend lagoon After considering this supplemental Sedimentation is considered under deposits, producing greater sediment information in addition to that which ESA Factor A—the present or transport and potentially leading to was available for the proposed rule, our threatened destruction, modification, or leeward reefs being flooded with turbid conclusion regarding sedimentation curtailment of its habitat or range—and lagoon waters or buried by off-bank remains unchanged from the proposed ESA Factor E—other natural or sediment transport. Sediment stress and rule. Sedimentation is a low to medium manmade factors affecting the turbidity also can induce bleaching, importance threat in assessing global continued existence of the species— although some corals may be more extinction risk for the 65 corals in this because the effect of the threat, resulting tolerant of elevated short-term levels of final rule. The impact of sedimentation from human activity, is both to limit the sedimentation. may be mediated by several factors and availability of habitat for corals and to Exposure to sedimentation can be the extent to which the extinction risk directly impact individuals of coral moderated by distance of some coral of a coral species is impacted by species. In the proposed rule we habitats from areas where sedimentation sedimentation depends on its particular described the threat of sedimentation as is chronically or sporadically heavy, level of susceptibility combined with it follows. Human activities in coastal and resulting in some habitats being spatial and demographic characteristics inland watersheds introduce sediment unaffected or very lightly affected by in the context of worsening into the ocean by a variety of sedimentation. Exposure to environmental conditions out to 2100, mechanisms, including river discharge, sedimentation for particular species which is considered for each species in surface runoff, groundwater seeps, and may also be moderated by depth of the Species-specific Information and atmospheric deposition. Humans also habitats. Exposure to sedimentation is Determinations section. introduce sewage into coastal waters expected to increase as human activities Nutrients (Low-Medium Importance through direct discharge, treatment that produce sedimentation expand over Threat, ESA Factors A and E) plants, and septic leakage. Elevated time. sediment levels are generated by poor Sedimentation is also likely to Nutrient enrichment is considered land use practices and coastal and interact with many other threats, such under ESA Factor A—the present or nearshore construction. as other land-based sources of pollution threatened destruction, modification, or The most common direct effect of and warming-induced bleaching, curtailment of its habitat or range—and sedimentation is deposition of sediment especially considering that ESA Factor E—other natural or on coral surfaces as sediment settles out sedimentation is likely to increase manmade factors affecting the from the water column. Corals with across the ranges of many of the 65 continued existence of the species— certain morphologies (e.g., mounding) species over the foreseeable future. For because the effect of the threat, resulting can passively reject settling sediments. example, when coral communities that from human activity, is both to limit the In addition, corals can actively displace are chronically affected by availability of habitat for corals and sediment by ciliary action or mucous sedimentation experience a warming- directly impact individuals of coral production, both of which require induced bleaching event, a disease species. In the proposed rule we energetic expenditures. Corals with outbreak, or a toxic spill, the described the threat of nutrient over- large calices (skeletal component that consequences for those corals can be enrichment as follows. Elevated holds the polyp) tend to be better at much more severe than in communities nutrients affect corals through two main actively rejecting sediment. Some coral not affected by sedimentation. mechanisms: Direct impacts on coral species can tolerate complete burial for Comment 25 underscored the physiology and indirect effects through several days. Corals that are importance of sedimentation as a nutrient-stimulation of other unsuccessful in removing sediment will considerable local threat to corals, and community components (e.g., be smothered and die. Sediment can highlighted the potential of macroalgal turfs and seaweeds, and also induce sublethal effects, such as sedimentation to interact and filter feeders) that compete with corals reductions in tissue thickness, polyp potentially exacerbate other threats. A for space on the reef. Increased nutrients swelling, zooxanthellae loss, and excess few commenters provided references can decrease calcification; however, mucus production. In addition, (Bonkosky et al., 2009; Herna´ndez- nutrients may also enhance linear suspended sediment can reduce the Delgado et al., 2012; Hernandez-Delgado extension, while reducing skeletal amount of light in the water column, et al., 2011) that discussed density. Either condition results in making less energy available for coral sedimentation as a threat to corals. corals that are more prone to breakage photosynthesis and growth. We also gathered supplemental or erosion, but individual species do Sedimentation also impedes fertilization studies on the threat of sedimentation have varying tolerances to increased of spawned gametes and reduces larval since the proposed rule was published. nutrients. The main vectors of settlement and survival of recruits and Three points in particular from the anthropogenic nutrients are point- juveniles. proposed rule were affirmed by the source discharges (such as rivers or Although it is difficult to supplemental studies. Sedimentation sewage outfalls) and surface runoff from quantitatively predict the extinction risk can have interactive effects with other modified watersheds. Natural processes,

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such as in situ nitrogen fixation and symbionts were more susceptible to caused by coastal inundation. The best delivery of nutrient-rich deep water by bleaching. available information suggests that sea internal waves and upwelling also bring We also gathered supplemental level will continue to rise due to nutrients to coral reefs. information on how elevated nutrients thermal expansion and the melting of Exposure to nutrients can be interact with other threats, including land and sea ice. Theoretically, any rise moderated by distance of some coral coral bleaching and disease. One study in sea-level could potentially provide habitats from areas where nutrients are tested the interactive effects of nutrient additional habitat for corals living near chronically or sporadically heavy (e.g., loading with both bleaching and disease the sea surface. Many corals that inhabit heavily populated areas). However, and found that coral disease prevalence the relatively narrow zone near the nutrient over-enrichment can still result and severity as well as coral bleaching ocean surface have rapid growth rates from sparsely populated areas; and were increased in nutrient enriched when healthy, which allowed them to these nutrients can be quickly plots (Vega Thurber et al., 2013). keep up with sea-level rise during the transported large distances. Therefore, Ateweberhan et al. (2013) note that most past periods of rapid climate change distance is less of a moderating factor studies on the subject of nutrient associated with deglaciation and for nutrients than for sedimentation. enrichment and high temperatures also warming. However, depending on the Similarly, although nutrient exposure present evidence of negative effects on rate and amount of sea-level rise, rapid may also be moderated by the depth of calcification due to higher nutrient rises can lead to reef drowning. Rapid some habitats, nutrient impacts extend levels, although both positive and rises in sea level could affect many of deeper than sedimentation impacts. negative effects have been reported. the proposed coral species by both Exposure to nutrients is expected to Nutrient enrichment can also interact submerging them below their common increase as human activities that with the threat of coral disease by depth range and, more likely, by produce nutrients expand over time. encouraging the proliferation of disease- degrading water quality through coastal Nutrients are likely to interact with causing microorganisms and bioeroders, erosion and potentially severe many other threats, especially such as boring sponges, and intensifying sedimentation or enlargement of lagoons the growth of fleshy macroalgae that considering that nutrient over- and shelf areas. Rising sea level is likely harbor and spread coral diseases enrichment is likely to increase across to cause mixed responses in the 65 (Ateweberhan et al., 2013; Vega Thurber the ranges of many of the 65 corals over corals depending on their depth et al., 2013). preferences, sedimentation tolerances, the foreseeable future. For example, After considering this supplemental when coral communities that are growth rates, and the nearshore information in addition to that which topography. Reductions in growth rate chronically affected by nutrients was available for the proposed rule, our experience a warming-induced due to local stressors, bleaching, conclusion regarding nutrient over- infectious disease, and ocean bleaching event, a disease outbreak, or enrichment remains unchanged from acidification may prevent the species a toxic spill, the consequences for corals the proposed rule. Nutrients are a low from keeping up with sea-level rise (i.e., can be much more severe than in to medium importance threat in from growing at a rate that will allow communities not affected by nutrients. assessing global extinction risk for the them to continue to occupy their Comment 26 supported and reiterated 65 corals in this final rule. The impact preferred depth range despite sea-level the effects nutrients can have on corals. of elevated nutrients may be mediated rise). Some of the individual commenters by several factors and the extent to provided studies (Bonkosky et al., 2009; which the extinction risk of a coral The rate and amount of future sea- Connolly et al., 2012; Cunning and species is impacted by nutrient level rise remains uncertain. Until the Baker, 2013; Fabricius et al., 2013; enrichment depends on its particular past few years, sea-level rise was Hernandez-Delgado et al., 2011; level of susceptibility, combined with predicted to be in the range of only Herna´ndez-Delgado et al., 2008; its spatial and demographic about one half meter by 2100. However, Me´ndez-La´zaro et al., 2012; characteristics in the context of more recent estimated rates are higher, Wiedenmann et al., 2013) to reinforce worsening environmental conditions based upon evidence that the Greenland their support. Bonkosky et al. (2009) out to 2100, which is considered for and Antarctic ice sheets are much more provided further evidence that elevated each species in the Species-specific vulnerable than previously thought. turbidity and nutrient enrichment from Information and Determinations section. While there is large variability in human waste discharge has an extensive predictions of sea-level rise, AR4 likely impact on coral reef ecosystems. In Sea-Level Rise (Low-Medium Threat, underestimated the rates under all response to contradictory results from ESA Factor A) scenarios. other studies as to whether nutrients Sea-level rise is considered under Fast-growing branching corals were increase thermal stress or increase ESA Factor A—the present or able to keep up with the first 3 m of sea- resistance to higher temperature for threatened destruction, modification, or level rise during the warming that led to corals, Fabricius et al. (2013) exposed curtailment of its habitat or range— the last interglacial period. However, corals to both elevated nutrients and because the effect of the threat is to the whether the 65 corals in this final rule heat stress. They found higher mortality availability of corals’ habitat and not will be able to survive 3 m or more of occurred in the elevated nutrient-heat directly to the species themselves. In the future sea-level rise will depend on stress treatments versus heat-stressed proposed rule we described the threat of whether growth rates are reduced as a alone and controls. Wiedenmann et al. sea-level rise as follows. The effects of result of other risk factors, such as local (2013) found that unfavorable ratios of sea-level rise may act on various coral environmental stressors, bleaching, dissolved inorganic nutrients in the life history events, including larval infectious disease, and ocean water column led to phosphate settlement, polyp development, and acidification. Additionally, lack of starvation of symbiotic algae, reducing juvenile growth, and can contribute to suitable new habitat, limited success in thermal tolerance. Cunning and Baker adult mortality and colony sexual recruitment, coastal runoff, and (2013) found higher nutrient loads can fragmentation, mostly due to increased coastal hardening will compound some lead to higher densities of symbionts, sedimentation and decreased water corals’ ability to survive rapid sea-level and corals with higher densities of quality (reduced light availability) rise.

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This threat is expected to final rule. The impact of sea-level-rise corallivorous species decline with disproportionately affect shallow areas may be mediated by some factors and depth. Exposure to predation can adjacent to degraded coastlines, as the extent to which the extinction risk increase over time as conditions change, ocean inundation results in higher of a coral species is impacted by sea- but may be moderated by distance and levels of sedimentation from the newly- level-rise depends on its particular level depth for certain species, which inundated coastlines to the shallow of susceptibility, combined with its depends upon the distribution and areas. Exposure to sea-level rise will be spatial and demographic characteristics abundances of the species. moderated by horizontal and vertical in the context of worsening Predation of coral colonies can distances of reef-building coral habitats environmental conditions out to 2100, increase the likelihood of the colonies from inundated, degraded coastlines. which is considered for each species in being infected by disease, and likewise Exposure to sea-level rise will increase the Species-specific Information and diseased colonies may be more likely to over time as the rate of rise increases. Determinations section. be preyed upon. There are likely other Sea-level rise is likely to interact with examples of cumulative and interactive other threats, especially considering that Predation (Low Threat, ESA Factor C) effects of predation with other threats to sea-level rise is likely to increase across Predation is considered under ESA corals. the ranges of the 65 corals over the Factor C—disease or predation. In the Comment 28 suggested predation and foreseeable future. In particular, the proposed rule we described the threat of exposure values for some individual inundation of developed areas (e.g., predation as follows. Predation on some species, but did not provide urban and agricultural areas) and other coral genera by many corallivorous supplemental information on the threat. areas where shoreline sediments are species of fish and invertebrates (e.g., We also gathered supplemental easily eroded by sea-level rise is likely snails and seastars) is a chronic, though information that supports and reiterates to degrade water quality of adjacent occasionally acute, energy drain. It is a the analysis presented in the proposed coral habitat through increased threat that has been identified for most rule. Bonaldo et al. (2011) documented sediment and nutrient runoff and the coral life stages. Thus, predation spatial and temporal variation in coral potential release of toxic contamination. factored into the extinction risk analysis predation by parrotfishes on the Great Comment 27 supported the Consensus for each of the 65 corals. Numerous Barrier Reef. Lenihan et al. (2011) Statement on Climate Change and Coral studies have documented the assessed the degree to which the Reefs, which specifies that sea-levels quantitative impact of predation by performance of recently recruited have already risen and that future rising various taxa on coral tissue and branching corals was influenced by sea-levels will be accompanied by skeleton. Predators can indirectly affect several factors, including corallivory. increased sedimentation levels. We the distribution of corals by They found that partial predation by received no additional supplemental preferentially consuming faster-growing corallivorous fishes is an important but information on this threat. coral species, thus allowing slower- habitat-modulated constraint for We also gathered supplemental growing corals to compete for space on branching corals and, overall, information to update the analysis the reef. The most notable example of corallivory had variable effects on corals presented in the proposed rule. In the predation impacts in the Indo-Pacific of different genera. Last, De’ath et al. proposed rule, we noted that AR4 likely are from large aggregations or outbreaks (2012) documented that 42 percent of underestimated rates of projected sea- of crown-of-thorns seastar. The specific the decline in coral cover on the GBR level rise. AR5’s WGI represents a cause of crown-of-thorns seastar is attributable to crown-of-thorns seastar substantial advance from AR4. The first outbreaks is unknown. Crown-of-thorns predation. section of WGI considers observations of seastar can reduce living coral cover to After considering this supplemental climate system change, which refers to less than one percent during outbreaks, information in addition to that which descriptions of past climate patterns. changing coral community structure, was available for the proposed rule, our WGI concludes it is virtually certain promoting algal colonization, and conclusion regarding predation remains that the global mean sea level rose by 19 affecting fish population dynamics. unchanged from the proposed rule. cm from 1901 to 2010. The Exposure to predation by corallivores Predation is a low importance threat in anthropogenic ocean warming observed is moderated by presence of predators of assessing global extinction risk for the since the 1970s has contributed to the corallivores. For example, 65 corals in this final rule. The impact global sea-level rise over this period corallivorous reef fish prey on corals, of predation may be mediated by several through ice melting and thermal and piscivorous reef fish and sharks factors and the extent to which the expansion. Projections for future sea- prey on the corallivores; thus, high extinction risk of a coral species is level-rise in RCP8.5 for the period 2081 abundances of piscivorous reef fish and impacted by predation depends on its to 2100 are 0.53 to 0.97 meter higher sharks moderate coral predation. particular level of susceptibility than the period 1986 to 2005. In Abundances of piscivorous reef fish and combined with its spatial and addition, WGI concluded that it is sharks vary spatially because of demographic characteristics in the virtually certain that global mean sea- different ecological conditions and context of worsening environmental level rise will continue beyond 2100. human exploitation levels. Exposure to conditions out to 2100, which is WGI also reported that it is very likely predation is also moderated by distance considered for each species in the that in the twenty-first century and from physical conditions that allow Species-specific Information and beyond, sea-level change will have a corallivore populations to grow. For Determinations section. strong regional pattern (IPCC, 2013). example, in the Indo-Pacific, high After considering this supplemental nutrient runoff from continents and Collection and Trade (Low Threat, ESA information in addition to that which high islands improves reproductive Factor B) was previously available, our conditions for crown-of-thorns seastar, Collection and trade is considered conclusion regarding sea-level rise thus coral predation by crown-of-thorns under ESA Factor B—overutilization for remains unchanged from the proposed seastar is moderated by distance from commercial, recreational, scientific, or rule. Sea-level rise is a low to medium such conditions. Predation can also be educational purposes. In the proposed importance threat in assessing global moderated by depth of many habitats rule, we described the threat of extinction risk for the 65 corals in this because abundances of many collection and trade as follows.

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Globally, 1.5 million live stony coral (Thornhill, 2012; Wood et al., 2012). We directly resulting from collection colonies are reported to be collected define aquaculture as the land-based practices (Thornhill, 2012). from at least 45 countries each year, (‘ex situ’) propagation or grow out of The rapid increase of coral reef with the United States consuming the corals. Examples of this include corals species entering markets in the United largest portion of live corals (64 percent) grown in home aquaria or terrestrial States and Europe and the sustainability and live rock (95 percent) for the coral farms. We define mariculture as of the aquarium trade in terms of aquarium trade. The imports of live the ocean-based (‘in situ’) propagation driving collection of wild specimens corals taken directly from coral reefs or grow out of corals. Examples of this have been of great concern to (not from aquaculture) increased by 600 include corals grown in coral farms and governments, scientists, percent between 1988 and 2007, while nursery areas in marine environments. conservationists, and conscientious the global trade in live coral increased The phrase ‘‘captive culture’’ is used aquarium hobbyists alike (Olivotto et by nearly 1,500 percent. Harvest of interchangeably to refer to captive al., 2011; Rhyne and Tlusty, 2012). stony corals is usually highly breeding of corals, both via aquaculture However, production of marine wildlife destructive, and results in removing and or mariculture techniques. for home aquaria (i.e., the aquarium discarding large amounts of live coral The ecological and socio-economic hobbyist trade) through captive culture that go unsold and damaging reef impacts of the ornamental trade is an increasingly growing sector of the habitats around live corals. While industry for corals are numerous, and ornamental trade industry. Recently, collection is a highly spatially-focused can include overharvesting, collateral advances in both aquaculture and impact, it can result in significant damage to coral reef habitat, and mariculture propagation techniques impacts and was considered to potential introduction of exotic species show promise in shifting the demand of contribute to individual species’ (Rhyne et al., 2012). Wild collection of the ornamental trade industry away extinction risk. However, we ultimately stony corals is usually highly from wild-collected corals to corals ranked this threat as low overall because destructive, resulting in removing and reared via captive-culture techniques. of species-specific factors (i.e., some discarding large amounts of live coral Such techniques are possible since species are preferentially affected) as that often go unsold for various reasons. many corals, especially fast-growing well as distance and depth factors that Additionally, collection techniques can branching corals, are capable of asexual create barriers to human access. be physically damaging to reef habitat reproduction via a process known as As described in Comments 29 and 30, around live corals. In a recent, thorough fragmentation or ‘‘fragging’’ (Brainard et al., 2011; Rhyne et al., 2012). According we received a significant amount of review of ecological impacts and supplemental information via public to CITES import and export reports, practices of the coral reef wildlife trade, comments and gathered supplemental maricultured corals accounted for Thornhill (2012) identifies and information on three aspects of the approximately 20 percent of total live describes five overarching potential threat of collection and trade on reef- trade in 2010 (Wood et al. 2012), but impacts: (1) Effects on target population building corals and coral reef other studies suggest that captive- such as over-exploitation and local ecosystems: (1) Wild collection of cultured corals account for only 2 population extirpations; (2) habitat corals, including information about the percent of the live coral trade impacts such as reduced coral cover, physical and ecological impacts of wild (Thornhill, 2012). diversity, and rugosity; (3) effects on collection of coral colonies and/or Globally, there are approximately two associated species such as decreased fragments from their natural habitats; (2) million aquarium hobbyists involved in captive culture including information abundance, biomass, and diversity of a complex trade network that sells an regarding the development of reef fish, invertebrates, and other estimated 50 million corals every year to mariculture and aquaculture operations, species due to loss or destruction of use (Rhyne et al., 2012). According to as well as the role of home aquaria as habitat; (4) ecosystem impacts such as the Florida Department of Agriculture they relate to trade, including all increased degradation and erosion and Consumer Services, there are 87 commercial, recreational, and leading to reduced resilience; and (5) certified aquaculture facilities listing educational coral-raising operations in socio-economic impacts such as user corals as a product in Florida alone. The marine environments as well as in group conflict between tourists, fishers, study hypothesized that a notable captivity; and (3) the global marine etc. decline in U.S. imports of corals ornamental trade industry, including Collection and trade of coral colonies occurred after 2006 as a result of detailed information regarding trade of can also increase the likelihood of the increased domestic coral production as both live and dead corals and other colonies being infected by disease, as a well as the global economic downturn. coral reef wildlife. result of both the directed and Import reports do not account for this For the purposes of this final rule, incidental breakage of colonies, which ‘‘hidden’’ domestic production, and collection and trade refers to the are then more easily infected (Brainard statistical tracking of this type of coral physical process of taking corals from et al., 2011). Further, destructive production is lacking (Rhyne et al., their natural habitat on coral reefs for practices for collection of other coral 2012). In addition to increasing the purpose of sale in the ornamental reef wildlife, such as the use of cyanide domestic production of corals, some trade industry. We define wild for capturing reef fish, can also have major source countries such as collection as the physical removal or deleterious effects on coral reef habitat Indonesia are increasing production via capture of coral colonies, fragments, and in general. Currently, cyanide fishing is mariculture activities to reduce wild polyps from their natural habitat. This practiced in 15 countries, many of collection pressure on coral reefs, and section also discusses the use of captive which are major marine wildlife trade supporting coral farming as a potential breeding techniques via aquaculture and exporters (Thornhill, 2012). There are alternative to fishing for reef fish and mariculture for the purposes of trade. likely many other examples of collection of wild corals (Pomeroy et al., Captive culture techniques are cumulative and interactive effects of 2006). For example, according to 2009 increasingly used to supply the collection and trade that pose a threat to U.S. import reports, 26 percent of aquarium trade industry and potentially corals. Given the paucity of data for the Acropora species were identified under reduce the amount of corals collected coral reef wildlife trade, it is difficult to CITES codes which indicated that these from the wild to meet demand accurately estimate mortality rates colonies were produced via captive-

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culture techniques (Rhyne et al., 2012). in size, and can be fragmented into represents a small portion of the coral However, since CITES codes are self- many smaller pieces. Additionally, reef wildlife trade, and public aquaria determined by exporter countries, there reporting of trade volume is inconsistent likely produce as many corals as they may be some inconsistencies in how and varies between reporting pieces and consume by using captive-culture those codes are applied (Wood et al., weight, and live rock and corals are techniques (Thornhill, 2012). 2012). As of 2008, there were 55 coral often confused with each other and There has been some significant farms scattered throughout the different misreported (Thornhill, 2012). progress in captive culture of coral provinces of Indonesia (Timotius et al., Currently, Indonesia is the primary species using aquaculture and/or 2009); however, this number may be source country of live corals; it exports mariculture for the purposes of trade. increasing since Indonesia’s government approximately one million corals Still, commercial-scale production of has mandated companies and traders annually and represents an estimated 91 most species currently suffers several involved in the coral trade to utilize percent of the global supply market as technical bottlenecks, including the captive culture techniques in hopes of of 2005 (Bruckner and Borneman, 2006; long and often arduous supply chain eventually phasing out wild collection Thornhill, 2012; Timotius et al., 2009). from ocean to aquarium (e.g., capture, of corals. Other major exporters of scleractinian collection, handling, and transport), There are a number of challenges corals include Fiji, Solomon Islands, which often results in mortality ranging associated with developing aquaculture Tonga, and Australia. The largest from a few percent up to 80 percent. For or mariculture operations for coral importers of coral reef wildlife include example, in an analysis of confiscated species, including technical capacity the United States, European Union, and coral shipments, a majority of the corals and know-how, high capital Japan. The United States accounted for were found in poor condition. On the investments and operating costs, and an average of 61 percent of global way to their final destination, coral high levels of production risk (Ferse et imports from 2000–2010 (Wood et al., colonies may experience significant al., 2012; Pomeroy et al., 2006). 2012). Imports of live corals into the temperature drops in the shipping Culturing corals has not been an easy United States taken directly from coral water, poor water quality, and physical task, predominantly due to the lack of reefs (not from aquacultured or damage from repeated handling of the knowledge regarding reproductive and maricultured sources) increased by 600 shipping boxes and bags resulting in larval biology for most traded species percent between 1988 and 2007, while mortality of a large proportion of (Olivotto et al., 2011). Further, most the global imports of live coral colonies through subsequent bacterial mariculture operations tend to focus increased by nearly 1,500 percent infections (Jones, 2008). These non- predominantly on fast-growing corals, (Brainard et al., 2011; Thornhill, 2012; reported rates of biomass loss may while successful propagation techniques Tissot et al., 2010). Import and export significantly underestimate the for the popular slow-growing, large- data shows overall increasing trends for ecological impacts of the trade as more polyp species have not yet been trade of live coral pieces between 2000– corals are collected to make up the developed (Wood et al., 2012). There is 2009, with a slight dip in 2010 (Wood losses (Cohen et al., 2013; Thornhill, also the increasingly popular trend of et al., 2012). In addition, 2012). Distinguishing between using ocean-based coral nurseries for undocumented, illegal live coral trade is specimens collected under regulated the purposes of propagating coral estimated to represent approximately 25 conditions from those collected using fragments to a suitable size and percent of the legal trade level, although illegal or destructive fishing practices is very difficult (Cohen et al., 2013; subsequently out-planting those coral these numbers are difficult to estimate fragments on degraded reefs to aid in Wabnitz, 2003). considering the secretive nature of the reef restoration efforts. These types of Traceability and tracking of cultured illegal trade (Jones, 2008; Thornhill, activities are also considered in the corals versus wild-collected corals is 2012). Conservation Efforts section of the rule. extremely difficult as there is no The export of marine organisms for The international coral trade was morphological or biological difference the ornamental trade industry is a global established by 1950 and was dominated between them, making distinction industry. As described in the proposed by the Philippines until 1977 when a almost impossible (Olivotto et al., 2011). rule, it is estimated that 1.5 million live national ban on wild collection and For example, a coral can be broken into stony coral colonies are collected from export was introduced (Wood et al., fragments and labeled as cultured, when at least 45 countries each year, with an 2012). It was then that Indonesia in fact it was collected from the wild. estimated 11 to 12 million coral pieces surpassed the Philippines to provide the There is some evidence to suggest that (i.e., fragments from larger colonies) majority of corals to the market. In the culture of live corals has the potential traded every year (Brainard et al., 2011; 1980s and 1990s, the international coral to affect trends in the trade industry by Wabnitz, 2003). In addition to live stony trade still focused on the trade of dead reducing wild collection and provide an corals, approximately 13 to 40 million coral skeletons for home de´cor and economically and financially feasible reef fish, four million pounds of dead curios. In recent years, the focus has alternative livelihood for local coral skeleton, and nine to 10 million shifted to live corals for the marine reef communities in the Indo-Pacific. Even other invertebrates are extracted from aquarium trade due to increased interest so, coral mariculture development in coral reef ecosystems across the world in home aquaria and advances in coral the Indo-Pacific is still in its infancy (Thornhill, 2012). For corals, trade can husbandry in North America and and requires a number of conditions to be broken down into several categories, Europe, as well as the advent of modern be met in order for these operations to including: Coral rock (i.e., rock and air cargo methods (Rhyne et al., 2012; be commercially profitable, sustainable, substrate that may have live settled Thornhill, 2012; Wood et al., 2012). As and traceable (Cohen et al., 2013; coral polyps among other marine stated previously, there is a complex Pomeroy et al., 2006). It is also organisms), live wild coral, live global trade network of approximately important to note that not all species maricultured coral, and dead coral two million aquarium hobbyists that lend themselves to culture. In fact, only skeleton. Yet, numbers of corals traded sells upwards of 50 million coral reef a small number of coral genera have the in these categories are very difficult to animals every year (Rhyne et al., 2012). ability to be commercially cultured accurately estimate for a variety of Collection of corals for display in public (Rhyne et al., 2012). According to some reasons. First, corals are colonial, vary aquaria for educational purposes sources, approximately 98 percent of

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live corals in the ornamental trade are and trade activities for the 65 corals candidate coral species in the proposed still collected from the wild, with only proposed for ESA listing was considered rule. 2 percent originating from captive bred to be ‘‘low’’ (Brainard et al., 2011). After The Final Management Report sources such as coral farms and considering this supplemental identified existing regulatory nurseries (Ferse et al., 2012; Thornhill, information in addition to that which mechanisms that were relevant to the 2012), but, according to a different was available for the proposed rule, our threats to coral species. It was organized analysis of import reports between 2000 conclusion regarding the threat of in two sections: (1) Existing regulatory and 2010, captive cultured corals made collection and trade remains unchanged mechanisms that are relevant to up approximately 20 percent of total from the proposed rule. Collection and addressing global-scale threats to imports, and these originated almost trade is a low importance threat in addressing other threats to corals. The entirely from Indonesia (Wood et al., assessing global extinction risk for the proposed rule summarized the 2012). Therefore, there are still 65 corals in this final rule, and even less information from that report as follows. significant data deficiencies and a large so for the seven Caribbean species due Greenhouse gas emissions are amount of uncertainty as to how much to undesirable appearance and growth regulated through multi-state of an impact captive cultured corals are characteristics for trade. The impact of agreements, at the international level, having on the ornamental trade. collection and trade may be mediated by and through statutes and regulations, at Significant supplemental information several factors and the extent to which the national, state, or provincial level. was received in public comments on the the extinction risk of a coral species is One of the key international agreements proposed rule or otherwise gathered on impacted by collection and trade relevant to attempts to control GHG collection and trade of coral species. As depends on its particular level of emissions, the Copenhagen Accord, was previously described in the SRR and susceptibility, combined with its spatial developed in 2009 by the Conference of proposed rule, there are numerous and demographic characteristics in the Parties to the United Nations ecological impacts from the physical context of worsening environmental Framework Convention on Climate process of removing corals and other conditions out to 2100, which is Change. The Copenhagen Accord wildlife from the reef. Trade practices considered for each species in the identifies specific information provided that rely on the collection of wild Species Information and Determinations by Parties on quantified economy-wide individuals may damage or destroy section. Information regarding the emissions targets for 2020 and on adult and juvenile reef corals. adequacy of regulations related to the nationally appropriate mitigation Additionally, removal of reef fish and actions to the goal of capping increasing marine ornamental trade such as CITES ° other organisms for trade purposes may and other laws can be found in the average global temperature at 2 C above also result in ecological impacts to reef Local Regulatory Mechanisms section of pre-industrial levels. Overall, the proposed rule concluded that existing ecosystems (Brainard et al., 2011). The the Final Management Report (NMFS, regulatory mechanisms with the ten most popular coral genera involved 2012b). Additionally, coral restoration objective of reducing GHG emissions in the ornamental trade by volume are: projects using ocean-based, nursery- were inadequate to prevent the impacts Acropora (Indo-Pacific only), Euphyllia, reared corals are also becoming to corals and coral reefs from ocean Goniopora, Trachyphyllia, Plerogyra, increasingly popular as a complement to warming, ocean acidification, and other Montipora, Heliofungia, Lobophyllia, existing management tools. Information climate change-related threats. After an Porites, and Turbinaria (Jones, 2008; related to the roles that coral farms, in-depth analysis of international Thornhill, 2012), all of which represent coral nurseries, and aquaria (both public 31 of the coral species considered in agreements to curb GHG emissions and and private) play in coral reef this final rule. Acropora species are in their respective progress, it appeared conservation is discussed in the the highest demand followed by the unlikely that Parties would be able to Conservation Efforts sub-section of the large polyp species such as Euphyllia collectively achieve, in the near term, rule. (Jones, 2008). Culturing corals through climate change avoidance goals outlined aquaculture and/or mariculture Inadequacy of Existing Regulatory via international agreements. techniques is becoming an increasingly Mechanisms (ESA Factor D) Additionally, none of the major global popular tool to help move the aquarium initiatives appeared to be ambitious trade away from collection of wild Regulatory mechanisms are enough, even if all terms were met, to corals. Still, these techniques are fairly considered under Factor D—Inadequacy reduce GHG emissions to the level new and in need of many improvements of Existing Regulatory Mechanisms. As necessary to minimize impacts to coral before being considered a viable previously described in the proposed reefs and prevent what are predicted to solution in shifting market demand from rule, we developed a Draft Management be severe consequences for corals wild-collected to captive cultured Report to assess the contribution of worldwide. The evidence suggested that corals. As it currently stands, the ‘‘inadequacy of regulatory mechanisms’’ existing regulatory mechanisms at the amount of unreported, illegal, and to the extinction risk of corals. The Draft global scale in the form of international unregulated collection, combined with Management Report identified: (1) agreements to reduce GHG emissions the large amount of biomass loss along Existing regulatory mechanisms relevant were insufficient to prevent widespread the supply chain raises serious to threats to the 82 candidate coral impacts to corals. questions as to the sustainability of the species; and (2) conservation efforts Existing regulatory mechanisms ornamental trade (Cohen et al., 2013). with regard to the status of the 82 directly or indirectly addressing the Overall, collection and trade of coral candidate coral species. This Draft was localized threats identified in the reef wildlife is considered to contribute peer reviewed and released with the proposed rule (i.e., those threats not to some individual species’ extinction SRR in April 2012, with a request for related to GHGs and global climate risk. any information that we may have change) are primarily national and local In our previous analysis, collection omitted. We incorporated all of the fisheries, coastal, and watershed and trade were generally considered to information we received into the Final management laws and regulations in the be a threat to coral reefs, as well as Management Report, which formed the 84 countries within the collective ranges particular individual coral species, but basis of our evaluation of this factor’s of the 82 coral species. Because of the extinction risk as a result of collection effect on the extinction risk of the 82 large number of threats, and the

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immense number of regulatory Updates to adequacy of global some additions of various local laws as mechanisms in the 84 countries, we regulatory mechanisms; (2) updates to well as supplemental information concluded in the proposed rule that a adequacy of local regulatory regarding regulations pertaining to regulation-by-regulation assessment of mechanisms; and (3) local management collection and trade of coral species. In adequacy was not possible. as it applies to reef resilience. addition, to better capture the breadth Furthermore, with the exception of Since the release of the Final and scope of existing regulatory Acropora palmata and A. cervicornis in Management Report, there have been mechanisms on a species-by-species the Caribbean, there was not enough two additional conferences of the basis, we evaluated the presence and information available to determine the Parties to the United National scope of five different categories of effects of specific regulatory Framework Convention on Climate regulatory mechanisms in each of the 84 mechanisms on individual coral Change. In 2012, the Parties met in countries throughout the ranges of the species, given the lack of information on Doha, Qatar, and they met again in 65 corals in this final rule. These specific locations of individual species Warsaw, Poland in 2013. The resulting categories of laws include: General (the adequacy of existing local decisions from both meetings were protection of corals, reef fishing, marine regulatory mechanisms relevant to primarily to continue ongoing efforts to protected areas, wild collection, and threats impacting the Caribbean reach a new agreement for emissions pollution. acroporids was evaluated in detail in reductions to be adopted at the 2015 For each coral species, we considered those species’ 2005 status review, and meeting in Paris, and to have those the relevant national laws, regulations, that information is incorporated into implemented by 2020. The new and other similar mechanisms that may this rule’s final findings for those agreement would maintain the same reduce any of the threats described in species). However, general patterns overall goal as the Copenhagen Accord, our threat analyses for all countries in included: (1) Fisheries management to cap additional warming at 2 °C. which the coral species has confirmed regimes regulate reef fishing in many Within the United States, President records of occurrence. To find each parts of the collective ranges of the Barack Obama released the President’s country where our 65 coral species have proposed coral species, albeit at varying Climate Action Plan in June 2013. The confirmed occurrence we used Veron’s levels of success; (2) laws addressing plan is three-pronged, including updated report on the listed coral land-based sources of pollution are less proposed actions for mitigation, species and their occurrence in various effective than those regulating fisheries; adaptation, and international ecoregions (Veron, 2014). In considering (3) coral reef and coastal marine leadership. The actions listed for countries’ regulatory mechanisms, we protected areas have increased several- mitigation include completing carbon give strongest weight to statutes and fold in the last decade, reducing some pollution standards for new and existing their implementing regulations and to threats through regulation or banning of power plants, accelerating clean energy management direction that stems from fishing, coastal development, and other permitting, increasing funding for clean those laws and regulations. activities contributing to localized energy innovation and technology, In analyzing local regulatory threats; and (4) the most effective increasing fuel economy standards, mechanisms available for each coral regulatory mechanisms address the increasing energy efficiency in homes species, five general categories emerged: threats other than climate change. We businesses and factories, and reducing General coral protection, coral generally concluded that because the other GHG emissions including collection control, fishing controls, local threats have impacted and hydrofluorocarbons and methane. The pollution controls, and managed areas. continue to impact corals across their plan states that the United States is still General coral protection regulatory ranges, collectively, the existing committed to reducing GHG emissions mechanisms include overarching regulations were not preventing or 17 percent below 2005 levels by 2020 if environmental laws that may protect controlling local threats. Further, there all other major economies agree to corals from damage, harm, and was insufficient information to similar reductions. Additional efforts destruction, and specific coral reef determine if an individual species was made domestically related to climate management laws. In some instances, impacted by inadequacy of individual change are more focused on facilitating these general coral protection regulatory existing regulations. adaptation to the impending changes to mechanisms are limited in scope We received public comments and the environment due to climate change because they apply only to certain areas supplemental information on the in order to maintain the country’s or only regulate coral reef damage and inadequacy of existing regulatory natural and economic resources, but do do not prohibit it completely. mechanisms. As a result, we not directly address the emission of Coral collection regulatory incorporated any information we GHGs. mechanisms include specific laws that received into this final rule, which As described in the proposed rule, prohibit the collection, harvest, and supplemented the basis for our final existing regulatory mechanisms directly mining of corals. In some instances, analysis and determination of the or indirectly addressing all of the these coral collection regulatory inadequacy of existing regulatory localized threats identified in the SRR mechanisms are limited in scope mechanisms in each species (i.e., those threats not related to GHGs because they apply only to certain areas determination. and global climate change) are primarily or are regulated but not prohibited. Comments 31–33 provided national and local fisheries, coastal, and Pollution control regulatory supplemental information, which we watershed management laws and mechanisms include oil pollution laws, incorporated into this final rule. regulations in the 84 countries within marine pollution laws, ship-based Specifically, we received information on the collective ranges of the 65 coral pollution laws, and coastal land use and how local management actions species. This final rule incorporates any development laws. In some instances, potentially confer resilience benefits to information we received via public pollution regulatory mechanisms are coral reef ecosystems. The public comment regarding recent local limited in scope because they apply comments and supplemental regulatory mechanisms or local only to certain areas or to specific information on the inadequacy of regulatory mechanisms that were either sources of pollution. existing regulatory mechanisms are previously mischaracterized or Fishing regulatory mechanisms discussed below in three sections: (1) inadvertently omitted. This includes include fisheries regulations that pertain

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to reefs or regulations that prohibit ecosystems survive predicted increases resilience (Burke et al., 2011; Keller et explosives, poisons and chemicals, in the frequency, duration, and severity al., 2009). electrocution, spearfishing, specific of mass coral bleaching events (Obura, In a 2013 global review of 10,280 mesh sizes of nets, or other fishing gear. 2005) and may help reduce the MPAs, it was found that approximately In some instances, fishing regulatory extinction risk of some individual coral 2.93 percent of the world’s oceans have mechanisms are limited in scope species. MPA coverage; however, coverage does because they apply only to certain areas, In terms of local management actions, not necessarily equate to protection. or not all reef-damaging fishing methods many acute disturbances such as coral Marine protected areas have often failed are prohibited, or reef-damaging fishing bleaching are out of the direct control of to prevent ongoing local threats such as methods are regulated but not reef managers and cannot be mitigated overfishing due to management and/or prohibited. directly. Actions that can be taken to design failure, as well as lack of local Managed area regulatory mechanisms build reef resilience and enhance reef support, poor compliance, and include the capacity to create national recovery include reducing physical inadequate resources to promote parks and reserves, sanctuaries, and disturbance and injury as a result of educational awareness and enforcement marine protected areas. In some recreational activities, managing local (Hughes et al., 2007; Hughes et al., 2010; instances, managed area regulatory watersheds and coastal areas to prevent Spalding et al., 2013). A study by the mechanisms are limited in scope, sedimentation and nutrient run-off, and World Resources Institute found that primarily because the managed area reducing fishing pressures on important only 6 percent of the world’s reefs occur in effectively managed MPAs (Burke et provides limited protection for coral herbivorous fish (Jackson et al., 2014; reefs, only small percentages of the al., 2011). Further, scientists are just Kennedy et al., 2013; Marshall and countries’ coral reefs are protected beginning to understand spatial patterns Schuttenberg, 2006; Mumby and within the managed areas, or the of coral responses to disturbance. Efforts Steneck, 2011). For example, a recent managed areas are not well to identify coral reef areas with the study shows that eutrophication can administered. greatest resilience are crucial for siting increase thermal stress on inshore reef The management results for each MPAs. This information has the communities and management actions species can be found in the Species- potential to assist in future MPA design to reduce coastal eutrophication can Specific Information and Determination and management so that resistant improve the resistance and resilience of section of this rule. It should be noted patches of coral reef can be protected to that while some of these regulatory vulnerable coastal coral reefs to ocean ensure continued connectivity and mechanisms were categorized as warming (Fabricius et al., 2013). subsequent recovery of nearby reefs that ‘‘limited in scope,’’ it does not Additionally, herbivorous fish play a are less resistant. These strategies of necessarily mean they are inadequate crucial role in the recovery of coral reefs tailoring management efforts across the under ESA section 4(a)(1) Factor D. after major disturbance events. Severe marine environment depending on We received a significant amount of warming and increases in ocean various responses to disturbance are information regarding the role of local acidification alone can reduce resilience still in their infancy, but it may management actions in building of coral reef ecosystems, particularly if eventually prove essential in adaptive resilience into reef ecosystems. This those systems are already subject to management of reef resources in the face section describes the emerging body of overfishing of the key functional groups of future climate change-related literature regarding the concept of reef of herbivorous reef fishes and nutrient disturbances (Mumby and Steneck, resilience, defined as an ecosystem’s loading (Anthony et al., 2011; Bellwood 2011). For these reasons, while MPAs capacity to absorb recurrent shocks or et al., 2004). Elevated populations of are an important tool in response to the disturbances and adapt to change herbivores have the potential to confer global degradation of coral reefs, they without compromising its ecological resilience benefits by encouraging should not be considered a panacea function or structural integrity. Until greater niche diversification and (Hughes et al., 2007). recently, the main drivers of coral reef creating functional redundancy. For In general, recent evidence suggests decline included overfishing of example, it has been demonstrated that that management of local scale herbivorous fish and nutrient loading two complementary herbivore species disturbances is essential to maintaining from agriculture and other land-based were more successful at controlling an adequate coral population density for sources of pollution. These stressors algal blooms than a single species on its successful reproduction and caused widespread changes in reef own, and management of herbivorous maintenance of genetic diversity and is ecosystems over the past couple of fish can help in reef regeneration after therefore crucial to maintaining centuries, and ultimately led to episodes of bleaching or disease that are complex, bio-diverse coral reef ecological shifts from coral-dominated impossible to locally regulate (Bellwood ecosystems, given the predicted systems to systems overrun by fleshy et al., 2004; Burkepile and Hay, 2008; widespread impacts of climate change algae. These localized disturbances are Roff and Mumby, 2012). Conversely, related threats (e.g., Anthony et al., now being compounded by climate even unexploited populations of 2011). The presence of effective local change related threats, including herbivorous fishes do not guarantee reef laws and regulations has the potential to increasingly frequent coral bleaching resilience; therefore, some reefs could help reduce impacts to coral reefs from events as a result of ocean warming. lose resilience even under relatively low threats on an ecosystem level, Many factors contribute to coral reef fishing pressure (Cheal et al., 2010). potentially extending the timeframe at ecosystem resilience, including Therefore, the entire suite of local which individual coral species may be ecosystem condition, biological threats and disturbances should be in danger of extinction by providing a diversity, connectivity between areas, minimized through local management protective temporal buffer (i.e., and local environmental conditions actions to ensure that reef resilience and resiliency). Some evidence suggests that (Marshall and Schuttenberg, 2006; recovery are also maximized. local management actions, particularly Obura, 2005). Implementing local Establishing MPA networks is generally of fisheries (specifically, no-take marine actions that either protect or strengthen accepted as one of the more common reserves) and watersheds, can enhance these resilience-conferring factors has management tools to help reduce the ability of species, communities, and the potential to help coral reef impacts to coral reefs and build ecosystems to tolerate climate change-

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related stressors, and potentially delay management actions may allow for coral that discuss the future impacts of reef loss by at least a decade under to persist while awaiting significant climate change on coral reefs indicate ‘‘business-as-usual’’ rises in GHG global progress to curb GHGs. Overall, variability in both the models emissions (Keller et al., 2008; Kennedy we maintain that in the absence of underlying these changes and the extent et al., 2013). In the Caribbean especially, effective global regulatory mechanisms of potential impacts to the coral local regulation of fisheries for to reduce impacts from climate change ecosystem. Recognizing uncertainty and herbivorous fish species (specifically to corals, the inadequacy of existing spatial variability in climate change parrotfish) is deemed one of the most regulatory mechanisms at global and projections, and the spatial variability in important local actions to safeguard local scales poses an extinction risk environmental conditions on coral coral reefs in the face of looming climate threat to all of the corals that are habitat, in our species determinations change threats (Jackson et al., 2014). It vulnerable to climate-related threats. we emphasize the role that also has been strongly suggested that heterogeneous habitat and spatial and Threats Evaluation Conclusion local management be combined with a demographic traits play in evaluating low-carbon economy to prevent further The above information on threats to extinction risk. We also consider in our degradation of reef structures and reef-building corals leads to several determinations that each species in this associated ecosystems (Birkeland et al., important overall points that apply both final rule experiences a wide variety of 2013; Kennedy et al., 2013). currently and over the foreseeable conditions throughout its range that After considering this supplemental future. First, the period of time over helps mitigate the impacts of global and information in addition to that which which individual threats and responses local threats to some degree. Finally, we was available for the proposed rule, our may be projected varies according to the don’t consider projections of impacts to conclusion regarding the inadequacy of nature of the threat and the type of coral reef ecosystems to definitively regulatory mechanisms addressing information available about that threat represent impacts to individual coral global threats to corals from GHG and the species’ likely response. The species, because coral reef communities emissions remains unchanged from the threats related to global climate change typically consist of dozens to hundreds proposed rule. That is, without any pose the greatest potential extinction of reef-building coral species, each of substantive changes in emissions risk to corals and have been evaluated which may respond differently to reduction pledges from any major with sufficient certainty out to the year environmental and ecological changes. economies and without any noteworthy 2100. Second, we expect an overall In addition, reef-building corals are not additional efforts to actually reduce increase in threats, especially those limited to occupying only coral reefs. GHG emissions, the supplemental related to global climate change as information considered in this final rule projected by RCP8.5 to 2100. Third, Risk Analyses regarding regulatory mechanisms does RCP8.5’s projections of conditions on Many factors can contribute to an not change the previous analysis. We coral reefs within the ranges of the individual species’ extinction risk. The reach the same conclusions regarding species covered by this rule over the process of extinction usually occurs in local regulatory mechanisms as foreseeable future are based on phases, first affecting individual described in the proposed rule, with the spatially-coarse analyses associated populations or sub-populations, and exceptions of Acropora palmata and A. with high uncertainty, in particular at then progressing to the species level. cervicornis. For these species, we have local spatial scales. Finally and most Extinction can occur as a result of incorporated into this final rule, the importantly, determining the effects of stochastic processes that affect birth and analysis of adequacy of regulatory global threats on an individual coral death and mortality from catastrophic mechanisms included in the 2005 status species over the foreseeable future is events. A species’ biological traits can review and 2006 listing of these species complicated by the combination of: (1) influence extinction risk both in terms as threatened. Those documents Uncertainty associated with projected of vulnerability to environmental concluded that existing regulatory ocean warming and acidification perturbations and effects on population mechanisms are inadequate to address threats; (2) regional and local variability dynamics. Extinction risk is also local and global threats affecting these in global threats; (3) large distributions influenced by depensatory effects, species, and as such are contributing to and high habitat heterogeneity of the which are self-reinforcing processes the threatened status of these species. species in this final rule; and (4) limited (i.e., positive feedbacks) that accelerate Because the local threats have species-specific information on species loss as its population density impacted and continue to impact corals responses to global threats. declines. across their ranges, we still generally Thus, in our species determinations, The proposed rule described our conclude that, collectively, the existing we recognize that the best available framework for evaluating extinction risk regulations are not currently preventing information indicates the impacts of and making listing determinations in or controlling local threats across the climate change will likely increase in the Risk Analyses section. There were entire range of any of the 65 species. We the foreseeable future. However, there multiple steps in our process of still do not have sufficient information are limitations to using this global, evaluating the listing status of each to determine if an individual species’ coarse-scale information for determining species. The initial step in developing extinction risk is exacerbated by vulnerability to extinction for the framework consisted of evaluating inadequacy of individual existing individual coral species. Climate change the ESA definitions of ‘‘endangered’’ regulations. On the other hand, the best projections over the foreseeable future and ‘‘threatened’’ and how those available information suggests that local are associated with three major sources definitions apply to corals. The management may confer resilience of uncertainty; (1) The projected rate of application of those definitions was benefits for coral reefs on an ecosystem increase for GHG concentrations; (2) based on the background of the Context level, which could extend the timeframe strength of the climate’s response to for Extinction Risk and General Threats at which individual coral species may GHG concentrations; and (3) large sections of the proposed rule. be at risk of extinction by providing a natural variations. The recent warming We then considered the elements that protective temporal buffer in the face of slow-down is an example of a large contribute to the extinction risk of climate change-related threats. That is, natural variation that was not corals in the Risk Analyses section of implementing effective local anticipated by previous models. Reports the proposed rule. The following is a list

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of the specific elements within their of time corresponding to the foreseeable including complexity and uncertainty, respective categories: (1) Vulnerability future is a function of the particular than was possible using the linear to threats, including each of the nine type of threats, the life-history Determination Tool in the proposed most important threats, based on a characteristics, and the specific habitat rule. In this section, we explain the final species’ susceptibility and exposure to requirements for the coral species under determination framework process that each of the threats; (2) demography, consideration. The timeframe we used to determine each of the including abundance, trends in established for the foreseeable future species’ statuses, how it is different abundance, and relative recruitment considered the time necessary to from the proposed rule, and how new rate; and (3) spatial structure, including provide for the conservation and and supplemental information was overall distribution, which is a recovery of each threatened species and incorporated. combination of geographic and depth the ecosystems upon which they In the proposed rule we described our distributions, and ocean basin. In order depend. It was also a function of the determination approach in the Risk to evaluate the best available reliability of available data regarding the Analyses and Detailed Description of information for each of the 82 candidate identified threats and extends only as Determination Tool Elements sections, corals and consider all elements in each far as the data allow for making in which we discussed the elements that of these categories, we developed a reasonable predictions about the affect a coral’s extinction risk. Below we Determination Tool to organize and species’ response to those threats. We describe how that determination consistently interpret the information in agreed with the BRT’s assessment that approach has been adapted for this final the SRR, FMR, and SIR and apply it to the threats related to climate change had rule and applied to the Statutory the definitions of threatened, been sufficiently characterized and Standards, in light of and in response to endangered, and not warranted species predicted through the end of this public comments. developed for corals, in a decision century. Therefore, in the proposed rule, Final Determination Framework framework that we developed to we determined the year 2100 to be the specifically apply to corals. appropriate outer limit of foreseeability Overview of Key Changes Applied in In the proposed rule, we linked the as to climate change-related threats. Final Determinations. We received major elements of our Risk Analyses, In the proposed rule, we evaluated many comments questioning the vulnerability to threats, demography, each species throughout its entire range, accuracy of the methods used to analyze and spatial structure, to the ESA listing because no SPOIRs were identified, and the available information to assess categories. We described endangered that assessment has not changed in the extinction risk and derive listing species as having a current extinction final rule as described further below in statuses for each of the proposed risk; they are highly vulnerable to one the Statutory Standards sub-section. species, including how the or more of the high importance threats While we did receive additional Determination Tool was used. After and have either already been seriously qualitative information on the considering these comments, and as adversely affected by one of these abundances and distributions of the 65 discussed above, our findings in the threats, as evidenced by a declining proposed species, nothing in that data proposed rule were influenced by how trend and high susceptibility to that indicated that any portions of the range we believed coral species would react to threat, or they lack a buffer to protect of any of the species warranted further environmental changes now and over them from serious adverse effects from evaluation under the applicable the foreseeable future. Given the current these threats in the future. We described standards of the final SPOIR Policy, as effects and projections of climate change threatened species as not currently discussed in the Statutory Standards impacts to the marine environment into being in danger of extinction, but are sub-section below. The last step in the foreseeable future and the likely to become so within the developing the proposed listing information we had at the time of the foreseeable future. They are highly or determinations was to evaluate proposed rule on coral response to moderately vulnerable to one or more of ‘‘Conservation Efforts’’ to determine if existing and predicted environmental the high importance threats or highly they would change the basis for listing stressors, we determined that many of vulnerable to one or more of the lower a species by alleviating threats or the coral species met the definition of importance threats, but have either not recovering populations. We concluded ‘‘endangered species’’ or ‘‘threatened yet exhibited effects in their populations that conservation efforts on global and species.’’ In explaining how the or they have the buffering protection of local scales did not change the status Determination Tool assessed risk and more common abundance or wider determined using our decision derived listing statuses we concluded overall distribution. We described not framework for any of the 82 candidate that, as some public comments warranted species as not being in danger species. suggested, the Determination Tool was of extinction currently and not likely to Comments 32–34 and 37–42 focused too linear and deterministic. This led to become so within the foreseeable future on four aspects of the listing listing determinations in the proposed because they have: Low vulnerability to determination process in the proposed rule that were based, in large part, on the high importance threats, or low or rule: (1) The Determination Tool, (2) the applying the endangered and threatened moderate vulnerability to all the lower foreseeable future, (3) the SPOIR standard to relative characteristics importance threats, and common analysis, and (4) conservation efforts. instead of applying the endangered and abundance or wide overall distribution. The comments we received identified threatened standard to each individual The proposed rule described the basis deficiencies in the proposed rule’s species independently to determine for our determination of the foreseeable Determination Tool, leading to a change their listing status. future for the purposes of projecting in our approach from a formulaic In this rule, we have changed our climate-related threats in the Threats framework to describe extinction risk, to determinations for many of the species Evaluation and Risk Analyses sections, a non-formulaic framework to describe for two general reasons: (1) Informed by and was supported by several other vulnerability to extinction. That is, the public comments, we refined the way sections (e.g., Global Climate Change— final determination framework we apply the available information to Overview). Consistent with our practice integrates different types of information determine vulnerability to extinction; for all species listing determinations, we in a holistic manner that better and (2) we received via public established that the appropriate period represents all the available information, comments, or gathered ourselves,

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information that expanded our existing conclusions about vulnerability to are limitations to using this global, knowledge. extinction. coarse-scale information for determining We received and gathered specific The final determination framework vulnerability to extinction for information about spatial, demographic, used in this final rule is composed of individual coral species. and other characteristics of individual seven elements. The first element is • In our species determinations, we coral species, and the public comments describing the statutory standards. The don’t consider projections of impacts to provided general scientific criticism second, third, fourth, and fifth elements coral reef ecosystems to definitively about how we weighed these factors. In are identifying and analyzing all the represent impacts to individual coral the proposed rule, we gave greater appropriate species-specific and general species, because coral communities consideration to susceptibility to threats characteristics that influence extinction typically consist of dozens to hundreds but did not fully recognize the extent to risk for a coral species. The sixth of coral species, each of which may which spatial, demographic, and other element is relating a species’ respond differently to environmental characteristics of corals can moderate characteristics to a particular extinction and ecological changes. vulnerability to extinction. After risk at appropriate spatial and temporal • Recognizing the uncertainty and considering all of the available scales. The seventh element is explicitly spatial variability in climate change information and public comments, in stating how each species’ extinction risk projections, and the spatial variability in this final rule we continue to recognize meets the statutory listing definitions as environmental conditions on coral the threats that the species face, but we applied to corals, resulting in an habitat, in our species determinations also place more emphasis on buffers ultimate listing status. A final we emphasize the role that against those threats and revisit the consideration in evaluating listing status heterogeneous habitat and absolute predicted population responses of is whether current or planned demographic and spatial characteristics individual species to the threats, giving conservation efforts improve the overall play in evaluating extinction risk. full consideration to their current status of any of the 65 species such that We have ordered the informational spatial, demographic, and other the additional protections of the ESA categories in the Species-specific characteristics. For example, we took are not warranted. Information and Determinations into account that many of the species, In moving to an integrated, non- sections below for clarity in describing when viewed on their own rather than formulaic framework, some of our key the species-specific elements and their in relation to other coral species or assumptions about vulnerability to interaction in contributing to each vertebrate species, have more extinction changed due to analyzing the species’ vulnerability to extinction as substantial absolute abundances than different aspects of each species’ follows: (1) Spatial Information—overall the prior methodology accounted for. characteristics independently (on an distribution and ocean basin, habitat; (2) We also took into account that in absolute scale), instead of being rated Demographic Information—abundance, many instances coral species occupy a with the other proposed corals species trends in abundance, relative wide range of habitats, including areas (on a relative scale). We rely on the recruitment rate; and (3) Susceptibility that can act as refugia from warming, following guiding principles extracted to threats based on a species’ which moderate the predicted impacts from each of the sections in the first part susceptibility to each of the nine threats. across coarse-scale areas. As explained of this rule, providing the context and Further, when information is available generally above, and in regard to background information for the species that does not fall into one of the individual species below, the species in determinations, in order to determine categories or elements identified above, this final rule will be negatively each species’ listing status: but is relevant to extinction risk, we impacted by future conditions, but in • Clonal, colonial organisms, such as provide it under the Other Biological light of our consideration of factors and corals, are vastly different in their Information category. In each species characteristics discussed above, we find biology and ecology than many other determination, we refer back to the they are not currently in danger of species listed by NMFS under the specific guiding principles that played a extinction and do not meet the Endangered Species Act. role in how we consider the species- definition of endangered. We do, • In our species determinations, we specific information and the sections in however, conclude that some species give appropriate consideration to the which they are described in more detail. are likely to become in danger of complex nature of coral biology and Statutory Standards extinction within the foreseeable future variability in responses to threats and thus meet the definition of between individual coral colonies and The definitions of endangered and threatened. We also find that listing is even between different portions of the threatened species under section 3 of not warranted for some species that same colony. the ESA, wherein (1) an ‘‘endangered were previously proposed for listing. • In our species determinations, species’’ is defined as ‘‘any species In this final rule, we acknowledge that absolute abundance and absolute which is in danger of extinction there are no recipes or formulas for distribution inform our evaluation of a throughout all or a significant portion of endangered, threatened, or not species’ current status and its capacity its range’’, and (2) a ‘‘threatened warranted coral species, especially to respond to changing conditions over species’’ is defined as ‘‘any species given the variability in coral species’ the foreseeable future. which is likely to become an biology and ecology, and the variability • The concept of heterogeneous endangered species in the foreseeable in available information from species to habitat influences extinction risk for all future throughout all or a significant species. Accordingly, the final species in this final rule because each portion of its range,’’ formed the basis framework allows for consideration of species experiences a wide variety of of our determination framework. each coral’s circumstances as a whole conditions throughout its range, which Considered at both the spatial and (simultaneously evaluating each allows for variable responses to global temporal scales applicable to each of species’ demography, spatial and local threats. those listing statuses, an endangered characteristics, threat susceptibilities, • We recognize that the best available species currently faces an extinction risk and current and future environmental information indicates the impacts of throughout all or a significant portion of conditions independently of the other climate change will likely increase in its range and a threatened species is species), leading us to species-specific the foreseeable future. However, there likely to become endangered throughout

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all or a significant portion of its range Foreseeable Future sub-section below in at higher extinction risk, such that its within the foreseeable future. In other the context of the particular species loss would render the entire species words, the primary statutory difference (corals) being considered for listing. endangered or threatened. An between a threatened and endangered Significant Portion of its Range evaluation is required only where there species is the timing of when a species (SPOIR). The ESA’s definitions of is information to suggest that a may be in danger of extinction, either ‘‘endangered species’’ and ‘‘threatened particular portion of the range is likely presently (endangered) or in the species’’ refer to two spatial scales, to be both ‘‘significant’’ as defined in foreseeable future (threatened). Further, providing that a species may be the policy and to qualify as endangered as discussed below, no significant imperiled ‘‘throughout all’’ of or ‘‘in a or threatened (79 FR 37586). portions of their ranges could be significant portion of’’ its range. 16 As described in the proposed rule, the determined for any of our proposed U.S.C. 1532(6); (20). NMFS has BRT did not identify any portions of the species; thus, the only spatial scale we interpreted the ‘‘significant portion of range for any of the 82 coral species as consider is each species’ entire range. its range’’ language in a policy that has being potentially ‘‘significant’’ or at a Court opinions produced in litigation recently been finalized. See ‘‘Final higher extinction risk. Because there challenging the listing of the polar bear Policy on Interpretation of the Phrase was a general lack of species-specific as threatened provides a thorough ‘Significant Portion of its Range’ in the data regarding quantitative abundance, discussion of the ESA’s definitions and Endangered Species Act’s Definitions of distribution, diversity, and productivity the Services’ broad discretion to ‘Endangered Species’ and ‘Threatened of coral species, we were not able to Species’ ’’ (79 FR 37578; July 1, 2014) identify any portions of any of the determine on a case-by-case basis (‘‘Final Policy’’). In developing our species’ ranges that could be considered whether a species is in danger of proposed rule, our analysis was unusually biologically significant. extinction (see, In Re Polar Bear informed by the Draft Policy that was Further, we had no information to Endangered Species Act Listing and published in December 2011 (76 FR indicate that particular local threats §4(d) Rule Litigation, 794 F. Supp.2d 65 76987; December 9, 2011). As we were more severe in a particular portion (D.D.C. 2011); aff’d, 709 F.3d 1 (D.C. Cir. explained in the proposed rule, we were of an individual species’ range. 2013); 748 F. Supp.2d 19 (D.D.C. 2010)). unable to identify any portions of the No supplemental information was The Court determined that the phrase species’ ranges that might require closer received in response to the proposed ‘‘in danger of extinction’’ is ambiguous. analysis as potential SPOIRs, due in rule that provides support for The Court held that there is a temporal large part to a lack of species-specific identification of a SPOIR for any of the distinction between endangered and information regarding abundance, proposed species. While we did receive threatened species in terms of the geographic distribution, diversity, and supplemental information on the proximity of the ‘‘danger’’ of extinction, productivity (77 FR 73247). qualitative abundances and noting that the definition of The Final Policy, which we must now distributions for some species, nothing ‘‘endangered species’’ is phrased in the apply, differs in two key respects from in that data suggests that any particular present tense, whereas a threatened the Draft Policy. Neither changes the portion of any proposed species range is species is ‘‘likely to become’’ so in the ultimate result in this case, which is unusually biologically significant. We future. However, the Court also ruled that no SPOIRs can be identified. First, do not have any information that would that neither the ESA nor its legislative the Final Policy specifies that no help elucidate whether any species is at history compels the interpretation of portions of a species’ range can be higher exposure to threats in a ‘‘endangered’’ as a species being in ‘‘significant,’’ and thus no SPOIR particular area of its range (i.e., where ‘‘imminent’’ risk of extinction. Thus, in analysis need be done, where the range- threats may be so acute or concentrated the context of the ESA, a key statutory wide status analysis leads to a that current conditions are likely to difference between a threatened and conclusion that listing the entire species render the species there at significantly endangered species is the timing of as threatened or endangered is higher risk of extinction than the overall when a species may be in danger of warranted. (Under the Draft Policy, even species). Thus, we did not identify any extinction, either now (endangered) or if a species were found to warrant SPOIR for any species, and so our in the foreseeable future (threatened). listing as ‘‘threatened,’’ the agency still determination as to each species is The Court ruled that although needed to consider whether any based on the best available information imminence of harm is clearly one factor portions of the range may be about the species’ status throughout its that the Services weigh in their significant). Second, the final policy range. decision-making process, it is not defines ‘‘significant’’ to include not only Foreseeable Future. The ‘‘foreseeable necessarily a limiting factor, and that those portions where the individuals are future’’ is integral to the definition of a Congress did not intend to make any so biologically significant that without threatened species. It is the timeframe single factor controlling when drawing them the entire species would meet the over which we evaluate a species’ the distinction between endangered and definition of ‘‘endangered’’ (the extinction risk if it is not currently in threatened species. In many cases, the standard in the Draft Policy), but also danger of extinction. As described in the Services might appropriately find that those portions whose loss would render proposed rule, the identification of the the imminence of a particular threat is the species ‘‘threatened.’’ foreseeable future is unique to every the dispositive factor that warrants In this case, our framework evaluates listing decision. It is based on the listing a species as ‘threatened’ rather each species throughout its range to particular type of threats, the life-history than ‘endangered,’ or vice versa. To be determine extinction risk. If a species is characteristics, and the specific habitat listed as endangered does not require determined to be threatened or requirements for the species under that extinction be certain or probable, endangered based on the rangewide consideration. and that it is possible for a species analysis, no further evaluation is For this Final Rule, we clarify that the validly listed as ‘‘endangered’’ to warranted. However, if a species is ‘‘foreseeable future’’ is that period of actually persist indefinitely. Due to the found to be not warranted at the spatial time over which we are able to make ambiguous nature of the statutory terms, scale of its entire range, we must reliable projections about all of the we have defined ‘‘endangered’’ and consider if a SPOIR exists that may be significant threats affecting the species ‘‘threatened’’ at the end of the both highly biologically important and and the species’ likely response to those

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threats. Projections need not be we reaffirm our choice of, identifying corals species evaluated, and the limited ‘‘certain’’ to be reliable, so long as we 2100 as the timeframe over which we availability and incomplete nature of are able to make predictions with a can make reliable predictions about quantitative data on these species, a reasonable degree of confidence based climate change-related threats. quantitative assessment of these on available information. In the However, global climate change is not projections is not possible. Therefore proposed rule, we identified the year the only relevant threat to the species, our assessment of the foreseeable future 2100 as marking the outer limit of the and the range of available data differs as is necessarily qualitative. Given the foreseeable future based upon the ability to these other threats (such as predation, biological traits and life history to make projections about the primary sedimentation, etc.). Further, in strategies of the corals evaluated in this threats to corals—those stemming from reaching our conclusions and ultimate rule, including their relatively long life- global climate change—over that period listing determinations, we need to spans, the period of time over which we (77 FR 73226). However, in identifying assess how the species will react to the are able to make reliable projections is 2100 as the limit of the foreseeable various stressors identified in this rule. the next several decades. This general future for purpose of analyzing those For example, to the extent it was timeframe thus frames our listing threats, we did not intend to establish available, we considered a significant determinations. Although we recognize that year as the only relevant benchmark amount of information on the current that climate related threats will persist for analyzing all threats to the species or spatial and demographic features of the beyond this horizon, we find it both the species’ response thereto. species, based on various types of infeasible on the information available Because neither the ESA nor information which support varying and unnecessary to attempt to identify implementing regulations define degrees of projection into the future. the foreseeable future across the full ‘‘foreseeable future,’’ the term is Thus, while the year 2100 is a reliable range of threats to the species and the ambiguous, and Congress has left broad end-point for projecting climate change- species’ response with more precision. discretion to the Secretary to determine related threats, it is not valid across the In the proposed rule, we considered what period of time is reasonable for range of threats for the species and how the temporal scales were each species. This does not require should not be misunderstood as driving appropriately factored into our identifying a specific year or period of our forecasts of the species’ statuses. evaluations of whether a species was in time to frame our analysis, particularly For all of these species, we concluded danger of extinction now, likely to where there is inadequate specific data based on the best available scientific become in danger of extinction in the to do so. See ‘‘Memorandum Opinion: and commercial information that their foreseeable future, or not warranted for The Meaning of ‘Foreseeable Future’ in spatial, demographic, or other listing. For example, two major factors Section 3(20) of the Endangered Species characteristics buffer them against determining the immediacy of the Act’’ (M–37021, Department of the current endangerment of extinction. danger of extinction for corals are the Interior Office of the Solicitor, January However, over the foreseeable future, relatively high degree of certainty of 16, 2009). The appropriate timescales the ability of spatial and demographic impacts from high importance threats for analyzing various threats will vary traits to provide a buffer against the and a species’ current or future capacity with the data available about each danger of extinction is expected to to resist adverse effects. Under the threat. In making our final listing diminish as colonies within particular proposed rule’s Determination Tool determinations we must synthesize all areas are impacted due to climate approach, endangered species were available information and forecast the change and other negative stressors. We species with a current high extinction species’ status into the future only as far considered, at a species level, whether risk; they were highly vulnerable to one as we reliably are able based on the best these predicted conditions may cause or more of the high importance threats available scientific and commercial the species to become in danger of and had either already been seriously information and best professional extinction within the foreseeable future. adversely affected by one of these judgment. However, there are varying degrees of threats, as evidenced by a declining In the case of corals, we can make certainty about the responses of corals trend, and high susceptibility to that reasonable assessments as to the most to stressors. We can be confident that threat, or they lacked a buffer to protect significant environmental factors facing certain mitigating elements of the life them from serious adverse effects from the coral species between now and history for some of these species will these threats in the future. While a 2100. We have explained that this time not change, such as their ability to threatened species under the proposed period, which is consistently used by reproduce asexually or the ability to rule might be impacted by the same most current global models and the persist in a range of depths. But we are threats as an endangered species, it was IPCC reports, allows for reliable and less confident in other aspects, such as less exposed or less susceptible, reasonable projections about climate precisely where and when local providing greater buffering capacity to change-related threats. As described in extirpations may occur. those same threats when compared to an the Threats Evaluation—Foreseeable For this final rule, then, we make endangered species. Future and Global Climate Change clear that our listing determinations are In response to public comments Overview sections above, 2100 was reached on the totality of the best critical of our equating species’ listing selected as the limit of foreseeability for available information about the threats statuses with outcomes of the climate change-related threats based on to the species and the species’ likely determination tool, here we more fully AR4’s and AR5 WGI’s use of 2100 as the response to them over time. Our explain the biological characteristics end-point for most of its global climate determinations reflect our consideration and distinctions between endangered change models (IPCC, 2013). Public of that information, as well as and threatened corals, and corals not comments asserted that the models used application of our professional warranting listing under the ESA. Under in climate predictions are too uncertain judgment regarding how far into the the final rule’s determination to reliably predict climate conditions future we can reliably project either the framework, an endangered species is at out to 2100. However, as we have underlying threats or the species’ such risk of extinction, that it is explained in our response to Comment response. However, in light of the currently ‘‘in danger’’ of extinction 38 and elsewhere in this final rule, number of variables pertaining to the throughout its range. As such, an supplemental information supports, and stressors and buffering traits among the endangered coral species is of such low

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abundance or is so spatially fragmented buffering capacity against threats that structure includes larger geographic that the species is currently in danger of cause elevated extinction risk. It is distributions with adequate connectivity extinction. Several processes may worth noting that this temporal to maintain proximity of populations contribute to the danger of extinction distinction is broad, and a threatened and individuals within the range. We (e.g., depensatory process, catastrophic species could likely become an consider geographic distribution and events). Depensatory processes include endangered species anytime within the depth distribution (and connectivity, reproductive failure from low density of foreseeable future. when we have that information) in reproductive individuals and genetic Under the final rule’s determination describing the overall distribution for processes such as inbreeding. A coral framework, a coral species that is not each species. species with these characteristics would warranted for listing has spatial and We also consider the ocean basin in be vulnerable to background demographic traits and threat which a species exists. As described in environmental variation if a large susceptibilities that, when considered in the Corals and Coral Reefs—Inter-basin proportion of the existing population combination, provide sufficient Comparisons, the Indo-Pacific occupies were concentrated in an area that buffering capacity against being in at least 60 million square km of water experienced an environmental anomaly danger of extinction within the (more than ten times larger than the leading to high mortality. Similarly, an foreseeable future throughout its range. Caribbean), and includes 50,000 islands endangered coral species could be of In other words, it has sufficient and over 40,000 km of continental such low abundance that one abundance and distribution, when coastline, spanning approximately 180 catastrophic event or a series of severe, considering the species’ threat degrees of longitude and 60 degrees of susceptibilities and future projections of sudden, and deleterious environmental latitude. Thus, occupying only a small threats, it is not likely to become of such events could cause mortality of a large portion of the Indo-Pacific basin can low abundance or so spatially enough proportion of the existing still be a geographically large fragmented to be in danger of extinction population that the remaining distribution for an individual coral within the foreseeable future throughout population would be unable to species. In contrast, the Caribbean basin its range. A not warranted species also reproduce and/or recover. A coral is relatively geographically small and may not be susceptible to the threats at species that meets the endangered partially enclosed, but biologically well- standard is not necessarily characterized a sufficient level to cause any major connected. The Caribbean also has by a single factor (e.g., abundance change in the species abundance. relatively high human population number, density, spatial distribution, or In summary, the basic structure of our densities with a long history of trend value) but could also be final determination framework is adversely affecting coral reef systems characterized by combinations of factors formed by the relevant spatial and across the basin. In the proposed rule encompassing multiple life history temporal scales over which each coral we determined that if a species is characteristics and other important species’ extinction risk is evaluated. An restricted to the Caribbean, its overall ecological features, as described above. endangered coral species is currently in range was considered narrow and its Different combinations of such factors danger of extinction throughout its extinction risk was significantly may result in endangered status from entire range. A threatened species is species to species. likely to become endangered throughout increased, which greatly contributed to Under the final rule’s determination its entire range within the foreseeable an endangered or threatened framework, a threatened coral species future. determination. Comment 40 criticizes our characterization of the Caribbean in also is at a risk of extinction due to its Spatial Structure spatial and demographic characteristics this manner, stating that the BRT’s and threat susceptibilities; however We consider spatial elements that determination that the entire Caribbean those traits still provide sufficient increase a species’ risk of extinction, is sufficiently limited in geographic buffering capacity against being in alone or in combination with other scale to be a factor that increases the danger of extinction currently. In other threats, under ESA Factor E—other extinction risk of all corals in the words, the species has an abundance natural or manmade factors affecting the Caribbean is at odds with genetic data. and distribution sufficient for it to be continued existence of the species. The commenter provided references to not currently of such low abundance or Spatial structure is important at a support the conclusion that, while it is so spatially fragmented to be in danger variety of scales. At small spatial scales clear that regional-scale processes such of extinction, but is likely to become so within a single population, issues of as bleaching and disease are acting on within the foreseeable future throughout gamete density and other Allee effects all these reefs in the Caribbean basin it range. Similar to an endangered can have significant impacts on simultaneously, all reefs should not be species, a coral species that meets the population persistence. At large spatial presumed to respond the same to these threatened standard is not necessarily scales, geographic distribution can disturbances. Upon consideration of the characterized by a single factor (e.g., buffer a population or a species from comment and the fact that the abundance number, density, spatial environmental fluctuations or Determination Tool ratings regarding distribution, or trend value) but could catastrophic events by ‘‘spreading the basin occupancy were an inadvertent also be characterized by combinations of risk’’ among multiple populations. We function of comparing the Caribbean factors encompassing multiple life explicitly described how exposure to basin to Indo-Pacific basin (i.e., the history characteristics and other individual threats varies at different automatic increase in extinction risk for important ecological features, as spatial scales in the Threats Evaluation species occurring in the smaller, more described above. Different combinations section above. Generally, having a larger disturbed Caribbean was only relative in of such factors may result in threatened geographic or depth distribution comparison to species occurring in the status from species to species. provides more potential area to occupy. larger, less disturbed Indo-Pacific) we Thus, there is a temporal distinction However, if populations become too re-evaluated our characterization of the between endangered and threatened isolated gene flow and larval Caribbean. We now consider the species in terms of the proximity of the connectivity may be reduced, making absolute (non-relative) size of the basin danger of extinction based on the the species less likely to recover from and the amount of heterogeneity in the sufficiency of characteristics to provide mortality events. Thus, a robust spatial system; therefore, we no longer

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conclude that presence within the determination framework, rarity or on a few studies on a few species. Caribbean basin automatically increases uncommonness may increase extinction Where possible, when we have species- extinction risk (because many of the risk, but alone it does not automatically specific cumulative or interactive effects Caribbean coral species occupy a large contribute to a finding of an endangered information, we have applied this portion of habitat compared to the total or threatened status. information to that particular species’ habitat available to them and the Trends in abundance directly susceptibilities in a more integrated heterogeneous nature of that habitat). In demonstrate how a particular species manner. Species-specific threat general, we still consider distribution in responds under current or recent-past susceptibilities are described in the the Caribbean to be problematic, but conditions. Generally, a continuing Species-specific Information and will now consider the influence of a downward trend likely increases Determinations section. Caribbean distribution on extinction extinction risk, while stabilization or a The three most important threats that risk on a species-by-species basis. For continuing upward trend likely contribute to the proposed coral species’ example, if a species has a Caribbean- decreases extinction risk. Trend data for extinction risk are ocean warming, wide geographic distribution and large the 65 species are scarce, but we disease, and ocean acidification. We depth distribution, and isn’t susceptible describe the extent to which an considered these threats to be the most to or exposed to threats now or through individual species’ extinction risk is significant threats posing extinction risk the foreseeable future, then a Caribbean influenced by its trend data when the to the proposed coral species currently basin distribution alone doesn’t information is available. and out to the year 2100. Threats of automatically increase the species’ Productivity is another important lower importance (trophic effects of reef extinction risk. In the Species-specific indicator of extinction risk. Productivity fishing, sedimentation, nutrients, sea- Information and Determinations section is defined here as the tendency of the level rise, predation, and collection and of this final rule, we describe the extent population to increase in abundance trade) also contributed to our findings to which an individual species’ and is often expressed as ‘‘recruits per on extinction risk, but to a lesser extent. extinction risk is influenced by its spawner,’’ although the term ‘‘recruit’’ can be difficult to apply in the case of Current and Future Environmental specific geographic, depth, and habitat Conditions distributions within each basin. corals, which reproduce both sexually and asexually (see Individual The general information described in Demography Delineation sub-section). Some of the the preceding sections of this final rule Demographic elements that cause a proposed coral species are long-lived, illustrates that the most important species to be at heightened risk of with low or episodic productivity, threats are currently increasing and extinction, alone or in combination with making them vulnerable to trends of likely to increase further in the threats under other listing factors, are increased mortality or catastrophic foreseeable future (Threats Evaluation), considered under ESA Factor E—other mortality events. Overall, recruitment but that the impacts from these threats natural or manmade factors affecting the rate estimates for the proposed species currently and in the foreseeable future continued existence of the species. In are scarce, but in cases where estimates are difficult to interpret and do not the proposed rule, we used species- were available analysis of how that necessarily correlate to an increased specific qualitative abundance species’ extinction risk is influenced by vulnerability to extinction due to the estimates, coded as ‘‘common,’’ its relative recruitment rate is biological and physical complexity of ‘‘uncommon,’’ or ‘‘rare’’ for the considered in the Species-specific corals and their habitat (Corals and candidate species because it was the Information and Determinations section Corals Reefs, Threats Evaluation). only abundance metric that was below. The information on corals, coral reefs, available for all of the 82 candidate coral habitat, and threats to reef- Susceptibility to Threats species. As mentioned above in the building corals in a changing climate Distribution and Abundance of Reef- Susceptibility of a coral species to a leads to several important points that building Corals sub-section, these threat is primarily a function of apply both currently and over the qualitative estimates are the subjective biological processes and characteristics, foreseeable future. First, the foreseeable opinion of particular authors on their and can vary greatly between and future for purposes of our ultimate particular survey data and are meant to within taxa. Susceptibility of a species listing determinations is described indicate relative abundance between the to a threat depends on the combination qualitatively and encompasses the next categories. That is, a rare species has of: (1) Direct effects of the threat on the several decades. For purposes of fewer individuals as compared to an species; and (2) the cumulative and analyzing the specific threats related to uncommon one, and an uncommon interactive (synergistic or antagonistic) climate change, we have identified the species has fewer individuals than a effects of the threat with the effects of foreseeable time period over which we common one. These estimates are also other threats on the species. In the can make reliable projections to extend meant to describe an author’s opinion of proposed rule, we considered how the over the period from now to the year the qualitative abundance of the species cumulative or interactive effects altered 2100. There is increased uncertainty throughout its range, but not an estimate the rating assigned to a threat over that time period as conditions that of the abundance at an individual susceptibility in isolation. However, are analyzed closer to the year 2100 location. In general, ‘‘rare’’ or upon further consideration, we need to become less foreseeable. That is, the ‘‘uncommon’’ species are more evaluate the extent to which one threat general trend in conditions during the vulnerable than ‘‘common’’ ones, influences the susceptibility of an period of time from now to 2100 is although some species are naturally rare individual species to another threat reasonably foreseeable as a whole, but and have likely persisted in that rare with more species-specific information, conditions become more difficult to state for tens of thousands of years or in connection with all the other accurately predict through time. longer. However, naturally rare species elements that influence a species’ Second, there is an overall increasing can be at greater risk of extinction than extinction risk. Generally, cumulative trend of threat severity, especially for naturally more common species when and interactive processes are complex threats related to global climate change confronted with global threats to which and uncertain and existing information as projected by RCP8.5 to 2100. Third, they are vulnerable. In our final about threats interactions is only based while some models suggest disastrous

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effects of RCP8.5 on coral reefs by 2100, on current and future environmental influence extinction risk for a coral such projections are based on spatially conditions, we relate those species. The sixth element is relating a coarse analyses associated with high characteristics to the particular species’ species’ characteristics to a particular uncertainty, especially at local spatial status. This is the key component of the extinction risk at appropriate spatial scales. In sum, determining the effects determination that explains how certain and temporal scales. The seventh of global threats on an individual coral species characteristics translate to a element is explicitly stating how each species over the foreseeable future is particular extinction risk at appropriate species’ extinction risk meets the complicated by the combination of: (1) spatial and temporal scales. These statutory listing definitions as applied to Uncertainty associated with projected determinations are heavily influenced corals, resulting in an ultimate listing ocean warming and acidification by the quantity and quality of species- status. A final consideration in threats; (2) regional and local variability specific information, especially the evaluating listing status is whether in global threats; (3) large distributions species’ demographic and distribution current or planned conservation efforts and high habitat heterogeneity of the characteristics. We received many improve the overall status of any of the species in this final rule; and (4) limited public comments regarding the lack of 65 species such that the additional species-specific information on quantity and quality of information protections of the ESA are not responses to global threats. available for each of the species; those warranted. We explicitly apply the commenters asserted that our species determination framework to each Vulnerability to Extinction determinations were therefore species in our narrative evaluations. The vulnerability of a species to unfounded. By specifically considering This approach provides consistency extinction is a complex function of all the currently available species- across all of the 65 final listing physiology, life history, morphology, specific information (both information determinations, but also produces spatial distribution, and interaction that we used in the proposed rule and individual determinations that are with threats (the biological context). The the considerable amount of information independent of the other 65 coral biological context for a species’ that has become available since the species. vulnerability to threats dictates the proposed rule), we are able to produce Conservation Efforts ecological interactions that ultimately more robust evaluations of the determine how a species responds to information and species determinations. The effect conservation efforts have threats, such as competition and Recognizing the uncertainty and spatial on an individual species’ listing status predation (the ecological context). For variability of climate change projections is the last consideration in making a example, a species that suffers high and the limited species-specific final determination. Because many mortality from a bleaching event also information on how species in this final conservation efforts are not species- may be able to recover quickly because rule respond to climate change, we specific, we provide our analysis of the its high dispersal and skeletal growth emphasize a species’ demographic and effectiveness of conservation efforts for enable efficient recolonization and spatial characteristics in how its corals generally prior to making strong competition. Thus, the initial vulnerability to extinction is affected individual species determinations. Our response to threats does not necessarily now and through the foreseeable future. conclusions regarding conservation mean the species is vulnerable. In finalizing a species determination efforts in this section apply to all of the Vulnerability of a coral species to we translate the species’ status directly proposed species. However, in some extinction also depends on the into a listing category using the cases, we are able to identify species- proportion of colonies that are exposed statutory standards. In the proposed specific conservation efforts and to threats and their different responses rule, we satisfied this step by using an therefore evaluate them separately in to those threats. In the proposed rule organizational process called the the Species-specific Information and there was little variation between outcome key, based on ratings in the Determinations section. species for exposure to a given threat in Determination Tool. The key was Section 4(b)(1)(A) of the ESA requires the assigned ratings (e.g., exposure to intended to identify the general species the Secretary, when making a listing ocean warming was rated the same for characteristics and combinations that determination for a species, to take into all 82 species, which should not equate to a particular listing status. account those efforts, if any, being made automatically be the case because for However, the outcome key in the by any State or foreign nation to protect species that have drastically different proposed rule was too formulaic, and the species. In evaluating the efficacy of distributions and abundances). For this did not explain our comprehensive protective efforts, we rely on the final rule, a coral species’ vulnerability consideration of the species Services’ joint ‘‘Policy for Evaluation of to extinction is now evaluated to be characteristics that influenced their Conservation Efforts When Making holistically influenced by its listing status, and was also based on Listing Decisions’’ (‘‘PECE;’’ 68 FR demographic and spatial characteristics, relative ratings from the Determination 15100; March 28, 2003). The PECE threat susceptibilities, and current and Tool. Therefore, the presentation of our requires us to consider whether any future environmental conditions. We final determination framework is more conservation efforts recently adopted or believe this more complete and clearly articulated in this final rule by implemented, but not yet proven to be integrated treatment of the factors that explicitly describing the considerations successful, will result in improving the influence a coral’s vulnerability to for each the 65 species in narrative species’ status to the point at which extinction will lead to a more accurate format and how they relate to the listing is not warranted, or contribute to characterization of whether or not a statutory standards a threatened rather than endangered species currently faces an extinction In summary, the determination status. risk throughout its entire range. framework used in this final rule is For the proposed rule, we developed composed of seven elements. The first a Management Report that identified Species Status element is describing the statutory existing conservation efforts relevant to After analyzing all of the relevant standards. The second, third, fourth, both global and local threats to corals. species-specific demographic and and fifth elements are identifying and A draft of this report was peer reviewed spatial characteristics, threat analyzing all the appropriate species- and made available to the public with susceptibilities, and general information specific and general characteristics that the SRR in April 2012. At that time, we

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requested any new or inadvertently algae removal, larval seeding, and active preserving the integrity of wild reefs overlooked existing information. The restoration via coral propagation and and coral species in Indonesia. information that we received was outplanting activities. As a result of the However, there are still many challenges incorporated into the Final Management 2009 American Recovery and and obstacles related to captive culture Report (NMFS, 2012b), which formed Reinvestment Act, Federal funding of corals that are detailed in the Threats the basis of our initial PECE evaluation. through NOAA enabled a network of Evaluation, Trade and Collection The information, analysis, and coral nurseries to expand throughout section above. Any relevant information conclusions regarding conservation south Florida and the U.S. Virgin regarding this topic has also been efforts in the proposed rule and Islands to help recover threatened incorporated into the analysis of supporting documents apply to this staghorn and elkhorn corals. These conservation efforts in this final rule. final rule, unless otherwise noted types of in-water coral nurseries have We received information regarding below. proven successful for propagating corals the role of local management actions Comments 30–32 focus on our and serving as genetic repositories to and conservation efforts with regard to consideration of conservation efforts in help replenish and restore denuded reef resilience. Conservation projects the proposed rule. In response to public reefs (Schopmeyer et al., 2012; Young et and programs such as international comments on the proposed rule, we al., 2012). In 2012 alone, it was agreements and memoranda of incorporated into our analyses in the estimated these nurseries housed 30,000 understanding, coral reef monitoring, final rule relevant information on corals, with more than 6,000 corals voluntary protected areas, restoration conservation efforts that are new or that outplanted to surrounding reefs (The activities, and outreach and education may have been inadvertently omitted or Nature Conservancy, 2012). Further, initiatives, among others, play an mischaracterized. Thus, this final rule successful spawning of these outplanted integral role in building and incorporates information we received as corals has been reported on several maintaining resilience within coral reef a result of the public comment period, occasions since the first event occurred ecosystems as well as raising public identifies existing conservation efforts in 2009 (Coral Restoration Foundation, awareness. More detailed information that are relevant to the threats to the 65 2013). Still, it should be emphasized regarding local actions as they relate to coral species in this final rule, both for that coral reef restoration should not be reef resilience are described above in global-scale threats to corals linked to expected to recover entire reef tracts or the Threats Evaluation, Inadequacy of GHG emissions and other threats to species; rather, coral reef restoration can Existing Regulatory Mechanisms section corals. In particular, we received serve as a complementary tool to other of this final rule. supplemental information regarding management strategies such as fisheries As described above, we received coral reef restoration efforts in Florida management, coastal zone and supplemental information about local and the wider-Caribbean. We also watershed management, marine conservation efforts since the received supplemental information protected areas, and others. In a publication of the proposed rule. regarding efforts to utilize captive- comprehensive review of restoration However, we did not receive any culture techniques to supplement the activities conducted in Florida and the supplemental information that changes coral reef wildlife trade industry and wider-Caribbean, Young et al. (2012) our previous conclusions regarding reduce collection pressure on wild coral found that most practitioners global conservation efforts to slow species. Specifically, we received recommended that active restoration climate change-related impacts. After information regarding Indonesia’s activities always be conducted in considering this supplemental mariculture operations as well as efforts conjunction with robust local and information in addition to that which in the United States to commercially regional management strategies to was available for the proposed rule, our and recreationally farm corals. This minimize the impacts of global and conclusions regarding conservation information on coral reef restoration, local threats. This is because coral reef efforts remain unchanged. Overall, the captive culture efforts for trade restoration efforts can prove futile if the numerous coral reef conservation purposes, and local conservation efforts initial elements of degradation have not projects are increasing and as it applies to reef resilience is been mitigated (Jaap, 2000; Precht and strengthening resiliency within coral described further below. reef ecosystems on a local level, and can We received some supplemental Aronson, 2006; Young et al., 2012). provide a protective temporal buffer for information regarding the ongoing coral As described above in the Threats corals in the face of climate change reef restoration efforts being made in Evaluation—Collection and Trade related threats. Coral reef restoration South Florida as well as the wider- section of this rule, we received a activities, particularly of the Caribbean Caribbean, predominantly for staghorn significant amount of information acroporid species, are expected to assist and elkhorn corals (Acropora regarding the potential conservation in recovery efforts, but they cannot be cervicornis and A. palmata, benefits of increasing international and considered a panacea. In the absence of respectively). We briefly mentioned domestic commercial and recreational effective global efforts to reduce impacts active coral restoration in the proposed production of corals via significant from climate change, there are no rule as an important conservation action advances in captive-culture techniques for corals, but did not describe these (i.e., mariculture and aquaculture). conservation efforts currently or efforts in great detail. Coral reef Specifically, we received supplemental planned in the future that are expected restoration efforts encompass a variety information regarding the mariculture to improve the overall status of any of of activities, and they are increasingly efforts conducted in Indonesia to reduce the listed species in this final rule, such utilized to enhance, restore, and recover the amount of corals collected in the that the additional protections provided coral reef ecosystems and species wild, thereby potentially reducing the by the ESA are not warranted. (Bowden-Kerby et al., 2005; Bruckner threat of the marine ornamental trade Species-Specific Information and and Bruckner, 2001; Lirman et al., industry on corals and coral reefs. As Determinations 2010b). These activities may include the largest exporter of corals in the post-ship grounding ‘‘triage’’ (e.g., world, shifting from wild-collected Introduction stabilizing substrate and salvaging corals to captive cultured corals is an This section summarizes the best corals and sponges), active predator and important conservation effort for available information for each of the 65

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species of coral considered in this final depths of 50 to 100 m on mesophotic 1979; Rogers et al., 1984; Shearer and rule. The best available information is reefs. Coffroth, 2006). comprised of the proposed rule and its The public comments did not provide Susceptibility to Threats supporting documents, and information any new or supplemental information that we either gathered ourselves or on Agaricia’s distribution, habitat, and The SRR and SIR did not provide any received as a result of public comments. depth range. Supplemental information genus level information on the To distinguish between the information we found includes the following. susceptibility of Agaricia to ocean on which the proposed rule was based Bongaerts et al. (2013) studied the depth warming, and the public comments did from new or supplemental information, distribution and genetic diversity of five not provide any new or supplemental we will only cite the primary literature agariciid species (A. humilis, A. information. Supplemental information for new or supplemental information. agaricites, A. lamarcki, A. grahamae, we found on the susceptibility of the For clarity, we will distinguish whether and Helioseris cucullata [= Leptoseris genus Agaricia to ocean warming the information was identified via cucullata]) and their symbiotic includes the following: Agaricia is public comment or if we gathered it zooxanthellae in Curac¸ao. They found a considered highly susceptible to ourselves. distinct depth distribution among the bleaching. Agaricia spp. were the most Spatial, demographic, and other species. Agaricia humilis and A. susceptible to bleaching of the corals relevant biological information, threat agaricites were more common at monitored during an unanticipated susceptibilities, and information on shallow depths, and A. lamarcki, A. bleaching event at a remote, regulatory mechanisms are all presented grahamae, and H. cucullata were more uninhabited island (Navassa), with for each species. Because species- common at deeper depths. They also higher bleaching prevalence at deeper specific information is limited for many found genetic segregation between coral sites (Miller et al., 2011a). During the of the proposed species, genus-level host-symbiont communities at shallow 1998 bleaching event in Belize, A. information is highly relevant to our and mesophotic depths. tenuifolia, a dominant coral, was nearly determinations. Therefore, we provide eradicated from the Channel Cay reef Demographic Information relevant information for each genus complex (Aronson et al., 2002). During prior to providing the specific The SRR and SIR provided the the 2005 bleaching event, nearly all information for species within that following genus level information on Agaricia spp. were bleached at long- genus. Specifically, genus-level Agaricia’s abundance and population term monitoring sites in Buck Island information on threat susceptibilities is trends: Coral specimens collected in National Monument, and they remained relevant to species when the available 2010 from a mesophotic reef at Pulley bleached comparatively longer than genus-level information can be Ridge, Florida suggest that corals, such other species monitored (Clark et al., appropriately applied to the species. as Agaricia spp., that appear live in 2009). Manzello et al. (2007) Therefore, in each genus description, we video images may actually be covered characterized Agaricia as having high provide a section that summarizes with algae rather than live coral tissue. susceptibility to bleaching in their study genus-level threat susceptibility The public comments did not provide identifying bleaching indices and information that was provided in the any new or supplemental information thresholds in the Florida Reef Tract, the SRR and SIR, as well as in the public on Agaricia’s abundance or population Bahamas, and St. Croix, U.S. Virgin comments and supplemental trends. Supplemental information we Islands. A long-term study in the information. Threat susceptibility found on Agaricia’s population trends Florida Keys found that bleaching conclusions are then provided includes the following: Stokes et al. prevalence was increased four to seven considering the applicability of the (2010) reported a decrease in cover of times by nutrient-enrichment in genus-level information to an unstudied Agaricia spp. in the Netherlands Agaricia spp., the only genus that species within that genus. These Antilles between 1982 and 2008 at all showed such a response (Vega Thurber conclusions will be applied, as depths surveyed (10 to 30 m). An et al., 2014). This study indicated that appropriate, in the appropriate species analysis of Caribbean monitoring data the temperature threshold for bleaching descriptions. from 1970 to 2012 found that large, may have been lowered by the nutrient plating Agaricia spp. were one of the enrichment. Notably, after removal of Caribbean Species Determinations species groups that suffered the greatest the nutrient enrichment, bleaching Genus Agaricia proportional losses (Jackson et al., prevalence returned to background 2014). levels. Thus, we conclude that, absent Introduction species-specific information, species in There are seven species in the genus Other Biological Information the genus Agaricia should be considered Agaricia, all of which occur in the The SRR and SIR provided the highly susceptible to ocean warming- Caribbean (Veron, 2000). Colonies are following information on the life history induced bleaching. composed of plates, which are flat, of the genus Agaricia. In general, The SRR and SIR did not provide any horizontal, or upright. The latter are Agaricia spp. are gonochoric brooders. genus level information on the usually contorted and fused. Some Several species such as Agaricia susceptibility of Agaricia to disease, and species such as A. humilis and Agaricia agaricites, A. tenuifolia, and A. humilis the public comments did not provide fragilis tend to be small and somewhat are known to use chemical cues from any new or supplemental information. circular in shape while others like crustose coralline algae to mediate Supplemental information we found on Agaricia lamarcki and Agaricia settlement. the susceptibility of the genus Agaricia grahamae can form large, plating The public comments did not provide to disease includes the following. A colonies. new or supplemental information on the study of coral diseases across the wider- life history of the genus Agaricia. Caribbean during the summer and fall of Spatial Information Supplemental information we found on 2005 found the genus Agaricia, along The SRR and SIR provided the Agaricia’s life history includes the with seven other major reef-building following genus-level information on following: Agaricia spp. can be one of genera, to be particularly susceptible to Agaricia’s distribution, habitat, and the dominant taxonomic groups found coral diseases including white plague depth range: Agaricia can be found at in recruitment studies (Bak and Engel, type II, Caribbean ciliate infection, and

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to be infected with multiple diseases at have some susceptibility to its morphology and the presence of the same time (Croquer and Weil, 2009). sedimentation. white stars at the mouths. Agaricia Agaricia agaricites decreased 87 percent The SRR and SIR did not provide any lamarcki does not appear to have in mean cover from the disease outbreak genus level information on the taxonomic problems. following the 2005 bleaching event in susceptibility of Agaricia to nutrients, The public comments did not provide the U.S. Virgin Islands (Miller et al., and the public comments did not new or supplemental information, and 2009). Thus, we conclude that, absent provide any new or supplemental we did not find any new or species-specific information, species in information. Supplemental information supplemental information on A. the genus Agaricia should be considered we found on the susceptibility of lamarcki’s morphology or taxonomy. highly susceptible to diseases. Agaricia spp. to nutrients includes the Spatial Information The SRR and SIR provided the following. Treatment of A. tenuifolia following information on the with low (5 mg per l) and high (25 mg The SRR and SIR provided the susceptibility of Agaricia to per l) doses of organic carbon resulted following information on A. lamarcki’s acidification. No specific research has in 73 to 77 percent mortality, distribution, habitat, and depth range. addressed the effects of acidification on respectively, compared to 10 percent Agaricia lamarcki can be found in the the genus Agaricia. However, most mortality of controls (Kuntz et al. 2005). western Atlantic off south Florida as far corals studied have shown negative Treatment of A. tenuifolia with nitrate north as Palm Beach County, in the Gulf relationships between acidification and (7.5 mM), ammonium (25 mM), and of Mexico including the Flower Garden growth, and acidification is likely to phosphate (2.5 mM) caused about 50 Banks, and throughout the Caribbean contribute to reef destruction in the percent mortality compared to 10 including the Bahamas. Agaricia future. While ocean acidification has percent in controls (Kuntz et al. 2005). lamarcki is rare in shallow reef not been demonstrated to have caused Thus, we conclude that, absent species- environments of 3 to 15 m, but is appreciable declines in coral specific information, species in the common at deeper depths of 20 to 100 populations so far, it is considered a genus Agaricia should be considered to m where it can be one of the dominant significant threat to corals by 2100. have high susceptibility to nutrient coral species. It is found in shaded or The public comments did not provide enrichment based on this study in reduced light environments, on slopes any new or supplemental information combination with the Vega Thurber et and walls, and on mesophotic reefs in on the susceptibility of Agaricia to al. (2014) study that found increased Curac¸ao, Florida, Jamaica, Puerto Rico, acidification. Supplemental information bleaching in the presence of chronic and the U.S. Virgin Islands. The public comments did not provide we found on the susceptibility of the nutrient enrichment. new or supplemental information on A. genus Agaricia to acidification includes The SRR and SIR did not provide any lamarcki’s distribution, habitat, or depth the following. Crook et al. (2012) information on the susceptibility of range. Supplemental information we surveyed coral populations near Agaricia spp. to any other threats. The found on A. lamarcki’s distribution submarine springs close to the public comments did not provide any includes the following. Veron (2014) Mesoamerican Reef in Mexico where new or supplemental information, and confirms the presence of A. lamarcki in water aragonite saturation state was we did not find any new or seven out of 11 possible ecoregions in naturally low due to groundwater supplemental information on the the western Atlantic and greater seepage. Agaricia spp. were found near susceptibility of Agaricia to any other the springs, but only in waters with an Caribbean that contain corals, and he threats. aragonite saturation state greater than strongly predicts the presence of A. 2.5, indicating these species may be less Genus Conclusion lamarcki in the ecoregion surrounding tolerant than other coral species that The studies cited above indicate that the Flower Garden Banks based on were able to grow in under-saturated Agaricia spp. are highly susceptible to published record or confirmed waters. Thus, we conclude that, absent warming. In at least one location, a occurrence in surrounding ecoregions. species-specific information, species in bleaching event resulted in 100 percent The three ecoregions in which it is not the genus Agaricia should be considered mortality of one Agaricia species. The reported are off the coasts of Bermuda, to have some susceptibility to genus also appears to be highly Brazil, and the southeast U.S. north of acidification. susceptible to diseases that can result in south Florida. We did not find any new The SRR and SIR provided genus high rates of mortality and to be highly or supplemental information on A. level information on the susceptibility susceptible to impacts of nutrients. lamarcki’s habitat or depth range. of Agaricia to sedimentation. The However, as described below, there is a typically small calices of Agaricia spp. Demographic Information fair amount of species-specific are not efficient at rejecting sediment, The SRR and SIR provided the information for individual Agaricia and species with horizontally-oriented following information on A. lamarcki’s species; therefore, we generally do not plates or encrusting morphologies could abundance and population trends. rely on the genus-level information to be more sediment-susceptible than Agaricia lamarcki is reported as inform species level determinations. species with vertically-oriented plates common. In the Netherlands Antilles, A. When necessary the appropriate as evidenced by fine sediment lamarcki increased in abundance or inference is described in the species- suspended in hurricanes that caused remained stable on reefs 30 to 40 m in specific information. higher mortality in platy corals than depth from 1973 to 1992. hemispherical or non-flat ones. The Agaricia lamarcki The public comments provided public comments did not provide any supplemental information on A. new or supplemental information on the Introduction lamarcki’s abundance. Population susceptibility of the genus Agaricia to The SRR and SIR provided the estimates of A. lamarcki in the Florida sedimentation, and we did not find any following information on A. lamarcki’s Keys extrapolated from stratified new or supplemental information. Thus, morphology and taxonomy. Agaricia random samples were 3.1 ± 1.3 million we conclude that, absent species- lamarcki has flat, unifacial, or (standard error (SE)) colonies in 2005 specific information, species in the encrusting plates that are commonly and 0.2 ± 0.2 million colonies in 2012. genus Agaricia should be considered to arranged in whorls. It is identifiable by No colonies were observed in 2009, but

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fewer deep sites (>20 m) were surveyed Population trends indicate this species A. lamarcki. Supplemental biological in 2009 and 2012 compared to 2005. may be declining in some areas, but information we found about A. lamarcki Most colonies observed were 20 to 30 because some of the trend data is includes the following. Out of five cm in diameter, and partial mortality lumped by genus or genus plus agariciid species sampled at a single reef was highest (50 percent) in the largest morphology, there is uncertainty that in Curac¸ao, A. lamarcki was the only size class (30 to 40 cm). Agaricia the trends represent A. lamarcki species that harbored multiple symbiont lamarcki ranked 35th in abundance out specifically. Thus, we conclude that A. profiles across depth distribution; the of 47 species in 2005 and 37th out of 40 lamarcki has likely declined in some other four species had only a single species in 2012. In the Dry Tortugas, areas and the population numbers at symbiont profile across depth. The Florida, where more deep sites were least in the tens of millions of colonies. symbiont community associated with A. surveyed, A. lamarcki ranked 12th out lamarcki at 40 m depth was Other Biological Information of 43 species in 2006, with population significantly different from those at both estimates extrapolated to 14.3 ± 2.6 The SRR and SIR provided the 10 m and 25 m (Bongaerts et al., 2013). million colonies. It ranked 22nd out of following information on A. lamarcki’s Susceptibility to Threats 40 species in 2008 with populations life history. No information on the estimates extrapolated to 2.1 ± 0.5 reproductive strategy of A. lamarcki is The threat susceptibility information million colonies. Most of the colonies in available, but congeners are gonochoric from the SRR and SIR was interpreted 2006 were 10 to 30 cm in diameter, but brooders. Larval settlement occurs in the proposed rule for A. lamarcki’s colonies greater than 90 cm were primarily at deeper depths (26 to 37 m), vulnerabilities to threats as follows: observed. Partial mortality was highest but the species has also been found at Moderate vulnerability to ocean in the 30 to 40 cm size class shallower depths. Recruitment rates of warming, disease, acidification, trophic (approximately 35 percent) in 2006 and A. lamarcki are low (e.g., only one of effects of fishing, sedimentation, and highest in the 20 to 30 cm size class 1,074 Agaricia recruits at the Flower nutrients; and low vulnerability to sea (approximately 20 percent) in 2008. In Garden Banks may have been A. level rise and collection and trade. No 2008, most of the colonies were 0 to 10 lamarcki), and net gains from sexual conclusions on A. lamarcki’s cm in size, and the largest colonies recruitment may be negligible at a vulnerability to predation were made observed were in the 50 to 60 cm size decadal time scale. Population numbers due to lack of available information on class (Miller et al., 2013). Because may be maintained through asexual its susceptibility to this threat. population estimates were extrapolated fission of larger colonies into smaller The SRR and SIR provided the from random samples, differences in daughter colonies. Growth rates are following information on the population numbers between years are slow; radial growth measurements from susceptibility of A. lamarcki to ocean more likely a function of sampling effort Jamaica ranged from zero to 1.4 cm per warming. Agaricia lamarcki is rather than population trends over time. year and averaged approximately 0.5 cm susceptible to bleaching from both high The public comments did not provide per year. Growth rates are a bit slower, and low temperature anomalies. In new or supplemental information on A. ranging from zero to 1.0 cm per year, at laboratory studies, A. lamarcki had lamarcki’s population trends. depths greater than 20 m. Maximum almost complete disruption of Supplemental information we found colony size is approximately two photosynthesis at 32 °C to 34 °C. on A. lamarcki’s abundance and meters. Agaricia lamarcki is a relatively Bleaching can be extensive; however, it population trends includes the long-lived species, and individual may not result in mortality in A. following. Between 1977 and 1987, colonies may persist for greater than a lamarcki. colonies of A. lamarcki in monitored century. Based on monitoring in Van Woesik et al. (2012) developed a plots in Jamaica decreased from 34 to 31 Jamaica, the half-life (mortality of half of coral resiliency index to evaluate colonies, indicating the net production monitored colonies) of A. lamarcki is 17 extinction risk due to bleaching, based by sexual and asexual means was not years. Mortality rates are size-specific on biological traits and processes. enough to compensate for mortality of (ranging from 10 to 25 percent), and Evaluations were performed at the the originally present colonies (Hughes, partial mortality rates are high (ranging genus level. They rated the resiliency of 1988). More than 40 percent of the from 22 to 90 percent). Overall, Agaricia as ¥2 out of a range of ¥6 to colonies present in 1987 were derived demographic characteristics are low 7 observed in other coral genera. Less from asexual fission of the original recruitment, high colony survival, and than or equal to ¥3 was considered colonies present in 1977, and none of high partial mortality. highly vulnerable to extinction, and the six sexual recruits survived until the The public comments did not provide greater than or equal to 4 was end of the study period (Hughes, 1988). new or supplemental information on A. considered highly tolerant. Thus, In the U.S. Virgin Islands, A. lamarcki lamarcki life history. Supplemental Agaricia was rated closer to the was the eleventh most common coral in information we found on A. lamarcki vulnerable end of the spectrum, though terms of cover out of 55 species, and life history includes the following. not highly vulnerable. This study was in average cover across 18 monitoring sites Darling et al. (2012) performed a trait- the SIR, but the findings specific to was 1.2 ± 0.3 (SE) percent in 2012 based analysis to categorize coral Agaricia were not included. The public (Smith, 2013). species into four life history strategies: comments (comment 47) indicated the All information on A. lamarcki’s Generalist, weedy, competitive, and results of this study should be abundance and population trends can stress-tolerant. The classifications were considered in the listing status of A. be summarized as follows. Based on primarily separated by colony lamarcki. population estimates, there are at least morphology, growth rate, and The public comments did not provide tens of millions of A. lamarcki colonies reproductive mode. Agaricia lamarcki any new or supplemental information present in the Florida Keys and Dry was classified as a ‘‘weedy’’ species, on the susceptibility of A. lamarcki to Tortugas combined. Absolute thus likely more tolerant of ocean warming. Supplemental abundance is higher than the estimate environmental stress. information we found on the from these two locations given the The SRR, SIR, and the public susceptibility of A. lamarcki to ocean presence of this species in many other comments did not provide new or warming includes the following. During locations throughout its range. supplemental biological information for the 2005 bleaching event, greater than

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80 percent of A. lamarcki colonies susceptible to several diseases, The SRR and SIR did not provide bleached at 12 sites in Puerto Rico including white plague, which has one species-specific information on the (Waddell and Clarke, 2008). In the U.S. of the fastest progression rates recorded effects of sea level rise on A. lamarcki. Virgin Islands, an average of 59 percent in the Caribbean. However, there is no The SRR described sea level rise as an of A. lamarcki colonies (n = 11) information on the population level overall low to medium threat for all bleached, and nine percent paled during effects of disease on A. lamarcki (e.g., coral species. The public comments did the 2010 bleaching event (Smith et al., rates of infection, percentage of not provide new or supplemental 2013b). Agaricia lamarcki had high population affected, and amounts of information on A. lamarcki’s resistance to both hot and cold water tissue loss). Genus-level information susceptibility to sea level rise, and we anomalies that impacted the Florida indicates high susceptibility to a disease did not find any new or supplemental Keys in 2005 and 2010, respectively, as outbreak following a bleaching event, information. Thus, we conclude that A. indicated by their low tissue mortality indicating A. lamarcki is likely highly lamarcki has some susceptibility to sea compared to other coral species susceptible to disease. level rise, but the available information monitored (Lirman et al., 2011). The SIR and SRR did not provide any does not provide a more precise All sources of information are used to species-specific information on the description of susceptibility. describe A. lamarcki’s susceptibility to trophic effects of fishing on A. lamarcki. The SRR and SIR provided the ocean warming as follows. Agaricia The public comments did not provide following information on the lamarcki has some susceptibility to new or supplemental information, and susceptibility of A. lamarcki to ocean warming as evidenced by we did not find new or supplemental collection and trade. Only light trade extensive bleaching during warm water information on the trophic effects of has been recorded with gross exports temperature anomalies but observed low fishing on A. lamarcki. However, due to averaging fewer than 10 pieces of coral bleaching-related mortality. The the level of reef fishing conducted in the annually between 2000 and 2005. The available information does not support Caribbean, coupled with Diadema die- public comments did not provide new a more precise description of off and lack of significant recovery, or supplemental information on the susceptibility. competition with algae can adversely susceptibility of A. lamarcki to The SRR and SIR did not provide any affect coral recruitment. Thus, A. collection and trade. Supplemental species-specific information on lamarcki likely has some susceptibility information we found confirms that susceptibility of A. lamarcki to ocean to the trophic effects of fishing because collection and trade of A. lamarcki acidification. The public comments did of low recruitment rates, though the remained low between 2000 and 2012 not provide new or supplemental available information does not support with gross exports averaging fewer than information on the susceptibility of A. a more precise description of 10 pieces of coral annually (data lamarcki to acidification, and we did susceptibility. available at http://trade.cites.org/). not find any new or supplemental Thus, we conclude that A. lamarcki has The SRR and SIR provided the information. low susceptibility to collection and following information on susceptibility All sources of information are used to trade. describe A. lamarcki’s susceptibility to of A. lamarcki to sedimentation. The SRR and SIR provided the acidification as follows. There is Agaricia lamarcki could be susceptible following information on the uncertainty about how A. lamarcki will to sedimentation based on calix and susceptibility of A. larmarcki to respond to ocean acidification, but there colony morphology. This conclusion predation. Predation effects on A. is genus-level evidence that Agaricia are was based on genus-level information lamarcki are unknown. The public not among the more tolerant species on susceptibility to sedimentation. The comments did not provide any new or from areas of water with naturally lower public comments did not provide new supplemental information, and we did aragonite saturation state. Thus, A. or supplemental information on the not find any new or supplemental lamarcki likely has some susceptibility susceptibility of A. lamarcki to information on the susceptibility of A. to ocean acidification, but the available sedimentation, and we did not find new lamarcki to predation. We conclude that information does not support a more or supplemental information. while A. lamarcki likely has some precise description of susceptibility. All sources of information are used to susceptibility to predation, available The SRR and SIR provided the describe A. lamarcki’s susceptibility to information is lacking, and we cannot following information on A. lamarcki’s sedimentation as follows. There is no say whether it is a threat. susceptibility to disease. White plague species-specific information on the Regulatory Mechanisms infections in A. lamarcki have been susceptibility of A. lamarcki to observed in Florida, Colombia, and St. sedimentation. However, based on In the proposed rule, we relied on Lucia, though no incidence of disease genus-level information, colony information from the Final Management was observed in the Florida Keys in morphology and skeletal structure of A. Report for evaluating the existing 1996 to 1998. Ciliate infections have lamarcki indicate it is likely poor at regulatory mechanisms for controlling been documented in A. lamarcki, and removing sediment. Thus, A. lamarcki threats to all corals. However, we did tumors may affect this species. The likely has some susceptibility to not provide any species-specific ecological and population impacts of sedimentation, but the available information on the regulatory disease have not been established for A. information does not support a more mechanisms or conservation efforts for lamarcki. precise description of susceptibility. A. lamarcki. Public comments were The public comments did not provide The SRR and SIR did not provide any critical of that approach, and we any new or supplemental information information on the susceptibility of A. therefore attempt to analyze regulatory on the susceptibility of A. lamarcki to lamarcki to nutrients, and the public mechanisms and conservation efforts on disease, and we did not find any new or comments did not provide any new or a species basis, where possible, in this supplemental information on A. supplemental information. final rule. Records confirm that Agaricia lamarcki’s susceptibility to disease. Supplemental information we gathered lamarcki occurs in eight Atlantic All source of information are used to at the genus-level indicates that A. ecoregions that encompass 26 describe A. lamarcki’s susceptibility to lamarcki is likely highly susceptible to kingdom’s and countries’ EEZs. The 26 disease as follows. Agaricia lamarcki is nutrient enrichment. kingdoms and countries are Antigua &

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Barbuda, Bahamas, Barbados, Belize, knowledge regarding the species’ least tens of millions of colonies in the Colombia, Costa Rica, Cuba, Dominica, abundance, distribution, and threat Florida Keys and Dry Tortugas Dominican Republic, French Antilles, susceptibilities. We developed our combined and is higher than the Grenada, Guatemala, Haiti, Kingdom of assessment of the species’ vulnerability estimate from these two locations due to the Netherlands, Honduras, Jamaica, to extinction using all the available the occurrence of the species in many Mexico, Nicaragua, Panama, St. Kitts & information. As explained in the Risk other areas throughout its range. Its Nevis, St. Lucia, St. Vincent & Analyses section, our assessment in this abundance, life history characteristics, Grenadines, Trinidad and Tobago, final rule emphasizes the ability of the and depth distribution, combined with United Kingdom (British Overseas species’ spatial and demographic traits spatial variability in ocean warming and Territories), United States (including to moderate or exacerbate its acidification across the species’ range, U.S. Caribbean Territories), and vulnerability to extinction, as opposed moderate vulnerability to extinction Venezuela. The regulatory mechanisms to the approach we used in the because the increasingly severe relevant to A. lamarcki, described first proposed rule, which emphasized the conditions expected in the foreseeable as a percentage of the above kingdoms species’ susceptibility to threats. future will be non-uniform, and there and countries that utilize them to any The following characteristics of A. will likely be a large number of colonies degree, and second as a percentage of lamarcki, in conjunction with the that are either not exposed or do not those countries and kingdoms whose information described in the Corals and negatively respond to a threat at any regulatory mechanisms may be limited Coral Reefs section, Coral Habitat sub- given point in time. in scope, are as follows: General coral section, and Threats Evaluation section Listing Determination protection (31 percent with 12 percent above, affect its vulnerability to limited in scope), coral collection (50 In the proposed rule, using the extinction currently and over the determination tool formula approach, A. percent with 27 percent limited in foreseeable future. Although it is scope), pollution control (31 percent lamarcki was proposed for listing as geographically located in the heavily threatened because of: Moderate with 15 percent limited in scope), disturbed Caribbean, A. lamarcki’s fishing regulations on reefs (73 percent vulnerability to ocean warming (E), predominant occurrence at depths of 20 disease (C), and acidification (E); low with 50 percent limited in scope), to 100 m reduces its exposure to managing areas for protection and relative recruitment rate (E); moderate disturbance events that have resulted in conservation (88 percent with 31 overall distribution (based on narrow the decreased resilience of reefs in the percent limited in scope). The most geographic distribution and wide depth Caribbean and moderates vulnerability common regulatory mechanisms in distribution (E); restriction to the to extinction over the foreseeable future. place for A. lamarcki are reef fishing Caribbean (E); and inadequacy of Agaricia lamarcki’s life history regulations and area management for regulatory mechanisms (D). characteristics of large colony size and protection and conservation. However, In this final rule, we changed the long life span have enabled it to remain half of the reef fishing regulations are listing determination for A. lamarcki relatively persistent despite slow growth limited in scope and may not provide from threatened to not warranted. We and low recruitment rates, thus substantial protection for the species. made this determination based on a General coral protection and collection moderating vulnerability to extinction. more species-specific and holistic laws, along with pollution control laws, Although we concluded that A. assessment of whether this species are much less common regulatory lamarcki is likely highly susceptible to meets the definition of either a mechanisms for the management of A. disease, population level effects of threatened or endangered coral, lamarcki. disease have not been documented in A. including more appropriate lamarcki thus far, indicating the consideration of the buffering capacity Vulnerability to Extinction currently low vulnerability to extinction of this species’ spatial and demographic As explained above in the Risk from this threat. Additionally, although traits to lessen its vulnerability to Analyses section, a species’ A. lamarcki has been observed to have threats. Thus, based on the best vulnerability to extinction results from high levels of warming-induced available information above on A. the combination of its spatial and bleaching, bleaching-related mortality lamarcki’ spatial structure, demography, demographic traits, threat appears to be low, indicating that threat susceptibilities, and management susceptibilities, and consideration of the vulnerability to extinction from ocean none of the five ESA listing factors, baseline environment and future warming is currently low. Deeper areas alone or in combination, are causing projections of threats. The SRR stated of A. lamarcki’s range will usually have this species to be likely to become that the factors that increase the lower temperatures than surface waters, endangered throughout its range within extinction risk for A. lamarcki include and acidification is generally predicted the foreseeable future, and thus it is not the widespread decline in to accelerate most in waters that are warranted for listing at this time environmental conditions in the deeper and cooler than those in which because: Caribbean, potential losses to disease, the species occurs. Agaricia lamarcki’s (1) Agaricia lamarcki’s predominant severe effects of bleaching, and limited habitat includes shaded or reduced light occurrence at depths of 20 to 100 m in sediment tolerance. Factors that reduce environments, slopes, walls, and heterogeneous habitats, including extinction risk include occurrence mesophotic reefs. This moderates shaded or reduced light environments, primarily at great depth, where vulnerability to extinction over the on slopes and walls, and on mesophotic disturbance events are less frequent, and foreseeable future because the species is reefs, throughout the Caribbean basin life history characteristics that have not limited to one habitat type but reduces exposure to any given threat allowed the species to remain relatively occurs in numerous types of reef event or adverse condition that does not persistent compared to other deep corals environments that are predicted, on occur uniformly throughout the species’ despite low rates of sexual recruitment. local and regional scales, to experience range. As explained above in the Subsequent to the proposed rule, we highly variable thermal regimes and Threats Evaluation section, we have not received and gathered supplemental ocean chemistry at any given point in identified any threat that is expected to species- or genus-specific information, time. Agaricia lamarcki’s absolute occur uniformly throughout the species described above, that expands our abundance has been estimated as at range within the foreseeable future; and

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(2) Agaricia lamarcki’s absolute information we found on was 0.6 ± 6.4 percent, which was the abundance is at least tens of millions of Mycetophyllia’s abundance and eighth highest out of 25 of the most colonies based on estimates from two population trends includes the abundant species (Lirman et al., 2011). locations. Absolute abundance is higher following. Percent cover of During the 2010 cold-water event, than estimates from these locations Mycetophyllia spp. between 2001 and average mortality of Mycetophyllia spp. since it occurs in many other locations 2006 was less than approximately 0.02 across 76 sites from the lower Florida throughout its range. This provides percent on St. John (233 sites surveyed) Keys to Martin County was 15.0 ± 28.3 buffering capacity in the form of and St. Croix (768 sites surveyed), U.S. percent, which was the eleventh highest absolute numbers of colonies and Virgin Islands and La Parguera, Puerto of the 25 most abundant species (Lirman variation in susceptibility between Rico (Waddell and Clarke, 2008). et al., 2011). individual colonies. As discussed in the Similarly, cover of Mycetophyllia spp. During the 2005 bleaching event, Corals and Coral Reefs section above, on the mesophotic Hind Bank in the Mycetophyllia spp. were among the the more colonies a species has, the U.S. Virgin Islands was 0.02 ± 0.01 most severely affected of 22 coral lower the proportion of colonies that are percent in 2007 (Smith et al., 2010). species reported to have bleached across likely to be exposed to a particular Cover of Mycetophyllia spp. was 0.1 91 of 94 sites in northeast St. Croix, U.S. threat at a particular time, and all percent between 2002 and 2004 on four Virgin Islands (Wilkinson and Souter, individuals that are exposed will not islands in the Bahamas Archipelago 2008). In the U.S. Virgin Islands, the one have the same response. (Roff et al., 2011). Between 2005 and colony of Mycetophyllia sp. observed at Notwithstanding the projections 2007, Mycetophyllia spp. comprised 0.1 18 sites, bleached during 2005. Six through 2100 that indicate increased percent or less of the coral cover and colonies were subsequently monitored severity over time of the three high occurred in densities of 1.0 colony per after the 2010 mild bleaching event with importance threats, the combination of 10 m2 in parts of southeast Florida and average of eight percent bleaching these biological and environmental the Florida Keys (Wagner et al., 2010). (Smith et al., 2013b). characteristics indicates that the species In Roatan, Honduras, Mycetophyllia sp. Supplemental information we found possesses sufficient buffering capacity cover in permanent photo-stations on the susceptibility of Mycetophyllia to to avoid being in danger of extinction increased between 1996 and 1998 from disease includes the following. White within the foreseeable future throughout 0.57 percent to 0.77 percent but plague (Nugues, 2002) and red band its range. It is possible that this species’ subsequently decreased to 0.26 percent disease (Waddell, 2005) have been extinction risk may increase in the in 2003 and 0.15 percent in 2005 (Riegl reported to infect Mycetophyllia species. future if global threats continue and et al., 2009). In 2004, prevalence of disease in worsen in severity, and the species’ Susceptibility to Threats Mycetophyllia was approximately two exposure to the threats increases to three percent in Mexico (Harvell et throughout its range. Should the species The SRR, SIR, and public comments al., 2007). experience reduced abundance or range did not provide information on constriction of a certain magnitude, the Mycetophyllia’s susceptibility to threats. Mycetophyllia ferox Supplemental information we found on ability of these characteristics to Introduction moderate exposure to threats will Mycetophyllia’s susceptibility to ocean diminish. However, A. lamarcki is not warming includes the following. During The SRR and SIR provided the likely to become of such low abundance the 1995 bleaching event in Belize, 24 following information on M. ferox’s or so spatially fragmented as to be in percent of 21 colonies monitored morphology and taxonomy. danger of extinction due to depensatory Mycetophyllia bleached (McField, Mycetophyllia ferox forms a thin, processes, the potential effects of 1999). In Roatan, Honduras, 11 percent encrusting plate that is weakly attached. environmental stochasticity, or the [sic]of 10 monitored Mycetophyllia sp. Mycetophyllia ferox is taxonomically potential for mortality from catastrophic colonies bleached and 11 percent [sic] distinct. Maximum colony size is 50 cm. events within the foreseeable future partially bleached during the 1998 Public comments did not provide new throughout its range. Therefore, A. bleaching event; mortality of or supplemental information on M. lamarcki is not warranted for listing at Mycetophyllia colonies was 11 percent ferox’s taxonomy or morphology. this time under any of the listing factors, (Riegl et al., 2009). Supplemental information we found on and we withdraw our proposal to list Bleaching of Mycetophyllia was 62 M. ferox’s taxonomy and morphology the species as threatened. percent across all 28 locations surveyed includes the following. Zlatarski and in Puerto Rico during the 2005 Estalella (1982) reported 14 out of 25 Genus Mycetophyllia temperature anomaly (Waddell and Mycetophyllia colonies collected from There are five species in the genus Clarke, 2008). Additionally, a post- Cuba were intermediate between M. Mycetophyllia that all occur in the bleaching outbreak of white plague ferox, and M. lamarkiana, and parts of western Atlantic and Caribbean (Veron, resulted in a massive collapse of two colonies were comparable to M. 2000). Most species of Mycetophyllia Mycetophyllia colonies at most reefs on ferox or M. lamarkiana, illustrating can be difficult to distinguish in the the east, south, and west coasts of potential morphological plasticity field, and many studies report data to Puerto Rico and reproductive failure between species. during the 2006 mass spawning the genus level rather than species. Spatial Information Therefore, all information reported for (Waddell and Clarke, 2008). Off Mona the genus appears in this section, and and Desecheo Islands, Puerto Rico in The SRR and SIR provided the information reported specifically for M. 2005, paling occurred in 65 percent of following information on M. ferox’s ferox is presented in the species section. Mycetophyllia colonies, and bleaching distribution, habitat, and depth range. occurred in 10 percent (Bruckner and Mycetophyllia ferox occurs in the Demographic Information Hill, 2009). western Atlantic and throughout the The SRR, SIR, and the public In surveys conducted between August wider Caribbean. It has not been comments did not provide information and October 2005 to 2009 from the reported in the Flower Garden Banks on Mycetophyllia abundance or lower Florida Keys to Martin County, (Gulf of Mexico) or in Bermuda. It has population trends. Supplemental average mortality of Mycetophyllia spp. been reported in reef environments in

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water depths of 5 to 90 m, including million (SE) in 2008. The number of (Waddell, 2005). Between 2005 and shallow and mesophotic habitats. colonies in 2006 was similar between 2010, M. ferox was one of 42 species The public comments did not provide the 0 to 10 cm and 10 to 20 cm size surveyed and was found the least new or supplemental information on M. classes, and the largest colonies were in abundant being observed at densities of ferox’s distribution, habitat, or depth the 20 to 30 cm size class. Greatest 0.02 and 0.01 colonies per 10 m2 on range. Supplemental information we partial mortality was around 10 percent. mid-channel reefs and fore-reefs, found on M. ferox’s distribution Two years later, in 2008, the highest respectively, on the Florida reef tract includes the following. Veron (2014) proportion of colonies was in the 20 to (Burman et al., 2012). confirms the occurrence of M. ferox in 30 cm size class, and the largest All information on M. ferox’s seven out of a possible 11 ecoregions in colonies were in the 40 to 50 cm size abundance and population trends can the Caribbean and western Atlantic that class. The greatest partial mortality was be summarized as follows. contain corals. The four ecoregions about 60 percent in the 30 to 40 cm size Mycetophyllia ferox has been reported where it is not reported are the Flower class, however the number of colonies at to occur on 3 to 50 percent of reefs Garden Banks, off the coasts of that size were few (Miller et al., 2013). surveyed and is one of the least Bermuda, Brazil, and the southeast U.S. Supplemental information we found common coral species observed. On north of south Florida. We did not find on M. ferox’s abundance and population reefs where M. ferox is found, it any supplemental information on M. trends confirms M. ferox’s low percent generally occurs at abundances of less ferox’s habitat or depth range. cover, encounter rate, and density. In a than one colony per 10 m2 and percent survey of Utila, Honduras between 1999 Demographic Information cover of less than 0.1 percent. Based on and 2000, M. ferox was observed at eight population estimates, there are at least The SRR and SIR provided the percent of 784 surveyed sites and was hundreds of thousands of M. ferox following information on M. ferox’s the 36th most commonly observed out colonies present in the Florida Keys and abundance and population trends. of 46 coral species; other Mycetophyllia Mycetophyllia ferox is usually Dry Tortugas combined. Absolute species were seen more commonly abundance is higher than the estimate uncommon or rare, constituting less (Afzal et al., 2001). In surveys of remote than 0.1 percent of all coral species at from these two locations given the southwest reefs of Cuba, M. ferox was presence of this species in many other generally less than one percent of the observed at one of 38 reef-front sites, benthic cover. Density of M. ferox in ± locations throughout its range. Low with average abundance was 0.004 encounter rate and percent cover southeast Florida and the Florida Keys 0.027 (standard deviation (SD)) colonies coupled with the tendency to include was approximately 0.8 colonies per 10 per 10 m transect; this was Mycetophyllia spp. at the genus level m2 between 2005 and 2007. There is comparatively lower than the other make it difficult to discern population indication that the species was much three Mycetophyllia species observed trends of M. ferox from monitoring data. more abundant in the upper Florida (Alcolado et al., 2010). Between 1998 However, reported losses of M. ferox Keys in the 1970s. In a survey of 97 and 2004, cover of M. ferox ranged from monitoring stations in the Florida stations in the Florida Keys, M. ferox between 0.3 and 0.4 percent in three of Keys and Dry Tortugas (63 to 80 percent declined in occurrence from 20 stations six sites monitored in Colombia loss) indicate population decline in in 1996 to four stations in 2009. At 21 (Rodriguez-Ramirez et al., 2010). In these locations. Based on declines in stations in the Dry Tortugas, M. ferox Barbados, M. ferox was observed on one declined in occurrence from eight of seven reefs surveyed, and the average Florida, we conclude M. ferox has likely stations in 2004 to three stations in cover was 0.04 percent (Tomascik and declined throughout its range. 2009. Sander, 1987). Other Biological Information The public comments provided the Benthic cover of M. ferox in the Red following supplemental information on Hind Marine Conservation District off The SRR and SIR provided the M. ferox’s abundance. In stratified St. Thomas, U.S. Virgin Islands, which following information on M. ferox’s life random surveys in the Florida Keys, M. includes mesophotic coral reefs, was history. Mycetophyllia ferox is a ferox ranked 39th most abundant out of 0.003 ± 0.004 percent in 2007, hermaphroditic brooding species. 47 in 2005, 43rd out of 43 in 2009, and accounting for 0.02 percent of coral Colony size at first reproduction is 40th out of 40 in 2012. Extrapolated cover, and ranking 20th highest in cover greater than 100 cm2. Recruitment of M. population estimates were 1.0 ± 0.7 (SE) out of 21 coral species (Nemeth et al., ferox appears to be very low, even in million in 2005, 9,500 ± 9,500 (SE) 2008; Smith et al., 2010). In the U.S. studies from the 1970s. colonies in 2009, and 7,000 ± 7,000 (SE) Virgin Islands between 2001 and 2012, The public comments did not provide in 2012 . These abundance estimates are cover of M. ferox appeared in 12 of 33 new or supplemental information on M. based on random surveys, and survey sites and accounted for 0.01 ferox’s life history. Supplemental differences between years are more percent of the benthos, and 0.07 percent information we found on M. ferox’s life likely a result of sampling effort rather of the coral cover, ranking as 13th most history includes the following. than population trends. The most common (Smith, 2013). Mycetophyllia ferox has a lower abundant size class was 10 to 20 cm In 1981, M. ferox was observed on one fecundity compared to M. aliciae, M. diameter that equaled the combined of four reefs surveyed in the upper lamarckiana and M. danaana (Morales abundance of the other size classes. The Florida Keys at 0.1 percent cover Tirado, 2006). Over a 10 year period, no largest size class was 30 to 40 cm. (Burns, 1985). In surveys of the Florida colonies of M. ferox were observed to Average partial mortality per size class Keys between 1996 and 2003, cover of recruit to an anchor-damaged site in the ranged from nearly 0 to 50 percent and M. ferox was 0.022, 0.005, and less than U.S. Virgin Islands although adults were was greatest in the 20 to 30 cm size class 0.001 percent on patch reefs, deep observed on the adjacent reef (Rogers (Miller et al., 2013). offshore reefs, and shallow offshore and Garrison, 2001). Darling et al. In the Dry Tortugas, Florida, M. ferox reefs, respectively (Somerfield et al., (2012) performed a biological trait-based ranked 35th most abundant out of 43 2008). At permanent monitoring stations analysis to categorize coral species into species in 2006 and 30th out of 40 in in the Florida Keys, the number of four life history strategies: Generalist, 2008. Population estimates were 0.5 ± stations where M. ferox was present weedy, competitive, and stress-tolerant. 0.4 (SE) million in 2006 and 0.5 ± 0.2 declined between 1996 and 2003 Mycetophyllia ferox was classified as a

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‘‘weedy’’ species, thus likely more However, the available information does causing heavy mortality at the genus tolerant of environmental stress. not support a more precise description level in Puerto Rico after the 2005 of susceptibility to this threat. bleaching event. We conclude that the Susceptibility to Threats The SRR and SIR provided the susceptibility of M. ferox to disease is The threat susceptibility information following information on the high. from the SRR and SIR was interpreted susceptibility of M. ferox to The SIR and SRR did not provide any in the proposed rule for M. ferox’s acidification. No specific research has species-specific information on the vulnerabilities to threats as follows: addressed the effects of acidification on trophic effects of fishing on M. ferox. High vulnerability to disease and the genus Mycetophyllia. However, most The public comments did not provide nutrient enrichment; moderate corals studied have shown negative new or supplemental information, and vulnerability to ocean warming, relationships between acidification and we did not find new or supplemental acidification, trophic effects of fishing, growth, and acidification is likely to information on the trophic effects of and sedimentation; and low contribute to reef destruction in the fishing on M. ferox. However, due to the vulnerability to sea level rise, predation, future. While ocean acidification has level of reef fishing conducted in the and collection and trade. not been demonstrated to have caused Caribbean, coupled with Diadema die- The SRR and SIR provided the appreciable declines in coral off and lack of significant recovery, following information on M. ferox’s populations to date, it is considered to competition with algae can adversely susceptibility to ocean warming. No become a significant threat to corals by affect coral recruitment. Thus, M. ferox bleached M. ferox colonies were 2100. likely has some susceptibility to the observed in Florida or Barbados in a The public comments did not provide trophic effects of fishing given its low wide-scale survey during the 2005 mass- new or supplemental information on the recruitment rates. The available bleaching event, although the number of susceptibility of M. ferox to information does not support a more colonies was small. acidification, and we did not find any precise description of susceptibility. The public comments did not provide new or supplemental information. The SRR and SIR provided the new or supplemental information on the All sources of information are used to following information on the susceptibility of M. ferox to ocean describe M. ferox’s susceptibility to susceptibility of M. ferox to nutrient warming. Supplemental information we acidification as follows. There is enrichment. Mycetophyllia ferox found on the susceptibility of M. ferox uncertainty about how M. ferox will appeared to be absent at fringing reef to ocean warming includes the respond to ocean acidification. Based on sites in Barbados impacted by sewage following. In surveys of the lower the negative effects of acidification on pollution. Florida Keys and Dry Tortugas during growth of most corals, M. ferox likely The public comments did not provide the 1998 bleaching event, approximately has some susceptibility to acidification. any new or supplemental information 20 percent of M. ferox colonies The available information does not on the susceptibility of M. ferox to bleached; out of the 14 species reported support a more precise description of nutrient enrichment, and we did not to have experienced bleaching of at least susceptibility. find any new or supplemental 50 percent of the colony, M. ferox was The SRR and SIR provided the information. one of the least affected (Waddell, following information on M. ferox’s All sources of information are used to 2005). Approximately 50 percent of M. susceptibility to disease. Mycetophyllia describe M. ferox’s susceptibility to ferox colonies bleached at 12 locations ferox is susceptible to white plague. nutrient enrichment as follows. in Puerto Rico during the 2005 Diseased M. ferox colonies were Mycetophyllia ferox may be susceptible bleaching event (Waddell and Clarke, reported in the upper Florida Keys in to nutrient enrichment as evidenced by 2008). During the 2005 Caribbean the mid-1970s; between 24 and 73 its absence from eutrophic sites in one bleaching event, neither of the two percent of M. ferox colonies were location. However, there is uncertainty colonies of M. ferox monitored at six infected per site. At one reef site, 20 to about whether the absence is a result of sites in Barbados bleached; an average 30 percent of the M. ferox colonies died eutrophic conditions or a result of of 71 percent of all coral colonies from disease during a one-year period. uncommon or rare occurrence. bleached at those six sites during the The public comments did not provide Therefore, we conclude that M. ferox event (Oxenford et al., 2008). new or supplemental information on the likely has some susceptibility to All sources of information are used to susceptibility of M. ferox to disease. nutrient enrichment. However, the describe M. ferox’s susceptibility to Supplemental information we found on available information does not support ocean warming as follows. The the susceptibility of M. ferox to disease a more precise description of bleaching reports available specifically includes the following. Porter et al. susceptibility. for M. ferox and at the genus level (2001) report the loss of M. ferox from The SRR and SIR did not provide any indicate similar trends of relatively low many of the permanent monitoring species or genus information on the bleaching observed in 1995, 1998, and stations (160 stations at 40 sites) in the susceptibility of M. ferox to 2010 (less than 25 percent) and higher Florida Keys between 1996 and 1998 sedimentation but provided the levels (50 to 65) or no bleaching in the due to coral disease. following. Land-based sources of more severe 2005 bleaching event. All sources of information are used to pollution (including sediment) often act Reproductive failure and a disease describe M. ferox’s susceptibility to in concert rather than individually and outbreak were reported for the genus disease as follows. From reports in the are influenced by other biological (e.g., after the 2005 bleaching event. Although Florida Keys, M. ferox appears to be herbivory) and hydrological factors. bleaching of most coral species is highly susceptible to disease, Collectively, land-based sources of spatially and temporally variable, specifically white plague, and reports of pollution are unlikely to produce understanding the susceptibility of M. high losses and correlation with higher extinction at a global scale; however, ferox is somewhat confounded by the temperatures date back to the mid-1970s they may pose significant threats at species’ low sample size in any given (Dustan, 1977). Although heavy impacts local scales and reduce the resilience of survey due to its low encounter rate. We of disease on M. ferox have not been corals to bleaching. conclude that M. ferox has some reported in other locations, an outbreak The public comments did not provide susceptibility to ocean warming. of white plague was credited with new or supplemental information on the

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susceptibility of M. ferox to encompass 26 kingdom’s or countries’ species’ spatial and demographic traits sedimentation, and we did not find any EEZs. The 26 kingdoms and countries to moderate or exacerbate its new or supplemental information. We are Antigua & Barbuda, Bahamas, vulnerability to extinction, as opposed conclude that M. ferox has some level of Barbados, Belize, Colombia, Costa Rica, to the approach we used in the susceptibility to sedimentation, but the Cuba, Dominica, Dominican Republic, proposed rule, which emphasized the available information does not support French Antilles, Grenada, Guatemala, species’ susceptibility to threats. a more precise description of Haiti, Honduras, Jamaica, Kingdom of The following characteristics of M. susceptibility. the Netherlands, Mexico, Nicaragua, ferox, in conjunction with the The SRR and SIR provided the Panama, St. Kitts & Nevis, St. Lucia, St. information described in the Corals and following information on the Vincent & Grenadines, Trinidad and Coral Reefs section, Coral Habitat sub- susceptibility of M. ferox to predation. Tobago, United Kingdom (British section, and Threats Evaluation section Mycetophyllia ferox has not been Overseas Territories), United States above, affect its vulnerability to susceptible to predation. Public (including U.S. Caribbean Territories), extinction currently and over the comments did not provide new or and Venezuela. The regulatory foreseeable future. Mycetophyllia ferox supplemental information on M. ferox’s mechanisms relevant to M. ferox, has declined due to disease in at least susceptibility to predation, and we did described first as a percentage of the a portion of its range and has low not find any new or supplemental above kingdoms and countries that recruitment, which limits its capacity information. We conclude that M. ferox utilize them to any degree, and, second for recovery from mortality events and has low susceptibility to predation. as the percentages of those kingdoms exacerbates vulnerability to extinction. The SRR and SIR did not provide and countries whose regulatory Despite the large number of islands and species-specific information on the mechanisms may be limited in scope, environments that are included in the effects of sea level rise on M. ferox. The are as follows general coral protection species’ range, geographic distribution SRR described sea level rise as an (31 percent with 12 percent limited in in the highly disturbed Caribbean overall low to medium threat for all scope), coral collection (50 percent with exacerbates vulnerability to extinction coral species. The public comments did 27 percent limited in scope), pollution over the foreseeable future because M. not provide new or supplemental control (31 percent with 15 percent ferox is limited to an area with high, information on M. ferox’s susceptibility limited in scope), fishing regulations on localized human impacts and predicted to sea level rise, and we did not find any reefs (73 percent with 50 percent increasing threats. Its depth range of five new or supplemental information. Thus, limited in scope), managing areas for to 90 meters moderates vulnerability to we conclude that M. ferox has some protection and conservation (88 percent extinction over the foreseeable future susceptibility to sea level rise, but the with 31 percent limited in scope). The because deeper areas of its range will available information does not provide most common regulatory mechanisms in usually have lower temperatures than a more precise description of place for M. ferox are reef fishing surface waters, and acidification is susceptibility. regulations and area management for generally predicted to accelerate most in The SRR and SIR provided the protection and conservation. However, waters that are deeper and cooler than following information on M. ferox’s half of the reef-fish fishing regulations those in which the species occurs. Its susceptibility to collection and trade. are limited in scope and may not habitat includes shallow and Mycetophyllia ferox is not reported to be provide substantial protection for the mesophotic reefs which moderates an important species for trade. Exports coral species. General coral protection vulnerability to extinction over the of M. ferox were ten pieces in 2000, two and collection laws, along with foreseeable future because the species in 2003, and five in 2007. pollution control laws, are much less occurs in numerous types of reef The public comments did not provide common regulatory mechanisms for the environments that are predicted, on new or supplemental information on the management of M. ferox. local and regional scales, to experience susceptibility of M. ferox to collection highly variable thermal regimes and and trade. Supplemental information we Vulnerability to Extinction ocean chemistry at any given point in found confirmed low collection and As explained above in the Risk time. Mycetophyllia ferox is usually trade of M. ferox with gross exports Analyses section, a species’ uncommon to rare throughout its range. between 2000 and 2012 averaging fewer vulnerability to extinction results from Its absolute abundance has been than two corals per year (data available the combination of its spatial and estimated as at least hundreds of at http://trade.cites.org/). Thus, we demographic traits, threat thousands of colonies in the Florida conclude that M. ferox has low susceptibilities, and consideration of the Keys and Dry Tortugas combined and is susceptibility to collection and trade. baseline environment and future higher than the estimate from these two projections of threats. The SRR stated locations due to the occurrence of the Regulatory Mechanisms that the factors that increase the species in many other areas throughout In the proposed rule, we relied on extinction risk for M. ferox include its range. Its abundance, combined with information from the Final Management disease, rare abundance, and observed spatial variability in ocean warming and Report for evaluating the existing declines in abundance. acidification across the species’ range, regulatory mechanisms for controlling Subsequent to the proposed rule, we moderate vulnerability to extinction threats to all corals. However, we did received and gathered supplemental because the threats are non-uniform, not provide any species-specific species- or genus-specific information, and there will likely be a large number information on the regulatory described above, that expands our of colonies that are either not exposed mechanisms or conservation efforts for knowledge regarding the species’ or do not negatively respond to a threat M. ferox. Public comments were critical abundance, distribution, and threat at any given point in time. of that approach, and we therefore susceptibilities. We developed our attempt to analyze regulatory assessment of the species’ vulnerability Listing Determination mechanisms and conservation efforts on to extinction using all the available In the proposed rule, using the a species basis, where possible, in this information. As explained in the Risk determination tool formula approach, final rule. Records confirm that M. ferox Analyses section, our assessment in this M. ferox was proposed for listing as occurs in seven Atlantic ecoregions that final rule emphasizes the ability of the endangered because of: High

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vulnerability to disease (C); moderate (5) Mycetophyllia ferox’s low not warrant listing as endangered at this vulnerability to ocean warming (E) and recruitment limits the capacity for time. acidification (E); high vulnerability to recovery from threat-induced mortality Range-wide, multitudes of nutrient over-enrichment (A and E); rare events throughout the range over the conservation efforts are already broadly general range-wide abundance (E); foreseeable future. employed that are likely benefiting M. decreasing trend in abundance (E); low The combination of these ferox. However, considering the global relative recruitment rate (E); moderate characteristics and future projections of scale of the most important threats to overall distribution (based on narrow threats indicates that the species is the species, and the ineffectiveness of geographic distribution and wide depth likely to be in danger of extinction conservation efforts at addressing the distribution (E); restriction to the within the foreseeable future throughout root cause of global threats (i.e., GHG Caribbean (E); and inadequacy of its range and warrants listing as emissions), we do not believe that any regulatory mechanisms (D). threatened at this time due to factors A, current conservation efforts or In this final rule, we changed the C, D, and E. conservation efforts planned in the listing determination for M. ferox from The available information above on future will result in affecting the endangered to threatened. We made this M. ferox’s spatial structure, species’ status to the point at which determination based on a more species- demography, threat vulnerabilities, and listing is not warranted. specific and holistic approach, management also indicate that the Genus Dendrogyra including consideration of the buffering species is not currently in danger of capacity of this species’ spatial and extinction and thus does not warrant The SRR and SIR provided the demographic traits, and the best listing as Endangered because: following information on morphology available information above on M. (1) While Mycetophyllia ferox’s and taxonomy of Dendrogyra. ferox’s spatial structure, demography, distribution within the Caribbean Dendrogyra cylindrus is the only species threat susceptibilities, and management. increases its risk of exposure to threats in the genus Dendrogyra. It is easily This combination of factors indicates as described above, its depth identifiable, and there is no taxonomic that M. ferox is likely to become distribution is five to 90 m and its confusion. The public comments did endangered throughout its range within habitat includes various shallow and not provide new or supplemental the foreseeable future, and thus mesophotic reef environments. This information on the morphology or warrants listing as threatened at this moderates vulnerability to extinction taxonomy of D. cylindrus, and we did time, because: currently because the species is not not find any new or supplemental (1) Mycetophyllia ferox is highly information. susceptible to disease (C) and limited to one habitat type but occurs in susceptible to ocean warming (ESA numerous types of reef environments Dendrogyra cylindrus that will experience highly variable Factor E), acidification (E), trophic Introduction effects of fishing (A), nutrients (A, E), thermal regimes and ocean chemistry on and sedimentation (A, E). These threats local and regional scales at any given The SRR and SIR provided the are expected to continue and increase point in time, as described in more following information on the into the future. In addition, the species detail in the Coral Habitat and Threats morphology of D. cylindrus. Dendrogyra is at heightened extinction risk due to Evaluation sections. There is no cylindrus forms cylindrical columns on inadequate existing regulatory evidence to suggest that the species is so top of encrusting bases. Colonies are mechanisms to address global threats spatially fragmented that depensatory generally grey-brown in color and may (D); processes, environmental stochasticity, reach three meters in height. Tentacles (2) Mycetophyllia ferox has or the potential for catastrophic events remain extended during the day, giving experienced significant declines in currently pose a high risk to the survival columns a furry appearance. of the species; and Florida and has likely experienced Spatial Information decline in other locations in its range; (2) Mycetophyllia ferox’s absolute (3) Mycetophyllia ferox has a usually abundance is at least hundreds of The SRR and SIR provided the uncommon to rare occurrence thousands of colonies based on following information on D. cylindrus’s throughout its range, which heightens estimates from two locations. Absolute distribution, habitat, and depth range. the potential effect of localized abundance is higher than estimates from Dendrogyra cylindrus is present in the mortality events and leaves the species these locations since M. ferox occurs in western Atlantic and throughout the vulnerable to becoming of such low many other locations throughout its greater Caribbean. The SRR reports a abundance within the foreseeable future range. This absolute abundance allows single known colony in Bermuda that is that it may be at risk from depensatory for variation in the responses of in poor condition. Dendrogyra cylindrus processes, environmental stochasticity, individuals to threats to play a role in inhabits most reef environments in or catastrophic events, as explained in moderating vulnerability to extinction water depths ranging from one to 25 m. more detail in the Corals and Coral for the species to some degree, as The public comments did not provide Reefs and Risk Analyses sections; described in more detail in the Corals new or supplemental information on D. (4) Mycetophyllia ferox is and Coral Reefs section. Its absolute cylindrus’s distribution, habitat, or geographically located in the highly abundance indicates it is currently able depth range. Supplemental information disturbed Caribbean where localized to avoid high mortality from we found on D. cylindrus’s distribution, human impacts are high and threats are environmental stochasticity, and habitat, and depth range include the predicted to increase as described in the mortality of a high proportion of its following. Dendrogyra cylindrus is Threats Evaluation section. A range population from catastrophic events. absent from the southwest Gulf of constrained to this particular geographic The combination of these Mexico (Tunnell, 1988). There is fossil area that is likely to experience severe characteristics indicates that the species evidence of the presence of D. cylindrus and increasing threats indicates that a does not exhibit the characteristics of off Panama less than 1000 years ago, but high proportion of the population of this one that is currently in danger of it has been reported as absent today species is likely to be exposed to those extinction, as described previously in (Florida Fish and Wildlife Conservation threats over the foreseeable future; and the Risk Analyses section, and thus does Commission, 2013). Veron (2014)

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confirms the presence of D. cylindrus in 600 surveys from Key Biscayne to Key declined to 0.44 percent in 2003 and seven out of a potential 11 ecoregions in West, Florida in 2012, with the authors 0.43 percent in 2005 (Riegl et al., 2009). the western Atlantic and wider- noting sampling design was not In the U.S. Virgin Islands, seven percent Caribbean that are known to contain optimized for this species. This species of 26 monitored colonies experienced corals. The four ecoregions in which it was not reported in the Dry Tortugas in total colony mortality between 2005 and is not reported are the Flower Garden 2006 and 2008, and rarely encountered 2007, though the very low cover of D. Banks and off the coasts of Bermuda, during pilot studies conducted over cylindrus (0.04 percent) remained Brazil, and the southeast U.S. north of several years (1999 to 2002) ranking relatively stable during this time period south Florida. Although D. cylindrus’s 49th out of 49 coral species (Miller et (Smith et al., 2013b). depth range is 1 to 25 m, it is most al., 2013). All sources of information on D. common between five and 15 m depth Supplemental information we found cylindrus’s abundance and population (Acosta and Acevedo, 2006; Cairns, on D. cylindrus’s abundance and trends can be summarized as follows. 1982; Goreau and Wells, 1967). population trends confirms the Based on population estimates, there are All information on D. cylindrus’s uncommon occurrence, rare encounter at least tens of thousands of D. cylindrus distribution can be summarized as rate, low percent cover, and low colonies present in the Florida Keys. follows. Dendrogyra cylindrus is density. During surveys of Utila, Absolute abundance is higher than the distributed throughout most of the Honduras between 1999 and 2000, D. estimate from this location given the greater Caribbean in most reef cylindrus was sighted in 19.6 percent of presence of this species in many other environments between 1 to 25 m depth. 784 surveys and ranked 26th most locations throughout its range. Although It currently appears to be absent from common in abundance out of 48 coral there is evidence of potentially higher Panama where it historically occurred species (Afzal et al., 2001). In surveys of population levels in some areas of the within the last 1000 years. the upper Florida Keys in 2011, D. Caribbean during the Pleistocence, D. cylindrus was the second rarest out of cylindrus is currently uncommon to Demographic Information 37 coral species and encountered at one rare. Few studies report D. cylindrus The SRR and SIR provided the percent of sites (Miller et al., 2011b). population trends, and the low following information on D. cylindrus’s In stratified random surveys from abundance and infrequent encounter abundance and population trends. Palm Beach County to the Dry Tortugas, rate in monitoring programs result in Dendrogyra cylindrus is uncommon but Florida between 2005 and 2010, D. small samples sizes. The low coral cover conspicuous with scattered, isolated cylindrus was seen only on the ridge of this species renders monitoring data colonies. It is rarely found in complex and mid-channel reefs at difficult to extrapolate to realize trends. aggregations. Dendrogyra cylindrus has densities of 1.09 and 0.1 colonies per 10 Therefore, we conclude that D. been reported to be common on m2, respectively (Burman et al., 2012). cylindrus is naturally uncommon to rare Pleistocene reefs around Grand Cayman, Average number of D. cylindrus and that trends are unknown. but rare on modern reefs. In monitoring colonies in remote reefs off southwest studies, cover is generally less than one Cuba was 0.013 ± 0.045 colonies per 10 Other Biological Information percent. Between 2005 and 2007, mean m transect, and the species ranked sixth The SRR and SIR provided the density of D. cylindrus was rarest out of 38 coral species (Alcolado following information on D. cylindrus’s approximately 0.5 colonies per 10 m2 in et al., 2010). life history. Dendrogyra cylindrus is a the Florida Keys. In a study of D. Out of 283 D. cylindrus colonies at gonochoric (separate sexes) broadcast cylindrus demographics at Providencia Providencia Island, Colombia, 70 were spawning species with relatively low Island, Colombia, a total of 283 D. fragments resulting from asexual annual egg production for its size. The cylindrus colonies were detected in a fragmentation, and no sexual recruits combination of gonochoric spawning survey of 1.66 km2 for and overall were observed. Size class distribution with persistently low population density of 172.0 ± 177.0 (SE) colonies was skewed to smaller size classes less densities is expected to yield low rates per km2. than 60 cm in height, and average of successful fertilization and low larval The public comments provided colony height was 73.8 ± 46.0 cm supply. Sexual recruitment of this supplemental information on D. (Acosta and Acevedo, 2006). species is low, and reported juvenile cylindrus’s abundance but not on Dendrogyra cylindrus’s average colonies in the Caribbean are lacking. population trends. In stratified random percent cover was 0.002 on patch reefs Dendrogyra cylindrus can propagate by samples of the Florida Keys, D. and 0.303 in shallow offshore reefs in fragmentation following storms or other cylindrus ranked least common out of annual surveys of 37 sites in the Florida physical disturbance. Average growth 47 coral species in 2005 and 41 out of Keys between 1996 and 2003 rates of 1.8 to 2.0 cm per year in linear 43 species in 2009. Based on random (Somerfield et al., 2008). At permanent extension have been reported in the surveys stratified by habitat type, monitoring stations in the U.S. Virgin Florida Keys compared to 0.8 cm per extrapolated abundance for the Florida Islands, D. cylindrus has been observed year in Colombia and Curac¸ao. Partial Keys was 23,000 ± 23,000 (SE) colonies in low abundance at 10 of 33 sites and, mortality rates are size-specific with in 2005 and 25,000 ± 25,000 (SE) where present, ranged in cover from less larger colonies having greater rates. colonies in 2009. Because these than 0.05 percent to 0.22 percent Frequency of partial mortality can be population estimates were based on (Smith, 2013). In Dominica, D. cylindrus high (65 percent of 185 colonies random sampling, differences between comprised less than 0.9 percent cover surveyed in Colombia), while the years is more likely a function of and was present at 13.3 percent of 31 amount of partial mortality per colony sampling effort rather than an indication surveyed sites (Steiner, 2003). At seven is generally low (average of 3 percent of of population trends. All D. cylindrus fringing reefs off Barbados, D. cylindrus tissue area affected per colony). colonies reported in 2005 were in the 70 was observed on one reef, and cover was The public comments did not provide to 80 cm diameter size class with less 2.7 ± 1.4 percent (Tomascik and Sander, new or supplemental information on D. than two percent partial mortality. Four 1987). In monitored photo-stations in cylindrus’s life history. Supplemental years later in 2009, all reported colonies Roatan, Honduras, cover of D. cylindrus information we found on D. cylindrus’s were greater than 90 cm. No D. increased slightly from 1.35 percent in life history includes the following. cylindrus colonies were encountered in 1996 to 1.67 percent in 1999 and then Spawning observations have been made

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several nights after the full moon of observed, but during the same event in All sources of information are used to August in the Florida Keys (Neely et al., Barbados 100 percent of 15 D. cylindrus describe D. cylindrus’s susceptibility to 2013; Waddell and Clarke, 2008). colonies bleached. ocean warming as follows. There are Darling et al. (2012) performed a Van Woesik et al. (2012) developed a conflicting characterizations of the biological trait-based analysis to coral resiliency index based on susceptibility of D. cylindrus to categorize coral species into four life biological traits and processes to bleaching. Some locations experienced history strategies: Generalist, weedy, evaluate extinction risk due to high bleaching of up to 100 percent of competitive, and stress-tolerant. The bleaching. Evaluations were performed D. cylindrus colonies during the 2005 classifications were primarily separated at the genus level. They rated the Caribbean bleaching event while others by colony morphology, growth rate, and resiliency of D. cylindrus as 3 out of a had a smaller proportion of colonies reproductive mode. Dendrogyra range of ¥6 to 7 observed in other coral bleach (10 to 50 percent). Reports of low cylindrus was classified as a genera. Less than or equal to ¥3 was mortality after less severe bleaching ‘‘competitive’’ species, thus likely more considered highly vulnerable to indicate potential resilience, though vulnerable to environmental stress. extinction, and greater than or equal to mortality information is absent from The SRR and SIR provided the 4 was considered highly tolerant. Thus, locations that reported high bleaching following other biological information D. cylindrus was rated as moderately frequency. Although bleaching of most for D. cylindrus. Dendrogyra cylindrus tolerant. While this study was included coral species is spatially and temporally appears to be sensitive to cold in the SIR, species-specific findings for variable, understanding the temperatures. Feeding rates (removal of Dendrogyra were not included. The susceptibility of D. cylindrus is further suspended particles in seawater) are low public comments (Comment 47) confounded by the species’ rarity and, relative to most other Caribbean corals, indicated the results of this study hence, low sample size in any given indicating it is primarily a tentacle should be considered in the listing survey. We conclude that although D. feeder rather than a suspension feeder. status of D. cylindrus. cylindrus appears to have resistance to However, D. cylindrus has a relatively The public comments did not provide bleaching from warmer temperatures in high photosynthetic rate, and stable new or supplemental information on the some portions of its range under some isotope values suggest it receives susceptibility of D. cylindrus to ocean circumstances, it is likely to have some substantial amounts of photosynthetic warming. Supplemental information we susceptibility to ocean warming, given products from its zooxanthellae. found confirms the variable the high rates of bleaching observed at The public comments did not provide susceptibility of D. cylindrus to ocean times. However, the available new or supplemental biological warming and bleaching. Dendrogyra information does not support a more information for D. cylindrus. cylindrus was among 42 species detailed description of susceptibility. Supplemental information we found reported not to have bleached at various The SRR and SIR provided the confirms that D. cylindrus is sensitive to locations in the western Atlantic following information on the cold temperatures and is summarized as (British Virgin Islands, Jamaica, and susceptibility of D. cylindrus to follows. In laboratory studies of cold Mona Island) during the 1987 bleaching acidification. No specific research has shock, D. cylindrus had the highest event, while the authors noted these addressed the effects of acidification on zooxanthellae expulsion rate of three species were reported bleached at other the genus Dendrogyra. However, most species tested at 12 degrees C locations or other areas by others corals studied have shown negative (Muscatine et al., 1991). During the (Williams and Bunkley-Williams, 1990). relationships between acidification and 2010 cold water event in the Florida None of the 18 D. cylindrus colonies growth, and acidification is likely to Keys, D. cylindrus was one of the most monitored in Roatan, Honduras contribute to reef destruction in the affected coral species with 100 percent experienced bleaching or mortality in future. While ocean acidification has mortality on surveyed inshore reefs the 1998 event where bleaching ranged not been demonstrated to have caused (Kemp et al., 2011). from zero to 89 percent in the 22 species appreciable declines in coral monitored (Riegl et al., 2009). Across 12 populations so far, it is considered a Susceptibility to Threats locations in Puerto Rico, 100 percent of significant threat to corals by 2100. The threat susceptibility information D. cylindrus colonies bleached during The public comments did not provide from the SRR and SIR was interpreted the 2005 temperature anomaly (Waddell new or supplemental information on the in the proposed rule for D. cylindrus’s and Clarke, 2008). However, Bruckner susceptibility of D. cylindrus to vulnerabilities to threats as follows: and Hill (2009) report less severe D. acidification, and we did not find any High vulnerability to disease; moderate cylindrus bleaching during the 2005 new or supplemental information. vulnerability to ocean warming, event in Puerto Rico; approximately 25 All sources of information are used to acidification, trophic effects of fishing, percent paled and 10 percent bleached describe D. cylindrus’s susceptibility to sedimentation, and nutrient enrichment; on reefs off Mona and Desecheo Islands, acidification as follows. Dendrogyra and low vulnerability to sea level rise, which was relatively low compared to cylindrus likely has some susceptibility predation, and collection and trade. some other species such as Orbicella to acidification, but the available The SRR and SIR provided the faveolata, which had approximately 60 information does not support a more following information on the percent bleached colonies. At Dairy Bull precise description of susceptibility to susceptibility of D. cylindrus to ocean Reef in Jamaica, 50 percent of D. this threat. warming. There are conflicting cylindrus colonies bleached during the The SRR and SIR provided the characterizations of bleaching 2005 bleaching event, but no mortality following information on the susceptibility of D. cylindrus in the was reported for this species (Quinn and susceptibility of D. cylindrus to disease. literature. The species was bleaching- Kojis, 2008). An average of 33 percent Dendrogyra cylindrus is susceptible to resistant during the 1983 mass- of the monitored D. cylindrus colonies black band disease and white plague, bleaching event in Florida. in the U.S. Virgin Islands bleached in though impacts from white plague are Characterizations of the 2005 mass- 2005, and 67 percent paled. None of the likely more extensive because of rapid bleaching event in southern Florida and monitored colonies bleached or paled progression rates. The large colony size in the U.S. Virgin Islands noted that no during the less severe 2010 bleaching suggests that individual colonies are bleached D. cylindrus colonies were event (Smith et al., 2013b). less likely to suffer complete mortality

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from a given disease exposure, but low conditions was intermediate among 19 mortality on D. cylindrus, despite its colony density suggests that even small Caribbean coral species tested. rarity. degrees of mortality increase extinction The public comments did not provide The public comments did not provide risk. new or supplemental information on the new or supplemental information on D. The public comments did not provide susceptibility of D. cylindrus to cylindrus’s susceptibility to predation. new or supplemental information on the sedimentation. Supplemental Supplemental information we found susceptibility of D. cylindrus to disease. information we found includes the includes the following. The sea urchin, Supplemental information we found on following. Dendrogyra cylindrus, along Diadema antillarum, has been reported the susceptibility of D. cylindrus to with Acropora spp. and Meandrina to cause partial mortality at the base of disease includes the following. In a meandrites, was found in fossil D. cylindrus colonies (Acosta and January 2002 survey at Providencia assemblages only on the reef tract and Acevedo, 2006). Island, Colombia, 4.2 percent of D. not on the lagoonal patch reefs around All sources of information are used to cylindrus colonies (n=185) exhibited Grand Cayman, suggesting that this describe D. cylindrus’s susceptibility to white plague type II (Acosta and species may be ineffective at sediment predation as follows. The low amounts Acevedo, 2006). The prevalence of rejection like the other two species or of observed mortality indicate D. diseased D. cylindrus colonies was may be intolerant of turbidity (Hunter cylindrus has low susceptibility to approximately three percent in Mexico and Jones, 1996). predation. The SRR and SIR did not provide from 2002 to 2004 (Ward et al., 2006). All sources of information are used to species-specific information on the Though white diseases were reported to describe D. cylindrus’s susceptibility to effects of sea level rise on D. cylindrus. cause colony mortality in some coral sedimentation as follows. Dendrogyra The SRR described sea level rise as an species in the U.S. Virgin Islands after cylindrus appears to be moderately overall low to medium threat for all the 2005 Caribbean bleaching event, capable of removing sediment from its coral species. The public comments did none of the monitored D. cylindrus tissue. However, D. cylindrus may be not provide new or supplemental colonies exhibited signs of white more sensitive to turbidity due to its information on D. cylindrus’s disease (Smith et al., 2013b). high reliance on nutrition from All sources of information are used to susceptibility to sea level rise, and we photosynthesis and as evidenced by the describe D. cylindrus’s susceptibility to did not find any new or supplemental geologic record. Therefore, we conclude disease as follows. Disease appears to be information. Thus, we conclude that D. that D. cylindrus has some susceptibility present in about three to four percent of cylindrus has some susceptibility to sea to sedimentation, but the available the population in some locations. level rise, but the available information information does not support a more Because no studies have tracked disease does not support a more precise precise description of susceptibility to progression in D. cylindrus, the effects description of susceptibility to this this threat. of disease are uncertain at both the threat. colony and population level. However, The SRR and SIR provided the The SRR and SIR provided the reported low partial mortality and following information on the information on D. cylindrus’s large colony size suggest that individual susceptibility of D. cylindrus to nutrient susceptibility to collection and trade. colonies are less likely to suffer enrichment. Along a eutrophication Overall trade reports indicate very low complete colony mortality from a given gradient in Barbados, D. cylindrus was rates of international trade of D. disease exposure. Therefore, we found at a single site, one of those cylindrus. It is possible that historical conclude that D. cylindrus has some farthest removed from pollution. The curio collecting of D. cylindrus may susceptibility to disease, but the public comments did not provide new have significantly reduced populations available information does not support or supplemental on the susceptibility of off Florida. a more precise description of D. cylindrus to nutrient enrichment, and The public comments did not provide susceptibility to this threat. we did not find any new or new or supplemental information of the The SIR and SRR did not provide any supplemental information. susceptibility of D. cylindrus to species-specific information on the All sources of information are used to collection and trade. Supplemental trophic effects of fishing on D. describe D. cylindrus’s susceptibility to information we found confirms what cylindrus. The public comments did not nutrient enrichment as follows. was provided by the SRR and SIR. Prior provide new or supplemental Dendrogyra cylindrus may be to its ban in the 1980s, collection of D. information, and we did not find new or susceptible to nutrient enrichment as cylindrus for curios was once supplemental information on the evidenced by its absence from eutrophic widespread off the coast of Florida trophic effects of fishing on D. sites in one location. However, there is (Florida Fish and Wildlife Conservation cylindrus. However, due to the level of uncertainty about whether its absence is Commission, 2013). From 2000 to 2012, reef fishing conducted in the Caribbean, a result of eutrophic conditions or a international trade of this species was coupled with Diadema die-off and lack result of its naturally uncommon or rare low with gross exports ranging from of significant recovery, competition occurrence. Therefore, we conclude that zero to nine corals per year (average less with algae can adversely affect coral D. cylindrus likely has some than two per year; data available at recruitment. This effect coupled with susceptibility to nutrient enrichment. http://trade.cites.org). the species’ low recruitment rate However, the available information does All sources of information are used to indicates it likely has some not support a more precise description describe D. cylindrus’s susceptibility to susceptibility to the trophic effects of of its susceptibility to this threat. collection and trade as follows. In the fishing. The available information does The SRR and SIR provided the past, collection and trade may have had not support a more precise description following information on the a large effect on the population in some of its susceptibility. susceptibility of D. cylindrus to locations like Florida. However, The SRR and SIR provided the predation. The corallivorous fireworm collection and trade likely does not have following information on the Hermodice carunculata has been a large impact on the population susceptibility of D. cylindrus to observed feeding on diseased colonies currently. Therefore, we conclude that sedimentation. The rate of sand removal of D. cylindrus, but generally, predation the susceptibility of D. cylindrus to from D. cylindrus tissues in laboratory is not observed to cause noticeable collection and trade is currently low.

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Regulatory Mechanisms number of sexually mature individuals declines thus far. Despite the large In the proposed rule, we relied on and evaluating the reproductive number of islands and environments information from the Final Management potential of the population over the next that are included in the species’ range, Report for evaluating the existing decade (Florida Fish and Wildlife geographic distribution in the highly regulatory mechanisms for controlling Conservation Commission, 2013). disturbed Caribbean exacerbates threats to all corals. However, we did However, the management plan vulnerability to extinction over the not provide any species-specific recognizes that there are threats to D. foreseeable future because D. cylindrus information on the regulatory cylindrus that need to be addressed is limited to an area with high, localized mechanisms or conservation efforts for outside the scope of the plan in order to human impacts and predicted D. cylindrus. Public comments were improve the status of this species. increasing threats. Dendrogyra cylindrus inhabits most reef environments in critical of that approach, and we Vulnerability to Extinction water depths ranging from 1 to 25 m therefore attempt to analyze regulatory As explained above in the Risk mechanisms and conservation efforts on which moderates vulnerability to Analyses section, a species’ extinction over the foreseeable future a species basis, where possible, in this vulnerability to extinction results from final rule. Records confirm that D. because the species occurs in numerous the combination of its demographic and types of reef environments that are cylindrus occurs in seven Atlantic spatial characteristics, threat ecoregions that encompass 26 predicted, on local and regional scales, susceptibilities, and consideration of the to experience highly variable thermal kingdom’s and countries’ EEZs. The 26 baseline environment and future regimes and ocean chemistry at any kingdoms and countries are Antigua & projections of threats. The SRR stated given point in time. It is naturally rare. Barbuda, Bahamas, Barbados, Belize, that the factors that increase the Estimates of absolute abundance are at Colombia, Costa Rica, Cuba, Dominica, extinction risk for D. cylindrus include least tens of thousands of colonies in the Dominican Republic, French Antilles, the overall low population density and Florida Keys, and absolute abundance is Grenada, Guatemala, Haiti, Kingdom of low population size, gonochoric higher than estimates from this location the Netherlands, Honduras, Jamaica, spawning mode and lack of observed due to the occurrence of the species in Mexico, Nicaragua, Panama, St. Kitts & sexual recruitment, and susceptibility to many other areas throughout its range. Nevis, St. Lucia, St. Vincent & observed disease mortality. The SRR It is a gonochoric broadcast spawner Grenadines, Trinidad and Tobago, acknowledged that, given the apparent with observed low sexual recruitment. United Kingdom (British Caribbean naturally rare status of this species, Its low abundance, combined with its Territories), United States (including some undescribed adaptations to low geographic location, exacerbates U.S. Caribbean Territories), and population density may exist in this vulnerability to extinction because Venezuela. The regulatory mechanisms species, particularly with regard to increasingly severe conditions within relevant to D. cylindrus, described first overcoming fertilization limitation the species’ range are likely to affect a as a percentage of the above kingdoms between spawned gametes from high proportion of its population at any and countries that utilize them to any gonochoric parent colonies that are at given point in time, and low sexual degree, and, second as the percentages great distance from one another. recruitment is likely to inhibit recovery of those kingdoms and countries whose Nonetheless, the pervasiveness of potential from mortality events, further regulatory mechanisms may be limited threats characterizing the Caribbean exacerbating its vulnerability to in scope, are as follows: General coral region was deemed to represent extinction. protection (31 percent with 12 percent substantial extinction risk given this limited in scope), coral collection (50 species’ low population size. Listing Determination percent with 27 percent limited in Subsequent to the proposed rule, we In the proposed rule, using the scope), pollution control (31 percent received and gathered supplemental determination tool formula approach, D. with 15 percent limited in scope), species- or genus-specific information, cylindrus was proposed for listing as fishing regulations on reefs (73 percent described above, that expands our endangered because of: High with 50 percent limited in scope), knowledge regarding the species’ vulnerability to disease (C); moderate managing areas for protection and abundance, distribution, and threat vulnerability to ocean warming (E) and conservation (88 percent with 31 susceptibilities. We developed our acidification (E); rare general range-wide percent limited in scope). The most assessment of the species’ vulnerability abundance (E); low relative recruitment common regulatory mechanisms in to extinction using all the available rate (E); narrow overall distribution place for D. cylindrus are reef fishing information. As explained in the Risk (based on narrow geographic regulations and area management for Analyses section, our assessment in this distribution and moderate depth protection and conservation. However, final rule emphasizes the ability of the distribution (E); restriction to the half of the reef fishing regulations are species’ spatial and demographic traits Caribbean (E); and inadequacy of limited in scope and may not provide to moderate or exacerbate its regulatory mechanisms (D). substantial protection for the species. vulnerability to extinction, as opposed In this final rule, we changed the General coral protection and collection to the approach we used in the listing determination for D. cylindrus laws, along with pollution control laws, proposed rule, which emphasized the from endangered to threatened. We are much less common regulatory species’ susceptibility to threats. made this determination based on a mechanisms for the management of D. The following characteristics of D. more species-specific and holistic cylindrus. cylindrus, in conjunction with the approach, including consideration of Dendrogyra cylindrus is listed as information described in the Corals and the buffering capacity of this species’ threatened on the State of Florida Coral Reefs section, Coral Habitat sub- spatial and demographic traits, and the endangered and threatened species list. section, and Threats Evaluation section best available information above on D. The state has an action plan for above, affect its vulnerability to cylindrus’s spatial structure, conservation of the species with several extinction currently and over the demography, threat susceptibilities, and objectives including stabilizing or foreseeable future. Dendrogyra cylindrus management. This combination of increasing the existing population, the is susceptible to a number of threats, but factors indicates that D. cylindrus is current area of occupancy, and the there is little evidence of population likely to become endangered throughout

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its range within the foreseeable future, above, its habitat includes most reef despite some uncertainty of whether or and thus warrants listing as threatened environments in water depths ranging not these are the same species. If D. at this time, because: from one to 25 m. This moderates stokesi is accepted to include all sizes (1) Dendrogyra cylindrus is vulnerability to extinction currently of calices, it is easy to identify; if not susceptible to ocean warming (ESA because the species is not limited to one then species delineations are somewhat Factor E), disease (C), acidification (E), habitat type but occurs in numerous arbitrary. We did not find any nutrient enrichment (A and E), types of reef environments that will supplemental information on sedimentation (A and E), and trophic experience highly variable thermal Dichocoenia’s taxonomy. effects of fishing (A). These threats are regimes and ocean chemistry on local expected to continue and increase into and regional scales at any given point in Dichocoenia stokesi the future. In addition, the species is at time, as described in more detail in the Introduction heightened extinction risk due to Coral Habitat and Threats Evaluation Dichocoenia stokesi forms mounding- inadequate existing regulatory sections. mechanisms to address global threats The combination of these spherical colonies that are usually (D). characteristics indicates that the species orange-brown but sometimes green. (2) Dendrogyra cylindrus is does not exhibit the characteristics of Spatial Information geographically located in the highly one that is currently in danger of The SRR and SIR provided the disturbed Caribbean where localized extinction, as described previously in following information on D. stokesi’s human impacts are high and threats are the Risk Analyses section, and thus does distribution, habitat, and depth range. predicted to increase as described in the not warrant listing as endangered at this Dichocoenia stokesi is located in the Threats Evaluation section. A range time. western Atlantic, Gulf of Mexico constrained to this particular geographic Last, D. cylindrus is listed as (including the Florida Middle Grounds area that is likely to experience severe threatened on the State of Florida and Flower Garden Banks), and and increasing threats indicates that a endangered and threatened species list, throughout the Caribbean. It is also high proportion of the population of this and an action plan for conservation has reported in Bermuda, though it is rare. species is likely to be exposed to those recently been developed. Dichocoenia stokesi occurs in most reef threats over the foreseeable future; Implementation of the action plan will (3) Dendrogyra cylindrus has an no doubt have benefits to the species, environments within its range, uncommon to rare occurrence but it is too soon to evaluate its including mesophotic reefs, back- and throughout its range, which heightens effectiveness for conserving the species. fore-reef environments, rocky reefs, the potential effect of localized Further, considering the global scale of lagoons, spur-and-groove formations, mortality events and leaves the species the most important threats to the channels, and occasionally at the base of vulnerable to becoming of such low species, and the ineffectiveness of reefs. It has been reported in water abundance within the foreseeable future conservation efforts at addressing the depths ranging from two to 72 m. that it may be at risk from depensatory root cause of global threats (i.e., GHG The public comments did not provide processes, environmental stochasticity, emissions), we do not believe that any any new or supplemental information or catastrophic events, as explained in current conservation efforts or on D. stokesi’s distribution, habitat, or more detail in the Corals and Coral conservation efforts planned in the depth range. Supplemental information Reefs and Risk Analyses sections; and future will result in affecting the we found includes the following. Veron (4) Dendrogyra cylindrus’s low sexual species’ status to the point at which (2014) confirmed the occurrence of D. recruitment limits its capacity for listing is not warranted. stokesi in nine out of 11 ecoregions in the western Atlantic and wider- recovery from threat-induced mortality Genus Dichocoenia events throughout its range over the Caribbean known to contain corals. The foreseeable future. The SRR and SIR provided the two ecoregions in which it is not The combination of these following information on Dichocoenia’s reported are off the coasts of Brazil, and characteristics and future projections of morphology and taxonomy. There are the southeast U.S. north of south threats indicates the species is likely to potentially two species in the genus Florida. Kahng et al. (2010) report that be in danger of extinction within the Dichocoenia: Dichocoenia stokesi and D. stokesi is relatively abundant and foreseeable future throughout its range Dichocoenia stellaris. Dichocoenia dominates the coral community on and warrants listing as threatened at this stellaris has been described as differing mesophotic reefs greater than 40 m time due to factors A, C, D, and E. from D. stokesi by its pancake-like depth in the northern Gulf of Mexico The available information above on D. colony morphology and dominance of but not in Belize, Puerto Rico, U.S. cylindrus spatial structure, demography, smaller, circular calices. Some coral Virgin Islands, Jamaica, Curacao, threat susceptibilities, and management taxonomists consider there to be only Florida, Bermuda, Bahamas, or also indicate that the species is not one species, D. stokesi, as specimens Barbados. currently in danger of extinction and have all variations of skeletal shape and All information on D. stokesi’s thus does not warrant listing as valley length. The public comments did distribution can be summarized as Endangered because: not provide any new or supplemental follows. Dichocoenia stokesi is (1) There is little evidence of D. information on Dichocoenia’s taxonomy distributed throughout most of the cylindrus population declines (i.e., the or morphology, and we did not find any greater Caribbean in most reef species continues to be naturally rare); new or supplemental information. environments within its range, (2) Dendrogyra cylindrus shows Most studies over the last several including mesophotic reefs. evidence of resistance to bleaching from decades describe D. stokesi and do not Demographic Information warmer temperatures in some portions separately report data for colonies with of its range under some circumstances D. stellaris morphology. Because D. The SRR and SIR provided the (e.g., Roatan, Honduras); and stokesi was petitioned for listing and D. following information on D. stokesi (3) While D. cylindrus’s distribution stellaris was not, we considered all abundance. Dichocoenia stokesi is within the Caribbean increases its risk information on D. stokesi and did not characterized as usually uncommon. In of exposure to threats as described consider information on D. stellaris, surveys of southeast Florida and the

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Florida Keys between 2005 and 2007, D. stokesi was most frequently shift in the size class distribution stokesi comprised between 1.8 and 7.0 encountered on shallow pavement (9 m) between 1998 and 2002 with a decrease percent of all coral colonies observed and comprised 15 percent of all coral in the frequency of smaller size classes and was present at a density of colonies counted; however on the and a shift from dominance by smaller approximately 1.7 colonies per 10 m2, deeper spur and groove (18 m) and fore- size classes to a more even distribution which was the ninth most abundant out reef (27 m), it comprised 2 and 0.7 across small to larger size classes. Two of an observed 43 coral species. percent of colonies counted, D. stokesi recruits were found after the The public comments provided the respectively (Steiner, 1999). Bak and disease but did not survive to the following supplemental information on Meesters (1999) report that about 50 following year. No colonies greater than D. stokesi’s abundance. In stratified percent of D. stokesi colonies surveyed 25 cm were observed in 1998, four years random surveys conducted by Miller et in Florida and Curacao were in the 10 later (2002) many colonies greater than al. (2013) in the Florida Keys, D. stokesi to 20 cm size class. 25 cm were observed up to 55 cm. ranked as the 8th most abundant species Between 1996 and 2003, average The public comments did not provide or higher in 2005, 2009, and 2012. cover of D. stokesi per habitat type new or supplemental information on D. Extrapolated abundance was 97.8 ± 13.1 ranged from 0.02 to 0.12 percent in the stokesi’s population trends, and we did (SE) million colonies in 2005, 53.8 ± 9.7 Florida Keys and was highest on patch not find any new or supplemental (SE) million colonies in 2009, and 81.6 reefs (Somerfield et al., 2008). Of three information. ± 10.0 (SE) million colonies in 2012. sites surveyed in Bermuda, cover of D. All information on D. stokesi’s Because population estimates were stokesi was 0.02 ± 0.03 percent at one abundance and population trends can based on random sampling, differences site (Dodge et al., 1982). In surveys off be summarized as follows. Dichocoenia between years are more likely a function Colombia from 1998 to 2004, D. stokesi stokesi has been characterized as of sampling effort rather than an cover ranged from 0.02 to 0.6 percent, usually uncommon but is usually indication of population trends. Most but the species was only present in nine reported as one of the top 10 most colonies were 30 cm or less in size, and out of 32 sites (Rodriguez-Ramirez et al., abundant species where estimates are size class distributions remained similar 2010). In the Bahamas Archipelago, available. Based on population among the three sample periods (2005, cover of D. stokesi was on average 0.01 estimates, there are at least tens of 2009, and 2012). Larger colonies to 0.02 percent in 2002 to 2004 (Roff et millions of D. stokesi colonies present in typically exhibited more partial al., 2011). In Dominica, D. stokesi was both the Florida Keys and Dry Tortugas. mortality, which ranged between 20 and observed in 47 percent of 31 sites Absolute abundance is higher than the 80 percent for colonies larger than 10 surveyed and comprised less than one estimate from these two locations given cm. percent cover (Steiner, 2003). the presence of this species in many In the Dry Tortugas, D. stokesi was Dichocoenia stokesi was present on four other locations throughout its range. ranked 12th and 14th most common in out of seven fringing reefs off Barbados The characterization of its occurrence as 2006 and 2008, respectively. and comprised between 0.1 and 0.6 usually uncommon gives the impression Extrapolated colony abundance was percent cover (Tomascik and Sander, of a lower population abundance than is 12.1 ± 4.1 (SE) million colonies in 2006 1987). indicated by population estimates. and 7.1 ± 1.1 (SE) million colonies in On remote reefs off southwest Cuba, Density estimates range from 0.05 to 2008. All D. stokesi colonies observed D. stokesi was observed on 30 reef front 2.35 colonies per 10 m2. The sometimes were 40 cm or less in 2006, and 20 cm sites at densities of 0.052 ± 0.096 (SD) low density and small colony size result or less in 2008. Partial mortality was colonies per 10 m transect, but was not in low percent cover estimates, higher in larger colonies and ranged observed at any of the 38 surveys of the generally between 0.01 and less than 1 from approximately 20 to 65 percent in reef crest (Alcolado et al., 2010). In percent, and make it difficult to track colonies larger than 10 cm (Miller et al., 1,176 sites surveyed in southeast population trends from percent cover 2013). Florida and the Florida Keys between data. Trend data indicate D. stokesi has Supplemental information we found 2005 and 2010, density of D. stokesi decreased in abundance in at least two on D. stokesi’s abundance includes the ranged from 0.07 to 2.35 colonies per 10 locations (i.e., the Florida Keys, and a following. In surveys of Utila, Honduras m2 on reef zones where they were bay in Curacao). Presence of juveniles in between 1999 and 2000, D. stokesi was found, and this species was the eighth several locations indicates recruitment the eighth most common species and most abundant species out of 42 coral is occurring. Recovery from severe was sighted in 52.6 percent of 784 species encountered (Burman et al., population declines in the Florida Keys surveys (Afzal et al., 2001). Dichocoenia 2012). after a disease event was not reported stokesi has been observed in low The SRR and SIR provided the seven years later. Thus, we conclude abundance at 17 of 33 monitoring sites following information on population that population decline has occurred in in the U.S. Virgin Islands and is the trends of D. stokesi. A comparison of some locations and that the species’ 33rd most common species by percent survey data from 19 sites in Spaanse absolute abundance is greater than cover (Smith, 2013). Off southeast Water, Curacao in 1961 and 1992 hundreds of millions of colonies. Florida, D. stokesi comprised 6.8 indicated an 80 percent decrease in percent of the coral population between relative abundance of D. stokesi Other Biological Information 9 and 32 m depth and was ranked the between the two survey periods. In The SRR and SIR provided the 5th most abundant coral species out of surveys of the Florida Keys between following information on D. stokesi’s 27 coral species encountered (Goldberg, 1995 and 2002 during and after a life history. Dichocoenia stokesi is a 1973). In surveys of Conch Reef in the disease outbreak, the average number of gonochoric broadcast spawner with an Florida Keys in 1995, juvenile D. stokesi D. stokesi colonies per 314-m2 site overall sex ratio of 2 to 1 (male to comprised between approximately two decreased from 44.3 to 11.2, a decline of female) in southeast Florida where a and six percent of the overall juvenile almost 75 percent. The maximum small portion of hermaphroditic coral population, and the highest number of D. stokesi colonies per site colonies (approximately 18 percent) proportion occurred at 14 m and decreased from 95 to 43, and the were observed. Minimum size at decreased with depth (Edmunds et al., minimum number of colonies per site reproduction was 160 cm2, and two 2004). Off South Caicos Island, D. decreased from ten to one. There was a potential spawning events per year were

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inferred: one in late August/early vulnerabilities to threats as follows: and Souter, 2008). None of the September and a second in October. High vulnerability to disease; moderate monitored D. stokesi colonies in the Recruitment levels, inferred from the vulnerability to ocean warming, U.S. Virgin Islands bleached, and 67 presence of juveniles, is intermediate acidification, trophic effects of fishing, percent paled during the 2005 bleaching compared to other Caribbean coral and sedimentation; and low event (Smith et al., 2013b). In the species. Very low densities of vulnerability to sea level rise, predation, Florida Keys, D. stokesi ranked 19th out Dichocoenia juveniles (approximately and collection and trade. of 25 species in amount of mortality one percent of total juvenile colonies) The SRR and SIR provided the during the 2005 bleaching event have been observed in the Netherlands following information on the (Lirman et al., 2011). Antilles. Mean D. stokesi juvenile susceptibility of D. stokesi to ocean All sources of information are used to density among 566 sites surveyed warming. Of the 28 coral species that describe D. stokesi’s susceptibility to during 1999 to 2009 averaged 0.11 per bleached along the Florida reef tract ocean warming as follows. Reported m2 but reached as high as one juvenile from Martin County through the lower bleaching of D. stokesi ranges from zero per m2 in certain habitats. The annual Florida Keys from 2005 to 2007, D. to about 60 percent. While reported growth rate of D. stokesi has been stokesi had the lowest bleaching bleaching of D. stokesi is temporally and reported as 2 to 7 mm per year in prevalence. During the 2005 Caribbean spatially variable, compared to other diameter and 2 to 5.2 mm per year in mass-bleaching event, it ranked 16th of Caribbean coral species, D. stokesi height. 21 species in bleaching prevalence in appears to be among the less susceptible The public comments did not provide Barbados and was observed to be to temperature-induced bleaching. new or supplemental information on the bleaching-tolerant in the U.S. Virgin Additionally, a report from the Florida life history of D. stokesi. Supplemental Islands. Keys indicates that bleaching-induced information we found on the life history Van Woesik et al. (2012) developed a mortality of D. stokesi was among the of D. stokesi includes the following. coral resiliency index based on lowest compared to other Caribbean Chiappone and Sullivan (1996) reported biological traits and processes to coral species. Thus, we conclude that D. density of juvenile D. stokesi range from evaluate extinction risk due to stokesi has some susceptibility to ocean 0.02 to 0.26 per m2 at five out of nine bleaching. Evaluations were performed warming. However, the available sites surveyed in the Florida Keys at the genus level. They rated the information does not support a more between 1993 and 1994. Darling et al. resiliency of Dichocoenia as 0 out of a precise description of susceptibility. (2012) performed a biological trait-based range of ¥6 to 7 observed in other coral The SRR and SIR provided the analysis to categorize coral species into genera. Less than or equal to ¥3 was following information on the four life history strategies: Generalist, considered highly vulnerable to susceptibility of D. stokesi to weedy, competitive, and stress-tolerant. extinction, and greater than or equal to acidification. No specific research has The classifications were primarily 4 was considered highly tolerant. Thus, addressed the effects of acidification on separated by colony morphology, Dichocoenia was rated in the middle. the genus Dichocoenia. However, most growth rate, and reproductive mode. The public comments did not provide corals studied have shown negative Dichocoenia stokesi was classified as a new or supplemental information on the relationships between acidification and ‘‘stress-tolerant’’ species, thus likely susceptibility of D. stokesi to ocean growth, and acidification is likely to more tolerant of environmental stress. warming. Supplemental information we contribute to reef destruction in the The SRR and SIR provided the found on the susceptibility of D. stokesi future. While ocean acidification has following other biological information to ocean warming includes the not been demonstrated to have caused about D. stokesi. The mounding following. During the 1998 bleaching appreciable declines in coral morphology and large corallite diameter event, an average of 20 percent of D. populations so far, it is considered a of D. stokesi enhance turbulence near stokesi colonies were greater than 50 significant threat to corals by 2100. the surface of colonies. This should, in percent bleached in the lower Florida The public comments did not provide turn, enhance mass transfer, which Keys and Dry Tortugas; however, this new or supplemental information on the affects photosynthesis and respiration in was the lowest of 14 species that susceptibility of D. stokesi to D. stokesi as well as prey capture and bleached (Waddell, 2005). Of the 22 acidification, and we did not find any nutrient uptake. Thresholds for uptake species monitored off Roatan, Honduras, new or supplemental information. of inorganic nitrogen in D. stokesi have D. stokesi was one of eight species that All sources of information are used to been reported to be fairly low (150 nM), did not bleach during the 1998 describe D. stokesi’s susceptibility to giving it a potential advantage in bleaching event (Riegl et al., 2009). acidification as follows. There is nutrient-poor conditions. During the 2005 temperature uncertainty about how D. stokesi will The public comments did not provide anomaly, D. stokesi colonies were fully respond to ocean acidification, but new or supplemental information on D. bleached around La Parguera, Puerto based on the negative effects of stokesi’s biology. Supplemental Rico but were less frequently bleached acidification on growth of most corals, information we found on D. stokesi’s at other locations around Puerto Rico D. stokesi likely has some susceptibility biology includes the following. At 76 (Waddell and Clarke, 2008). Off of Mona to acidification. The available sites surveyed in the Florida Keys and Desecheo Islands, Puerto Rico, information does not support a more during the 2010 cold-water event, about 25 percent of D. stokesi paled and precise description of susceptibility. approximately 15 percent of D. stokesi about 10 percent bleached; in the 16 The SRR and SIR provided the paled, and approximately one percent coral species surveyed, bleaching following information on D. stokesi’s bleached. Mortality was approximately ranged from less than five percent to susceptibility to disease. Black band four percent (The Nature Conservancy, approximately 60 percent of colonies disease, dark spot syndrome, and white 2010). (Bruckner and Hill, 2009). During the plague have been reported to affect D. 2005 bleaching event, approximately 30 stokesi. In an outbreak of white plague Susceptibility to Threats percent of D. stokesi colonies on six in St. Lucia in 1997, six surveyed The threat susceptibility information reefs bleached in Barbados, and D. colonies of D. stokesi were infected, and from the SRR and SIR was interpreted stokesi around Grand Cayman average tissue mortality was about 65 in the proposed rule for D. stokesi’s experienced total bleaching (Wilkinson percent. In surveys in Dominica

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between 2000 and 2002, D. stokesi was disease as follows. Although D. stokesi stokesi is more tolerant of sedimentation one of four coral species most is susceptible to several diseases, the than other coral species as it has the commonly affected by disease, and most severe impacts have been the ability to remove both larger grain size white plague predominantly affected result of white plague. Low prevalence and finer sediment. However, prolonged larger-sized colonies. Of 17 species of diseased D. stokesi colonies have exposure (several days) to turbidity has affected by white plague in the Florida been reported from some locations, but been shown to cause physiological Keys, D. stokesi was the most outbreaks of white plague have caused stress. We conclude that D. stokesi has susceptible. rapid and substantial mortality in some some susceptibility to sedimentation. The public comments did not provide other sites. Outbreaks in Puerto Rico However, the available information does new or supplemental information on the and St. Lucia, while affecting D. stokesi, not support a more precise description susceptibility of D. stokesi to disease. do not appear to have caused as severe of susceptibility. Supplemental information we found on mortality as in the Florida Keys and The SRR and SIR did not provide any the susceptibility of D. stokesi to disease U.S. Virgin Islands. Thus, we conclude species or genus information on the includes the following. In 1991, an that D. stokesi has high susceptibility to susceptibility of D. stokesi to nutrients outbreak of white plague was observed disease. but provided the following. Land-based on Mona Island, Puerto Rico that The SIR and SRR did not provide any sources of pollution (including affected 14 species, with the highest species-specific information on the nutrients) often act in concert rather prevalence among small, massive corals trophic effects of fishing on D. stokesi. than individually and are influenced by including D. stokesi, many of which The public comments did not provide other biological (e.g., herbivory) and died within one to two weeks (Waddell, any new or supplemental information hydrological factors. Collectively, land- 2005). In Mexico, disease was prevalent on the trophic effects of fishing on D. based sources of pollution are unlikely on approximately one percent of D. stokesi, and we did not find any new or to produce extinction at a global scale; stokesi colonies surveyed in 2004 (Ward supplemental information. However, however, they may pose significant et al., 2006). due to the level of reef fishing threats at local scales and reduce the During an outbreak of white plague conducted in the Caribbean, coupled resilience of corals to bleaching. type II in the Florida Keys in 1995, with Diadema die-off and lack of The public comments did not provide mortality of D. stokesi averaged 26 significant recovery, competition with new or supplemental information on the percent and ranged from 0 to 38 percent algae can adversely affect coral susceptibility of D. stokesi to nutrients, (Richardson et al., 1998). The disease recruitment. Based on D. stokesi’s and we did not find any new or routinely caused whole colony mortality inferred recruitment rates, we conclude supplemental information. Based on our within two to three days due to its that it likely has low susceptibility to knowledge that nutrients in general infection of small coral colonies trophic effects of fishing. have a negative effect on corals, we (usually less than 10 cm in diameter) The SRR and SIR provided the conclude that D. stokesi has some level and aggressive progression rate (up to 2 following information on susceptibility of susceptibility to nutrients, but the cm per day; Richardson, 1998). Between of D. stokesi to sedimentation. A available information does not support 1996 and 1998, out of 160 monitoring laboratory study examining oil/ a more precise description of stations at 40 sites in the Florida Keys, sediment rejection indicated that out of susceptibility. the number of stations with D. stokesi 19 Caribbean coral species examined, D. The SRR and SIR provided the colonies affected by disease increased stokesi was intermediate in the rate of following information on the through time with two stations affected sediment removal from its tissues. In susceptibility of D. stokesi to predation. in 1996, 22 in 1997, and 45 in 1998 laboratory experiments, D. stokesi Dichocoenia stokesi is minimally (Porter et al., 2001). However, no white exhibited significant increases in affected by predation. Sponges such as plague was observed in D. stokesi in respiration after 3 days of exposure to Chondrilla nucula and Ectoplaysia ferox 2002 at the sites with the reported turbidity levels of 28 to 30 NTU, which can overgrow and cause tissue loss in D. outbreak in 1995 (Richardson and Voss, are within allowable levels as regulated stokesi, especially if unchecked by 2005). by the State of Florida for coastal spongivores. Dichocoenia stokesi had Disease surveys at St. Croix, U.S. construction projects. While light levels the highest density of boring bivalves Virgin Islands during the summer of and photosynthesis were not affected, (average 7.5 bivalves per colony) of the 2001 revealed that D. stokesi had the after six days of exposure to 14 to 16 three coral species examined. highest prevalence of white plague type NTU of turbidity, gross photosynthesis The public comments provided II out of seven species infected and the to respiration ratios were less than one supplemental information on D. highest disease-related mortality in this species, and excessive mucus stokesi’s susceptibility to predation. (Kaczmarsky et al., 2005). The production was observed. Predation by Coralliophila snails was prevalence of white plague type II on D. The public comments did not provide recorded on 1.8 percent of the 502 D. stokesi was 41 percent at one location new or supplemental information on the stokesi colonies assessed for condition and 60 percent at a second site. Of 107 susceptibility of D. stokesi to in 2012 surveys in the Florida Keys D. stokesi colonies, 38 were infected, sedimentation. Supplemental (Miller et al., 2013). We did not find any and 26 percent of the infected colonies, information we found on the new or supplemental information on the or 9.4 percent of the sample population, susceptibility of D. stokesi to susceptibility of D. stokesi to predation. died within two months (Kaczmarsky et sedimentation includes the following. All sources of information confirm al., 2005). After the 2005 bleaching The large calices, number of septa, and that predation does not appear to event, 100 percent of monitored D. calical relief of D. stokesi give this significantly affect D. stokesi. Thus, we stokesi colonies in the U.S. Virgin species the capability to remove both conclude that D. stokesi has low Islands were infected with disease in fine sediment and larger grain sizes susceptibility to predation. 2006, but none of the colonies through polyp distension (Hubbard and The SRR and SIR provided the experienced total colony mortality Pocock, 1972). following information on the (Smith et al., 2013b). All sources of information are used to susceptibility of D. stokesi to collection All sources of information are used to describe D. stokesi’s susceptibility to and trade. Collection and trade are not describe D. stokesi’s susceptibility to sedimentation as follows. Dichocoenia considered a threat to D. stokesi. The

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public comments did not provide new scope), pollution control (31 percent geographically located in the heavily or supplemental information. with 15 percent limited in scope), disturbed Caribbean, D. stokesi occurs Supplemental information we found on fishing regulations on reefs (73 percent in a wide range of habitats, including collection and trade includes the with 50 percent limited in scope), mesophotic reefs, back- and fore-reef following. Collection and trade of D. managing areas for protection and environments, rocky reefs, lagoons, stokesi appear to be low and primarily conservation (88 percent with 31 spur-and-groove formations, channels, for scientific purposes. Gross exports percent limited in scope). The most and occasionally at the base of reefs. between 2000 and 2012 averaged 35 common regulatory mechanisms in This distribution in a wide range of corals per year (data available at http:// place for D. stokesi are reef-fish fishing environments suggests the species will trade.cites.org). Thus, we conclude that regulations and area management for be better able to withstand changing D. stokesi has low susceptibility to protection and conservation. However, environmental conditions and collection and trade. half of the reef-fish fishing regulations moderates vulnerability to extinction The SRR and SIR did not provide are limited in scope and may not over the foreseeable future because the species-specific information on the provide substantial protection for the numerous types of reef environments in effects of sea level rise on D. stokesi. species. General coral protection and which the species occurs are predicted, The SRR described sea level rise as an collection laws, along with pollution on local and regional scales, to overall low to medium threat for all control laws, are much less common experience highly variable thermal coral species. The public comments did regulatory mechanisms for the regimes and ocean chemistry at any not provide new or supplemental management of D. stokesi. given point in time. It has been reported information on D. stokesi’s Vulnerability to Extinction in water depths ranging from 2 to 72 m. susceptibility to sea level rise, and we Deeper areas of D. stokesi’s range will did not find any new or supplemental As explained above in the Risk usually have lower temperatures than information. Thus, we conclude that D. Analyses section, a species’ surface waters, and acidification is stokesi has some susceptibility to sea vulnerability to extinction results from generally predicted to accelerate most in level rise, but the available information the combination of its spatial and waters that are deeper and cooler than does not provide a more precise demographic traits, threat those in which the species occurs. The description of susceptibility. susceptibilities, and consideration of the species is highly susceptible to disease, baseline environment and future Regulatory Mechanisms and outbreaks have resulted in high projections of threats. The SRR stated colony mortality in some locations in its In the proposed rule, we relied on that the factors that increase the range. However, D. stokesi’s abundance information from the Final Management potential extinction risk for D. stokesi has been estimated as at least tens of Report for evaluating the existing include documented population-level millions of colonies in both the Florida regulatory mechanisms for controlling impacts from disease. Factors that Keys and Dry Tortugas and is higher threats to all corals. However, we did reduce potential extinction risk are than the estimate from these two not provide any species-specific relatively high abundance and locations due to the occurrence of the information on the regulatory persistence across many habitat types, species in many other areas throughout mechanism or conservation efforts for D. including nearshore and mesophotic its range. Additionally, sexual stokesi. Public comments were critical reefs. Residency in a wide range of recruitment, as evidenced by presence of that approach, and we therefore habitat types suggests the species has a attempt to analyze regulatory wide tolerance to environmental of juvenile colonies, is comparatively mechanisms and conservation efforts on conditions and, therefore, better higher than many other Caribbean coral a species basis, where possible, in this capacity to deal with changing species, enhancing recovery potential final rule. Records confirm that environmental regimes. from mortality events, thus moderating Dichocoenia stokesi occurs in nine Subsequent to the proposed rule, we vulnerability to extinction. The Atlantic ecoregions that encompass 26 received and gathered supplemental combination of wide habitat occupancy, kingdom’s and countries’ EEZs. The 26 species- or genus-specific information, abundance, life history characteristics, kingdoms and countries are Antigua & described above, that expands our and depth distribution, combined with Barbuda, Bahamas, Barbados, Belize, knowledge regarding the species’ spatial variability in ocean warming and Colombia, Costa Rica, Cuba, Dominica, abundance, distribution, and threat acidification across the species’ range, Dominican Republic, French Antilles, susceptibilities. We developed our moderates vulnerability to extinction Grenada, Guatemala, Haiti, Kingdom of assessment of the species’ vulnerability because the increasingly severe the Netherlands, Honduras, Jamaica, to extinction using all the available conditions expected in the foreseeable Mexico, Nicaragua, Panama, St. Kitts & information. As explained in the Risk future will be non-uniform, and there Nevis, St. Lucia, St. Vincent & Analyses section, our assessment in this will likely be a large number of colonies Grenadines, Trinidad and Tobago, final rule emphasizes the ability of the that are either not exposed or do not United Kingdom (British Overseas species’ spatial and demographic traits negatively respond to a threat at any Territories), United States (including to moderate or exacerbate its given point in time. U.S. Caribbean Territories), and vulnerability to extinction, as opposed Listing Determination Venezuela. The regulatory mechanisms to the approach we used in the relevant to D. stokesi, described first as proposed rule, which emphasized the In the proposed rule, using the a percentage of the above countries and species’ susceptibility to threats. determination tool formula approach, D. kingdoms that utilize them to any The following characteristics of D. stokesi was proposed for listing as degree, and second as the percentages of stokesi, in conjunction with the threatened because of: High those countries and kingdoms whose information described in the Corals and vulnerability to disease (C); moderate regulatory mechanisms may be limited Coral Reefs section, Coral Habitat sub- vulnerability to ocean warming (E) and in scope, are as follows: General coral section, and Threats Evaluation section acidification (E); moderate overall protection (31 percent with 12 percent above, affect its vulnerability to distribution (based on narrow limited in scope), coral collection (50 extinction currently and over the geographic distribution and wide depth percent with 27 percent limited in foreseeable future. Although it is distribution (E); restriction to the

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Caribbean (E); and inadequacy of (4) Presence of juvenile D. stokesi species by their current taxonomic regulatory mechanisms (D). colonies indicates that recruitment is classification in the genus Orbicella. We In this final rule, we changed the likely occurring, enhancing recovery did not find any new or supplemental listing determination for D. stokesi from potential from mortality events. information on Orbicella’s taxonomy or threatened to not warranted. We made Notwithstanding the projections morphology. this determination based on a more through 2100 that indicate increased Some studies report on the species species-specific and holistic assessment severity over time of the three high complex rather than individual species of whether this species meets the importance threats, the combination of since visual distinction can be difficult definition of either a threatened or these biological and environmental from video or photographic surveys or endangered coral, including more characteristics indicates that the species in small colonies where morphology is appropriate consideration of the possesses sufficient buffering capacity more difficult to discern. This section buffering capacity of this species’ spatial to avoid being in danger of extinction will report information on the species and demographic traits to lessen its within the foreseeable future throughout complex and on O. annularis from vulnerability to threats. Thus, based on its range. This species’ extinction risk studies pre-dating 1994 when the the best available information above on may increase in the future if global species was split into three nominal D. stokesi’s spatial structure, threats continue and worsen in severity species. demography, threat susceptibilities, and and the species’ exposure to the threats Spatial Information management, none of the five ESA increases throughout its range. Should listing factors, alone or in combination, the species experience reduced The SRR and SIR provide the are causing this species to be likely to abundance or range constriction of a following information on Orbicella’s become endangered throughout its range certain magnitude, the ability of these distribution, habitat, and depth range. within the foreseeable future, and thus characteristics to moderate exposure to The species complex has been found at it is not warranted for listing at this time threats will diminish. However, D. depths to 90 m. It is dominant on because: stokesi is not likely to become of such mesophotic reefs in Puerto Rico and the (1) Dichocoenia stokesi’s distribution low abundance or so spatially U.S. Virgin Islands at depths of 30 to 45 in depths of two to 72 m in fragmented as to be in danger of m, and it is found at depths up to 70 to heterogeneous habitats, including extinction due to depensatory processes, 90 m in these locations. The public comments did not provide mesophotic reefs, back- and fore-reef the potential effects of environmental new or supplemental information on environments, rocky reefs, lagoons, stochasticity, or the potential for Orbicella’s distribution, habitat, or spur-and-groove formations, channels, mortality from catastrophic events depth range. Supplemental information and occasionally at the base of reefs, within the foreseeable future throughout we found on Orbicella’s depth range throughout the Caribbean basin reduces its range. Therefore, D. stokesi is not includes the following. All three species exposure to any given threat event or warranted for listing at this time under occupy a large depth range. Although adverse condition that does not occur any of the listing factors, and we there is depth overlap in species uniformly throughout the species’ range. withdraw our proposal to list the occurrence, there is larger variance and As explained above in the Threats species as threatened. Evaluation section, we have not overlap in species abundances in identified any threat that is expected to Genus Orbicella (formerly Montastraea) shallow versus deep water (Pandolfi and Budd, 2008). Orbicella faveolata tends occur uniformly throughout the species Introduction range within the foreseeable future; to have the shallowest depth (2) Dichocoenia stokesi is usually The SRR and SIR provided the distribution, and O. franksi tends to reported in the top ten most abundant following information on the taxonomy have the deepest (Pandolfi and Budd, coral species in the Caribbean, and its and morphology of the genus 2008; Weil and Knowlton, 1994). At total absolute abundance is at least tens Montastraea. The genus Montastraea three study sites in Belize, O. faveolata of millions of colonies based on contained four Caribbean species: M. was the most abundant member of the estimates from two locations. Absolute cavernosa, M. annularis, M. faveolata, species complex between 2 and 5 m abundance is higher than estimates from and M. franksi. Prior to the 1990s, M. depth; O. annularis was the most these locations since it occurs in many annularis, M. faveolata, and M. franksi abundant at depths of 10 to 15 m, and other locations throughout its range. were considered one species, M. O. franksi was the most abundant at This provides buffering capacity in the annularis. However, M. annularis was depths of 20 to 30 m (Pandolfi and form of absolute numbers of colonies broken into the three sibling species Budd, 2008). Orbicella annularis species and variation in susceptibility between based on behavioral, biochemical, and complex can be relatively abundant at individual colonies. As discussed in the morphological criteria. These three mesophotic depths in the Bahamas, Corals and Coral Reefs section above, species are often grouped into the M. Belize, Jamaica, Puerto Rico, U.S. Virgin the more colonies a species has, the annularis species complex. Subsequent Islands, and Curacao (Kahng et al., lower the proportion of colonies that are reproductive and genetic studies have 2010). likely to be exposed to a particular generally supported the partitioning of threat at a particular time, and all the complex into three species. Demographic Information individuals that are exposed will not Montastraea faveolata is the most The SRR and SIR provided the have the same response; genetically distinct while M. annularis following information on abundance (3) Dichocoenia stokesi occurs in most and M. franksi are less so. and population trends of the Orbicella reef habitats, including mesophotic The public comments provided the annularis species complex. The species reefs, back- and fore-reef environments, following new information on complex has historically been a rocky reefs, lagoons, spur-and-groove Montastraea’s taxonomy. In 2012, the dominant component on Caribbean formations, channels, and occasionally genus Montastraea was split, and M. coral reefs, characterizing the so-called at the base of reefs, indicating wide annularis, M. faveolata, and M. franksi ‘‘buttress zone’’ and ‘‘annularis zone’’ in tolerance of environmental conditions were assigned to the genus Orbicella the classical descriptions of Caribbean and better capacity to deal with (Budd et al., 2012). From this point reefs. The species complex is the major changing environmental regimes; and forward, we will refer to the genus and reef-builder in the greater Caribbean,

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since the die-off of Acropora spp., due off Mona and Desecheo Islands, Puerto ranged between approximately 25 and to their large size and high abundance. Rico: 47 percent on reefs off Desecheo 50 percent on three of the reefs, and no Numerous examples of population Island and 32 percent off Mona Island. O. annularis species complex colonies decline of the Orbicella annularis In 2008 live cover of O. annularis were observed in transects on the fourth species complex were described, and species complex ranged from 0 to 14 reef (Burns, 1985). In stratified random the results are summarized as follows. percent with 95 percent decline off surveys in 2007–2008, O. annularis Decline in the Florida Keys between the Desecheo Island and 78 percent decline species complex was the dominant coral late 1970s and 2003 was approximately off Mona Island. This was accompanied by percent cover in the Red Hind 80 to 95 percent, with further losses with large changes in the size frequency Marine Conservation District off St. during the 2012 cold weather event. distribution and extent of partial Thomas, U.S. Virgin Islands, at depths Decadal-scale declines across the remote mortality, with size structure remaining of 34 to 47 m. Orbicella annularis islands of Navassa, Mona, and Desecheo constant. The amount of living tissue species complex averaged 15 percent in the central Caribbean impacted 85 declined by 55 percent due to partial cover (range zero to 48 percent) and percent of colonies found there. In the mortality affecting medium and large made up 92 percent of the 25 percent U.S. Caribbean (U.S. Virgin Islands and colonies, with an increase in the average coral cover (Nemeth et al., Puerto Rico), an 80 to 90 percent decline number of colonies with small (less than 2008). has been reported over the past two 10 cm diameter) tissue remnants. In a survey of 185 sites in five decades. Percent cover was reportedly Sponges and macroalgae colonized countries (Bahamas, Bonaire, Cayman stable in Curacao in the mid-1970s, an newly exposed area, and sponges Islands, Puerto Rico, and St. Kitts and 85 percent increase in partial mortality appeared to be preventing re-sheeting of Nevis) in 2010 to 2011, density of O. occurred between 1998 and 2005. tissue remnants. No Orbicella spp. annularis species complex ranged from Between 1975 and 1998 at Glovers Reef recruits were observed during the ten 0.3 to 2.7 colonies per m2 and in Belize, a 38 to 75 percent decline in year study (Bruckner and Hill, 2009). comprised between 9 and 30 percent of relative cover occurred with a further 40 Surveys at three reefs in western all corals greater than 4 cm diameter. percent decline since. Colonies in Curacao in 1998 found 46 percent of all The mean diameter ranged from 44 to 89 Colombia were stable between 1998 and corals were O. annularis species cm, and the size structure (planar 2003 although demographic changes complex. In 2005, O. annularis species surface area) had a bell shaped imply some degree of decline. Surveys complex remained the dominant coral distribution, with only a few colonies of population structure across five species but declined in abundance to 38 less than 500 cm2 or greater than 10,000 countries found a significant increase in percent of the overall coral population cm2 (Bruckner, 2012a). small ramets (tissue isolates that are (decreases in abundance occurred in O. In surveys of juvenile corals (less than genetically identical but physiologically faveolata and O. annularis, but not O. 4 cm diameter) on nine reefs in the separate from the parent colony) less franksi). In 1998 mean diameter of O. Florida Keys between 1993 and 1994, than 500 cm2 (211 percent for O. annularis species complex colonies density of O. annularis species complex annularis, 168 percent for O. faveolata, were 62 cm and less than 10 percent of ranged between 0.02 and 0.04 juvenile 137 percent for O. franksi), while the all O. annularis species complex corals per m2 on six of the nine reefs. proportion of large (1,500- 30,000 cm2), colonies were less than 30 cm in Density of O. annularis species complex completely live colonies declined by 51 diameter. Partial mortality of O. juveniles was correlated with non- to 57 percent. annularis species complex increased 85 juvenile O. annularis species complex The public comments did not provide percent between 1997 and 2005 with density and with depth. The majority of new or supplemental information on losses of O. annularis and O. faveolata non-juveniles were smaller than the Orbicella’s abundance and population (partial mortality 42 to 48 percent and reproductive size of 100 cm2 trends. Supplemental information we total mortality 6 percent for the two (Chiappone and Sullivan, 1996). found on Orbicella’s abundance and species combined) larger than O. Surveys in Bonaire in 2008 showed population trends is provided as franksi. The most significant losses were that the O. annularis species complex follows. In a survey of 185 sites in five due to yellow band disease and white dominated coral cover in depths less countries (Bahamas, Bonaire, Cayman plague. No recruits of O. annularis than 20 m and cover was similar to that Islands, Puerto Rico, and St. Kitts and species complex were observed between reported in 1982. However, all sites Nevis) between 2010 and 2011, 1997 and 2005 in transects or on surveyed in 2008 showed signs of Orbicella annularis species complex skeletons of tagged colonies exposed disease and partial mortality in a large exhibited mean tissue mortality of 29 to through mortality from disease number of the massive colonies, and 66 percent, which was higher than other (Bruckner and Bruckner, 2006a). many were reduced to a patchwork of species exhibiting mean 8 to 17 percent McClanahan and Muthiga (1998) live tissue and dead areas colonized by tissue mortality. Total mortality of O. surveyed 20 patch reefs in Glovers Reef algae (Stokes et al., 2010). annularis species complex were atoll off Belize between 1996 and 1997 At 25 sites surveyed in Bonaire in observed (five to seven percent of the and compared their results to surveys of 2011, O. annularis species complex was total); however mortality of large 16 patch reefs in the same general area the dominant coral taxa occupying colonies mostly resulted in multiple conducted between 1970 and 1971. approximately 20 to 25 percent of the smaller ramets Mortality was attributed They found that O. annularis species benthos and making up 46 percent of primarily to outbreaks of white plague complex experienced an overall 62 the total live coral cover. It was and yellow band disease, which percent decrease in cover. Average dominant in terms of abundance, emerged as corals began recovering from cover of O. annularis species complex making up approximately 27 percent of mass bleaching events. This was was seven percent in 1996 and 1997. all corals. Orbicella annularis was followed by increased predation and The O. annularis species complex significantly more abundant than O. removal of live tissue by damselfish to often makes up the largest proportion of franksi and O. faveolata on the northern cultivate algal lawns (Bruckner, 2012a). coral cover on Caribbean reefs. In reefs but not on southern reefs. Most In 1998 O. annularis species complex surveys conducted on four reefs in colonies were between 30 and 80 cm covered more of the benthos than any Biscayne National Park, Florida in 1981, diameter with size structure of O. other coral taxon at nine monitored sites cover of O. annularis species complex annularis species complex in a bell

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shaped distribution around this range; percent), with a few colonies of O. of decline, but hurricanes may have also there were few colonies less than 20 cm faveolata (6 percent). Despite a played a role (Harvell et al., 2007). and few very large colonies greater than reduction in total cover, O. annularis Size transition matrices were derived 200 cm, with a small peak at the 150 to species complex remained spatially from Orbicella growth, mortality, and 199 cm range. There was a notable dominant in 1998 at 96 percent of the recruitment rates between 1998 and absence of colonies less than 10 cm coral cover (Edmunds, 2002). Coral 2003 from four sites in the lower Florida diameter (as measured by the skeleton, cover at this site again declined an Keys. Forecasting 15 years into the not live tissue) and an absence of additional 65 percent between 1999 and future predicted a steady decline in all recruits. A total of 73 out of 1602 2011 to seven percent cover, with O. size classes except the smallest (less colonies (4.5 percent) had completely annularis species complex remaining than 5 cm) due to insufficient died. Surviving colonies (n=1529) had a dominant at 77 percent of the coral recruitment to offset mortality and low mean of 28 percent partial mortality. On cover (Edmunds, 2013). growth rates of the smaller size classes. average, each colony was divided into At Tektite Reef, St. John, U.S. Virgin Mortality rates were assumed at 6.6 tissue remnants. Several sites Islands, total coral cover increased from approximately 40 percent for the contained a high abundance of large, 32 percent in 1987 to 43 percent in 1998 smallest size class declining to about 5 unblemished O. annularis species but then decreased to 29 percent in 2011 percent for the largest (Smith and complex colonies (Bruckner, 2012c). (Edmunds, 2002; Edmunds, 2013). In Aronson, 2006). Between 1999 and 2009, overall cover 1988, 79 percent of the species complex All information on Orbicella’s of O. annularis species complex in the was O. annularis, with lesser amounts abundance and population trends can Florida Keys declined, but differed by of O. faveolata (one percent) and O. be summarized as follows. The O. habitat type (Ruzicka et al., 2013). franksi (21 percent) (Edmunds, 2002). annularis species complex historically Percent cover declined on the deep and Greater than 72 percent of coral was O. dominated fore-reef sites throughout the shallow fore-reefs but remained stable annularis species complex in all survey Caribbean both in abundance and cover on patch reefs (Ruzicka et al., 2013). The years (Edmunds, 2013). and formed dense assemblages of large, hundreds-of-years old colonies and few 2010 cold-water event reduced cover of Surveys of the Flower Garden Banks O. annularis species complex from 4.4 small colonies (Bruckner, 2012a). between 1974 and 1980 found cover of percent to 0.6 percent on four patch However, recent declines in O. O. annularis species complex between reefs in the upper and middle Florida annularis species complex cover have approximately 23 and 40 percent in Keys. Greater than 50 percent of O. been reported. Major declines range areas less than 36 m depth (Bright et al., annularis species complex colonies from approximately 50 to 95 percent in 1984). Orbicella annularis species across all size classes suffered lethal or locations including Puerto Rico, Belize, complex was the dominant coral severe mortality, and 93 percent of all the Florida Keys, Mexico, and the U.S. between 2002 and 2003 at 32 percent O. annularis species complex colonies Virgin Islands, and lower levels of cover (Aronson et al., 2005). In random surveyed suffered complete or partial decline (5 to 33 percent) have been surveys between 2002 and 2006, O. mortality. The species complex suffered reported at individual sites within some the highest mortality of all coral species annularis species complex of these same locations. There have also affected (Colella et al., 2012). A (predominantly O. franksi) was the been reports of more stable percent comparison of 1995 and 2005 surveys of dominant coral in the Flower Garden cover trends (e.g., Bonaire) and periods O. annularis species complex at 13 Banks comprising between 27 and 40 of increase (e.g., Flower Garden Banks). patch reefs in the Florida Keys reported percent benthic cover (Hickerson et al., Observed declines in total coral cover in ten sites had between 5 and 40 percent 2008). In permanent photo quadrats (8 the Caribbean, since the major decline 2 more dead areas (Gischler, 2007). m total), cover of O. annularis species of Acropora spp. in the 1980s, have Density of juvenile O. annularis complex (as measured by planar surface often been a result of the decline of the species complex increased from 0.07 area of individual colonies) fluctuated O. annularis species complex since the juveniles per m2 prior to 2008, to 0.15 between approximately 20 and 45 taxa can make up a large proportion of juveniles per m2 and continued at 0.12 percent cover in the East Flower the total coral cover. Despite decreases, juveniles per m2 in 2009 at 4 km area Gardens between 1992 and 2006 with the O. annularis species complex on the south side of St. John, U.S. Virgin periods of sharp increase and decrease continues to be reported as the Islands that has been monitored for 16 in cover (Hickerson et al., 2008). Cover dominant coral taxa, albeit at times its years. These densities were driven by in west Flower Gardens was between 22 relative dominance has decreased to a seven to nine colonies per year, and the and 40 percent over the same time lower percentage of the total coral cover increased density did not extend period and had less annual variability (e.g., Curacao, U.S. Virgin Islands). outside the initial survey area when and a generally increasing or stable expanded to other areas around St. John. trend through time (Hickerson et al., Other Biological Information While not possible to distinguish the 2008). The SRR and SIR provided the species in the field, the authors Surveys of five sites in the Mexican following information on Orbicella life conclude juveniles were most likely O. Yucatan in 1985 and 2005 revealed a history. Orbicella spp. have growth rates annularis due to the abundance of O. decrease in relative cover of O. of approximately 1 cm per year, ranging annularis on adjacent reefs and the annularis species complex. At four out from 0.06 to 1.2 cm per year. They grow rarity of the presence of the other two of the five sites, cover of O. annularis more slowly in deeper water and in less species in water less than 9 m species complex decreased from clear water. Large colonies have lower (Edmunds et al., 2011). between approximately 50 and 60 total mortality rates than juvenile and At Yawzi Point, St. John, U.S. Virgin percent in 1985 to between small colonies. Islands, the percentage of total coral approximately 10 and 25 percent in All three species of the O. annularis cover declined by more than 50 percent 2005. The fifth site had a less dramatic complex are hermaphroditic broadcast between 1987 to 1998, from 45 percent decrease in relative cover from spawners, with spawning concentrated to 20 percent. In 1988, 94 percent of the approximately 35 percent to 30 percent on six to eight nights following the full coral cover at Yawzi was O. annularis cover during this 20-year interval. moon in late August, September, or species complex mostly O. annularis (97 Disease appeared to be the main cause early October. Orbicella faveolata is

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largely reproductively incompatible All sources of information are used to yellow band disease increased with with O. franksi and O. annularis, and it summarize Orbicella’s life history as increasing temperatures. spawns about one to two hours earlier. follows. Orbicella species have slow The public comments did not provide Fertilization success measured in the growth rates, late reproductive maturity, new or supplemental information on the field was generally below 15 percent for and low recruitment rates. Colonies can susceptibility of Orbicella to ocean all three species being closely linked to grow very large and live for centuries. warming. Supplemental information we the number of colonies concurrently Large colonies have lower total found on Orbicella’s susceptibility to spawning. In Puerto Rico, minimum mortality than small colonies, and ocean warming confirms and expands size at reproduction for the O. annularis partial mortality of large colonies can the information in the SRR and SIR. The species complex was 83 cm2. result in the production of ramets. The O. annularis species complex often has Successful recruitment by the O. historical absence of small colonies and one of the highest bleaching levels annularis species complex species has few observed recruits, even though large among reported species. Extended seemingly always been rare. Only a numbers of gametes are produced on an recovery times have been reported, and single recruit of Orbicella was observed annual basis, suggests that recruitment disease outbreaks have often followed over 18 years of intensive observation of events are rare and were less important bleaching events. On Carysfort Reef in 12 m2 of reef in Discovery Bay, Jamaica. for the survival of the O. annularis the Florida Keys, greater than 90 percent Many other studies throughout the species complex in the past (Bruckner, of O. annularis species complex Caribbean also report negligible to 2012a). Large colonies in the species colonies were bleached in March 1988 absent recruitment of the species complex maintain the population until after the 1987 Caribbean bleaching complex. conditions favorable for recruitment event; however, no colony mortality was The public comments did not provide occur; however, poor conditions can observed between 1986 and 1988 (Fitt et new or supplemental information on the influence recruitment periodicity. While al., 1993). Colonies of the O. annularis life history of Orbicella. Supplemental the life history strategy of the O. species complex in the Florida Keys that information we found on the life history annularis species complex has allowed remained bleached seven months of Orbicella includes the following. the taxa to remain abundant, we following the 1987 bleaching event Orbicella franksi spawns an average of conclude that the buffering capacity of experienced reproductive failure during 110 minutes before O. annularis, and this life history strategy has been the reproductive season following the 120 minutes before O. faveolata (Fogarty reduced by recent population declines bleaching event. Colonies that recovered et al., 2012a). Gametes can disperse over and partial mortality, particularly in after bleaching events were able to 500 m in 100 minutes, and O. franksi large colonies. follow a normal reproductive cycle, but sperm viability decreases after two bleached colonies of O. annularis The SRR, SIR, and public comments hours (Levitan et al., 2004). Orbicella species complex were unable to did not provide other biological franksi and O. annularis gametes are complete gametogenesis (Szmant and compatible, though other mechanisms information on the Orbicella annularis Gassman, 1990). Compared to recovered associated with the temporal isolation of species complex. Supplemental colonies, bleached colonies had lower spawning, including gamete aging, biological information we found on tissue biomass, lower carbon-to-nitrogen dilution, and dispersal, make Orbicella is provided as follows. The ratios, and reduced growth, indicating hybridization less likely (Knowlton et Orbicella annularis species complex is the energy reserves needed for al., 1997; Levitan et al., 2004). All three sensitive to cold water. In laboratory successful reproduction were not species are largely self-incompatible experiments, O. annularis species available (Szmant and Gassman, 1990). (Knowlton et al., 1997; Szmant et al., complex released zooxanthellae when During the 1987 bleaching event, 90 1997). Size at sexual maturity is shocked with cold water between 12 percent of all O. annularis species generally about 200 cm2 (Szmant- and 18 degrees C, and the response complex colonies surveyed at 30 m in Froelich, 1985). Colonies that were decreased with increasing temperature the Cayman Islands were bleached. fragmented experimentally to sizes (Muscatine et al., 1991). Bleaching was less severe at 46 m with smaller than 100 cm2 were generally Susceptibility to Threats 14 percent of O. annularis species found to have lower fecundity complex colonies bleached. Five indicating that frequent fragmentation The SRR and SIR provided the months after bleaching was first and partial mortality can affect following information on Orbicella’s observed in the Cayman Islands, 54 reproductive capacity (Szmant-Froelich susceptibility to ocean warming. The percent of bleached O. annularis species 1985). Orbicella annularis species complex is complex colonies had not recovered. Smith and Aronson (2006) reported moderately to highly susceptible to Orbicella annularis species complex 18 Orbicella recruits between 1998 and bleaching. The composition of had the slowest recovery of the 28 coral 2003 in 384 permanent monitoring zooxanthellae in at least some areas species observed to bleach (Ghiold and quadrats (237 m2) in the lower Florida changes in response to bleaching. Smith, 1990). Keys. The ability of the species complex Bleaching has been shown to prevent In a 1995 bleaching event in Belize, O. to dominate with such low recruitment reproduction in the following season annularis species complex was the most rates has been described as a storage after recovering normal pigmentation. affected coral taxon with 76 percent of effect whereby large, old colonies are Particularly well documented mortality the 2,126 surveyed colonies affected. able to persist and maintain the following severe mass bleaching in 2005 Seven percent of the 904 colonies population until favorable conditions highlights the immense impact thermal surveyed six months after the bleaching for recruitment occur (Edmunds and stress events and their aftermath can event remained bleached. Twenty-six Elahi, 2007). However, potential have on the Orbicella annularis species percent of tagged O. annularis species problems may exist for species complex. A significant correlation was complex colonies (n=19) exhibited employing storage effects if favorable found between bleaching in 2005 and partial mortality due to bleaching or conditions for recruitment occur so the prevalence of yellow band disease post-bleaching infection by black band infrequently that they fall outside the and white plague affecting the Orbicella disease (McField, 1999). life span of the cohort (Foster et al., species complex. Additionally, in In 20 surveys across 302 sites 2013). laboratory experiments, mortality due to throughout the wider Caribbean, O.

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annularis species complex and Agaricia Additionally, the severe tissue loss and about four percent. Orbicella annularis tenuifolia were the taxa most impacted prolonged bleaching stress resulted in species complex lost a large proportion by the 1998 bleaching event (Ginsburg reproductive collapse of O. annularis of colonies in the largest size class and and Lang, 2003; Kramer, 2003). species complex during the 2006 mass showed a significant increase in colony Subsequent disease outbreaks were also spawning cycle (Waddell and Clarke, abundance, likely due to the increase in recorded in O. annularis and O. 2008). abundance of colonies in smaller size faveolata off Curac¸ao, the Cayman The 2005 bleaching affected greater classes resulting from partial mortality Islands, Costa Rica, and some of the than 95 percent of O. annularis species of larger colonies. Virgin Islands after the bleaching event. complex in Mona and Desecheo Islands, Van Woesik et al. (2012) developed a Bleaching and disease related mortality Puerto Rico and was followed by a coral resiliency index based on heavily impacted the O. annularis disease outbreak that both caused biological traits and processes to species complex (Ginsburg and Lang, extensive mortality (Bruckner and Hill, evaluate extinction risk due to 2003). 2009). A study of 36 sites across six bleaching. Evaluations were performed During the 2005 bleaching event, countries (Grenada, Curac¸ao, Panama´, at the genus level, but genera were approximately 70 percent of O. Puerto Rico, Cayman Islands, and separated between the Caribbean and annularis species complex colonies Bermuda) and three depth habitats (less Indo-Pacific. They rated the resilience bleached both in sites less than 10 m in than 4 m, 5 to 12 m, and greater than score for the O. annularis species depth and in sites greater than 15 m in 15 m) found a significant correlation complex as four out of a range of -6 to 7 observed in other coral genera. Less depth on the west and southwest coasts between the 2005 bleaching and of Barbados (Oxenford et al., 2008). than or equal to -3 was considered prevalence of yellow band disease and Bleaching was observed in 2005 at 86 of highly vulnerable to extinction, and white plague in O. annularis species 94 sites (91 percent) surveyed in Buck greater than or equal to 4 was complex (Croquer and Weil, 2009). Island Reef, U.S. Virgin Islands. Ninety- considered highly tolerant. Thus, O. Orbicella annularis species complex four percent of the cover of O. annularis annularis species complex was rated as bleached at all depths surveyed in species complex bleached (Clark et al., highly tolerant. However, Smith et al. Grenada (23 to 52 percent of colonies), 2009). (2013b) concluded that large faviids, Puerto Rico (21 to 40 percent), and The 2005 bleaching event resulted in such as the O. annularis species Cayman Islands (16 to 44 percent). The a 51 percent decrease in the cover of O. complex, seem very susceptible to long- annularis species complex at five sites species complex did not experience term population declines because of in the U.S. Virgin Islands between 2005 bleaching in Curacao or Bermuda, both their poor response to stress response and 2007. Bleaching occurred in 16 of locations reported very low bleaching when bleaching, disease, and mortality the 21 species of coral at the five sites across all genera examined (Croquer and were considered. The O. annularis with maximum tissue area bleached Weil, 2009). Bleaching of O. annularis species complex was found to be likely between 98 to 99.5 percent for the O. species complex varied by depth in less equipped to recovery after annularis species complex. Mortality Panama with bleaching occurring in 11 bleaching because they tend to grow after the bleaching event occurred percent of colonies in depths less than slowly, have lower fecundity, and are primarily from a subsequent regional 4 m and in15 percent of colonies in more susceptible to mortality when outbreak of coral disease, depths between 5 and 12 m, but no small (Smith et al., 2013b). While the predominantly white plague, not the bleaching occurred in deep depths van Woesik et al. (2012) study was in bleaching itself. The highest rate of greater than 15 m (Croquer and Weil, the SIR, the findings specific to mortality of the 19 species affected by 2009). Smith et al. (2013b) described Orbicella were not included. The public the white plague was the Orbicella species responses to the 2005 and 2010 comments indicated the results of this annularis species complex with 94.5 bleaching events in St. Thomas, St. study should be considered in the percent of disease lesions occurring on Croix, and St. John, U.S. Virgin Islands. listing status of the three species in the Orbicella annularis species complex. The response of the O. annularis species Orbicella species complex. Total coral cover declined from 21 complex (mostly O. faveolata and O. All sources of information are used to percent to 10 percent, and species- franksi with the likelihood of small describe Orbicella’s susceptibility to specific changes in coral cover affected numbers of O. annularis) to the 2005 ocean warming as follows. The O. the relative abundance of coral species bleaching event was high to moderate annularis species complex is highly on the reef. Overall relative abundance initial response of bleaching prevalence, susceptible to ocean warming. of O. annularis species complex high disease prevalence, high mortality, Bleaching often occurs in 76 to 94 declined from an initial average of 79 to a large decline in coral cover, and percent of O. annularis species complex 59 percent of live coral cover (Miller et increasing or stable colony abundance. colonies during bleaching events, and al., 2009). Average bleaching was 66 percent, and Orbicella spp. are one of the taxa most Stratified random surveys on back- paling was 27 percent in 2005. Disease affected by high temperatures. Colonies reefs and fore-reefs between one and 30 prevalence in O. annularis complex was in deeper water have been reported to m depth off Puerto Rico (Mona and 17 percent after the 2005 bleaching bleach less severely. Recovery from Desecho Islands, La Parguera, event. In the milder 2010 bleaching bleaching can take longer for the species Mayaguez, Boqueron, and Rincon) in event, 35 percent of O. annularis species complex than for other coral species, 2005 and 2006 revealed bleaching was complex colonies bleached, and 47 and prolonged stress from bleaching has most severe in O. annularis species percent of O. annularis species complex been cited as a possible reason for complex with 94 percent of colonies colonies paled. Less than one percent of reproductive failure following bleaching bleached. After bleaching, a disease O. annularis species complex colonies events. Mortality from temperature outbreak occurred, and O. annularis suffered total mortality, but percent anomalies is often due to subsequent species complex suffered extensive cover decreased from seven percent disease outbreaks. Thus, we conclude partial and total mortality. Coral cover cover of O. annularis species complex that the O. annularis species complex is declined between 40 and 60 percent and in 2005 before bleaching to less than highly susceptible to ocean warming. was primarily driven by mortality of O. three percent in 2007. By 2010, there The SRR and SIR provided the annularis species complex. was a slight increase in percent cover to following information on Orbicella’s

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susceptibility to acidification. The only complex colonies (Smith et al., 2010). from 2000 to 2005. Yellow band disease study conducted regarding the impact of White plague is one of the most affected larger corals more frequently acidification on this genus is a field aggressive coral diseases in the than small corals. Over 21 percent of the study that did not find any change in O. Caribbean with progression rates of 1 to colonies tagged with yellow band faveolata calcification in field-sampled 10 cm per day (Bruckner and Hill, disease between 1997 and 1999 were colonies from the Florida Keys up 2009). Tissue loss from yellow band still infected in 2005. Of the remainder, through 1996. Preliminary experiments disease is slow, averaging 0.5 to 1 cm 44 percent died, 2 percent were affected testing effects of acidification on per month, though tissue loss can be by other diseases, and 32 percent no fertilization and settlement success of O. significant over the long term since longer had signs of yellow band disease annularis species complex show results colonies can remain infected for years but had large amounts (most greater that are consistent with the significant and can have multiple lesions per than 90 percent) of partial mortality impairments demonstrated for A. colony (Bruckner and Bruckner, 2006b). (Bruckner and Bruckner, 2006a). palmata. In the Florida Keys, the prevalence of Disease prevalence in O. annularis The public comments did not provide white plague increased between 1996 species complex (O. annularis and O. new or supplemental information on the and 2002. No O. annularis species faveolata) at three reefs off Mexico susceptibility of the Orbicella species complex colonies with white plague increased from between zero and four complex to acidification. Supplemental were reported within monitoring percent in 1996 and 1998 to between 26 information we found on the stations in 1996, but infected colonies and 37 percent in 2001. The increase susceptibility of the Orbicella species appeared in 32 stations in 2002 was due to the proliferation of yellow complex to acidification includes the (Waddell, 2005). Orbicella annularis band disease, though black band disease following. In laboratory experiments, species complex had the highest and white plague were also present. reproduction of O. faveolata was prevalence (up to 12 percent) of the 21 Partial mortality also increased over this negatively impacted by increasing species affected by white plague in same period from 20 to 35 percent of O. carbon dioxide, and impairment of Puerto Rico between 1998 and 2008 annularis species complex colonies at fertilization was exacerbated at lower (Bruckner and Hill, 2009). In Mexico, O. one site and from 35 to 52 percent at sperm concentrations (Albright, 2011b). annularis species complex had the another (Jordan-Dahlgren et al., 2005). Fertilization success was reduced by 25 highest disease prevalence in surveys At 253 sites surveyed in 2009 in St. percent at 529 matm (43 percent during 2004 (27 percent, Ward et al., Croix and St. John, U.S. Virgin Islands fertilization) and 40 percent at 712 matm 2006). Surveys in four locations and La Parguera, Puerto Rico, the (34 percent fertilization) compared to (Netherlands Antilles, Grenada, Turks average number of healthy O. annularis controls at 435 matm (57 percent and Caicos, and U.S. Virgin Islands) species complex colonies was 182 (± 33 fertilization; Albright, 2011a). between 1997 and 1998 revealed that SE) per 100 m2. Yellow band was Additionally, growth rate of O. faveolata prevalence of yellow band in O. present on an average of about one was reduced under lower pH conditions annularis species complex ranged from percent of colonies (Muller and van (7.6) compared to higher pH conditions 18 to 91 percent. Woesik, 2012). (8.1) after 120 days of exposure (Hall et Tagged colonies with yellow band All sources of information are used to al., 2012). disease in Puerto Rico lost an average of describe Orbicella’s susceptibility to All sources of information are used to 32 percent of their tissue over four disease as follows. Disease can affect a describe Orbicella’s susceptibility to years, and the percent of partial large proportion of the Orbicella spp. acidification as follows. Laboratory mortality appeared to increase with population (3 to 91 percent), studies indicate that Orbicella is colony size (Bruckner and Bruckner, particularly during outbreaks following susceptible to ocean acidification both 2006b). Eight percent of infected bleaching events, and can cause through reduced fertilization of gametes colonies died completely (most were 50 extensive mortality. Partial mortality and reduced growth of colonies. Thus, cm or less in size), and larger colonies can be high (32 to greater than 90 we conclude that the Orbicella species lost between 60 and 85 percent of their percent) and can result in multiple complex is highly susceptible to ocean tissue (Bruckner and Bruckner, 2006b). ramets. White plague and yellow band acidification. Eighty-five percent of colonies with disease have had the greatest effect and The SRR and SIR provided the yellow band disease tagged in 1999 still can disproportionately affect larger following information on Orbicella’s had active signs of the disease in 2003 colonies in the species complex. Total susceptibility to disease. White plague (Bruckner and Bruckner, 2006b). In colony mortality is less likely for larger and yellow band (also called yellow 1999, yellow band disease affected up to colonies than for smaller colonies, and blotch) disease have caused profound 50 percent of all O. annularis species partial mortality can lead to changes in population decline of the Orbicella complex colonies at permanent sites in colony size distribution as observed in annularis species complex both with Puerto Rico, including many of the Puerto Rico, U.S. Virgin Islands, and a and without prior bleaching. largest (2 to 3 m diameter and height) study in Bahamas, Bonaire, Cayman The public comments did not provide and presumably oldest colonies Islands, and St. Kitts and Nevis. Thus, new or supplemental information on the (Waddell and Clarke, 2008). we conclude that the O. annularis susceptibility of Orbicella spp. to In Curacao, yellow band disease species complex is highly susceptible to disease. Supplemental information we affected from three to 49 percent of all disease. found on Orbicella’s susceptibility to O. annularis species complex colonies The SIR and SRR did not provide any disease confirms and expands the within transects conducted on western information on the trophic effects of information in the SRR and SIR. reefs between 1997 and 2005. The fishing on Orbicella. The public Orbicella spp. are susceptible to black highest prevalence of yellow band comments did not provide new or band disease and dark spot syndrome disease occurred in 1997 and 1998. supplemental information, and we did (Alcolado et al., 2010). Additionally, an Thirty-one to 49 percent of O. annularis not find new or supplemental unknown disease was observed in the species complex colonies were affected information on the trophic effects of Red Hind Marine Conservation District in eastern Curacao, and 24 percent were fishing on Orbicella. However, as in the U.S. Virgin Islands and affected affected in western Curacao. The described above in Caribbean Genera 39 percent of O. annularis species numbers of new infections declined and Species—Introduction, due to the

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level of reef fishing conducted in the Additionally, decreasing growth rate of Public comments did not provide new Caribbean, coupled with Diadema die- Orbicella over a 30-year period was or supplemental information on the off and lack of significant recovery, attributed to deterioration of water susceptibility of Orbicella to predation. competition with algae can adversely quality. Supplemental information we found on affect coral recruitment. This effect The public comments did not provide the susceptibility of the Orbicella coupled with Orbicella’s low new or supplemental information on the species complex includes the following. recruitment rate indicates it likely has susceptibility of Orbicella to nutrient Surveys of six sites in Navassa found some susceptibility to the trophic effects enrichment. Supplemental information between zero and 33 percent of O. of fishing. The available information we found on the susceptibility of the annularis species complex colonies does not support a more precise Orbicella species complex confirms and (average 17 percent across all sites) were description of its susceptibility. expands the information in the SRR and affected by C. abbreviata (Miller et al., The SRR and SIR provided the SIR. Two growth forms of O. annularis 2005). The O. annularis species following information on the species complex, columnar (likely O. complex was the preferred target of susceptibility of Orbicella to faveolata) and lobate (likely O. parrotfish across all reef habitats in a sedimentation. Orbicella has shown a annularis) were found to have study on the Belize barrier reef. decline in growth at sediment impacted increasing average growth rates with Incidence of parrotfish grazing was sites in Puerto Rico and during periods improving environmental conditions of construction in Aruba. Along a away from a eutrophication gradient in highest on O. annularis (over 55 percent gradient of continental influence in the Barbados (Tomascik, 1990). Although of colonies), followed by O. franksi and southern Gulf of Mexico, density and nutrient concentration was negatively O. faveolata, respectively (Rotjan, 2007). calcification rate of O. annularis correlated with growth, suspended In most habitats, a few colonies of decreased with increasing turbidity and particulate matter resulting from Orbicella spp. were more heavily grazed sedimentation while extension rate eutrophication, rather than the nutrients by parrotfishes, while the majority increased with increasing turbidity and themselves, was postulated to be the showed little or no parrotfish grazing sedimentation. cause of observed decreased growth (Rotjan and Lewis, 2006). The public comments did not provide rates (Tomascik and Sander, 1985). A All sources of information are used to new or supplemental information on the general pattern of decreasing growth describe Orbicella’s susceptibility to susceptibility of Orbicella to rates of the columnar growth form predation as follows. The O. annularis sedimentation. Supplemental between 1950 and 1983 may be directly species complex is susceptible to information we found on the related to the deterioration of water several predators. Current effects of susceptibility of the Orbicella annularis quality along the west coast of the predation appear to be low. Thus, we species complex confirms the island (Tomascik, 1990). Additionally, conclude the O. annularis species information in the SRR and SIR. The Orbicella spp. did not recruit to complex has low susceptibility to Orbicella annularis species complex settlement plates on the most eutrophic predation. appears to be moderately capable of reef, and recruitment of Orbicella spp. removing sediment from the colony increased at sites with decreasing The SRR and SIR did not provide surface. Colonies receiving single eutrophication along the eutrophication information on the effects of sea level applications of 200 or 400 mg sediment gradient (Tomascik, 1991). Field rise on Orbicella. The SRR described sea per cm2 showed no evidence of damage experiments indicate that nutrient level rise as an overall low to medium while 800 mg per cm2 caused mortality enrichment significantly increases threat for all coral species. The public (Rogers, 1983). Sedimentation has been yellow band disease severity in O. comments did not provide new or found to negatively affect O. annularis annularis and O. franksi through supplemental information on Orbicella’s species complex primary production, increased tissue loss (Bruno et al., susceptibility to sea level rise, and we growth rates, and abundance (Pastorok 2003). did not find any new or supplemental and Bilyard, 1985). An observed All sources of information are used to information. Thus, we conclude that difference in average colony size at two describe Orbicella’s susceptibility to Orbicella has some susceptibility to sea sites in Puerto Rico led Loya (1976) to nutrient enrichment as follows. The level rise, but the available information conclude turbidity negatively affects Orbicella annularis species complex is does not support a more precise growth of O. annularis species complex susceptible to nutrient enrichment description of susceptibility to this since colony size was half as large at the through reduced growth rates, lowered threat. sediment-impacted site (23 cm versus 9 recruitment, and increased disease The SRR and SIR provided the cm). severity. Thus, we conclude that the O. following information on the All sources of information are used to annularis species complex is highly describe Orbicella’s susceptibility to susceptible to nutrient enrichment. susceptibility of the Orbicella species sedimentation as follows. Although the The SRR and SIR provided the complex to collection and trade. The species complex is moderately capable following information on the Orbicella complex species have a very of removing sediment from the colony susceptibility of Orbicella to predation. low occurrence in the CITES trade surface, sedimentation negatively affects Predators of the O. annularis species databases. Hence, collection and trade is primary production, growth rates, complex include the corallivorous snail not considered a significant threat to the calcification, colony size, and Coralliophila abbreviata and some Orbicella annularis complex species. abundance. Thus, we conclude that the species of parrotfish including The public comments did not provide O. annularis species complex is highly Sparisoma viride and S. aurofrenatum. new or supplemental information on the susceptible to sedimentation. Additionally, damselfish remove live susceptibility of the Orbicella species The SRR and SIR provided the coral tissue to build algal gardens. The complex to trade. Supplemental following information on the large decline of Acropora spp. in the information we found on the susceptibility of Orbicella to nutrient Caribbean, likely resulted in greater susceptibility of species in the Orbicella enrichment. Orbicella had an increasing impacts by damselfishes on other high- complex to collection and trade is growth rate with improving dimension corals, including the O. described in each of the individual environmental conditions in Barbados. annularis species complex. species sections.

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Genus Conclusion reefs, suggesting the potential for deep random surveys, differences between refugia for O. faveolata. years may be attributed to sampling The O. annularis species complex is The public comments did not provide effort rather than population trends distributed throughout the Caribbean new or supplemental information on O. (Miller et al., 2013). and occupies a variety of habitats across faveolata’s distribution, habitat, or Supplemental information we found a large depth range, including depth range. Supplemental information on O. faveolata’s abundance and mesophotic depths to 90 m. Over the we found includes the following. Veron population trends includes the last twenty years, major declines of (2014) confirmed the occurrence of O. following. In a survey of 31 sites in approximately 50 to 95 percent have faveolata in five out of his 11 ecoregions Dominica between 1999 and 2002, O. occurred. In addition, changes in size in the west Atlantic and greater faveolata was present at 80 percent of frequency distribution have sometimes Caribbean known to contain corals and the sites at one to ten percent cover accompanied decreases in cover, strongly predicted its presence in an (Steiner, 2003). In a 1995 survey of 16 resulting in fewer large colonies that additional three ecoregions (off reefs in the Florida Keys, O. faveolata impact the buffering capacity of the Colombia and Venezuela; Jamaica and ranked as the coral species with the species complex’s life history strategy. Cayman Islands; and Florida and the second highest percent cover (Murdoch Despite decline, the O. annularis Bahamas). Many studies have confirmed and Aronson, 1999). On 84 patch reefs species complex continues to be the presence of O. faveolata in these (3 to 5 m depth) spanning 240 km in the reported as the dominant coral taxon, additional three ecoregions (Bayraktarov Florida Keys, O. faveolata was the third sometimes at a lower percentage of the et al., 2012; Bruckner, 2012a; Burman et most abundant coral species comprising total coral cover. al., 2012). The ecoregions where Veron seven percent of the 17,568 colonies The species complex has highly (2014) reported the absence of O. encountered and was present at 95 susceptibility to ocean warming, faveolata are off the coasts of Brazil, percent of surveyed reefs between 2001 acidification, disease, sedimentation, Bermuda, and the southeastern U.S. and 2003 (Lirman and Fong, 2007). In and nutrients; some susceptibility to north of southern Florida (Veron, 2014). surveys of 280 sites in the upper Florida trophic effects of fishing and sea level Smith (2013) reported that O. faveolata Keys in 2011, O. faveolata was present rise; and low susceptibility to predation. is found in the U.S. Virgin Islands at 87 percent of sites visited (Miller et Susceptibility to collection and trade is across all depths to about 45 m. al., 2011b). In 2003 on the East Flower described in each of the individual Garden Bank, O. faveolata comprised Demographic Information species sections. ten percent of the 76.5 percent coral The SRR and SIR provided the cover on reefs 32 to 40 m, and partial Orbicella faveolata following information on O. faveolata’s mortality due to bleaching, disease, and Introduction abundance and population trends. predation were rare at monitoring Orbicella faveolata is considered stations (Precht et al., 2005). The SRR and SIR provided the common. Colony density ranges from following information on O. faveolata’s The public comments did not provide approximately 0.1 to 1.8 colonies per 10 morphology. Orbicella faveolata grows new or supplemental information on O. m2 and varies by habitat and location. in heads or sheets, the surface of which faveolata’s population trends but In surveys along the Florida reef tract may be smooth or have keels or bumps. provided the following supplemental from Martin County to the lower Florida The skeleton is much less dense than in information on O. faveolata’s Keys, density of O. faveolata was the other two Orbicella species. Colony abundance. Extrapolated population approximately 1.6 colonies per 10 m2 diameter can reach up to 10 m with a estimates from stratified random (Wagner et al., 2010). On remote reefs height of 4 to 5 m. The public comments samples in the Florida Keys were 39.7 off southwest Cuba, density of O. did not provide new or supplemental ± 8 million (SE) colonies in 2005, 21.9 faveolata was 0.12 ± 0.20 (SD) colonies information on O. faveolata’s ± 7 million (SE) colonies in 2009, and per 10 m transect on 38 reef-crest sites morphology, and we did not find any 47.3 ± 14.5 million (SE) colonies in and 1.26 ± 1.06 colonies per 10 m new or supplemental information. 2012. The greatest proportion of transect on 30 reef-front sites (Alcolado colonies tended to fall in the 10 to 20 Spatial Information et al. 2010). In surveys of 1,176 sites in cm and 20 to 30 cm size classes in all southeast Florida, the Dry Tortugas, and The SRR and SIR provided the survey years, but there was a fairly large the Florida Keys between 2005 and following information on the proportion of colonies in the greater 2010, density of O. faveolata ranged distribution, habitat and depth range of than 90 cm size class. Partial mortality between 0.17 and 1.75 colonies per 10 O. faveolata. Orbicella faveolata occurs of the colonies was between 10 and 60 m2 and was highest on mid-channel in the western Atlantic and throughout percent surface across all size classes. In reefs followed by offshore patch reefs the Caribbean, including Bahamas, the Dry Tortugas, Florida, O. faveolata and fore-reefs (Burman et al., 2012). Flower Garden Banks, and the entire ranked seventh most abundant out of 43 Along the east coast of Florida, density Caribbean coastline. There is conflicting coral species in 2006 and fifth most was highest in areas south of Miami at information on whether or not it occurs abundant out of 40 in 2008. 0.94 colonies per 10 m2 compared to in Bermuda. Orbicella faveolata has Extrapolated population estimates were 0.11 colonies per 10 m2 in Palm Beach been reported in most reef habitats and 36.1 ± 4.8 million (SE) colonies in 2006 and Broward Counties (Burman et al., is often the most abundant coral and 30 ± 3.3 million (SE) colonies in 2012). between 10 and 20 m in fore-reef 2008. The size classes with the largest Orbicella faveolata is the sixth most environments. The depth range of O. proportion of colonies were 10 to 20 cm abundant species by percent cover in faveolata has been reported as 0.5 to 40 and 20 to 30 cm, but there was a fairly permanent monitoring stations in the m, though the species complex has been large proportion of colonies in the U.S. Virgin Islands. The species reported to depths of 90 m, indicating greater than 90 cm size class. Partial complex had the highest abundance and O. faveolata’s depth distribution is mortality of the colonies ranged included all colonies where species likely deeper than 40 m. Orbicella between approximately two percent and identification was uncertain. Therefore, species are a common, often dominant 50 percent. Because these population O. faveolata is likely more abundant. component of Caribbean mesophotic abundance estimates are based on Population estimates in the 49 km2 Red

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Hind Marine Conservation District are at faveolata from Mona and Descheo classifications were primarily separated least 16 million colonies (Smith, 2013). Islands, Puerto Rico include a 36 to 48 by colony morphology, growth rate, and Population trend data exists for percent reduction in abundance and a reproductive mode. Orbicella faveolata several locations. At nine sites off Mona decrease of 42 to 59 percent in its was classified as a ‘‘generalist’’ species, and Desecheo Islands, Puerto Rico, no relative abundance (i.e., proportion thus likely less vulnerable to species extirpations were noted at any relative to all coral colonies). High environmental stress. site over ten years of monitoring partial mortality of colonies has led to The SRR and SIR provided the between 1998 and 2008 (Bruckner and smaller colony sizes and a decrease of following other biological information Hill, 2009). Both O. faveolata and O. larger colonies in some locations such on O. faveolata. Surveys at an inshore annularis sustained the large losses as the Bahamas, Bonaire, Puerto Rico, patch reef in the Florida Keys that during the period. The number of Cayman Islands, and St. Kitts and Nevis. experienced temperatures less than 18 colonies of O. faveolata decreased by 36 Partial colony mortality is lower in degrees C for 11 days revealed species- and 48 percent at Mona and Desecheo some areas such as the Flower Garden specific cold-water susceptibility and Islands, respectively (Bruckner and Hill, Banks. We conclude that O. faveolata survivorship. Orbicella faveolata was 2009). In 1998, 27 percent of all corals has declined but remains common and one of the more susceptible species with at six sites surveyed off Mona Island likely has at least tens of millions of 90 percent of colonies experiencing total were O. faveolata colonies, but colonies throughout its range. colony mortality, including some decreased to approximately 11 percent Additionally as discussed in the genus colonies estimated to be more than 200 in 2008 (Bruckner and Hill, 2009). At section, we conclude that the buffering years old (Kemp et al., 2011). In surveys Desecheo Island, 12 percent of all coral capacity of O. faveolata’s life history from Martin County to the lower Florida colonies were O. faveolata in 2000 strategy that has allowed it to remain Keys, O. faveolata was the second most compared to seven percent in 2008. abundant has been reduced by the susceptible coral species experiencing In a survey of 185 sites in five recent population declines and amounts an average of 37 percent partial countries (Bahamas, Bonaire, Cayman of partial mortality, particularly in large mortality (Lirman et al., 2011). Islands, Puerto Rico, and St. Kitts and colonies. The public comments did not provide Nevis) between 2010 and 2011, size of any new or supplemental biological O. faveolata colonies was significantly Other Biological Information information on O. faveolata. greater than O. franksi and O. annularis. The SRR and SIR provided the Supplemental biological information we The total mean partial mortality of O. following information on O. faveolata’s found on O. faveolata includes the faveolata at all sites was 38 percent. The life history. In many life history following. Samples (n = 182) of O. total live area occupied by O. faveolata characteristics, including growth rates, faveolata from the upper and lower declined by a mean of 65 percent, and tissue regeneration, and egg size, O. Florida Keys and Mexico showed three mean colony size declined from 4005 faveolata is considered intermediate well-defined populations based on five cm2 to 1413 cm2. At the same time, between O. annularis and O. franksi. genetic markers, but the populations there was a 168 percent increase in Spatial distribution may affect fecundity were not stratified by geography, small tissue remnants less than 500 cm2, on the reef, with deeper colonies of O. indicating they were shared among the while the proportion of completely live faveolata being less fecund due to three regions (Baums et al., 2010). Of ten large (1,500 to 30,000 cm2) colonies greater polyp spacing. O. faveolata colonies observed to spawn decreased. Orbicella faveolata colonies The public comments did not provide at a site off Bocas del Toro, Panama, in Puerto Rico were much larger and new or supplemental information on the colonies sorted into three spatially sustained higher levels of mortality life history of O. faveolata. arranged genotypes (Levitan et al., compared to the other four countries. Supplemental information we found on 2011). Colonies in Bonaire were also large but O. faveolata’s life history includes the Orbicella faveolata larvae are experienced much lower levels of following. Reported growth rates of O. sensitive to ultraviolet radiation during mortality. Mortality was attributed faveolata range between 0.3 and 1.6 cm the motile planula stage through the primarily to outbreaks of white plague per year (Cruz-Pin˜ o´n et al., 2003; onset of larval competence (Aranda et and yellow band disease, which Tomascik, 1990; Villinski, 2003; al., 2011). Of six Caribbean coral species emerged as corals began recovering from Waddell, 2005). Graham and van exposed to high solar irradiation, O. mass bleaching events. This was Woesik (2013) report that 44 percent of faveolata and Stephanocoenia followed by increased predation and small colonies of O. faveolata in Puerto intersepta had the most severe decline removal of live tissue by damselfish to Morelos, Mexico, resulting from partial in photochemical efficiency resulting in cultivate algal lawns (Bruckner, 2012a). colony mortality produced eggs at sizes severe tissue loss and mortality (Fournie All information on O. faveolata’s smaller than maturation. The number of et al., 2012). abundance and population trends can eggs produced per unit area of smaller Experiments exposing O. faveolata to be summarized as follows. Orbicella fragments was significantly less than in high temperatures (up to 35 degrees C) faveolata is a common species larger size classes. Szmant and Miller revealed that the corals produced heat throughout the greater Caribbean. Based (2005) reported low post-settlement shock proteins at temperatures between on population estimates, there are at survivorship for O. faveolata 33 and 35 degrees C even for very short least tens of millions of colonies present transplanted to the field with only three exposures (2 h) but did respond at in each of several locations including to 15 percent remaining alive after 30 temperatures between 27 and 31 degrees the Florida Keys, Dry Tortugas, and the days. Post-settlement survivorship was C when exposed from 2 hours to one U.S. Virgin Islands. Absolute abundance much lower than the 29 percent week (Black et al., 1995). is higher than the estimate from these observed for A. palmata after seven Thornhill et al. (2006) repeatedly three locations given the presence of months (Szmant and Miller, 2005). sampled symbiont composition of this species in many other locations Darling et al. (2012) performed a colonies of six coral species in the throughout its range. Population decline biological trait-based analysis to Bahamas and the Florida Keys in 1998 has occurred over the past few decades categorize coral species into four life and 2000 to 2004, during and after the with a 65 percent loss in O. faveolata history strategies: Generalist, weedy, 1997–98 bleaching event. Symbioses in cover across five countries. Losses of O. competitive, and stress-tolerant. The O. faveolata remained stable at virtually

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all sites in the Bahamas and the Florida bleaching prevalence with decreased for embryos kept at 29 and Keys. Individual colonies usually approximately 37 percent of colonies 31.5 degrees C, and increased for showed fidelity over time to one bleached (van Hooidonk et al., 2012). embryos kept at 27.5 degrees C. particular Symbiodinium partner, and Coral cores from 92 colonies of O. Increased temperatures may lead to changing symbiont types was rare, thus faveolata from the Mesoamerican Reef oxidative stress, apoptosis, and a indicating acclimation to warming around Belize and Honduras indicate structural reconfiguration of the temperatures may not occur by that the bleaching event in 1998 was cytoskeletal network. However, embryos symbiont shuffling. unprecedented in the prior century responded differently depending on despite periods of higher temperatures Susceptibility to Threats exposure time and temperature level. and solar irradiance (Carilli et al., 2010). Embryos showed expression of stress- The threat susceptibility information The authors of the study concluded that related genes at a temperature of 29 from the SRR and SIR was interpreted bleaching in 1998 likely stemmed from degrees C but seemed to be able to in the proposed rule for O. faveolata’s reduced thermal tolerance due to the counteract the initial response over vulnerabilities to threats as follows: synergistic impacts of chronic local time. Embryos at 31.5 degrees C High vulnerability to ocean warming, stressors stemming from land-based displayed continuous expression of disease, acidification, sedimentation, sources of pollution (Carilli et al., 2010). stress genes. and nutrient enrichment; moderate Coral cores collected from four sites in During the 2005 bleaching event, vulnerability to the trophic effects of Belize indicate that O. faveolata that larger colonies of O. faveolata fishing; and low vulnerability to sea experienced higher chronic stress were experienced more intensive bleaching level rise, predation, and collection and more severely affected by bleaching and than smaller colonies at inshore patch trade. had a much slower recovery after the reefs of the Florida Keys (Brandt, 2009). The SRR and SIR provided the severe 1998 bleaching event (Carilli et Orbicella faveolata was one of the most following information on the al., 2009). Coral growth rates at sites affected species with approximately 80 susceptibility of O. faveolata to ocean with higher local anthropogenic percent of colonies (n = 77) bleached warming. Recent work in the stressors remained suppressed for at Mesoamerican reef system indicated and, out of eight species that bleached, least eight years, while coral growth had the fourth highest bleaching that O. faveolata had reduced thermal rates at sites with lower stress recovered tolerance in locations with increasing prevalence (Brandt, 2009). Orbicella in two to three years (Carilli et al., faveolata colonies with greater human populations and over time, 2009). Based on samples of O. faveolata implying increasing local threats. At bleaching intensities later developed and O. franksi collected from the white plague disease (Brandt and sites in Navassa, O. faveolata and Mesoamerican Barrier Reef, calcification Agaricia spp. were the most susceptible McManus, 2009). White plague affected of these two species is projected to cease approximately ten percent of O. to bleaching. Approximately 90 percent at 35 degrees C in this location, even faveolata colonies and resulted in less of O. faveolata colonies (n = 334) without an increase in acidification than five percent tissue loss in all but bleached at deeper sites (>18 m), and (Carricart-Ganivet et al., 2012). two infected corals which experienced approximately 60 percent of O. Collections from Chinchorro Bank greater than five percent tissue loss faveolata colonies (n = 20) bleached at indicate that calcification of O. (Brandt and McManus, 2009). shallower sites (<10 m) in 2006. During faveolata decreased 20 percent over the a moderate bleaching event in Colombia period of 1985 to 2009 where there was All sources of information are used to in 2010, 100 percent of O. faveolata a 0.6 degree C increase in sea surface describe O. faveolata’s susceptibility to colonies bleached at a site in Gayraca temperature (equivalent to 2.4 degrees C ocean warming as follows. Orbicella Bay, and 50 percent of O. faveolata per century; Carricart-Ganivet et al., faveolata is highly susceptible to colonies were dead and completely 2012). elevated temperatures. In lab overgrown by algae in 2011 Polato et al. (2010) raised O. faveolata experiments, elevated temperatures (Bayraktarov et al., 2012). larvae derived from three to four resulted in misshapen embryos and The public comments did not provide colonies from Florida and Mexico under differential gene expression in larvae new or supplemental information on the mean and elevated (1 to 2 degrees above that could indicate negative effects on susceptibility of O. faveolata to ocean summer mean) temperatures. Both larval development and survival. warming. Supplemental information we locations had misshapen embryos at the Bleaching susceptibility is generally found on the susceptibility of O. elevated temperature, but the percentage high with 37 to 100 percent of O. faveolata to ocean warming includes the was higher in the embryos from Florida. faveolata colonies reported to bleach following. Stratified random surveys on They found conserved and location- during several bleaching events. back-reefs and fore-reefs between one specific variation in gene expression in Chronic local stressors can exacerbate and 30 m depth off Puerto Rico (Mona processes related to apoptosis the effects of warming temperatures, and Desecho Islands, La Parguera, (programmed cell death), cell which can result in slower recovery Mayaguez, Boqueron, and Rincon) in structuring, adhesion and development, from bleaching, reduced calcification, 2005 and 2006 revealed severe energy and protein metabolism, and and slower growth rates for several bleaching in O. faveolata with response to stress. years following bleaching. Additionally, approximately 90 percent of colonies Voolstra et al. (2009) exposed O. disease outbreaks affecting O. faveolata bleached (Waddell and Clarke, 2008). faveolata embryos to temperatures of have been linked to elevated Surveys from 2005 to 2007 along the 27.5, 29, and 31.5 degrees C directly temperature as they have occurred after Florida reef tract from Martin County to after fertilization and measured bleaching events. We conclude that O. the lower Florida Keys indicated that O. differences in gene expression after 12 faveolata is highly susceptible to faveolata had the 13th highest bleaching and 48 hours. They found a higher elevated temperature. prevalence out of 30 species observed to number of misshapen embryos after 12 The SRR and SIR provided the bleach (Wagner et al., 2010). During a hours at 29 and 31.5 degrees C in following information on O. faveolata’s 2009 bleaching event on Little Cayman, comparison to embryos kept at 27.5 susceptibility to acidification. A field of the ten coral species that bleached, O. degrees C. However, after 48 hours, the study did not find any change in O. faveolata had the third highest proportion of misshapen embryos faveolata’s calcification in field-

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sampled colonies from the Florida Keys disease at 4.7 to 10.4 percent across fecundity compared to un-diseased up through 1996. geographic locations (Weil et al., 2002). controls (Weil et al., 2009). The public comments did not provide Surveys at five sites along the west All sources of information are used to new or supplemental information on the coast of Dominica between 2000 and describe O. faveolata’s susceptibility to susceptibility of O. faveolata to 2002 revealed that O. faveolata was one disease as follows. Orbicella faveolata is acidification. Supplemental information of the species most susceptible to often among the coral species with the we found on the susceptibility of O. disease. Of the 12 species infected by highest disease prevalence and tissue faveolata to acidification includes the white plague in 2000, O. faveolata loss. Outbreaks have been reported to following. In laboratory experiments, ranked second highest in disease affect ten to 19 percent of O. faveolata reproduction of O. faveolata was prevalence (18.4 percent of infected colonies, and yellow band disease and negatively impacted by increasing CO2, colonies were O. faveolata); it ranked white plague have the greatest effect. and impairment of fertilization was third in 2001 out of 14 species (12.7 Disease often affects larger colonies, and exacerbated at lower sperm percent) and second in 2002 out of 13 reported tissue loss due to disease concentrations (Albright, 2011b). species (18.8 percent). In addition, ranges from five to 90 percent. Fertilization success was reduced by 25 white plague infected the larger size Additionally, yellow band disease percent at 529 matm (43 percent classes of O. faveolata. Although only results in lower fecundity in diseased fertilization) and 40 percent at 712 matm one colony experienced total colony and recovered colonies of O. faveolata. (34 percent fertilization) compared to mortality, O. faveolata had the highest Therefore, we conclude that O. controls at 435 matm (57 percent amount of tissue loss in each year and faveolata is highly susceptible to fertilization; Albright, 2011a). in the three years combined (Borger and disease. Additionally, growth rate of O. faveolata Steiner, 2005). The SIR and SRR did not provide any was reduced under lower pH conditions Yellow band disease in O. faveolata species-specific information on the (7.6) compared to higher pH conditions increased in abundance between 1999 trophic effects of fishing on O. (8.1) after 120 days of exposure (Hall et and 2004 on reefs near La Parguera and faveolata. The public comments did not Desecheo and Mona Islands, Puerto Rico al., 2012). provide new or supplemental (Waddell, 2005). Yellow band disease information, and we did not find All sources of information are used to mean lesion growth rates on O. supplemental information on the describe O. faveolata’s susceptibility to faveolata in La Parguera, Puerto Rico trophic effects of fishing on O. acidification as follows. Laboratory had a significant positive correlation faveolata. However, due to the level of studies indicate that O. faveolata is with mean yearly surface water reef fishing conducted in the Caribbean, susceptible to ocean acidification both temperatures between 1998 and 2010 coupled with Diadema die-off and lack through reduced fertilization of gametes (Burge et al., 2014). In Curacao colonies of significant recovery, competition and reduced growth of colonies. Thus, of O. faveolata infected with yellow with algae can adversely affect coral we conclude that O. faveolata is highly band disease lost 90 percent of their recruitment. Thus, O. faveolata likely susceptible to ocean acidification. tissue between 1997 and 2005 (Bruckner has some susceptibility to the trophic The SRR and SIR did not provide any and Bruckner, 2006a). Only the effects of fishing given its low species-specific information on the unaffected parts of colonies continued recruitment rates. However, the susceptibility of O. faveolata to disease. to grow, and only the smallest lesions available information does not support The public comments also did not caused by disease healed (Bruckner and a more precise description of provide new or supplemental Bruckner, 2006a). Partial mortality was susceptibility to this threat. information on the susceptibility of O. higher in 2005 (average of 40 percent) The SRR and SIR did not provide faveolata to disease. Supplemental than in 1998 (Bruckner and Bruckner, species-specific information on the information we found on the 2006a). Outbreaks of white plague susceptibility of O. faveolata to susceptibility of O. faveolata to disease occurred in 2001 and 2005 and infected sedimentation, and the public confirms the information on the O. faveolata and O. annularis with the comments did not provide new or Orbicella species complex and includes highest frequency (Bruckner and supplemental information on its the following. Disease affected corals in Bruckner, 2006a). susceptibility to this threat. Puerto Rico after the 2005 bleaching Yellow band disease significantly Supplemental information we found event, and O. faveolata was the species affects O. faveolata reproductive output. confirms the information on the most affected (Bruckner and Hill, 2009). Fecundity of diseased lesions was susceptibility of the Orbicella species A 1998 outbreak of white plague on significantly lower than transition and complex to sedimentation and includes three surveyed reefs in St. Lucia affected healthy-looking tissues on diseased the following. In St. Lucia, rates of 19 percent of O. faveolata colonies, and colonies. Diseased lesions had 99 partial mortality of O. annularis and O. O. faveolata was the species most percent fewer eggs compared to un- faveolata were higher close to river affected (Nugues, 2002). Larger colonies diseased control colonies. Fecundity in mouths where sediments were in St. Lucia were more likely to get transition areas was 24 percent less than deposited than they were farther from infected, but they were less likely to healthy-looking areas of diseased the river mouths, indicating the suffer complete mortality (Nugues, colonies and was significantly lower (50 sensitivity of these two species to 2002). Tissue mortality of marked O. percent) than in un-diseased control sedimentation (Nugues and Roberts, faveolata colonies was 51 percent, and colonies. Healthy-looking tissues of 2003). no colonies showed regrowth during the diseased colonies had 27 percent lower All sources of information are used to 8 month study period (Nugues, 2002). fecundity compared to un-diseased describe O. faveolata’s susceptibility to Disease surveys conducted between control colonies. Furthermore, in sedimentation as follows. August and December 1999 at 19 reef colonies that had recovered from Sedimentation can cause partial sites from six geographic areas across disease, small tissue remnants (less than mortality of O. faveolata, and genus- the wider Caribbean (Bermuda, Puerto 100 cm2) had 84 percent lower level information indicates that Rico, Bonaire, Venezuela, Colombia, fecundity compared to un-diseased sedimentation negatively affects and Jamaica) revealed that O. faveolata controls, and large tissue remnants (400 primary production, growth rates, showed the second highest incidence of to 1000 cm2) had 64 percent lower calcification, colony size, and

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abundance. Therefore, we conclude that available information does not support limited in scope), coral collection (50 O. faveolata is highly susceptible to a more precise description of percent with 27 percent limited in sedimentation. susceptibility to this threat. scope), pollution control (31 percent The SRR, SIR, and public comments The SRR and SIR did not provide with 15 percent limited in scope), did not provide information on the species-specific information on the fishing regulations on reefs (73 percent susceptibility of O. faveolata to nutrient susceptibility of O. faveolata to with 50 percent limited in scope), enrichment, and we did not find any collection and trade, and the public managing areas for protection and new or supplemental information on the comments did not provide new or conservation (88 percent with 31 susceptibility of O. faveolata to nutrient supplemental information on its percent limited in scope). The most enrichment. susceptibility to this threat. common regulatory mechanisms in All sources of information are used to Supplemental information we found place for O. faveolata are reef fishing describe O. faveolata’s susceptibility to confirms the information in the SRR and regulations and area management for nutrient enrichment as follows. SIR that collection and trade is not a protection and conservation. However, Although there is no species-specific significant threat for the Orbicella half of the reef fishing regulations are information, the Orbicella species species complex. Over the last decade, limited in scope and may not provide complex is susceptible to nutrient collection and trade of this species has substantial protection for the species. enrichment through reduced growth been primarily for scientific research General coral protection and collection rates, lowered recruitment, and rather than commercial purposes. Gross laws, along with pollution control laws, increased disease severity. Therefore, exports for collection and trade of O. are much less common regulatory based on genus-level information, we faveolata between 2000 and 2012 mechanisms for the management of O. conclude that O. faveolata is likely averaged 271 specimens (data available faveolata. highly susceptible to nutrient at http://trade.cites.org). We conclude enrichment. that O. faveolata has low susceptibility Vulnerability to Extinction The SRR and SIR provided the to collection and trade. As explained above in the Risk following information on the Analyses section, a species’ susceptibility of O. faveolata to Regulatory Mechanisms vulnerability to extinction results from predation. Under laboratory conditions, In the proposed rule, we relied on the combination of its spatial and black band disease was transmitted to information from the Final Management demographic traits, threat healthy O. faveolata fragments in the Report for evaluating the existing susceptibilities, and consideration of the presence of the butterflyfish Chaetodon regulatory mechanisms for controlling baseline environment and future capistratus but not in aquaria without threats to all corals. However, we did projections of threats. The SRR stated the fish present, suggesting that the fish not provide any species-specific that the factors that increase the acts as a disease vector (Aeby and information on the regulatory extinction risk for O. faveolata are its Santavy, 2006). mechanism or conservation efforts for extremely low productivity (growth and The public comments did not provide O. faveolata. Public comments were recruitment), documented dramatic new or supplemental information on the critical of that approach, and we recent declines, and its restriction to the susceptibility of O. faveolata to therefore attempt to analyze regulatory highly disturbed/degraded wider predation. Supplemental information mechanisms and conservation efforts on Caribbean region. we found on the susceptibility of O. a species basis, where possible, in this Subsequent to the proposed rule, we faveolata to predation includes the final rule. Records confirm that O. received and gathered supplemental following. In surveys of the Florida Keys faveolata occurs in five Atlantic species- or genus-specific information, in 2012, two percent of O. faveolata ecoregions, and studies and described above, that expands our colonies were affected by predation by observations have confirmed the knowledge regarding the species’ the corallivorous snail C. abbreviata presence of O. faveolata in an additional abundance, distribution, and threat (Miller et al., 2013). Parrotfish consume three ecoregions (Burman et al., 2012). susceptibilities. We developed our O. annularis and O. faveolata more These eight ecoregions encompass 26 assessment of the species’ vulnerability intensively than other coral species, but kingdom’s and countries’ EEZs. The 26 to extinction using all the available tissue regeneration capabilities appear kingdoms and countries are Antigua & information. As explained in the Risk to be high enough to counterbalance Barbuda, Bahamas, Barbados, Belize, Analyses section, our assessment in this loss from predation (Mumby, 2009). Colombia, Costa Rica, Cuba, Dominica, final rule emphasizes the ability of the All sources of information are used to Dominican Republic, French Antilles, species’ spatial and demographic traits describe O. faveolata’s susceptibility to Grenada, Guatemala, Haiti, Kingdom of to moderate or exacerbate its predation as follows. Orbicella faveolata the Netherlands, Honduras, Jamaica, vulnerability to extinction, as opposed is affected by a number of predators, but Mexico, Nicaragua, Panama, St. Kitts & to the approach we used in the losses appear to be minimal. We Nevis, St. Lucia, St. Vincent & proposed rule, which emphasized the conclude that O. faveolata has low Grenadines, Trinidad and Tobago, species’ susceptibility to threats. susceptibility to predation. United Kingdom (British Caribbean The following characteristics of O. The SRR and SIR did not provide Territories and possibly Bermuda), faveolata, in conjunction with the information on the effects of sea level United States (including U.S. Caribbean information described in the Corals and rise on O. faveolata. The SRR described Territories), and Venezuela. The Coral Reefs section, Coral Habitat sub- sea level rise as an overall low to regulatory mechanisms relevant to O. section, and Threats Evaluation section medium threat for all coral species. The faveolata, described first as a percentage above, affect its vulnerability to public comments did not provide new of the above kingdoms and countries extinction currently and over the or supplemental information on O. that utilize them to any degree, and foreseeable future. The species has faveolata’s susceptibility to sea level second as the percentages of those undergone major declines mostly due to rise, and we did not find any new or kingdoms and countries whose warming-induced bleaching and supplemental information. Thus, we regulatory mechanisms may be limited disease. There is evidence of synergistic conclude that O. faveolata has some in scope, are as follows: General coral effects of threats for this species susceptibility to sea level rise, but the protection (31 percent with 12 percent including disease outbreaks following

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bleaching events and reduced thermal or do not negatively respond to a threat Additionally, shifts to smaller size tolerance due to chronic local stressors at any given point in time. classes via fission and partial mortality of older, larger colonies, have reduced stemming from land-based sources of Listing Determination pollution. Orbicella faveolata is highly the buffering capacity of O. faveolata’s susceptible to a number of threats, and In the proposed rule, using the life history strategy. cumulative effects of multiple threats determination tool formula approach, O. The combination of these have likely contributed to its decline faveolata was proposed for listing as characteristics and future projections of and exacerbate vulnerability to endangered because of: High threats indicates that the species is extinction. Despite high declines, the vulnerability to ocean warming (E), likely to be in danger of extinction disease (C), and ocean acidification (E); species is still common and remains one within the foreseeable future throughout high vulnerability to sedimentation (A of the most abundant species on its range, and warrants listing as and E) and nutrient over-enrichment (A Caribbean reefs. Its life history threatened at this time due to factors A, and E); decreasing trend in abundance C, D, and E. characteristics of large colony size and (E); low relative recruitment rate (E); The available information above on O. long life span have enabled it to remain moderate overall distribution (based on faveolata’s spatial structure, relatively persistent despite slow growth narrow geographic distribution and demography, threat susceptibilities, and and low recruitment rates, thus wide depth distribution) (E); restriction management also indicate that the moderating vulnerability to extinction. to the Caribbean (E); and inadequacy of species is not currently in danger of However, the buffering capacity of these regulatory mechanisms (D). extinction and thus does not warrant life history characteristics is expected to In this final rule, we changed the listing as Endangered because: decrease as colonies shift to smaller size listing determination for O. faveolata (1) While Orbicella faveolata’s classes as has been observed in from endangered to threatened. We distribution within the Caribbean locations in its range. Its absolute made this determination based on a increases its risk of exposure to threats population abundance has been more species-specific and holistic as described above, its known depth estimated as at least tens of millions of approach, including consideration of distribution is between 0.5 and 45 m, colonies in each of several locations the buffering capacity of this species’ with occurrence by the complex as deep including the Florida Keys, Dry spatial and demographic traits, and the as 90 m, and its habitat includes various Tortugas, and the U.S. Virgin Islands best available information above on O. shallow and mesophotic reef and is higher than the estimate from faveolata’s spatial structure, environments. This moderates these three locations due to the demography, threat susceptibilities, and vulnerability to extinction currently occurrence of the species in many other management. This combination of because the species is not limited to one areas throughout its range. Despite the factors indicates that O. faveolata is habitat type but occurs in numerous large number of islands and likely to become endangered throughout types of reef environments that will environments that are included in the its range within the foreseeable future, experience highly variable thermal species’ range, geographic distribution and thus warrants listing as threatened regimes and ocean chemistry on local in the highly disturbed Caribbean at this time, because: and regional scales at any given point in exacerbates vulnerability to extinction (1) Orbicella faveolata is highly time, as described in more detail in the over the foreseeable future because O. susceptible to ocean warming (ESA Coral Habitat and Threats Evaluation faveolata is limited to an area with high, Factor E), disease (C), ocean sections. There is no evidence to suggest localized human impacts and predicted acidification (E), sedimentation (A, E), that the species is so spatially increasing threats. Its depth range of 0.5 and nutrients (A, E) and susceptible to fragmented that depensatory processes, to at least 40 m, possibly up to 90 m, trophic effects of fishing (A). These environmental stochasticity, or the potential for catastrophic events moderates vulnerability to extinction threats are expected to continue and currently pose a high risk to the survival over the foreseeable future because increase into the future. In addition, the species is at heightened extinction risk of the species; and deeper areas of its range will usually (2) Although O. faveolata’s abundance have lower temperatures than surface due to inadequate existing regulatory mechanisms to address global threats has declined, it still has a common waters, and acidification is generally (D); occurrence and remains one of the most predicted to accelerate most in waters (2) Orbicella faveolata is dominant corals in the Caribbean. Its that are deeper and cooler than those in geographically located in the highly absolute abundance is at least tens of which the species occurs. Orbicella disturbed Caribbean where localized millions of colonies based on estimates faveolata occurs in most reef habitats, human impacts are high and threats are from three locations. Absolute including both shallow and mesophotic predicted to increase as described in the abundance is higher than estimates from reefs, which moderates vulnerability to Threats Evaluation section. A range these locations since it occurs in many extinction over the foreseeable future constrained to this particular geographic other locations throughout its range. because the species occurs in numerous area that is likely to experience severe This absolute abundance allows for types of reef environments that are and increasing threats indicates that a variation in the responses of individuals predicted, on local and regional scales, high proportion of the population of this to threats to play a role in moderating to experience highly variable thermal species is likely to be exposed to those vulnerability to extinction for the regimes and ocean chemistry at any threats over the foreseeable future; species to some degree, as described in given point in time. Its abundance, life (3) Orbicella faveolata has more detail in the Corals and Coral history characteristics, and depth experienced substantial declines in Reefs section. There is no evidence of distribution, combined with spatial abundance and percent cover over the depensatory processes such as variability in ocean warming and past two decades; and reproductive failure from low density of acidification across the species’ range, (4) Orbicella faveolata’s slow growth reproductive individuals and genetic moderate vulnerability to extinction rate and low sexual recruitment limit its processes such as inbreeding affecting because the threats are non-uniform, capacity for recovery from threat- this species. Thus, its absolute and there will likely be a large number induced mortality events throughout its abundance indicates it is currently able of colonies that are either not exposed range over the foreseeable future. to avoid high mortality from

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environmental stochasticity, and supplemental information on O. cm. Partial colony mortality ranged from mortality of a high proportion of its franksi’s habitat or depth range. approximately ten to 55 percent. Two population from catastrophic events. Supplemental information we found on years later in 2008 no size class was The combination of these O. franksi’s distribution includes the found to dominate, and proportion of characteristics indicates that the species following. Veron (2014) confirmed the colonies in the medium to large size does not exhibit the characteristics of occurrence of O. franksi in six out of his classes (60 to 90 cm) appeared to be less one that is currently in danger of 11 ecoregions in the western Atlantic than in 2006. The number of colonies in extinction, as described previously in and greater Caribbean known to contain the largest size class of greater than 90 the Risk Analyses section, and thus does corals and strongly predicted its cm remained consistent. Partial colony not warrant listing as endangered at this presence in an additional three mortality ranged from approximately 15 time. ecoregions (off Colombia/Venezuela, to 75 percent (Miller et al., 2013). Range-wide, multitudes of Cuba/Cayman Islands, and Jamaica). Supplemental information we found conservation efforts are already broadly Other studies confirm the presence of O. on O. franksi’s abundance and employed that are likely benefiting O. franksi in three other ecoregions population trends includes the faveolata. However, considering the (Alcolado et al., 2010; Bayraktarov et al., following. In a 1995 survey of 16 reefs global scale of the most important 2012; Bruckner, 2012c; Weil et al., in the Florida Keys, O. franksi has the threats to the species, and the 2002). The two ecoregions where O. highest percent cover of all species ineffectiveness of conservation efforts at franksi has not been found are off the (Murdoch and Aronson, 1999). In a addressing the root cause of global coasts of Brazil and the southeastern survey of 31 sites in Dominica between threats (i.e., GHG emissions), we do not U.S. north of southern Florida (Veron, 1999 and 2002, O. franksi was present believe that any current conservation 2014). in seven percent of the sites at less than one percent cover (Steiner, 2003). In efforts or conservation efforts planned Demographic Information in the future will result in affecting the 2003 on the east Flower Garden Bank, species’ status to the point at which The SRR and SIR provided the O. franksi comprised 46 percent of the listing is not warranted. following information on O. franksi’s 76.5 percent coral cover on reefs 32 to abundance and population trends. 40 m in depth, and partial coral Orbicella franksi Orbicella franksi is reported as mortality due to bleaching, disease, and Introduction common. predation was rare in survey stations The public comments provided the (Precht et al., 2005). The SRR and SIR provided the following supplemental information on Reported density is variable by following information on O. franksi’s O. franksi’s abundance and population location and habitat and is reported to morphology. Orbicella franksi is trends. In surveys throughout the range from 0.02 to 1.05 colonies per 10 distinguished by large, unevenly Florida Keys, O. franksi in 2005 ranked m2. In surveys of 1,176 sites in arrayed polyps that give the colony its 26th most abundant out of 47 coral southeast Florida, the Dry Tortugas, and characteristic irregular surface. Colony species, 32nd out of 43 in 2009, and the Florida Keys between 2005 and form is variable, and the skeleton is 33rd out of 40 in 2012. Extrapolated 2010, density of O. franksi ranged dense with poorly developed annual population estimates from stratified between 0.04 and 0.47 colonies per 10 bands. Colony diameter can reach up to random surveys were 8.0 ± 3.5 million m2 and was highest on the offshore 5 m with a height of up to 2 m. The (SE) colonies in 2005, 0.3 ± 0.2 million patch reef and fore-reef habitats public comments did not provide new (SE) colonies in 2009, and 0.4 ± 0.4 (Burman et al., 2012). In south Florida, or supplemental information on O. million (SE) colonies in 2012. The density was highest in areas south of franksi’s morphology, and we did not authors note that differences in Miami at 0.44 colonies per 10 m2 find any new or supplemental extrapolated abundance between years compared to 0.02 colonies per 10 m2 in information. were more likely a function of sampling Palm Beach and Broward Counties effort rather than an indication of Spatial Information (Burman et al., 2012). Along the Florida population trends. In 2005, the greatest reef tract from Martin County to the The SRR and SIR provided the proportions of colonies were in the lower Florida Keys, density of O. franksi following information on O. franksi’s smaller size classes of 10 to 20 cm and was approximately 0.9 colonies per 10 distribution, habitat, and depth range. 20 to 30 cm. Partial colony mortality m2 (Wagner et al., 2010). On remote Orbicella franksi is distributed in the ranged from zero to approximately 73 reefs off southwest Cuba, colony density western Atlantic and throughout the percent and was generally higher in was 0.083 ± 0.17 (SD) per 10 m transect Caribbean Sea including in the larger colonies (Miller et al., 2013). on 38 reef-crest sites and 1.05 ± 1.02 Bahamas, Bermuda, and the Flower In the Dry Tortugas, Florida, O. colonies per 10 m transect on 30 reef- Garden Banks. Orbicella franksi tends to franksi ranked fourth highest in front sites (Alcolado et al., 2010). The have a deeper distribution than the abundance out of 43 coral species in number of O. franksi colonies in Cuba other two species in the Orbicella 2006 and eighth out of 40 in 2008. with partial colony mortality were far species complex. Extrapolated population estimates were more frequent than those with no It occupies most reef environments 79 ± 19 million (SE) colonies in 2006 mortality across all size classes, except and has been reported from water and 18.2 ± 4.1 million (SE) colonies in for one (i.e., less than 50 cm) that had depths ranging from 5 to 50 m, with the 2008. The authors note the difference in similar frequency of colonies with and species complex reported to 90 m. estimates between years was more likely without partial mortality (Alcolado et Orbicella species are a common, often a function of sampling effort rather than al., 2010). dominant, component of Caribbean population decline. In the first year of In the U.S. Virgin Islands, O. franksi mesophotic reefs, suggesting the the study (i.e., 2006), the greatest is the second most abundant species by potential for deep refugia for O. franksi. proportion of colonies were in the size percent cover at permanent monitoring The public comments did not provide class 20 to 30 cm with twice as many stations. However, because the species new or supplemental information on O. colonies as the next most numerous size complex, which is the most abundant by franksi’s distribution, habitat, or depth class, and a fair number of colonies in cover, was included as a category when range. We did not find new or the largest size class of greater than 90 individual Orbicella species could not

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be identified with certainty, it is likely to smaller colony size across five mortality during summer surveys that O. franksi is the most abundant. countries, suggest that population between 2005 and 2009. Population estimates of O. franksi in the decline has occurred in some areas; The public comments did not provide 49 km2 Red Hind Marine Conservation colony abundance appears to be stable new or supplemental biological District are at least 34 million colonies in other areas. We conclude that while information on O. franksi. (Smith, 2013). population decline has occurred, O. Supplemental biological information we Abundance in Curacao and Puerto franksi is still common with the number found on O. franksi includes the Rico and appears to be stable over an of colonies at least in the tens of following. Of 351 O. franksi colonies eight to ten year period. In Curacao, millions. Additionally, as discussed in observed to spawn at a site off Bocas del abundance was stable between 1997 and the genus section, we conclude that the Toro, Panama, 324 were unique 2005, with partial mortality similar or buffering capacity of O. franksi’s life genotypes. Over 90 percent of O. franksi less in 2005 compared to 1998 history strategy that has allowed it to corals on this reef were the product of (Bruckner and Bruckner, 2006a). remain abundant has been reduced by sexual reproduction, and 19 genetic Abundance was also stable between the recent population declines and individuals had asexually propagated 1998–2008 at nine sites off Mona and amounts of partial mortality, colonies made up of two to four Desecheo Islands, Puerto Rico. In 1998, particularly in large colonies. spatially adjacent ramets each. 4 percent of all corals at six sites Individuals within a genotype spawned surveyed off Mona Island were O. Other Biological Information more synchronously than individuals of franksi colonies in 1998 and The SRR and SIR provided the different genotypes. Additionally, approximately five percent in 2008; at following information on O. franksi’s within 5m, colonies nearby spawned Desecheo Island, about two percent of life history. The growth rate for O. more synchronously than farther spaced all coral colonies were O. franksi in both franksi is reported to be slower, and colonies, regardless of genotype. At 2000 and 2008 (Bruckner and Hill, spawning is reported to be about one to distances greater than 5m, spawning 2009). two hours earlier than O. annularis and was random between colonies (Levitan On the other hand, colony size has O. faveolata. et al., 2011). decreased over the past several decades. The public comments did not provide In a study of symbiont composition of A survey of 185 sites (2010 and 2011) new or supplemental information on O. repeatedly sampled colonies of six in five countries (Bahamas, Bonaire, franksi’s life history. Supplemental species in the Bahamas and the Florida Cayman Islands, Puerto Rico, and St. information we found on O. franksi’s Keys (1998, and 2000 to 2004), major Kitts and Nevis) reported the size of O. life history includes the following. Of changes in symbiont dominance over franksi and O. annularis colonies as 361 colonies of O. franksi tagged in time were observed at certain Florida significantly smaller than O. faveolata. Bocas del Toro, Panama, larger colonies Keys reefs in O. annularis and O. The total mean partial mortality of O. were noted to spawn more frequently franksi. Some colonies of O. annularis franksi was 25 percent. Overall, the total than smaller colonies between 2002 and and O. franksi exhibited shifts in their live area occupied by O. franksi 2009 (Levitan et al., 2011). Darling et al. associations attributed to recovery from declined by a mean of 38 percent, and (2012) performed a biological trait-based the stresses of the 1997–98 bleaching mean colony size declined from 1356 analysis to categorize coral species into event. Most transitions in symbiont cm2 to 845 cm2. At the same time there four life history strategies: Generalist, identity ended in 2002, three to five was a 137 percent increase in small weedy, competitive, and stress-tolerant. years after the 1997–98 bleaching event tissue remnants less than 500 cm2, along The classifications were primarily (Thornhill et al., 2006). with a decline in the proportion of large separated by colony morphology, Susceptibility to Threats (1,500 to 30,000 cm2), completely alive growth rate, and reproductive mode. colonies. Mortality was attributed Orbicella franksi was classified as a The threat susceptibility information primarily to outbreaks of white plague ‘‘generalist’’ species, thus likely less from the SRR and SIR was interpreted and yellow band disease, which vulnerable to environmental stress. in the proposed rule for O. franksi’s emerged as corals began recovering from The SRR and SIR provided the vulnerability to threats as follows: High mass bleaching events. This was following other biological information vulnerability to ocean warming, disease, followed by increased predation and on O. franksi. Low tissue biomass can acidification, sedimentation, and removal of live tissue by damselfish to render specific colonies of O. franksi nutrient enrichment; moderate cultivate algal lawns (Bruckner, 2012a). susceptible to mortality from stress vulnerability to the trophic effects of All information on O. franksi’s events, such as bleaching or disease. fishing; and low vulnerability to sea abundance and population trends can This suggests that differential mortality level rise, predation, and collection and be summarized as follows. Based on among individuals, species, and reefs trade. population estimates, there are at least from stress events such as bleaching or The SRR and SIR did not provide tens of millions of colonies present in disease may be at least partially a species-specific information on the both the Dry Tortugas and U.S. Virgin function of differential colony biomass susceptibility of O. franksi to ocean Islands. Absolute abundance is higher (indicating overall coral health) as warming. The public comments did not than the estimate from these two opposed to genetic or physiologic provide new or supplemental locations given the presence of this differences among corals or their information on the susceptibility of O. species in many other locations symbionts. franksi to ocean warming. Supplemental throughout its range. The frequency and In a 2010 cold-water event that information we found on the extent of partial mortality, especially in affected south Florida, O. franksi ranked susceptibility of O. franksi to ocean larger colonies of O. franksi, appear to as the 14th most susceptible coral warming includes the following. A high be high in some locations such as species out of 25 of the most abundant percentage of O. franksi colonies Florida and Cuba, though other coral species. Average partial mortality experience bleaching during warm locations like the Flower Garden Banks was eight percent in surveys from water temperature anomalies. Stratified appear to have lower amounts of partial Martin County to the lower Florida Keys random surveys on back-reefs and fore- mortality. A decrease in O. franksi after the 2010 cold-water event reefs between one and 30 m depth off percent cover by 38 percent, and a shift compared to 0.4 percent average Puerto Rico (Mona and Desecho Islands,

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La Parguera, Mayaguez, Boqueron, and Bonaire, Venezuela, Colombia, and franksi to nutrient enrichment includes Rincon) in 2005 and 2006 revealed Jamaica) revealed that O. franksi had the the following. Field experiments severe bleaching in O. franksi with third highest incidence of disease at 1.1 indicate that nutrient enrichment approximately 90 percent of colonies to 5.6 percent across geographic significantly increases yellow band bleached (Waddell and Clarke, 2008). locations (Weil et al., 2002). Between disease severity in O. annularis and O. Surveys from 2005 to 2007 along the 1998 and 2000, O. franksi was one of six franksi through increased tissue loss Florida reef tract from Martin County to coral species identified in the Virgin (Bruno et al., 2003). the lower Florida Keys indicated O. Islands as most susceptible to disease All sources of information are used to franksi had the tenth highest bleaching (Waddell, 2005). In 2004 in Mexico, describe O. franksi’s susceptibility to prevalence out of 30 species observed to disease prevalence was highest in O. nutrient enrichment as follows. Genus bleach (Wagner et al., 2010). During a franksi with 41 percent of colonies level information indicates O. franksi is moderate bleaching event in Colombia infected, followed by 34 percent of O. likely susceptible to nutrient in 2010, 88 percent of O. franksi annularis colonies and 31 percent of O. enrichment through reduced growth bleached, and 12 percent paled at a site faveolata colonies (Ward et al., 2006). In rates and lower recruitment. in Gayraca Bay (Bayraktarov et al., Curacao colonies of O. franksi infected Additionally, nutrient enrichment has 2012). In 2011, 75 percent of O. franksi with yellow band disease lost an been shown to increase the severity of were dead and completely overgrown by average of 30 percent of their tissue yellow band disease in O. franksi. Thus, algae (Bayraktarov et al., 2012). Based between 1997 and 2005, but some we conclude that O. franksi is highly on samples of O. franksi and O. tagged colonies exhibited re-sheeting susceptible to nutrient enrichment. faveolata collected from the over disease lesions (Bruckner and The SRR and SIR do not provide Mesoamerican Barrier Reef, calcification Bruckner, 2006a). species-specific information on the of these two species is projected to cease All sources of information are used to susceptibility of O. franksi to predation. at 35 degrees C in this location in the describe O. franksi’s susceptibility to Likewise, the public comments do not absence of acidification (Carricart- disease as follows. Orbicella franksi is provide new or supplemental Ganivet et al., 2012). often reported as among the species information on the susceptibility of O. All sources of information are used to with the highest disease prevalence. franksi to predation. Supplemental describe O. franksi’s susceptibility to Although there are few quantitative information we found on the ocean warming as follows. Available studies of the effects of disease on O. susceptibility of O. franksi to predation information indicates that O. franksi is franksi, there is evidence that partial includes the following. Incidence of highly susceptible to warming mortality can average about 25 to 30 parrotfish grazing on the Belize barrier temperatures with a reported 88 to 90 percent and that disease can cause shifts reef was second highest on O. franksi. percent bleaching frequency. Reported to smaller size classes. Thus, we However, in most habitats, the majority bleaching-related mortality from one conclude that O. franksi is highly of Orbicella spp. showed little or no study is high at 75 percent. There is susceptible to disease. parrotfish grazing while only a few indication that symbiont shuffling after The SIR and SRR did not provide any colonies were more heavily grazed, bleaching in O. franksi. We conclude species-specific information on the indicating low impact to the species that O. franksi is highly susceptible to trophic effects of fishing on O. franksi. overall (Rotjan, 2007). ocean warming. The public comments did not provide All sources of information are used to The SRR and SIR did not provide any new or supplemental information, and describe O. franksi’s susceptibility to species-specific information on the we did not find new or supplemental predation as follows. Genus-level susceptibility of O. franksi to information on the trophic effects of information indicates O. franksi is acidification, and the public comments fishing on O. franksi. However, due to affected by a number of predators, but did not provide new or supplemental the level of reef fishing conducted in the both species-level and genus-level information on its susceptibility to this Caribbean, coupled with Diadema die- impacts appear to be minimal. We threat. We did not find any new or off and lack of significant recovery, conclude that O. franksi has low supplemental information on the competition with algae can adversely susceptibility to predation. susceptibility of O. franksi to affect coral recruitment. Thus, O. The SRR and SIR did not provide acidification. Although there is no franksi likely has some susceptibility to information on the effects of sea level species-specific information on the the trophic effects of fishing given its rise on O. franksi. The SRR described susceptibility of O. franksi to ocean low recruitment rates. sea level rise as an overall low to acidification, genus information The SRR, SIR, and public comments medium threat for all coral species. The indicates that the species complex has did not provide information on the public comments did not provide new reduced growth and fertilization success susceptibility of O. franksi to or supplemental information on O. under acidic conditions. Thus, we sedimentation, and we did not find any franksi’s susceptibility to sea level rise, conclude O. franksi likely has high new or supplemental information. All and we did not find any new or susceptibility to ocean acidification. sources of information are used to supplemental information. Thus, we The SRR and SIR did not provide any describe O. franksi’s susceptibility to conclude that O. franksi has some species-specific information on the sedimentation as follows. Genus susceptibility to sea level rise, but the susceptibility of O. franksi to disease. information indicates sedimentation available information does not support The public comments did not provide negatively affects primary production, a more precise description of new or supplemental information on the growth rates, calcification, colony size, susceptibility to this threat. susceptibility of O. franksi to disease. and abundance. Therefore, we conclude The SRR and SIR do not provide Supplemental information we found on that O. franksi is highly susceptible to species-specific information on the the susceptibility of O. franksi to sedimentation. susceptibility of O. franksi to collection disease includes the following. Disease The SRR, SIR, and public comments and trade, and the public comments do surveys conducted between August and do not provide information on the not provide new or supplemental December 1999 at 19 reef sites from six susceptibility of O. franksi to nutrient information on its susceptibility to this geographic areas across the wider enrichment. Supplemental information threat. Supplemental information we Caribbean (Bermuda, Puerto Rico, we found on the susceptibility of O. found confirms the information in the

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SRR and SIR that collection and trade is limited in scope and may not provide declines, the species is still common not a significant threat for the Orbicella substantial protection for the species. and remains one of the most abundant species complex. Over the last decade, General coral protection and collection species on Caribbean reefs. Its life collection and trade of O. franksi has laws, along with pollution control laws, history characteristics of large colony been primarily for scientific research are much less common regulatory size and long life span have enabled it rather than commercial purposes. mechanisms for the management of O. to remain relatively persistent despite Annual gross exports for collection and franksi. slow growth and low recruitment rates, trade of O. franksi between 2000 and thus moderating vulnerability to Vulnerability to Extinction 2012 averaged 40 specimens (data extinction. However, the buffering available at http://trade.cites.org). Thus, As explained above in the Risk capacity of these life history we conclude that O. franksi has low Analyses section, a species’ characteristics is expected to decrease as susceptibility to collection and trade. vulnerability to extinction results from colonies shift to smaller size classes as the combination of its spatial and has been observed in locations in its Regulatory Mechanisms demographic traits, threat range. Its absolute population In the proposed rule, we relied on susceptibilities, and consideration of the abundance has been estimated as at information from the Final Management baseline environment and future least tens of millions of colonies in both Report for evaluating the existing projections of threats. The SRR stated a portion of the U.S. Virgin Islands and regulatory mechanisms for controlling that the factors that increase the the Dry Tortugas and is higher than the threats to all corals. However, we did extinction risk for O. franksi are estimate from these two locations due to not provide any species-specific extremely low productivity (growth and the occurrence of the species in many information on the regulatory recruitment), documented dramatic other areas throughout its range. Despite mechanism or conservation efforts for recent declines, and its restriction to the the large number of islands and O. franksi. Public comments were highly disturbed and degraded wider environments that are included in the critical of that approach, and we Caribbean region. All of these factors species’ range, geographic distribution therefore attempt to analyze regulatory combined to yield a very high estimated in the highly disturbed Caribbean mechanisms and conservation efforts on extinction risk. It had a marginally exacerbates vulnerability to extinction a species basis, where possible, in this lower risk estimate than the other two over the foreseeable future because O. final rule. Records confirm that O. O. annularis complex species because of franksi is limited to an area with high, franksi occurs in six Atlantic greater distribution in deep and localized human impacts and predicted ecoregions, and studies have confirmed mesophotic depth habitats, which are increasing threats. Its depth range of five the presence of O. franksi in an expected to experience lesser exposure to at least 50 m, possibly up to 90 m, additional three ecoregions. These nine to some surface-based threats. moderates vulnerability to extinction ecoregions encompass 26 kingdoms’ and Subsequent to the proposed rule, we over the foreseeable future because countries’ EEZs, and the 26 kingdoms received and gathered supplemental deeper areas of its range will usually and countries are Antigua & Barbuda, species- or genus-specific information, have lower temperatures than surface Bahamas, Barbados, Belize, Colombia, described above, that expands our waters, and acidification is generally Costa Rica, Cuba, Dominica, Dominican knowledge regarding the species’ predicted to accelerate most in waters Republic, French Antilles, Grenada, abundance, distribution, and threat that are deeper and cooler than those in Guatemala, Haiti, Kingdom of the susceptibilities. We developed our which the species occurs. Orbicella Netherlands, Honduras, Jamaica, assessment of the species’ vulnerability franksi occurs in most reef habitats, Mexico, Nicaragua, Panama, St. Kitts & to extinction using all the available including both shallow and mesophotic Nevis, St. Lucia, St. Vincent & information. As explained in the Risk reefs, which moderates vulnerability to Grenadines, Trinidad and Tobago, Analyses section, our assessment in this extinction over the foreseeable future United Kingdom (British Caribbean final rule emphasizes the ability of the because the species occurs in numerous Territories and Bermuda), United States species’ spatial and demographic traits types of reef environments that are (including U.S. Caribbean Territories), to moderate or exacerbate its predicted, on local and regional scales, and Venezuela. The regulatory vulnerability to extinction, as opposed to experience highly variable thermal mechanisms relevant to O. franksi, to the approach we used in the regimes and ocean chemistry at any described first as a percentage of the proposed rule, which emphasized the given point in time. Its abundance, life above kingdoms and countries that species’ susceptibility to threats. history characteristics, and depth utilize them to any degree, and second The following characteristics of O. distribution, combined with spatial as the percentage of those kingdoms and franksi, in conjunction with the variability in ocean warming and countries whose regulatory mechanisms information described in the Corals and acidification across the species’ range, may be limited in scope, are as follows: Coral Reefs section, Coral Habitat sub- moderate vulnerability to extinction General coral protection (31 percent section, and Threats Evaluation section because the threats are non-uniform, with 12 percent limited in scope), coral above, affect its vulnerability to and there will likely be a large number collection (50 percent with 27 percent extinction currently and over the of colonies that are either not exposed limited in scope), pollution control (31 foreseeable future. The species has or do not negatively respond to a threat percent with 15 percent limited in undergone declines most likely from at any given point in time. scope), fishing regulations on reefs (73 disease and warming-induced percent with 50 percent limited in bleaching. There is evidence of Listing Determination scope), managing areas for protection synergistic effects of threats for this In the proposed rule, using the and conservation (88 percent with 31 species including increased disease determination tool formula approach, O. percent limited in scope). The most severity with nutrient enrichment. franksi was proposed for listing as common regulatory mechanisms in Orbicella franksi is highly susceptible to endangered because of: High place for O. franksi are reef fishing a number of threats, and cumulative vulnerability to ocean warming (E) regulations and area management for effects of multiple threats have likely disease (C), and ocean acidification (E); protection and conservation. However, contributed to its decline and exacerbate high vulnerability to sedimentation (A half of the reef fishing regulations are vulnerability to extinction. Despite and E) and nutrient over-enrichment (A

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and E); decreasing trend in abundance The available information above on O. not warrant listing as endangered at this (E); low relative recruitment rate (E); franksi spatial structure, demography, time. moderate overall distribution (based on threat susceptibilities, and management Range-wide, multitudes of narrow geographic distribution and also indicate that the species is not conservation efforts are already broadly wide depth distribution (E); restriction currently in danger of extinction and employed that are likely benefiting O. to the Caribbean (E); and inadequacy of thus does not warrant listing as franksi. However, considering the global regulatory mechanisms (D). Endangered because: scale of the most important threats to In this final rule, we changed the (1) While Orbicella franksi’s the species, and the ineffectiveness of listing determination for O. franksi from distribution within the Caribbean conservation efforts at addressing the endangered to threatened. We made this increases its risk of exposure to threats root cause of global threats (i.e., GHG determination based on a more species- as described above, its known depth emissions), we do not believe that any specific and holistic approach, distribution is between 5 and 50 m, with current conservation efforts or including consideration of the buffering occurrence by the species complex as conservation efforts planned in the capacity of this species’ spatial and deep as 90 m, and its habitat includes future will result in affecting the demographic traits, and the best various shallow and mesophotic reef species’ status to the point at which available information above on O. environments. This moderates listing is not warranted. franksi’s spatial structure, demography, vulnerability to extinction currently threat susceptibilities, and management. because the species is not limited to one Orbicella annularis This combination of factors indicates habitat type but occurs in numerous Introduction that O. franksi is likely to become types of reef environments that will endangered throughout its range within experience highly variable thermal The SRR and SIR provided the the foreseeable future, and thus regimes and ocean chemistry on local following information on O. annularis’ warrants listing as threatened at this and regional scales at any given point in morphology. Orbicella annularis time, because: time, as described in more detail in the colonies grow in columns that exhibit (1) Orbicella franksi is highly Coral Habitat and Threats Evaluation rapid and regular upward growth. In susceptible to ocean warming (ESA sections. There is no evidence to suggest contrast to the other two Orbicella Factor E), disease (C), nutrients (A, E), that the species is so spatially species, margins on the sides of ocean acidification (E), and fragmented that depensatory processes, columns are typically dead. Live colony sedimentation (A, E) and susceptible to environmental stochasticity, or the surfaces usually lack ridges or bumps. trophic effects of fishing (A). These potential for catastrophic events The public comments did not provide threats are expected to continue and currently pose a high risk to the survival new or supplemental information on O. increase into the future. In addition, the of the species; annularis’ morphology, and we did not species is at heightened extinction risk (2) Although O. franksi has declined find any new or supplemental due to inadequate existing regulatory in percent cover and colony size, there information. mechanisms to address global threats is evidence that population abundance Spatial Information (D); has remained stable in some locations (2) Orbicella franksi is geographically over a decadal time scale; and The SRR and SIR provided the located in the highly disturbed (3) Orbicella franksi has a common following information on the Caribbean where localized human occurrence and remains one of the most distribution, habitat and depth range of impacts are high and threats are dominant corals in the Caribbean. It has O. annularis. Orbicella annularis is predicted to increase as described in the an absolute abundance of at least tens of common throughout the western Threats Evaluation section. A range millions of colonies based on estimates Atlantic and greater Caribbean constrained to this particular geographic from two locations. Absolute abundance including the Flower Garden Banks but area that is likely to experience severe is higher than estimates from these may be absent from Bermuda. Two and increasing threats indicates that a locations since it occurs in many other personal communications were cited: high proportion of the population of this locations throughout its range. This one confirming its rarity in Bermuda, species is likely to be exposed to those absolute abundance allows for variation and the other stating O. annularis had threats over the foreseeable future; in the responses of individuals to not been seen in Bermuda. Orbicella (3) Orbicella franksi has experienced threats to play a role in moderating annularis is reported from most reef a decline in benthic cover over the past vulnerability to extinction for the environments in depths of 0.5 to 20 m. two decades; and species to some degree, as described in The Orbicella species complex is a (4) Orbicella franksi’s slow growth more detail in the Corals and Coral common, often dominant component of rate and low sexual recruitment limits Reefs section. There is no evidence of Caribbean mesophotic reefs, suggesting its capacity for recovery from threat- depensatory processes such as the potential for deep refugia across a induced mortality events throughout its reproductive failure from low density of broader depth range, but O. annularis is range over the foreseeable future. reproductive individuals and genetic generally described with a shallower Additionally, shifts to smaller size processes such as inbreeding affecting distribution. classes via fission and partial mortality this species. Thus, its absolute The public comments did not provide of older, larger colonies, have reduced abundance indicates it is currently able new or supplemental information on O. the buffering capacity of O. franksi’s life to avoid high mortality from annularis’ distribution, habitat, or depth history strategy. environmental stochasticity, and range. Supplemental information we The combination of these mortality of a high proportion of its found includes the following. Veron characteristics and future projections of population from catastrophic events. (2014) confirmed the occurrence of O. threats indicates that the species is The combination of these annularis in nine out of his 11 likely to be in danger of extinction characteristics indicates that the species ecoregions in the western Atlantic and within the foreseeable future throughout does not exhibit the characteristics of greater Caribbean known to contain its range, and warrants listing as one that is currently in danger of corals, but indicated one of these threatened at this time due to factors A, extinction, as described previously in ecoregions (Bermuda) has published C, D, and E. the Risk Analyses section and thus does records of occurrence that need further

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investigation. Locke (2013) indicated 20 percent of the sites at one to ten 10 years of monitoring between 1995 early records of O. annularis in percent cover (Steiner, 2003). and 2008. However, O. faveolata and O. Bermuda may be incorrect since this Colony density varies by habitat and annularis sustained the largest losses species was historically undifferentiated location, and range from less than 0.1 to with the number of colonies of O. from O. franksi and O. faveolata. The greater than one colony per 10 m2. In annularis decreasing by 19 and 20 two ecoregions in which it is not found surveys of 1,176 sites in southeast percent at Mona and Desecheo Islands, are off the coasts of Brazil and the Florida, the Dry Tortugas, and the respectively. In 1998, eight percent of southeastern U.S. north of southern Florida Keys between 2005 and 2010, all corals at six sites surveyed off Mona Florida (Veron, 2014). density of O. annularis ranged between Island were O. annularis colonies, 0.09 and 0.84 colonies per 10 m2 and dipping to approximately 6 percent in Demographic Information was highest on mid-channel reefs 2008. At Desecheo Island, 14 percent of The SRR and SIR provided the followed by inshore reefs, offshore all coral colonies were O. annularis in following information on O. annularis’ patch reefs, and fore-reefs (Burman et 2000 and 13 percent in 2008 (Bruckner abundance and population trends. al., 2012). Along the east coast of and Hill, 2009). Orbicella annularis has been described Florida, density was highest in areas Surveys of a degraded and a less as common overall. Demographic data south of Miami (0.34 colonies per 10 degraded site in a marine protected area 2 collected in Puerto Rico over nine years m ) compared to Palm Beach and in Cartagena, Colombia, revealed that straddling the 2005 bleaching event Broward Counties (0.04 colonies per 10 while large, old colonies of O. annularis 2 showed that population growth rates m , Burman et al., 2012). In surveys were present, colonies had experienced were stable in the pre-bleaching period between 2005 to 2007 along the Florida high partial mortality that caused high (2001–2005) but declined one year after reef tract from Martin County to the fission rates and a dominance of small, the bleaching event. Population growth lower Florida Keys, density of O. non-reproductive ramets. Ramets that rates declined even further two years annularis was approximately 1.3 2 were non-reproductive or less fertile after the bleaching event but returned to colonies per 10 m (Wagner et al., 2010). (less than 46 cm2) accounted for 72 stasis the following year. Off southwest Cuba on remote reefs, O. ± percent and 55 percent of the The public comments provided the annularis density was 0.31 0.46 (SD) population at the surveyed sites, and per 10 m transect on 38 reef-crest sites following supplemental information on ± only one percent and six percent of the O. annularis’ abundance and population and 1.58 1.29 colonies per 10 m ramets at the sites were large enough transect on 30 reef-front sites. Colonies trends. In the Florida Keys, abundance (200 cm2) to be fully reproductive. In with partial mortality were far more of O. annularis ranked 30 out of 47 coral addition to the small ramet size, the lack frequent than those with no partial species in 2005, 13 out of 43 in 2009, of sexual recruitment led the authors to mortality which only occurred in the and 12 out of 40 in 2012. Extrapolated conclude that both populations were in size class less than 100 cm (Alcolado et population estimates from stratified decline, especially at the more degraded al., 2010). random samples were 5.6 million ± 2.7 reef where mortality was higher and ± Population trends are available from a million (SE) in 2005, 11.5 million 4.5 number of studies. In a study of sites ramets were smaller, as individual million (SE) in 2009, and 24.3 million colonies seemed to be growing old ± inside and outside a marine protected 12.4 million (SE) in 2012. Size class area in Belize, O. annularis cover without being replaced (Alvarado- distribution was somewhat variable declined significantly over a ten year Chacon and Acosta, 2009). between survey years, with a larger period (1998/99 to 2008/09) In a survey of 185 sites in five proportion of colonies in the smaller (Huntington et al., 2011). In a study of countries (Bahamas, Bonaire, Cayman size classes in 2005 compared to 2009 ten sites inside and outside of a marine Islands, Puerto Rico, and St. Kitts and and 2012 and a greater proportion of reserve in the Exuma Cays, Bahamas, Nevis) in 2010 to 2011, size of O. colonies in the largest size class (>90 cover of O. annularis increased between annularis and O. franksi colonies was cm) in 2012 compared to 2005 and 2004 and 2007 inside the protected area significantly less than O. faveolata. 2009. Partial colony mortality was and decreased outside the protected Total mean partial mortality of O. lowest less than 10 cm (as low as area (Mumby and Harborne, 2010). annularis colonies at all sites was 40 approximately 5 percent) up to Between 1996 and 2006, O. annularis percent. Overall, the total area occupied approximately 70 percent in the larger declined in cover by 37 percent in by live O. annularis declined by a mean size classes. In the Dry Tortugas, permanent monitoring stations in the of 51 percent, and mean colony size Florida, abundance of O. annularis Florida Keys (Waddell and Clarke, declined from 1927 cm2 to 939 cm2. ranked 41 out of 43 in 2006 and 31 out 2008), and, cover of O. annularis in There was a 211 percent increase in of 40 in 2008. The extrapolated permanent monitoring stations between small tissue remnants less than 500 cm2, ± population estimate was 0.5 million 1996 and 1998 on a reef in the upper while the proportion of completely live 0.3 million (SE) colonies in 2008. Florida Keys declined 71 percent (Porter large (1,500–30,000 cm2) colonies Differences in population estimates et al., 2001). declined. Orbicella annularis colonies between years may be attributed to Orbicella annularis is the third most in Puerto Rico were much larger with sampling effort rather than population abundant coral by percent cover in large amounts of dead sections. In trends (Miller et al., 2013). permanent monitoring stations in the contrast, colonies in Bonaire were also Supplemental information we found U.S. Virgin Islands. A decline of 60 large with greater amounts of live tissue. on O. annularis’ abundance and percent was observed between 2001 and The presence of dead sections was population trends includes the 2012 primarily due to bleaching in attributed primarily to outbreaks of following. In Utila, Honduras, O. 2005. However, most of the mortality white plague and yellow band disease, annularis was present at 80 percent of was partial mortality, and colony which emerged as corals began sites surveyed between 1999 and 2000 density in monitoring stations did not recovering from mass bleaching events. and was the second most common coral change (Smith, 2013). This was followed by increased species (Afzal et al., 2001). In a survey At nine sites off Mona and Desecheo predation and removal of live tissue by of 31 sites in Dominica between 1999 Islands, Puerto Rico, no species damselfish algal lawns (Bruckner, and 2002, O. annularis was present at extirpations were noted at any site over 2012a).

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Hughes and Tanner (2000) annularis at this site within 50 years capacity of O. annularis’ life history documented the demographics of O. (Edmunds and Elahi, 2007). strategy that has allowed it to remain annularis in Jamaica from 1977 to 1993. Orbicella annularis colonies were abundant has been reduced by the At the beginning of the study, 86 monitored between 2001 and 2009 at recent population declines and amounts colonies were present within monitored Culebra Island, Puerto Rico. The of partial mortality, particularly in large stations. The number of colonies population was in demographic colonies. equilibrium (high rates of survival and increased 40 to 42 percent between 1986 Other Biological Information and 1987 due to fission (occurring at the stasis) before the 2005 bleaching event same time as a decline in cover) and but suffered a significant decline in The SRR and SIR provided the subsequently declined steadily to 40 growth rate (mortality and shrinkage) for following information on O. annularis’ colonies by 1993. Rates of survival, two consecutive years after the life history. Orbicella annularis is population growth, and recruitment bleaching event. Partial tissue mortality reported to have slightly smaller egg declined over time, and the size due to bleaching caused dramatic size and potentially smaller size/age at structure became increasingly colony fragmentation that resulted in a first reproduction that the other two dominated by smaller size classes population made up almost entirely of species of the Orbicella genus. (Hughes and Tanner, 2000). Mortality small colonies by 2007 (97 percent were The public comments did not provide increased sharply between 1990 and less than 50 cm2). Three years after the new or supplemental information on the 1993 due to the presence of smaller, bleaching event, the population life history of O. annularis. more vulnerable colonies formed by stabilized at a number of colonies Supplemental information we found on partial mortality of larger colonies reduced by about half, with fewer O. annularis’ life history includes the (Hughes, 1996). The persistence of large medium to large size colonies and more following. The reported growth rate of colonies had the greatest effect on smaller colonies (Herna´ndez-Pacheco et O. annularis is 0.4 to 1.2 cm per year (Cruz-Pin˜ o´n et al., 2003; Tomascik, population growth, and simulations al., 2011). 1990). Darling et al. (2012) performed a indicated that the levels of recruitment All information on O. annularis’ biological trait-based analysis to needed to maintain population levels at abundance and population trends can categorize coral species into four life 1977 levels increased sharply over time be summarized as follows. Historically, history strategies: Generalist, weedy, (Hughes and Tanner, 2000). Simulations O. annularis was considered to be one competitive, and stress-tolerant. The with no sexual recruitment indicated of the most abundant species in the classifications were primarily separated that the population dynamics in the Caribbean (Weil and Knowlton, 1994). by colony morphology, growth rate, and most recent period (1987 to 1993) Percent cover has declined between 37 reproductive mode. Orbicella annularis forecasted a population of zero within to 90 percent over the past several was classified as a ‘‘stress-tolerant’’ approximately 25 years. Simulation decades at reefs at Jamaica, Belize, Florida Keys, Bahamas, Bonaire, species, thus likely less vulnerable to using the population dynamics observed Cayman Islands, Curacao, Puerto Rico, environmental stress. between 1982 to 1987 would result in a U.S. Virgin Islands, and St. Kitts and The SRR and SIR provided the slower decline while the dynamics Nevis. Based on population estimates, following other biological information observed between 1977 and 1982 would there are at least tens of millions of O. for O. annularis. Eight percent of O. result in population growth (Hughes annularis colonies present in the annularis genotypes across three sites in and Tanner, 2000). Florida Keys and Dry Tortugas Belize were clones. Low tissue biomass Cover of O. annularis at Yawzi Point, combined. Absolute abundance is can render specific colonies of O. St. John, U.S. Virgin Islands declined higher than the estimate from these two annularis susceptible to mortality from from 41 percent in 1988 to locations given the presence of this stress events, such as bleaching or approximately 12 percent by 2003 with species in many other locations disease. This suggests that differential a rapid decline beginning with the throughout its range. Orbicella mortality among individuals, species, aftermath of Hurricane Hugo in 1989 annularis remains common in and reefs from stress events such as and continuing between 1994 and 1999 occurrence. Abundance has decreased bleaching or disease may be at least during a time of two hurricanes (1995) in some areas between 19 to 57 percent, partially a function of differential and a year of unusually high sea and shifts to smaller size classes have colony biomass (indicating overall coral temperature (1998), and remaining occurred in locations such as Jamaica, health) as opposed to genetic or statistically unchanged between 1999 Colombia, Bahamas, Bonaire, Cayman physiologic differences among corals or and 2003. Colony abundances declined Islands, Puerto Rico, U.S. Virgin Islands, their symbionts. from 47 to 20 colonies per m2 between and St. Kitts and Nevis. At some reefs, In a 2010 cold-water event that 1988 and 2003, due mostly to the death a large proportion of the population is affected south Florida, mortality of O. and fission of medium to large colonies comprised of non-fertile or less- annularis was higher than any other (≥151 cm2). Meanwhile, the population reproductive size classes. Several coral species in surveys from Martin size class structure shifted between population projections indicate County to the lower Florida Keys. 1988 and 2003 to a higher proportion of population decline in the future is likely Average partial mortality was 56 percent smaller colonies in 2003 (60 percent less at specific sites, and local extirpation is during the cold-water event compared than 50 cm2 in 1988 versus 70 percent possible within 25 to 50 years at to 0.3 percent from 2005 to 2009. in 2003) and lower proportion of large conditions of high mortality, low Surveys at a Florida Keys inshore patch colonies (6 percent greater than 250 cm2 recruitment, and slow growth rates. We reef, which experienced temperatures in 1988 versus 3 percent in 2003). The conclude that while substantial less than 18 degrees C for 11 days, changes in population size structure population decline has occurred in O. revealed O. annularis was one of the indicated a population decline annularis, it is still common throughout most susceptible coral species with all coincident with the period of apparent the Caribbean and remains one of the colonies experiencing total colony stable coral cover. Population modeling dominant species numbering at least in mortality. forecasts the 1988 size structure would the tens of millions of colonies. The public comments did not provide not be reestablished by recruitment and Additionally, as discussed in the genus new or supplemental biological a strong likelihood of extirpation of O. section, we conclude that the buffering information on O. annularis.

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Supplemental biological information we In a study of symbiont composition of months after the onset of bleaching found includes the following. Of 117 repeatedly sampled colonies of six (Alcolado et al., 2001). colonies of O. annularis observed to species in the Bahamas and the Florida Eight of 15 colonies of O. annularis spawn at a reef site off Bocas del Toro, Keys in 1998 and 2000 to 2004, major monitored in Jamaica from 1994 to 1997 Panama, there were 21 distinct changes in symbiont dominance with bleached in 1995. Bleaching affected genotypes, meaning that 82 percent of time were observed in O. annularis and polyp tissue depth, skeletal extension the colonies were clones (Levitan et al., O. franksi at certain reefs in the Florida rate, reproduction, and density band 2011). Individuals within a genotype Keys. Some colonies of O. annularis and formation, but the rate of recovery of spawned more synchronously than O. franksi exhibited shifts in their each of these characteristics varied. individuals of different genotypes. associations attributed to recovery from Tissue depth recovered within 4 to 8 Colonies nearby spawned more the stresses of the 1997–1998 bleaching weeks after normal color returned, and synchronously regardless of genotype, event. Most transitions in symbiont growth rates returned to pre-bleaching out to about 5 m. When colonies were identity ended in 2002, three to five levels once color and tissue depth farther away, spawning was random. years after the 1997–98 bleaching event returned. However, one year post Of 137 O. annularis colonies sampled (Thornhill et al., 2006). bleaching, reproductive failure occurred in Honduras, 118 were distinct All other biological information can in severely bleached colonies (bleached genotypes, meaning that 14 percent of be summarized as follows. Asexual for 4 months and pale for an additional the colonies were clones. Over 90 fission and partial mortality can lead to 3 months), and colonies that bleached percent of genotypes were represented multiple ramets. The percentage of mildly (bleached for 2 months with pale by a single colony, and 8 percent of the unique genotypes is variable by location color for an additional 1 to 3 months) genotypes were represented by two or and is reported to range between 18 and experienced reduced reproduction. three colonies. One genotype had 14 86 percent (14 to 82 percent are clones). Reproductive output of bleached colonies. Distance between clones Colonies in areas with higher colonies continued to be reduced two ranged between 0.15 m to 6.94 m (Foster disturbance from hurricanes tend to years after bleaching (Mendes and et al., 2007). have more clonality. Genetic data Woodley, 2002). indicate that there is some population Stratified random surveys on back- Genetic sampling of 698 O. annularis structure in the eastern, central, and reefs and fore-reefs between one and 30 colonies from 18 reefs within five western Caribbean with population m depth off Puerto Rico (Mona and countries in the Caribbean (Belize, connectivity within areas but not across. Desecho Islands, La Parguera, Bahamas, Columbia, Curacao, and Although O. annularis is still abundant, Mayaguez, Boqueron, and Rincon) in Honduras) revealed 466 distinct it may exhibit high clonality in some 2005 and 2006 revealed severe genotypes (approximately 33 percent locations. bleaching in O. annularis with greater clones). Genotypic diversity varied than 95 percent of colonies bleached across the species’ range from Susceptibility to Threats (Waddell and Clarke, 2008). Surveys genetically diverse populations in The threat susceptibility information from 2005 to 2007 along the Florida reef Colombia, where every colony was from the SRR and SIR was interpreted tract from Martin County to the lower unique, to genetically depauperate in the proposed rule for O. annularis’ Florida Keys indicated that O. annularis populations in Belize and Curacao, vulnerabilities to threats as follows: had the seventh highest bleaching where a few genetic clones dominated. High vulnerability to ocean warming, prevalence out of 30 species observed The contribution of clones to the local disease, acidification, sedimentation, (Wagner et al., 2010). During a 2009 abundance of O. annularis increased in and nutrient enrichment; moderate bleaching event on Little Cayman, of the areas with greater hurricane frequency. vulnerability to the trophic effects of ten coral species that bleached, O. Sites with higher genotypic diversity fishing; and low vulnerability to sea annularis had the second highest were dominated by larger colonies, and level rise, predation, and collection and bleaching prevalence with sites that experienced more frequent trade. approximately 45 percent of colonies hurricanes were composed of smaller The SRR and SIR provided the bleached (van Hooidonk et al., 2012). colonies than sites with less frequent following information on the Surveys at Culebra Island, Puerto Rico hurricanes (Foster et al., 2013). susceptibility of O. annularis to ocean revealed extensive bleaching in 2005 Tissue samples of 1,424 O. annularis warming. Simulation models using with all of the O. annularis colonies in colonies at 26 reefs in 16 regions of the demographic data collected in Puerto monitored transects bleached, and many Caribbean (Bahamas, Cuba, Dominican Rico over nine years straddling the 2005 of the surviving colonies remained pale Republic, Puerto Rico, British Virgin bleaching forecasted extinction of the in color after a year. Cover of O. Islands, Dominica, Barbados, Tobago, population within 100 years at a annularis was reduced from 28 percent Venezuela, Netherlands Antilles, bleaching frequency of once every five prior to the bleaching event in 2005 to Colombia, Nicaragua, Jamaica, Cayman to ten years. 8 percent in 2009 (Herna´ndez-Pacheco Islands, Belize, and Honduras) The public comments did not provide et al., 2011). produced 943 distinct genotypes (34 new or supplemental information on the In Barbados, the prevalence and percent clones). Three coarse susceptibility of O. annularis to ocean abundance of the zooxanthellae population clusters of O. annularis were warming. Supplemental information we Symbiodinium trenchi (D1a) increased detected: eastern (Lesser Antilles, found on the susceptibility of O. in colonies of O. annularis in the weeks Venezuela, and Netherlands Antilles), annularis to ocean warming includes leading up to and during the 2005 western (Bahamas, Cuba, Belize, and the following. Surveys from 19 locations bleaching event, and disproportionately Cayman Islands), and central (Jamaica, throughout the Caribbean indicated the dominated O. annularis colonies that Honduras, Nicaragua, Colombia, Puerto bleaching event of 1995–96 was most did not bleach. In the 2-year period Rico, British Virgin Islands, and extensive in the central and western following the bleaching event, S. trenchi Dominican Republic). No barrier to gene Caribbean but only slight in the Lesser was displaced by other strains of flow based on absolute geographic Antilles and Bermuda. Mortality of O. Symbiodinium that were more distance was apparent (Foster et al., annularis from bleaching ranged from 2 competitive under less stressful 2012). to 30 percent at eight locations six conditions. The authors concluded that

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it was unclear whether the rise and fall new or supplemental information on the All sources of information are used to of S. trenchi was ecologically beneficial susceptibility of O. annularis to disease. describe O. annularis’ susceptibility to or whether its increased prevalence was Supplemental information we found on disease as follows. Most studies report an indicator of weakening coral health the susceptibility of O. annularis to O. annularis as among the species with (LaJeunesse et al., 2009). disease confirms the information on the the highest disease prevalence. Disease Across the U.S. Virgin Islands, Orbicella species complex and includes can cause extensive loss in coral cover, average bleaching of O. annularis was the following. Surveys at five sites along high levels of partial colony mortality, 66 percent, and paling was 16 percent, the west coast of Dominica between and changes in the relative proportions during the 2005 bleaching event. 2000 and 2002 revealed O. annularis of smaller and larger colonies, Disease prevalence of O. annularis was was one of the species most susceptible particularly when outbreaks occur after 5 percent after the 2005 bleaching. In to disease. Of the 12 species infected by bleaching events. Thus, we conclude the milder 2010 bleaching event, 58 white plague in 2000, O. annularis that O. annularis is highly susceptible to percent of O. annularis colonies ranked third highest in disease disease. bleached, and 28 percent of the colonies prevalence (14.1 percent of infected The SRR and SIR provided the paled. No O. annularis colonies suffered colonies were O. annularis). It ranked following information on the total mortality, but percent cover second in 2001 out of 14 species (20.3 susceptibility of O. annularis to the decreased from the 2.5 percent cover in percent) and third in 2002 out of 13 trophic effects of fishing. Interactions 2005 before bleaching to about one species (12.7 percent). Although only between O. annularis and four types of percent in 2010. There was a reduction one colony experienced total colony benthic algae (encrusting calcified red in the proportion of larger sized mortality, O. annularis had the third algae, fleshy brown macroalgae, upright colonies and an increase in the highest amount of tissue loss in the calcareous green algae, and a mixed proportion of smaller sized colonies due three years combined (11,717 cm2). assemblage of turf algae) indicate that to fission of larger colonies. The authors Black band disease affected O. annularis each alga exerts its own characteristic concluded that the susceptibility to in 2000 but not in any of the other suite of effects on the coral holobiont, disease increased the impact of survey years (Borger and Steiner, 2005). and that micro-scale dynamics have the bleaching, making O. annularis less In a 1998 outbreak of white plague in potential to drive changes in reef tolerant overall to ocean warming St. Lucia, three percent of O. annularis community composition. Negative (Smith et al., 2013b). were affected, which was the lowest impacts spanned the range from micro- All sources of information are used to prevalence of disease of six species scale changes in microbial communities describe O. annularis’ susceptibility to studied (Nugues, 2002). In surveys after and oxygen drawdown to colony-scale ocean warming as follows. Orbicella the 2010 bleaching event and the effects such as damage to adjacent annularis is highly susceptible to polyps and lowered fecundity of the passage of a hurricane, 93 percent of bleaching with 45 to 100 percent of adjacent colony. The public comments diseased colonies (111 of 119 colonies) colonies observed to bleach. Reported did not provide new or supplemental surveyed in radial transects in Brewers mortality from bleaching ranges from information on the susceptibility of O. Bay, U.S. Virgin Islands were O. two to 71 percent. Recovery after annularis to the trophic effects of annularis (Brandt et al., 2013). Yellow bleaching is slow with paled colonies fishing, and we did not find any new or band disease in O. annularis increased observed for up to a year. Reproductive supplemental information. failure can occur a year after bleaching, in prevalence between 1999 and 2004 All sources of information are used to and reduced reproduction has been on reefs near La Parguera and Desecheo describe O. annularis’ susceptibility to observed two years post bleaching. and Mona Islands, Puerto Rico the trophic effects of fishing as follows. There is indication that symbiont (Waddell, 2005). Due to the level of reef fishing shuffling can occur prior to, during, and Disease surveys conducted between conducted in the Caribbean, coupled after bleaching events and result in August and December 1999 at 19 reef with Diadema die-off and lack of bleaching resistance in individual sites from six geographic areas across significant recovery, competition with colonies. We conclude that O. annularis the wider Caribbean (Bermuda, Puerto algae can adversely affect coral is highly susceptible to ocean warming. Rico, Bonaire, Venezuela, Colombia, recruitment. In addition, competition The SRR and SIR did not provide any and Jamaica) revealed that O. annularis with algae can lead to micro-scale to species-specific information on the showed the highest incidence of disease colony-level negative impacts to O. susceptibility of O. annularis to at 5.5 to 12.6 percent across geographic annularis. Thus, we conclude that O. acidification, and the public comments locations. Yellow band disease showed annularis has some susceptibility to the did not provide new or supplemental higher incidences in Bonaire and trophic effects of fishing. The available information on its susceptibility to this Venezuela where a high proportion of information does not support a more threat. We did not find any new or recently dead ramets of O. annularis precise description of susceptibility to supplemental information on the that most probably died from the this threat. susceptibility of O. annularis to disease were observed (Weil et al., The SRR and SIR did not provide acidification. Although there is no 2002). species-specific information on the species-specific information on the In Curacao, colonies of O. annularis susceptibility of O. annularis to susceptibility of O. annularis to ocean infected with yellow band disease lost sedimentation, and the public acidification, genus information 90 percent of their tissue between 1997 comments did not provide new or indicates the species complex has and 2005. Only the unaffected parts of supplemental information on its reduced growth and fertilization success colonies continued to grow, and only susceptibility to this threat. under acidic conditions. Thus, we the smallest lesions healed. Partial Supplemental information we found conclude O. annularis likely has high mortality was higher in 2005 (average of confirms the information on the susceptibility to ocean acidification. 40 percent) than in 1998. Outbreaks of susceptibility of the Orbicella species The SRR and SIR did not provide any white plague occurred in 2001 and 2005 complex to sedimentation and includes species-specific information on the and infected O. faveolata and O. the following. In St. Lucia, rates of susceptibility of O. annularis to disease. annularis with the highest frequency partial mortality of O. annularis and O. The public comments did not provide (Bruckner and Bruckner, 2006a). faveolata were higher close to river

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mouths where sediments were corallivorous snail C. abbreviata was annularis occurs in nine Atlantic deposited than they were farther from present on 2.5 percent of O. annularis ecoregions that encompass 26 the river mouths, indicating sensitivity colonies surveyed in the Florida Keys in kingdom’s and countries’ EEZs. The 26 of these two species to sedimentation 2012 (Miller et al., 2013). Parrotfish kingdoms and countries are Antigua & (Nugues and Roberts, 2003). consume O. annularis and O. faveolata Barbuda, Bahamas, Barbados, Belize, Additionally, at five study sites in more intensively than other coral Colombia, Costa Rica, Cuba, Dominica, Puerto Rico, the cover of O. annularis species, but tissue regeneration Dominican Republic, French Antilles, decreased significantly with a high capabilities appear to be high enough to Grenada, Guatemala, Haiti, Kingdom of content of terrigenous sediments (Torres counterbalance loss from predation the Netherlands, Honduras, Jamaica, and Morelock, 2002). (Mumby, 2009). Mexico, Nicaragua, Panama, St. Kitts & All sources of information are used to All sources of information are used to Nevis, St. Lucia, St. Vincent & describe O. annularis’ susceptibility to describe O. annularis’ susceptibility to Grenadines, Trinidad and Tobago, sedimentation as follows. predation as follows. Orbicella United Kingdom (British Caribbean Sedimentation can cause partial annularis is affected by a number of Territories and possibly Bermuda), mortality and decreased coral cover of predators, but losses appear to be United States (including U.S. Caribbean O. annularis. In addition, genus minimal. We conclude that O. annularis Territories), and Venezuela. The information indicates sedimentation has low susceptibility to predation. regulatory mechanisms relevant to O. negatively affects primary production, The SRR and SIR did not provide annularis, described first as a growth rates, calcification, colony size, information on the effects of sea level percentage of the above kingdoms and and abundance. Therefore, we conclude rise on O. annularis. The SRR described countries that utilize them to any that O. annularis has high susceptibility sea level rise as an overall low to degree, and second as the percentage of to sedimentation. medium threat for all coral species. The those kingdoms and countries whose The SRR, SIR, and public comments public comments did not provide new regulatory mechanisms may be limited do not provide information on the or supplemental information on O. in scope, are as follows: General coral susceptibility of O. annularis to nutrient annularis’ susceptibility to sea level protection (31 percent with 12 percent enrichment. Supplemental information rise, and we did not find any new or limited in scope), coral collection (50 we found on the susceptibility of O. supplemental information. Thus, we percent with 27 percent limited in annularis to nutrient enrichment conclude that O. annularis has some scope), pollution control (31 percent includes the following. Field susceptibility to sea level rise, but the with 15 percent limited in scope), experiments indicate that nutrient available information does not support fishing regulations on reefs (73 percent enrichment significantly increases a more precise description of with 50 percent limited in scope), yellow band disease severity in O. susceptibility to this threat. managing areas for protection and annularis and O. franksi through The SRR and SIR did not provide conservation (88 percent with 31 increased tissue loss (Bruno et al., species-specific information on the percent limited in scope). The most 2003). In laboratory experiments, susceptibility of O. annularis to common regulatory mechanisms in dissolved organic carbon caused collection and trade, and the public place for O. annularis are reef fishing significantly higher mortality of O. comments did not provide new or regulations and area management for annularis after 30 days of exposure supplemental information on its protection and conservation. However, compared to controls while nutrients susceptibility to this threat. half of the reef fishing regulations are (phosphate, nitrate, and ammonia) did Supplemental information we found limited in scope and may not provide not (Kline et al., 2006; Kuntz et al., confirms the information in the SRR and substantial protection for the species. 2005). Dissolved organic carbon levels SIR that collection and trade is not a General coral protection and collection that resulted in significantly higher significant threat for the Orbicella laws, along with pollution control laws, mortality compared to controls were species complex. Over the last decade, are much less common regulatory 12.5 mg per L glucose, and 25 mg per collection and trade of this species has mechanisms for the management of O. L lactose, starch, galactose, and glucose, been primarily for scientific research annularis. which were all levels reported for rather than commercial purposes. impacted reefs (Kline et al., 2006; Kuntz Annual gross exports for collection and Vulnerability to Extinction et al., 2005). trade of O. annularis between 2000 and As explained above in the Risk All sources of information are used to 2012 averaged 1,178 specimens (data Analyses section, a species’ describe O. annularis’ susceptibility to available at http://trade.cites.org). Thus, vulnerability to extinction results from nutrient enrichment as follows. Elevated we conclude that O. annularis has a low the combination of its spatial and nutrients cause increased disease susceptibility to collection and trade. demographic traits, threat severity in O. annularis. Genus level susceptibilities, and consideration of the information indicates elevated nutrients Regulatory Mechanisms baseline environment and future also cause reduced growth rates and In the proposed rule, we relied on projections of threats. The SRR stated lowered recruitment. Therefore, we information from the Final Management that the factors that increase the conclude that O. annularis has high Report for evaluating the existing extinction risk for O. annularis include susceptibility to nutrients. regulatory mechanisms for controlling very low productivity (growth and The SRR and SIR do not provide threats to all corals. However, we did recruitment), documented dramatic species-specific information on the not provide any species-specific declines in abundance, restriction to the susceptibility of O. annularis to information on the regulatory degraded reefs of the wider Caribbean predation. Likewise, the public mechanism or conservation efforts for region, and preferential occurrence in comments do not provide information O. annularis. Public comments were shallow habitats (yielding potentially on the susceptibility of O. annularis to critical of that approach, and we greater exposure to surface-based predation. Supplemental information therefore attempt to analyze regulatory threats. we found on the susceptibility of O. mechanisms and conservation efforts on Subsequent to the proposed rule, we annularis to predation includes the a species basis, where possible, in this received and gathered supplemental following. Predation by the final rule. Records confirm that O. species- or genus-specific information,

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described above, that expands our annularis is limited to an area with (2) Orbicella is geographically located knowledge regarding the species’ high, localized human impacts and in the highly disturbed Caribbean where abundance, distribution, and threat predicted increasing threats. Orbicella localized human impacts are high and susceptibilities. We developed our annularis occurs in most reef habitats threats are predicted to increase as assessment of the species’ vulnerability 0.5 to 20 m in depth which moderates described in the Threats Evaluation to extinction using all the available vulnerability to extinction over the section. A range constrained to this information. As explained in the Risk foreseeable future because the species particular geographic area that is likely Analyses section, our assessment in this occurs in numerous types of reef to experience severe and increasing final rule emphasizes the ability of the environments that are predicted, on threats indicates that a high proportion species’ spatial and demographic traits local and regional scales, to experience of the population of this species is likely to moderate or exacerbate its highly variable thermal regimes and to be exposed to those threats over the vulnerability to extinction, as opposed ocean chemistry at any given point in foreseeable future; to the approach we used in the time. Its abundance and life history (3) Orbicella annularis has undergone proposed rule, which emphasized the characteristics combined with spatial declines in abundance and percent species’ susceptibility to threats. variability in ocean warming and cover over the past two decades; (4) Orbicella annularis’ slow growth The following characteristics of O. acidification across the species’ range, rate and low sexual recruitment limit its annularis, in conjunction with the moderate vulnerability to extinction capacity for recovery from threat- information described in the Corals and because the threats are non-uniform, induced mortality events throughout its Coral Reefs section, Coral Habitat sub- and there will likely be a large number of colonies that are either not exposed range over the foreseeable future. section, and Threats Evaluation section Additionally, shifts to smaller size above, affect its vulnerability to or do not negatively respond to a threat at any given point in time. classes via fission and partial mortality extinction currently and over the of older, larger colonies, have reduced foreseeable future. The species has Listing Determination the buffering capacity of O. annularis’ undergone major declines mostly due to In the proposed rule, using the life history strategy; and warming-induced bleaching and (5) Several population projections and determination tool formula approach, O. disease. Several population projections simulations predict continued annularis was proposed for listing as indicate population decline in the population declines and local endangered because of: High future is likely at specific sites and that extirpation at specific sites within the vulnerability to ocean warming (E) local extirpation is possible within 25 to foreseeable future. 50 years at conditions of high mortality, disease (C), and ocean acidification (E); The combination of these low recruitment, and slow growth rates. high vulnerability to sedimentation (A characteristics and future projections of There is evidence of synergistic effects and E) and nutrient over-enrichment (A threats indicates that the species is of threats for this species including and E); decreasing trend in abundance likely to be in danger of extinction disease outbreaks following bleaching (E); low relative recruitment rate (E); within the foreseeable future throughout events and increased disease severity narrow overall distribution (based on its range, and warrants listing as with nutrient enrichment. Orbicella narrow geographic distribution and threatened at this time due to factors A, annularis is highly susceptible to a moderate depth distribution (E); C, D, and E. number of threats, and cumulative restriction to the Caribbean; and The available information above on O. effects of multiple threats have likely inadequacy of regulatory mechanisms annularis’ spatial structure, contributed to its decline and exacerbate (D). demography, threat susceptibilities, and vulnerability to extinction. Despite high In this final rule, we changed the management also indicate that the declines, the species is still common listing determination for O. annularis species is not currently in danger of and remains one of the most abundant from endangered to threatened. We extinction and thus does not warrant species on Caribbean reefs. Its life made this determination based on a listing as Endangered because: history characteristics of large colony more species-specific and holistic (1) While Orbicella annularis’ size and long life span have enabled it approach, including consideration of distribution within the Caribbean to remain relatively persistent despite the buffering capacity of this species’ increases its risk of exposure to threats slow growth and low recruitment rates, spatial and demographic traits, and the as described above, its habitat includes thus moderating vulnerability to best available information above on O. most reef environments in water depths extinction. However, the buffering annularis’ spatial structure, ranging from 0.5 to 20 m. This capacity of these life history demography, threat susceptibilities, and moderates vulnerability to extinction characteristics is expected to decrease as management. The combination of these currently because the species is not colonies shift to smaller size classes as factors indicates that O. annularis is limited to one habitat type but occurs in has been observed in locations in its likely to become endangered throughout numerous types of reef environments range. Its absolute population its range within the foreseeable future, will experience highly variable thermal abundance has been estimated as at and thus warrants listing as threatened regimes and ocean chemistry on local least tens of millions of colonies in the at this time, because: and regional scales at any given point in Florida Keys and Dry Tortugas (1) Orbicella annularis is susceptible time, as described in more detail in the combined and is higher than the to ocean warming (ESA Factor E), Coral Habitat and Threats Evaluation estimate from these two locations due to disease (C), sedimentation (A, E), sections. There is no evidence to suggest the occurrence of the species in many nutrients (A, E), and ocean acidification that the species is so spatially other areas throughout its range. Despite (E) and susceptible to trophic effects of fragmented that depensatory processes, the large number of islands and fishing (A). These threats are expected environmental stochasticity, or the environments that are included in the to continue and increase into the future. potential for catastrophic events species’ range, geographic distribution In addition, the species is at heightened currently pose a high risk to the survival in the highly disturbed Caribbean extinction risk due to inadequate of the species; exacerbates vulnerability to extinction existing regulatory mechanisms to (2) Although O. annularis’ abundance over the foreseeable future because O. address global threats (D); has declined, it still has a common

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occurrence and remains one of the most Acropora cervicornis and A. palmata 1984; Jaap et al., 1989; Schuhmacher dominant corals in the Caribbean. Its can interbreed to form the hybrid A. and Zibrowius, 1985; Wheaton and Jaap, absolute abundance is at least tens of prolifera (Brainard et al., 2011). 1988). At the northern extent of its millions of colonies based on estimates Acropora cervicornis shows genetic range, it grows in deeper water (16 to 30 from two locations. Absolute abundance evidence of introgression or back- m; Goldberg, 1973). Historically, is higher than estimates from these crossing with the hybrid A. prolifera staghorn coral was one of the primary locations since it occurs in many other while A. palmata does not (Brainard et constructors of mid-depth (10 to 15 m) locations throughout its range. This al., 2011). The reason may be that A. reef terraces in the western Caribbean, absolute abundance allows for variation palmata eggs are more resistant to including Jamaica, the Cayman Islands, in the responses of individuals to fertilization in comparison to A. Belize, and some reefs along the eastern threats to play a role in moderating cervicornis eggs, as evidenced by an Yucatan peninsula (Adey, 1978). In the vulnerability to extinction for the order of magnitude higher sperm Florida Keys, A. cervicornis occurs in species to some degree, as described in needed to maximize conspecific various habitats but is most prevalent on more detail in the Corals and Coral fertilization, lower rates of patch reefs as opposed to their former Reefs section. There is no evidence of heterospecific fertilization, and reduced abundance in deeper fore-reef habitats depensatory processes such as viability after four hours (Fogarty et al., (Miller et al., 2008). There is no reproductive failure from low density of 2012c). evidence of range constriction, though reproductive individuals and genetic Caribbean acroporiids are easily loss of A. cervicornis at the reef level processes such as inbreeding affecting distinguishable and heavily studied. has occurred (Acropora Biological this species. Thus, its absolute Therefore, this final rule does not Review Team, 2005). abundance indicates it is currently able provide an exhaustive discussion of the The public comments did not provide to avoid high mortality from spatial, demographic, and threat new or supplemental information on A. environmental stochasticity, and vulnerabilities at the genus level. That cervicornis’ habitat or depth range. The mortality of a high proportion of its information is described below for each public comments provided the population from catastrophic events; species. following supplemental information on and the distribution of A. cervicornis. Precht (3) Some evidence shows that Acropora cervicornis and Aronson (2004) postulate that symbiont shuffling can occur prior to, Introduction coincident with climate warming, A. during, and after bleaching events and cervicornis only recently re-occupied its result in bleaching resistance in Acropora cervicornis is characterized historic range after contracting to south individual colonies. This indicates O. by antler-like colonies with straight or of Miami, Florida during the late annularis may have some buffering slightly curved, cylindrical branches. Holocene. They based this idea on the capacity against warming-induced The diameter of branches ranges from presence of large thickets off Ft. bleaching. 0.25 to 5 cm (Lirman et al., 2010a), and Lauderdale, Florida which were The combination of these linear branch growth rates have been discovered in 1998 and had not been characteristics indicates that the species reported to range between 3 and 11.5 cm reported in the 1970s or 1980s (Precht does not exhibit the characteristics of per year (Acropora Biological Review and Aronson, 2004). However, because one that is currently in danger of Team, 2005). The species can exist as the presence of A. cervicornis in Palm extinction, as described previously in isolated branches, individual colonies Beach County, north of Ft. Lauderdale, the Risk Analyses section and thus does up to about 1.5 m diameter, and thickets was reported in the early 1970s (though not warrant listing as endangered at this comprised of multiple colonies that are no thicket formation was reported; time. difficult to distinguish (Acropora Goldberg, 1973), there is uncertainty Range-wide, multitudes of Biological Review Team, 2005). associated with whether these thickets conservation efforts are already broadly Spatial Information were present prior to their discovery or employed that are likely benefiting O. if they recently appeared coincident annularis. However, considering the Information on A. cervicornis’ with warming. global scale of the most important distribution, habitat, and depth range We did not find any new or threats to the species, and the that we considered in the proposed rule supplemental information on habitat or ineffectiveness of conservation efforts at includes the following. Acropora depth range. Supplemental information addressing the root cause of global cervicornis is distributed throughout the we found on A. cervicornis’ distribution threats (i.e., GHG emissions), we do not Caribbean, in the southwestern Gulf of is consistent with information believe that any current conservation Mexico, and in the western Atlantic. considered in the proposed rule and efforts or conservation efforts planned The fossil record indicates that during includes the following. Veron (2014) in the future will result in affecting the the Holocene, A. cervicornis was present confirms the presence of A. cervicornis species’ status to the point at which as far north as Palm Beach County in in seven out of a potential 11 ecoregions listing is not warranted. southeast Florida (Lighty et al., 1978), in the western Atlantic and greater which is also the northern extent of its Caribbean that are known to contain Genus Acropora (Caribbean) current distribution (Goldberg, 1973). corals. The four ecoregions in which it Acropora is the only genus Acropora cervicornis naturally occurs is not found are the Flower Garden considered in this rule that has species on spur and groove, bank reef, patch Banks and off the coasts of Bermuda, from both the Caribbean and the Indo- reef, and transitional reef habitats, as Brazil, and the southeast U.S. north of Pacific. Genus-level information for the well as on limestone ridges, terraces, south Florida. The proportion of reefs Indo-Pacific species is described later and hardbottom habitats (Cairns, 1982; with A. cervicornis present decreased under the section heading Genus Davis, 1982; Gilmore and Hall, 1976; dramatically after the Caribbean-wide Acropora (Indo-Pacific). Colonies in the Goldberg, 1973; Jaap, 1984; Miller et al., mass mortality in the 1970s and 1980s, Caribbean are all branching. There are 2008; Wheaton and Jaap, 1988). It indicating the spatial structure of the over 300 nominal species in the genus commonly grows in water ranging from species has been affected by extirpation Acropora, but in the Caribbean, there five to 20 m in depth and has rarely from many localized areas throughout are only two species and one hybrid. been found to 60 m (Davis, 1982; Jaap, its range (Jackson et al., 2014).

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Demographic Information 2008; Muller et al., 2008; Rogers and estimates were based on random Information on A. cervicornis’ Muller, 2012; Williams et al., 2008). sampling, differences in abundance abundance and population trends that Public comments provided the estimates between years may be more we considered in the proposed rule following supplemental information on likely a function of sampling effort includes the following. Acropora A. cervicornis’ abundance and rather than population trends. In both population trends. There are some small cervicornis has been described as the Florida Keys and Dry Tortugas, most pockets of remnant robust populations sometimes common (Veron, 2000) and of the population was dominated by such as in southeast Florida (Vargas- uncommon (Carpenter et al., 2008). small colonies less than 30 cm diameter. Angel et al., 2003), Honduras (Keck et Acropora cervicornis historically was In the Florida Keys, partial mortality al., 2005; Riegl et al., 2009), and one of the dominant species on most was highest in 2005, with up to 80 Dominican Republic (Lirman et al., Caribbean reefs, forming large, percent mortality observed, and lowest 2010a). Additionally, Lidz and Zawada monotypic thickets and giving rise to in 2007 with a maximum of 30 percent. (2013) observed 400 colonies of A. In 2012, partial mortality ranged from the nominal distinct zone in classical cervicornis along 70.2 km of transects 20 to 50 percent across most size descriptions of Caribbean reef near Pulaski Shoal in the Dry Tortugas classes. morphology (Goreau, 1959). Massive, where the species had not been seen Supplemental information we found Caribbean-wide mortality, apparently since the cold water die-off of the 1970s. on A. cervicornis’ abundance and primarily from white band disease Cover of A. cervicornis increased on a population trends includes the (Aronson and Precht, 2001), spread Jamaican reef from 0.6 percent in 1995 following. Acropora cervicornis was throughout the Caribbean in the mid- to 10.5 percent in 2004 (Idjadi et al., observed in 21 out of 301 stations 1970s to mid-1980s and precipitated 2006). between 2011 and 2013 in stratified widespread and radical changes in reef Riegl et al. (2009) monitored A. random surveys designed to detect community structure (Brainard et al., cervicornis in photo plots on the Acropora colonies along the south, 2011). In addition, continuing coral fringing reef near Roatan, Honduras southeast, southwest, and west coasts of mortality from periodic acute events from 1996 to 2005. Acropora cervicornis Puerto Rico, and it was observed at an such as hurricanes, disease outbreaks, cover was 0.42 percent in 1996, additional 16 sites outside of the and mass bleaching events has added to declined to 0.14 percent in 1999 after surveyed area (Garcı´a Sais et al., 2013). the decline of A. cervicornis (Brainard et the Caribbean bleaching event in 1998 The largest colony was 60 cm, and al., 2011). In locations where and mortality from run-off associated density ranged from 1 to 10 colonies per quantitative data are available (Florida, with a Category 5 hurricane, and 15 m2 (Garcı´a Sais et al., 2013). Jamaica, U.S. Virgin Islands, Belize), decreased further to 0.09 percent in While cover of A. cervicornis there was a reduction of approximately 2005. Acropora cervicornis colony increased from 0.6 percent in 1995 to 92 to greater than 97 percent between frequency decreased 71 percent between 10.5 percent in 2004 (Idjadi et al., 2006) the 1970s and early 2000s (Acropora 1997 and 1999. In sharp contrast, and 44 percent in 2005 on a Jamaican Biological Review Team, 2005). offshore banks near Roatan had dense reef, it collapsed after the 2005 Fossil evidence from the Dominican thickets of A. cervicornis with 31 bleaching event and subsequent disease Republic indicates that Holocene A. percent cover in photo-quadrats in 2005 to less than 0.5 percent in 2006 (Quinn cervicornis was capable of thriving for and appeared to survive the 1998 and Kojis 2008). A cold water die-off in thousands of years under highly bleaching event and hurricane, most the Florida Keys in January 2010 variable temperature and salinity likely due to bathymetric separation resulted in the complete mortality of all conditions and suggests that the recent from land and greater flushing. A. cervicornis colonies at 45 of the 74 decline in A. cervicornis is anomalous Modeling showed that under reefs surveyed (61 percent), spanning (Greer et al., 2009). Additional fossil undisturbed conditions, retention of the the lower to upper Florida Keys evidence from Belize indicates that the dense A. cervicornis stands on the banks (Schopmeyer et al., 2012). Walker et al. recent decline of A. cervicornis is off Roatan is likely with a possible (2012) report increasing size of two without precedent during the late increased shift towards dominance by thickets (expansion of up to 7.5 times Holocene (Aronson and Precht, 2001). other coral species. However, the the original size of one of the thickets) In contrast, two 500 year gaps in the authors note that because their data and monitored off southeast Florida and also fossil record, around 3 and 4.5 thousand the literature seem to point to extrinsic noted that cover within monitored plots years ago where dated A. cervicornis factors as driving the decline of A. concurrently decreased by about 50 fragments were not observed in samples cervicornis, it is unclear what the future percent, highlighting the dynamic from the Florida Keys, suggests that the may hold for this dense population nature of A. cervicornis distribution via recent decline may not be without (Riegl et al., 2009). fragmentation and re-attachment. precedent (Shinn et al., 2003). However, Miller et al. (2013) extrapolated New information we found on this study was based on radiocarbon population abundance of A. cervicornis population trends includes the dating of A. cervicornis fragments, for in the Florida Keys and Dry Tortugas following. A report on the status and which the time of transport and from stratified random samples across trends of Caribbean corals over the last deposition are not known, so there is habitat types. Population estimates of A. century indicates that cover of A. uncertainty of whether these gaps cervicornis in the Florida Keys were cervicornis has remained relatively represent the absence of A. cervicornis 10.2 ± 4.6 (SE) million colonies in 2005, stable (though much reduced) or variable storm depositional history 6.9 ± 2.4 (SE) million colonies in 2007, throughout the region since the large (Shinn et al., 2003). and 10.0 ± 3.1 (SE) million colonies in mortality events of the 1970s and 1980s. Since the 2006 listing of A. 2012. In the Dry Tortugas population The frequency of reefs at which A. cervicornis as threatened, continued estimates were 0.4 ± 0.4 (SE) million cervicornis was described as the population declines have occurred in colonies in 2006 and 3.5 ± 2.9 (SE) dominant coral has remained stable. some locations with certain populations million colonies in 2008, though the The number of reefs with A. cervicornis of both species decreasing up to an authors note their sampling scheme in present declined during the 1980s (from additional 50 percent or more (Colella et the Dry Tortugas was not optimized for approximately 50 to 30 percent of reefs), al., 2012; Lundgren and Hillis-Starr, A. cervicornis. Because these population remained relatively stable through the

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1990s, and decreased to approximately et al., 2006). The estimated size at 2007). This fine-scale population 20 percent of the reefs 2000–2004, and sexual maturity is 17 cm branch length, structure was greater when considering approximately 10 percent 2005–2011 and large colonies produce genes of A. palmata introgressed in A. (Jackson et al., 2014). proportionally more gametes than small cervicornis due to back-crossing of the We summarize all sources of colonies (Soong and Lang, 1992). Basal hybrid A. prolifera with A. cervicornis information on A. cervicornis’ and branch tip tissue is not fertile (Garcia Reyes and Schizas, 2010; abundance and population trends as (Soong and Lang, 1992). Sexual Vollmer and Palumbi, 2007). follows. Based on population estimates, recruitment rates are low, and this Populations in Florida and Honduras there are at least tens of millions of species is generally not observed in are genetically distinct from each other colonies present in the Florida Keys and coral settlement studies. However, and other populations in the U.S. Virgin Dry Tortugas combined. Absolute laboratory studies have found that Islands, Puerto Rico, Bahamas, and abundance is higher than the estimate certain species of crustose-coralline Navassa (Baums et al., 2010), indicating from these two locations given the algae facilitate larval settlement and little to no larval connectivity. However, presence of this species in many other post-settlement survival (Ritson- some potential connectivity between the locations throughout its range. The Williams et al., 2010). U.S. Virgin Islands and Puerto Rico was effective population size is smaller than Reproduction occurs primarily detected and also between Navassa and indicated by abundance estimates due through asexual fragmentation that the Bahamas (Baums et al., 2010). to the tendency for asexual produces multiple colonies that are Florida populations of A. cervicornis reproduction. There is no evidence of genetically identical (Tunnicliffe, 1981). have high levels of both genetic range constriction or extirpation at the The combination of branching diversity and connectivity, with island level. However the species is morphology, asexual fragmentation, and evidence suggesting the western absent at the reef level. Populations fast growth rates can lead to persistence Caribbean has historically been the appear to consist mostly of isolated of large areas dominated by A. source of genetic variation for Florida colonies or small groups of colonies cervicornis. (Hemond and Vollmer, 2010). Colonies compared to the vast thickets once The public comments did not provide of A. cervicornis in Florida mostly prominent throughout its range, with new or supplemental information on A. harbored zooxanthellae Clade A, but thickets still a prominent feature at only cervicornis’ life history. Supplemental colonies from inshore and mid-channel a handful of known locations. Across information we found on life history reefs, which experience higher the Caribbean, percent cover appears to includes the following. Darling et al. sedimentation and temperature have remained relatively stable since (2012) performed a biological trait-based fluctuations than reefs further offshore, the population crash in the 1980s. analysis to categorize coral species into had a higher prominence of Clades C Frequency of occurrence has decreased four life history strategies: Generalist, and D, revealing the influence of habitat since the 1980s. There are examples of weedy, competitive, and stress-tolerant. on zooxanthellae associations (Baums et increasing trends in some locations (Dry The classifications were primarily al., 2010). Tortugas and southeast Florida), but not separated by colony morphology, The public comments did not provide over larger spatial scales or longer time growth rate, and reproductive mode. new or supplemental biological frames. Population model projections Acropora cervicornis was classified as a information on A. cervicornis, and we from Honduras at one of the only ‘‘competitive’’ species, thus likely more did not find any new or supplemental known-remaining thickets indicate the vulnerable to environmental stress. biological information. All information retention of this dense stand under All information on A. cervicornis’ life on A. cervicornis’ biology can be undisturbed conditions. If refuge history can be summarized as follows. summarized as follows. Connectivity populations are able to persist, it is The combination of rapid skeletal over distances of greater than 500 km is unclear whether they would be able to growth rates and frequent asexual limited, and there is evidence of repopulate nearby reefs as observed reproduction by fragmentation can restricted gene flow over much smaller sexual recruitment is low. Thus, we enable effective competition and can spatial scales. Genetic diversity appears conclude that the species has undergone facilitate potential recovery from to be relatively high in some areas like substantial population decline and disturbances when environmental the Florida Keys. decreases in the extent of occurrence conditions permit. However, low sexual Susceptibility to Threats throughout its range. Percent benthic reproduction can lead to reduced cover and proportion of reefs where A. genetic diversity and limits the capacity Information on threat susceptibilities cervicornis is dominant have remained to repopulate sites. was interpreted in the proposed rule for stable since the mid-1980s and since the Other biological information on A. A. cervicornis’ vulnerabilities to threats listing of the species as threatened in cervicornis that we considered in the as follows: High vulnerability to ocean 2006. We also conclude that population proposed rule includes the following. warming, disease, acidification, abundance is at least tens of millions of Vollmer and Palumbi (2007) examined sedimentation, and nutrient enrichment; colonies, but likely to decrease in the 22 populations of A. cervicornis from moderate vulnerability to the trophic future with increasing threats. nine regions in the Caribbean (Panama, effects of fishing and predation; and low Belize, Mexico, Florida, Bahamas, Turks vulnerability to sea level rise and Other Biological Information and Caicos, Jamaica, Puerto Rico, and collection and trade. Information on A. cervicornis’ life Curac¸ao) and concluded that Information on A. cervicornis’ history that we considered in the populations greater than 500 km apart susceptibility to disease that we proposed rule includes the following. are genetically differentiated with low considered in the proposed rule Acropora cervicornis is a gene flow across the greater Caribbean. includes the following. Disease is hermaphroditic broadcast spawning Fine-scale genetic differences have been believed to be the primary cause of the species. The spawning season occurs detected at reefs separated by as little as region-wide decline of A. cervicornis several nights after the full moon in 2 km, suggesting that gene flow in A. beginning in the late 1970s (Aronson July, August, or September, but may be cervicornis may not occur at much and Precht, 2001) and continues to have split over the course of more than one smaller spatial scales (Garcia Reyes and a large impact on the species. White lunar cycle (Szmant, 1986; Vargas-Angel Schizas, 2010; Vollmer and Palumbi, band disease is generally associated

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with the majority of disease-related Supplemental information we found seasonally between March 2000 and mortalities, but several other diseases on the susceptibility of A. cervicornis to August 2004, showed that colonies of A. affect A. cervicornis. Ritchie and Smith disease includes the following. In cervicornis were stable with their (1995; 1998) described white band Honduras, diseases were present in 32 associations with Symbiodinium type disease type II which is linked with a percent of colonies (n = 181) monitored A3 but sometimes had mixed symbiosis bacterial infection by Vibrio carchariae annually from 1996 to 2005 (Riegl et al., with Symbiodinium type (B1) (Thornhill (Ritchie and Smith, 1998), also referred 2009). Between zero and 30 percent of et al., 2006). The associations with to as V. charchariae and V. harveyi (Gil- A. cervicornis colonies monitored in the Symbiodinium type (B1) were always Agudelo et al., 2006). Williams and middle Florida Keys were affected by short-lived (gone by next sampling Miller (2005) reported an outbreak of a disease from 2011 to 2012 (Lunz, 2013). period) and did not appear to be transmissible disease that caused rapid About five percent were affected by correlated with seasonal fluctuations or tissue loss on A. cervicornis in the rapid tissue loss during each quarterly to follow the 1997 to 1998 bleaching Florida Keys in 2003. The disease monitoring period (Lunz, 2013). event (Thornhill et al., 2006). Most of manifested as irregular, multifocal All information on the susceptibility the mixed symbiosis events were tissue lesions with apparently healthy of A. cervicornis to disease can be limited to a single colony except for one tissue remaining in between, a summarized as follows. Acropora sampling period in August 2001 when description similar to A. palmata cervicornis is highly susceptible to all colonies at one of the Bahamian sites afflicted with white pox. Additionally disease as evidenced by the mass- had mixed symbionts. ciliate infections have been reported by mortality event in the 1970s and 1980s. The public comments did not provide Croquer et al. (2006) at several locations Although disease is both spatially and new or supplemental information on the in the Caribbean. temporally variable, about five to six susceptibility of A. cervicornis to ocean Few studies follow the progression of percent of A. cervicornis colonies warming. Supplemental information we disease in individual colonies over time, appear to be affected by disease at any found on the susceptibility of A. but there are reports of instantaneous one time, though incidence of disease cervicornis to ocean warming includes levels of disease at various locations. has been reported to range from zero to the following. In Roatan, Honduras, The Acropora Biological Review Team 32 percent and up to 72 percent during Riegl et al. (2009) monitored A. (2005) reported that in the 1997 to 2000 an outbreak. There is indication that cervicornis and found none were AGRRA surveys, at least 6 percent of A. some colonies may be resistant to white bleached fully during the 1998 band disease. Acropora cervicornis is cervicornis colonies were diseased, with bleaching event, with the fourth highest also susceptible to several diseases greater prevalence documented from the partial bleaching frequency, and the including one that causes rapid tissue Turks and Caicos (21 percent), Cayman highest mortality of 22 species loss from multi-focal lesions. Because Islands (20 percent), U.S. Virgin Islands monitored. During the 2005 bleaching few studies track diseased colonies over (13 percent), and Cuba (8 percent). No event with 17 species observed, only A. time, determining the present-day disease was recorded on A. cervicornis cervicornis and A. palmata bleached colony and population level effects of in Jamaica, Mexico, Netherlands 100 percent (all colonies bleached disease is difficult. One study that Antilles, Panama, and Venezuela during completely white) at two reefs in monitored individual colonies during the 1997 to 2000 AGRRA surveys Jamaica with 90 percent mortality at one an outbreak found that disease can be a site and 10 percent at the other (Quinn (Acropora Biological Review Team, major cause of both partial and total and Kojis, 2008). 2005). Between 2001 and 2002, disease colony mortality (Williams and Miller, was detected at all monitored thickets 2005). Thus, we conclude that A. Van Woesik et al. (2012) developed a off Ft. Lauderdale, Florida with cervicornis is highly susceptible to coral resiliency index based on mortality ranging from 0.1 to 7.5 percent disease. biological traits and processes to per site and a mean of 1.8 percent of Information on A. cervicornis’ evaluate extinction risk due to colony surface area affected (Vargas- susceptibility to ocean warming that we bleaching. Evaluations were performed Angel et al., 2003). Evidence of white considered in the proposed rule at the genus level with genera separated band disease was observed on 5.3 includes the following. Acropora between the Caribbean and Indo-Pacific. percent of A. cervicornis colonies in cervicornis was one of the most heavily They reported A. cervicornis as highly February 2010 at Cabezos del Cayo, affected species during a 1987 to 1988 vulnerable to extinction due to Dominican Republic (Lirman et al., bleaching event in the Cayman Islands bleaching. 2010a). During a disease outbreak in the with 100 percent of colonies bleached All information on the susceptibility Florida Keys in 2003, 72 percent of the on the deep reef terrace (18 to 29 m of A. cervicornis to ocean warming can 20 tagged A. cervicornis colonies were depth) and 83 percent bleached on the be summarized as follows. Acropora infected; 28 percent of these suffered shallow reef terrace (Ghiold and Smith, cervicornis is highly susceptible to complete mortality while many more 1990). In Puerto Rico, about 75 percent bleaching in comparison to other coral colonies ended up as remnants of live of A. cervicornis colonies bleached at 12 species, and mortality after bleaching tissue (less than 10 percent of colony monitored sites during the 2005 events is variable. Algal symbionts did alive; Williams and Miller, 2005). Caribbean bleaching event (Waddell and not shift in A. cervicornis after the 1998 The public comments provided the Clarke, 2008). At Culebra Island, Puerto bleaching event, indicating the ability of following supplemental information on Rico approximately 90 percent of the A. this species to acclimatize to rising the susceptibility of A. cervicornis to cervicornis colonies had partial or total temperatures may not occur through disease. No disease was detected in mortality during and after the 2005 this mechanism. Data from Puerto Rico stratified random surveys in the Florida bleaching event, and bleaching stress and Jamaica following the 2005 Keys in 2007 (Miller et al., 2013). and mortality are believed to have Caribbean bleaching event indicate that Vollmer and Kline (2008) found that six resulted in the reproductive failure to temperature anomalies can have a large percent of A. cervicornis genotypes subsequently spawn in 2006 (Waddell impact on total and partial mortality (three out of 49) were resistant to white and Clarke, 2008). and reproductive output. Thus, we band disease during in situ transmission Repeat sampling of colonies in the conclude that A. cervicornis is highly assays in Bocas del Toro, Panama. Florida Keys and Bahamas in 1998, and susceptible to ocean warming.

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Information on A. cervicornis’ recruitment habitat is limited. Thus, we were more algae on the branches and susceptibility to acidification that we conclude that A. cervicornis has some further disintegration of branch tips. considered in the proposed rule susceptibility to the trophic effects of Fossil material collected from Bocas includes the following. Renegar and fishing due to its low recruitment rates. del Toro, Panama indicated that A. Riegl (2005) performed laboratory However, the available information does cervicornis declined in lagoonal areas experiments to examine the effect of not support a more precise description prior to 1960, coincident with intensive nutrients and carbon dioxide on A. of susceptibility to this threat. land clearing, and continued to decline cervicornis growth. They found All information on A. cervicornis’ offshore after 1960, with community significantly reduced growth under susceptibility to sedimentation that we structure more tolerant of turbid carbon dioxide levels of 700 to 800 considered in the proposed rule conditions (Cramer et al., 2012). matm, predicted to occur this century, includes the following. Exposure to The public comments did not provide compared to controls. In addition, when drilling mud reduced calcification rates new or supplemental information on A. elevated carbon dioxide was combined and protein concentrations in A. cervicornis’ susceptibility to with increased nitrate and phosphate, cervicornis, and exposure to equivalent sedimentation, and we did not find any growth rates were further reduced. The concentrations of kaolin produced no new or supplemental information. All effect of combined nitrate, phosphate, drop in proteins and a lower drop in information on the susceptibility of A. and carbon dioxide appeared to be calcification rate, indicating the toxic cervicornis to sedimentation can be antagonistic at lower nutrient effects of drilling mud are not due solely summarized as follows. Acropora concentrations and additive at higher to increases in turbidity (Kendall et al., cervicornis is susceptible to concentrations (compared to those 1983). sedimentation through its sensitivity to nutrients paired with carbon dioxide Acropora cervicornis has poor turbidity, and increased run-off from separately). All corals in the combined capacity to remove coarser sediments land clearing has resulted in mortality nitrate, phosphate, and carbon dioxide (250–2000 mm) and only slightly more of this species. In addition, laboratory treatment experienced total mortality, capacity for removing finer sediments studies indicate the combination of indicating the severe stress this (62–250 mm; Hubbard and Pocock, sedimentation and nutrient enrichment combination induced. 1972). Water movement (turbulence) appears to be worse than the effects of The public comments did not provide and gravity are probably more important either of these two stressors alone. Thus, new or supplemental information on the in removing sediments from this species we conclude that A. cervicornis has high susceptibility of A. cervicornis to than its capabilities of sloughing susceptibility to sedimentation. acidification. Supplemental information sediments in still water (Porter, 1987). Information on A. cervicornis’ we found on the susceptibility of A. In field experiments in Puerto Rico, A. susceptibility to nutrient enrichment cervicornis to acidification includes the cervicornis was less sensitive to single that we considered in the proposed rule following. Enochs et al. (2014) applications (200 mg per cm2, 400 mg includes the following. Renegar and examined the effects of carbon dioxide per cm2, and 800 mg per cm2) of coarse Riegl (2005) performed laboratory and light intensity on A. cervicornis. sediment (mean grain size 0.5 mm) than experiments to examine the effect of They found that carbon dioxide levels A. palmata and Orbicella annularis, nutrients and carbon dioxide on A. projected to occur by the end of the likely due to morphology that facilitated cervicornis growth. Under the nutrient century from ocean acidification caused passive sediment removal, though some treatments alone, A. cervicornis reduced calcification and skeletal bleaching near the base of the colonies experienced significantly lower growth density but no change in linear did occur (Rogers, 1983). rates under the higher nitrate and higher extension, surface area, or volume. High Lab experiments testing the effects of phosphate treatments, though not under light intensity did not ameliorate sedimentation and phosphate on A. the lower levels, and the combined reductions in calcification, and the cervicornis indicated that sediment- nitrate and phosphate treatment authors concluded that the high light clearing rates declined with increased produced significantly lower growth intensity necessary to reach saturation exposure from less than two hours to up under both the low and high levels. All of photosynthesis and calcification in A. to 24 hours after four weeks of corals in the combined nitrate, cervicornis may limit the effectiveness treatment. Treatments resulted in phosphate, and carbon dioxide of this potentially protective degenerative changes to tissue, treatment experienced total mortality, mechanism. zooxanthellae, and gonad development indicating the severe stress this All information on the susceptibility and were more severe in sediment and combination induced. of A. cervicornis to acidification can be sediment plus phosphate treatments in Lab experiments testing the effects of summarized as follows. Acropora comparison to controls and phosphate sedimentation and phosphate on A. cervicornis is susceptible to alone (Hodel and Vargas-Angel, 2007). cervicornis indicated that degenerative acidification through reduced growth, Acropora cervicornis is sensitive to changes to tissue, zooxanthellae, and calcification, and skeletal density, and turbidity because it is highly reliant on gonad development were more severe in the effects of increased carbon dioxide sunlight for nutrition (Lewis, 1977; sediment plus phosphate treatments in combined with increased nutrients Porter, 1976). Rogers (1979) shaded a 20 comparison to controls and phosphate appear to be much worse than either m2 area of reef as a partial simulation of alone (Hodel and Vargas-Angel, 2007). stressor alone, and caused 100 percent conditions from turbidity and found The public comments did not provide mortality in some combination in one that A. cervicornis was the first species new or supplemental information on the laboratory study. Therefore, we to respond by bleaching. Three weeks susceptibility of A. cervicornis to conclude that A. cervicornis is highly after shading was initiated, most nutrient enrichment, and we did not susceptible to acidification. colonies of A. cervicornis were find any new or supplemental There is no species-specific bleached. After shading was terminated information on its susceptibility to this information on the trophic effects of at five weeks, at the sixth week, most threat. All information on the fishing on A. cervicornis. However, due branches were dead and covered with susceptibility of A. cervicornis to to the level of reef fishing conducted in algae with growth tips deteriorating or nutrient enrichment can be summarized the Caribbean, coupled with Diadema grazed away, but a few branches as follows. Elevated nutrients can cause die-off and lack of significant recovery, recovered. After seven weeks, there decreased growth in A. cervicornis. The

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combined effects of nutrients with other percent of A. cervicornis colonies in threats to all corals. However, we did stressors such as elevated carbon 2010 (Lirman et al., 2010a). In not provide any species-specific dioxide and sedimentation appear to be permanent monitoring plots in the information on the regulatory worse than the effects of nutrients alone, middle Florida Keys between 2011 and mechanisms or conservation efforts for and can cause colony mortality in some 2012, about ten percent of fate-tracked A. cervicornis. Public comments were combinations. Thus, we conclude that A. cervicornis colonies were affected by critical of that approach, and we A. cervicornis is highly susceptible to fireworm predation, about five percent therefore attempt to analyze regulatory nutrient enrichment. were affected by damselfish, and about mechanisms and conservation efforts on Information on A. cervicornis’ five percent were affected by a species basis, where possible, in this susceptibility to predation that we corallivorous snails (Lunz, 2013). final rule. We also incorporate here, the considered in the proposed rule All information on the susceptibility evaluation of threats to this species includes the following. Known of A. cervicornis to predation can be conducted in the 2005 status review. predators of A. cervicornis include the summarized as follows. Predators can Records confirm that A. cervicornis corallivorous snail Coralliophila have a negative impact on A. cervicornis occurs in seven Atlantic ecoregions that abbreviata and the polychaete fireworm through both tissue removal and the encompass 26 kingdom’s and countries’ Hermodice carunculata. Fireworms spread of disease. Predation pressure EEZs. The 26 kingdoms and countries engulf growing branch tips and devour appears spatially variable. Removal of are Antigua & Barbuda, Bahamas, the live tissue; removal of tissue from tissue from growing branch tips of A. Barbados, Belize, Colombia, Costa Rica, growing branch tips of A. cervicornis cervicornis may negatively affect colony Cuba, Dominica, Dominican Republic, may negatively affect colony growth. growth, but the impact is unknown as French Antilles, Grenada, Guatemala, Corallivorous snails have also been most studies do not report on the same Haiti, Kingdom of the Netherlands, shown to transmit a disease that causes colonies through time, inhibiting Honduras, Jamaica, Mexico, Nicaragua, rapid tissue loss in A. cervicornis evaluation of the longer-term impact of Panama, St. Kitts & Nevis, St. Lucia, St. (Williams and Miller, 2005). Several these predators on individual colonies Vincent & Grenadines, Trinidad and species of fish including, threespot and populations. We conclude that A. Tobago, United Kingdom (British damselfish Stegastes planifrons and cervicornis is highly susceptible to Caribbean Territories), United States yellowtail damselfish Microspathodon predation. (including U.S. Caribbean Territories), chrysurus, do not directly feed on coral Information on A. cervicornis’ and Venezuela. The regulatory but remove live tissue to cultivate algal susceptibility to collection and trade mechanisms relevant to A. cervicornis, gardens. that we considered in the proposed rule described first as a percentage of the In all thickets monitored off Ft. includes the following. Over the last above kingdoms and countries that Lauderdale, Florida between 2001 and decade, collection and trade of this utilize them to any degree, and second 2002, densities of fireworms ranged species has been low. as the percentages of those kingdoms between 18 and 86 individuals per The public comments did not provide and countries whose regulatory hectare, with predation scars affecting new or supplemental information on the mechanisms may be limited in scope, less than 0.2 percent of the A. susceptibility of A. cervicornis to are as follows: General coral protection cervicornis cover (Vargas-Angel et al., collection and trade. Supplemental (31 percent with 12 percent limited in 2003). Within the survey quadrats, information we found includes the scope), coral collection (50 percent with fireworm scar sizes ranged from 1.0 to following. Over the last decade, 27 percent limited in scope), pollution 8.0 cm, and densities ranged from 0 to collection and trade of this species has control (31 percent with 15 percent 30 per m2 (Vargas-Angel et al., 2003). been primarily for scientific research limited in scope), fishing regulations on Evidence of fireworm predation was rather than commercial purposes. Gross reefs (73 percent with 50 percent observed on 20.3 percent of colonies in exports averaged approximately 2,500 limited in scope), managing areas for Cabezos del Cayo, Dominican Republic pieces of coral per year between 2000 protection and conservation (88 percent in 2010 (Lirman et al., 2010a). and 2012 (data available at http:// with 31 percent limited in scope). The Yellowtail damselfish and three-spot trade.cites.org). We conclude that A. most common regulatory mechanisms in damselfish were present on A. cervicornis has low susceptibility to place for A. cervicornis are fishing cervicornis colonies at a density of 0.50 collection and trade. and 0.96 fish per m2, respectively, in the There is no species-specific regulations and area management for Dry Tortugas National Park, near Garden information on the susceptibility of A. protection and conservation. However, Key, Florida in 2004 (Wilkes et al., cervicornis to sea level rise. The SRR half of the fishing regulations are 2008). described sea level rise as an overall low limited in scope and may not provide The public comments provided the to medium threat for all coral species. substantial protection for the species. following supplemental information on The public comments did not provide General coral protection and collection the susceptibility of A. cervicornis to new or supplemental information on A. laws, along with pollution control laws, predation. In stratified random samples cervicornis’ susceptibility to sea level are much less common regulatory in the Florida Keys, damselfish algal rise, and we did not find any new or mechanisms for the management of A. gardens were detected on 1.9 percent of supplemental information. Thus, we cervicornis. The 2005 status review and colonies in 2007 and 2.6 percent of conclude that A. cervicornis has some 2006 listing concluded that existing colonies in 2012. Snail predation was susceptibility to sea level rise, but the regulatory mechanisms are inadequate detected on 1.3 percent of colonies in available information does not support to control both global and local threats, 2012 (Miller et al., 2013). a more precise description of and are contributing to the threatened Supplemental information we found susceptibility to this threat. status of the species, and we incorporate on the susceptibility of A. cervicornis to that analysis here. predation includes the following. In Regulatory Mechanisms Additionally, the public comments Cabezos del Cayo, Dominican Republic, In the proposed rule, we relied on suggested that we did not fully consider 30 percent of colonies occurred within information from the Final Management the effects that conservation efforts have established damselfish territories, and Report for evaluating the existing on the status of A. cervicornis. corallivorous snails were found on 11.3 regulatory mechanisms for controlling Therefore, conservation efforts are

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described as follows. Conservation Allee effect (in which fertilization previous determination, we identified efforts have been underway for A. success declines greatly as adult density ocean acidification only as a factor that cervicornis for a number of years. Of 60 declines). ‘‘may be contributing’’ to the status of Acropora restoration efforts identified The species was not listed as two species, in comparison to our in 14 Caribbean countries, 88 percent endangered, i.e., currently in danger of current understanding that ocean used A. cervicornis including efforts in extinction, because: (1) It was showing acidification is one of the three highest Belize, Colombia, Curac¸ao, Dominican limited, localized recovery; (2) range- order threats affecting extinction risk for Republic, Guadalupe, Honduras, wide, the rate of decline appeared to corals. Jamaica, Mexico, Puerto Rico, Turks and have stabilized and was comparatively As explained above in the Risk Caicos, U.S. Virgin Islands, and the slow as evidenced by persistence at Analyses section, a species’ Florida Keys (Young et al., 2012). The reduced abundances for the past two vulnerability to extinction results from most popular method is to use coral decades; (3) it was buffered against the combination of its spatial and nurseries to propagate A. cervicornis for major threats by the large number of demographic traits, threat restoration (Johnson et al., 2011; Young colonies, large geographic range, and susceptibilities, and consideration of the et al., 2012). Fast growth rates, asexual reproduction; and (4) as shown baseline environment and future branching morphology, and asexual by the geologic record, the species has projections of threats. Subsequent to the reproduction through fragmentation persisted through climate cooling and proposed rule, we received and gathered make A. cervicornis an ideal candidate heating fluctuation periods over supplemental species- or genus-specific for active propagation. The use of coral millions of years, whereas other corals information, described above, that nursery techniques has been shown to have gone extinct. expands our knowledge regarding the be effective and only temporarily affect In 2012, A. cervicornis was proposed species’ abundance, distribution, and wild donor colonies from which for listing as endangered because threat susceptibilities. We developed fragments are taken to initially stock information available since the original our assessment of the species’ nurseries (Lirman et al., 2010b). 2006 listing as threatened suggested: (1) vulnerability to extinction using all the Survivorship is high (greater than 70 Population declines have continued to available information. As explained in percent) in nurseries during the first occur, with certain populations of both the Risk Analyses section, our year, but mortality due to storms, species decreasing up to an additional assessment in this final rule emphasizes temperature anomalies, predation, and 50 percent or more since the time of the ability of the species’ spatial and water quality have been reported listing; (2) there are documented demographic traits to moderate or (Young et al., 2012). Survival rates are instances of recruitment failure in some exacerbate its vulnerability to variable after transplanting, ranging populations; (3) minimal levels of extinction, as opposed to the approach between 43 and 95 percent during the thermal stress (e.g., 30 degrees C) have we used in the proposed rule, which first year (Hollarsmith et al., 2012; been shown to impair larval emphasized the species’ susceptibility Young et al., 2012). Mortality rates of development, larval survivorship, and to threats. non-nursery raised transplanted A. settlement success of A. palmata; (4) The following characteristics of A. cervicornis after five years were similar near-future levels of acidification have cervicornis, in conjunction with the to those of reference or wild colonies been demonstrated to impair information described in the Corals and (Garrison and Ward, 2008). fertilization, settlement success, and Coral Reefs section, Coral Habitat sub- In conclusion, there are many post-settlement growth rates in A. section, and Threats Evaluation section conservation efforts aimed at increasing palmata; (5) on average 50 percent of above, affect its vulnerability to abundance and diversity of A. the colonies are clones, meaning the extinction currently and over the cervicornis throughout the Caribbean. effective number of genetic individuals foreseeable future. The species has These efforts are important, but not is half the total population size; (6) the undergone substantial population enough to ensure conservation unless species’ ranges are not known to have decline and decreases in the extent of combined with efforts to reduce the contracted, but with continued declines occurrence throughout its range due underlying threats and causes of local extirpations are likely, resulting in mostly to disease. Although localized mortality (Young et al., 2012). Thus, a reduction of absolute range size. mortality events have continued to while conservation efforts will likely Furthermore, we took into account that occur, percent benthic cover and enhance recovery and conservation of the BRT identified restriction to the proportion of reefs where A. cervicornis A. cervicornis at small spatial scales, Caribbean as a spatial factor increasing is dominant have remained stable over they are unlikely to affect the overall extinction risk, though, among other its range since the mid-1980s. There is status of the species, given the global things, exposure to high levels of human evidence of synergistic effects of threats nature of threats. disturbance that result in pollution and for this species including worse effects breakage impacts. Also, while asexual of nutrients in combination with Vulnerability to Extinction reproduction (fragmentation) provides a acidification and sedimentation. In 2006, A. cervicornis was listed as source for new colonies (albeit clones) Acropora cervicornis is highly threatened, i.e., likely to become in that can buffer natural demographic and susceptible to a number of threats, and danger of extinction within the next 30 environmental variability remains true, cumulative effects of multiple threats years, due to: (1) Recent drastic declines we believed that reliance on asexual are likely to exacerbate vulnerability to in abundance of the species that have reproduction is not sufficient to prevent extinction. Despite the large number of occurred throughout its geographic extinction of the species. Last, the islands and environments that are range and abundances at historic lows; previous status review and listing included in the species’ range, (2) the potential constriction of broad determination underestimated the geographic distribution in the highly geographic ranges due to local global climate change-associated disturbed Caribbean exacerbates extirpations resulting from a single impacts to A. palmata and A. vulnerability to extinction over the stochastic event (e.g., hurricanes, new cervicornis, based on our current foreseeable future because A. cervicornis disease outbreak); (3) limited sexual knowledge of trends in emissions, likely is limited to an area with high, localized recruitment in some areas and unknown warming scenarios, and ocean human impacts and predicted levels in most; and (4) occurrence of the acidification. In particular, in the increasing threats. Acropora cervicornis

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commonly occurs in water ranging from the buffering capacity of this species’ vulnerability to extinction currently 5 to 20 m in depth, though occurs in spatial and demographic traits, and the because the species is not limited to one deeper depths of 16–30 m at the best available information above on A. habitat type but occurs in numerous northern extent of its range, and has cervicornis’ spatial structure, types of reef environments that will been rarely found to 60 m in depth. It demography, threat susceptibilities, and experience highly variable thermal occurs in spur and groove, bank reef, management. The combination of these regimes and ocean chemistry on local patch reef, and transitional reef habitats, factors indicates that A. cervicornis is and regional scales at any given point in as well as on limestone ridges, terraces, likely to become endangered throughout time, as described in more detail in the and hardbottom habitats. This habitat its range within the foreseeable future, Coral Habitat and Threats Evaluation heterogeneity moderates vulnerability to and thus warrants listing as threatened sections; extinction over the foreseeable future at this time, because: (2) Acropora cervicornis’ absolute because the species occurs in numerous (1) Acropora cervicornis is highly abundance is at least tens of millions of types of reef environments that are susceptible to ocean warming (ESA colonies based on estimates from two predicted, on local and regional scales, Factor E), disease (C), ocean locations. Absolute abundance is higher to experience highly variable thermal acidification (E), sedimentation (A, E), than estimates from these locations regimes and ocean chemistry at any nutrients (A, E), and predation (C) and since A. cervicornis occurs in many given point in time. Its absolute susceptible to trophic effects of fishing other locations throughout its range, population abundance has been (A), depensatory population effects from including a few small pockets of robust estimated as at least tens of millions of rapid, drastic declines and low sexual remnant populations. This absolute colonies in the Florida Keys and Dry recruitment (E), and anthropogenic and abundance allows for variation in the Tortugas combined and is higher and is natural abrasion and breakage (A, E). responses of individuals to threats to higher than the estimate from these two These threats are expected to continue play a role in moderating vulnerability locations due to the occurrence of the and increase into the future. In addition, to extinction for the species to some species in many other areas throughout the species is at heightened extinction degree, as described in more detail in its range. Acropora cervicornis has low risk due to inadequate existing the Corals and Coral Reefs section; sexual recruitment rates, which regulatory mechanisms to address both (3) Recent information indicates that exacerbates vulnerability to extinction local and global threats (D); percent cover and proportions of due to decreased ability to recover from (2) Acropora cervicornis is Caribbean sites where A. cervicornis is mortality events when all colonies at a geographically located in the highly dominant have stabilized; site are extirpated. In contrast, its fast disturbed Caribbean where localized (4) Acropora cervicornis shows growth rates and propensity for human impacts are high and threats are evidence of limited population formation of clones through asexual predicted to increase as described in the expansion in some portions of its range fragmentation enables it to expand Threats Evaluation section. A range under some circumstances (e.g., Dry between rare events of sexual constrained to this particular geographic Tortugas, southeast Florida); and recruitment and increases its potential area that is likely to experience severe (5) Acropora cervicornis has fast for local recovery from mortality events, and increasing threats indicates that a growth rates and high capacity to thus moderating vulnerability to high proportion of the population of this produce clones through asexual extinction. Its abundance and life species is likely to be exposed to those fragmentation, which can aid in history characteristics, combined with threats over the foreseeable future; and recovery from mortality events. spatial variability in ocean warming and (3) Acropora cervicornis’ abundance The combination of these acidification across the species’ range, is still a fraction of what it was before characteristics indicates that the species moderate vulnerability to extinction the mass mortality in the 1970s and does not exhibit the characteristics of because the threats are non-uniform, 1980s, and its presence on reefs one that is currently in danger of and there will likely be a large number throughout its range has continued to extinction, as described previously in of colonies that are either not exposed decrease over the last decade. the Risk Analyses section, and thus does or do not negatively respond to a threat The combination of these not warrant listing as endangered at this at any given point in time. characteristics and future projections of time. Therefore, we withdraw our threats indicates that the species is proposal to list A. cervicornis as Listing Determination likely to be in danger of extinction endangered. In the proposed rule, using the within the foreseeable future throughout Progress has been made with A. determination tool formula approach, A. its range and warrants listing as cervicornis-specific conservation and cervicornis was proposed for listing as threatened at this time due to factors A, restoration projects, albeit small-scale, endangered because of: High C, D, and E. and these projects are likely to increase vulnerability to ocean warming (E), The available information above on A. in the future. Within some countries, A. ocean acidification (E) and disease (C); cervicornis’ spatial structure, cervicornis-specific conservation and high vulnerability to sedimentation (A demography, threat susceptibilities, and restoration projects show promise for and E) and nutrient over-enrichment (A management also indicate that the enhancing species recovery at very and E); uncommon abundance (E); species is not currently in danger of small spatial scales and for facilitating decreasing trend in abundance (E); low extinction and thus does not warrant the persistence of the species in some relative recruitment rate (E); narrow listing as Endangered because: areas in the face of continuing threats. overall distribution (E); restriction to the (1) While A. cervicornis’ distribution Range-wide, a multitude of conservation Caribbean (E); and inadequacy of within the Caribbean increases its risk efforts are already broadly employed regulatory mechanisms (D). of exposure to threats as described specifically for A. cervicornis. However, In this final rule, we changed the above, its habitat includes spur and considering the global scale of the most listing determination for A. cervicornis groove, bank reef, patch reef, and important threats to the species, and the from endangered to threatened. We transitional reef habitats, as well as ineffectiveness of conservation efforts at made this determination based on a limestone ridges, terraces, and addressing the root cause of global more species-specific and holistic hardbottom habitats in water depths threats (i.e., GHG emissions), we do not approach, including consideration of ranging from 5 to 60 m. This moderates believe that any current conservation

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efforts or conservation efforts planned 12 m depth, it also occurs in back-reef at 10 to 20 m depth within the lagoon in the future will result in affecting the environments and in depths up to 30 m. of Serrano Bank (Sanchez and Pizarro, species’ status to the point at which Extensive stands of dead colonies 2005). listing is not warranted. throughout the range occurred after mass mortalities during the 1970s and Demographic Information A. palmata 1980s (see Demographic Information Information on A. palmata’s Introduction Below). There is no evidence of overall abundance and population trends that range constriction from the mass we considered in the proposed rule Acropora palmata colonies have mortalities, but local extirpations are includes the following. Acropora frond-like branches, which appear likely (Jackson et al., 2014), resulting in palmata has been described as usually flattened to near round, and typically a reduction of absolute range size. common (Veron, 2000) and uncommon radiate out from a central trunk and The public comments did not provide (Carpenter et al., 2008). Acropora angle upward. Branches are up to 50 cm new or supplemental information on A. palmata was historically one of the wide and range in thickness from 4 to palmata’s habitat or depth range but dominant species on Caribbean reefs, 5 cm. Individual colonies can grow to at provided the following supplemental forming large, monotypic thickets and least 2 m in height and 4 m in diameter information on its distribution. Precht giving rise to the nominal distinct zone (Acropora Biological Review Team, and Aronson (2004) suggested that the in classical descriptions of Caribbean 2005). Colonies of A. palmata can grow recent expansion of A. palmata to the reef morphology (Goreau, 1959). Mass in nearly mono-specific, dense stands Flower Garden Banks (Zimmer et al., mortality, apparently from white-band and form an interlocking framework 2006) is possibly due to climate disease (Aronson and Precht, 2001), known as thickets. warming. spread throughout the Caribbean in the Spatial Information Supplemental information we found mid-1970s to mid-1980s and on A. palmata’s distribution is precipitated widespread and radical Information on A. palmata’s consistent with prior information. Veron changes in reef community structure distribution, habitat, and depth range (2014) confirms the occurrence of A. (Brainard et al., 2011). This mass that we considered in the proposed rule palmata in eight of a potential 11 mortality occurred throughout the range includes the following. Acropora ecoregions in the western Atlantic and of the species within all Caribbean palmata is distributed throughout the wider-Caribbean that are known to countries and archipelagos, even on western Atlantic, Caribbean, and Gulf of contain corals. The three ecoregions in reefs and banks far from localized Mexico. The northern extent of the which A. palmata is not found are off human influence (Aronson and Precht, range in the Atlantic is Broward County, the coasts of Bermuda, Brazil, and the 2001; Wilkinson, 2008). In addition, Florida where it is relatively rare (only southeast U.S. north of south Florida. continuing coral mortality from periodic a few known colonies), but fossil A. The presence of the species in the acute events such as hurricanes, disease palmata reef framework extends into Flower Garden Banks may represent a outbreaks, and mass bleaching events Palm Beach County, Florida. There are recent re-occupation of its historic range added to the decline of A. palmata two known colonies of A. palmata, since fossil evidence indicates this (Brainard et al., 2011). In locations which were discovered only recently in species occupied the Flower Garden where historic quantitative data are 2003 and 2005, at the Flower Garden Banks during the early Holocene but available (Florida, Jamaica, U.S. Virgin Banks, located 161 km off the coast of disappeared in the middle Holocene Islands), there was a reduction of greater Texas in the Gulf of Mexico (Zimmer et due to sea level rise and possibly than 97 percent between the 1970s and al., 2006). cooling temperatures (Precht et al., early 2000s (Acropora Biological Acropora palmata often grows in 2014). Finally, the spatial structure of Review Team, 2005). thickets in fringing and barrier reefs the species has been affected by Since the 2006 listing of A. palmata (Jaap, 1984; Tomascik and Sander, 1987; extirpation from many localized areas as threatened, continued population Wheaton and Jaap, 1988) and formed throughout its range (Jackson et al., declines have occurred in some extensive barrier-reef structures in 2014). locations with certain populations of A. Belize (Cairns, 1982), the greater and Supplemental information we found palmata and A. cervicornis decreasing lesser Corn Islands, Nicaragua (Lighty et on A. palmata’s habitat and depth up to an additional 50 percent or more al., 1982), and Roatan, Honduras, and includes the following. Goreau (1959) (Colella et al., 2012; Lundgren and built extensive fringing reef structures described ten habitat zones on a Hillis-Starr, 2008; Muller et al., 2008; throughout much of the Caribbean Jamaican fringing reef from inshore to Rogers and Muller, 2012; Williams et (Adey, 1978). Acropora palmata the deep slope, finding A. palmata in al., 2008). In addition, Williams et al. commonly grows in turbulent water on eight of the ten zones. Acropora (2008) reported recruitment failure the fore-reef, reef crest, and shallow palmata was very abundant in the reef between 2004 and 2007 in the upper spur-and-groove zone (Cairns, 1982; crest zones, but also common in several Florida Keys after a major hurricane Miller et al., 2008; Rogers et al., 1982; other zones further inshore (the reef flat, season in 2005; less than five percent of Shinn, 1963) in water ranging from 1 to rear, channel or lagoon, and inshore the fragments produced recruited into 5 m depth. Early studies termed the reef zones), and rare on the reef slope to 15 the population. crest and adjacent seaward areas from meters depth. Although A. palmata is The public comments provided the the surface to five or six meters depth currently much less common following supplemental information on the ‘‘palmata zone’’ because of the throughout its range than it was prior to A. palmata’s abundance and population domination by the species (Goreau, the mid-1980s, it still occurs in multiple trends. Several studies describe A. 1959; Shinn, 1963). Maximum depth of habitats and to depths of one to 30 m. palmata populations that are showing framework construction ranges from 3 to For example, a 2005 study of Bonaire some signs of recovery or are in good 12 m, and colonies generally do not back-reefs found A. palmata at three of condition including in the Turks and form thickets below a depth of 5 m six sites, including within inshore and Caicos Islands (Schelten et al., 2006), (Lighty et al., 1982). Although A. lagoon habitats, ranging from seven to U.S. Virgin Islands (Grober-Dunsmore et palmata’s predominant habitat is reef 15 m depth. In 2003, aggregations of A. al., 2006; Mayor et al., 2006; Rogers and crests and shallow fore-reefs less than palmata were reported from patch reefs Muller, 2012), Venezuela (Zubillaga et

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al., 2008), and Belize (Macintyre and Puerto Rico contains the greatest Supplemental information we found Toscano, 2007). known extent of A. palmata in the U.S. on A. palmata’s population trends Extrapolated population estimates of Caribbean. Between 2006 and 2007, a includes the following. At eight of 11 A. palmata from stratified random survey of 431 random points in habitat sites in St. John, U.S. Virgin Islands, samples across habitat types in the suitable for A. palmata in six marine colonies of A. palmata increased in Florida Keys were 0.6 ± 0.5 million (SE) protected areas in Puerto Rico revealed abundance, between 2001 and 2003, colonies in 2005, 1.0 ± 0.3 million (SE) a variable density of zero to 52 A. particularly in the smallest size class, colonies in 2007, and 0.5 ± 0.3 million palmata colonies per 100 m2 (0.52 with the number of colonies in the colonies in 2012. Because these colonies per m2), with average density largest size class decreasing (Grober- population estimates are based on of 3.3 colonies per 100 m2 (0.03 colonies Dunsmore et al., 2006). Colonies of A. random sampling, differences between per m2). Total loss of A. palmata was palmata monitored monthly between years may be a function of sampling evidenced in 13.6 percent of the random 2003 and 2009 in Haulover Bay on St. effort rather than an indication of survey areas where only dead standing John, U.S. Virgin Islands suffered population trends. Relative to the colonies were present (Scha¨rer et al., bleaching and mortality from disease abundance of other corals in the Florida 2009). but showed an increase in abundance Keys region, A. palmata was among the In stratified random surveys along the and size at the end of the monitoring least abundant, ranking among corals south, southeast, southwest, and west period (Rogers and Muller, 2012). The that are naturally rare in abundance. No coasts of Puerto Rico designed to locate overall density of A. palmata colonies colonies of A. palmata were observed in Acropora colonies, A. palmata was around St. John did not significantly surveys of the Dry Tortugas in 2006 and observed at five out of 301 stations with differ between 2004 and 2010 with six 2008. The size class distribution of the sightings outside of the survey area at an out of the ten sites showing an increase Florida Keys population included both additional two stations (Garcı´a Sais et in colony density. Size frequency small and large individuals (> 260 cm), al., 2013). Acropora palmata colonies distribution did not significantly change but after 2005 the majority of the were absent from survey sites along the at seven of the 10 sites, with two sites colonies were smaller in size. These southeast coast. Maximum density was showing an increased abundance of smallest corals (0 to 20 cm) had 18 colonies per 15 m2 (1.2 colonies per large-sized (> 51 cm) colonies (Muller et approximately zero to two percent m2), and maximum colony size was 2.3 al., 2014). partial mortality during all three survey m in diameter (Garcı´a Sais et al., 2013). In Colombia, A. palmata was present years. Partial mortality across all other Zubillaga et al. (2005) report densities at four of the 32 plots (three of the six size classes was approximately 20 to 70 of 3.2 colonies of A. palmata per 10 m2 reefs) monitored annually from 1998 to percent in 2005, 5 to 50 percent in 2007, (0.32 colonies per m2) in Los Roques 2004. Coverage of A. palmata ranged and 15 to 90 percent in 2012 (Miller et National Park, Venezuela. At ten sites from 0.8 to 2.4 percent. Over the eight- al., 2013). surveyed in the national park in 2003 to year period, the species was stable at Supplemental information we found 2004, density ranged from 0 to 3.4 two reefs and declined at the other reef, on A. palmata’s abundance includes the colonies per 10 m2 (0 to 0.34 colonies likely in response to a hurricane in 1999 following. Relatively abundant A. per m2) with four of the sites showing (Rodriguez-Ramirez et al., 2010). palmata communities have been only standing dead colonies (Zubillaga MacIntyre and Toscano (2007) report documented from various locations, et al., 2008). In the six sites with live the return of ‘‘numerous large colonies’’ including Cuba (Alcolado et al., 2010; colonies, small (0.1 to 50 cm2) and of A. palmata on the shallow fore-reef Gonza´lez-Dı´az et al., 2010), Colombia medium-sized (50 to 4,550 cm2) at the southern limit of Carrie Bow Cay, (Sanchez and Pizarro, 2005), Venezuela colonies predominated over larger-sized Belize though no quantitative data were (Martı´nez and Rodrı´guez Quintal, 2012), (4,550 to16,500 cm2) colonies. presented. Navassa (Bruckner, 2012b), Jamaica At Los Colorados reef in northwestern Colonies monitored in the upper (Jackson et al., 2014), and the U.S. Cuba, a 2006 study at 12 reef crest Florida Keys showed a greater than 50 Virgin Islands (Muller et al., 2014). sampling stations reported average A. percent loss of tissue as well as a Density estimates from sites in Cuba palmata densities of 0.18 colonies per decline in the number of colonies, and range from 0.14 colonies per m2 m2, and that A. palmata made up 8.7 a decline in the dominance by large (Alcolado et al., 2010) to 0.18 colonies percent of the total live coral colonies at colonies between 2004 and 2010 (Vardi per m2 (Gonza´lez-Dı´az et al., 2010). the study sites. The study also reported et al., 2012; Williams and Miller, 2012). Maximum A. palmata density at ten that the nearby Baracoa and Rincon de Elasticity analysis from a population sites in St. John, U.S. Virgin Islands was Guanabo reefs had similar A. palmata model based on data from the Florida 0.18 colonies per m2 (Muller et al., densities (Gonza´lez-Dı´az et al., 2010). Keys has shown that the largest 2014). The size of A. palmata colonies individuals have the greatest Mayor et al. (2006) reported the indicates some recruitment in Cuba, but contribution to the rate of change in abundance of A. palmata in Buck Island not the proportions of sexual versus population size (Vardi et al., 2012). Reef National Monument, St. Croix, U.S. asexual recruits. In a 2005 study of 280 Between 2010 and 2013 A. palmata in Virgin Islands. They surveyed 617 sites A. palmata colonies at four sites on the the middle and lower Florida Keys had from May to June 2004 and extrapolated north coast of Cuba, 30.4 percent were mixed trends. Population densities density observed per habitat type to less than 10 cm in diameter (Gonza´lez- remained relatively stable at two sites total available habitat. Within an area of Dı´az et al., 2008). In a 2006 study of and decreased at two sites by 21 and 28 795 ha, they estimated 97,232–134,371 approximately 1,100 A. palmata percent (Lunz, 2013). (95% confidence limits) A. palmata colonies at three sites on the north coast Acropora palmata monitored in colonies with any dimension of of Cuba, diameter and height size- Curac¸ao between 2009 and 2011 connected live tissue greater than one classes were measured (<2, 3–5, 6–7, 8– decreased in abundance, increased in meter. Mean densities (colonies ≥ 1 m) 10, 11–80, and >80 cm). For the three colony size, with stable tissue were 0.019 colonies per m2 in branching sites combined, there were abundance following hurricane damage coral-dominated habitats and 0.013 approximately 25 to 100 colonies in (Bright et al., 2013). The authors colonies per m2 in other hard bottom each of the four smaller size classes explained that the apparently habitats. (Perera-Pe´rez et al., 2012). conflicting trends of increasing colony

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size but similar tissue abundance likely The effective population size is smaller today than they were several decades resulted from the loss of small-sized than indicated by abundance estimates ago (Brainard et al., 2011). colonies that skewed the distribution to due to the tendency for asexual Acropora palmata is a hermaphroditic larger size classes, rather than colony reproduction. Across the Caribbean, broadcast spawning species that growth. percent cover appears to have remained reproduces after the full moon of July, Simulation models using data from relatively stable since the population August, and/or September (Acropora matrix models of A. palmata colonies crash in the 1980s. Frequency of Biological Review Team, 2005). The from specific sites in Curac¸ao (2006– occurrence has decreased since the estimated size at sexual maturity is 1600 2011), the Florida Keys (2004–2011), 1980s, indicating potential decreases in cm2, and growing edges and encrusting Jamaica (2007–2010), Navassa (2006 and the extent of occurrence and effects on base areas are not fertile (Soong and 2009), Puerto Rico (2007 and 2010), and the species’ range. However, the Lang, 1992). Larger colonies have higher the British Virgin Islands (2006 and proportions of Caribbean sites where A. fecundity per unit area, as do the upper 2007) indicate that most of these studied palmata is present and dominant have branch surfaces (Soong and Lang, 1992). populations will continue to decline in recently stabilized. There are locations Although self-fertilization is possible, A. size and extent by 2100 if background such as the U.S. Virgin Islands where palmata is largely self-incompatible environmental conditions remain populations of A. palmata appear stable (Baums et al., 2005a; Fogarty et al., unchanged (Vardi, 2011). In contrast, or possibly increasing in abundance and 2012b). the studied populations in Jamaica were some such as the Florida Keys where Reproduction occurs primarily projected to increase in abundance, and population number appears to be through asexual fragmentation that studied populations in Navassa were decreasing. In some cases when size produces multiple colonies that are projected to remain stable. Studied class distribution is not reported, there genetically identical (Bak and Criens, populations in the British Virgin Islands is uncertainty of whether increases in 1982; Highsmith, 1982; Lirman, 2000; were predicted to decrease slightly from abundance indicate growing Miller et al., 2007; Wallace, 1985). their initial very low levels. Studied populations or fragmentation of larger Storms can be an important mechanism populations in Florida, Curac¸ao, and size classes into more small-sized to produce fragments to establish new Puerto Rico were predicted to decline to colonies. From locations where size colonies (Fong and Lirman, 1995). zero by 2100. Because the study period class distribution is reported, there is Fragmentation is an important mode of did not include physical damage evidence of recruitment, but not the reproduction in many reef-building (storms), the population simulations in proportions of sexual versus asexual corals, especially for branching species Jamaica, Navassa, and the British Virgin recruits. The best evidence of recovery such as A. palmata (Highsmith, 1982; Islands may have contributed to the would come from multi-year studies Lirman, 2000; Wallace, 1985). However, differing projected trends at sites in showing an increase in the overall in the Florida Keys where populations have declined, there have been reports these locations. amount of living tissue of this species, New information we found on of failure of asexual recruitment due to growth of existing colonies, and an population trends includes the high fragment mortality after storms increase in the number of small corals following. A report on the status and (Porter et al., 2012; Williams and Miller, arising from sexual recruitment (Rogers trends of Caribbean corals over the last 2010; Williams et al., 2008). and Muller, 2012). Simulation models century indicates that cover of A. Sexual recruitment rates are low, and predict by 2100 that A. palmata will palmata has remained relatively stable this species is generally not observed in become absent at specific sites in at approximately one percent coral settlement studies. Laboratory several locations (Florida, Curacao, and throughout the region since the large studies have found that certain species Puerto Rico), decrease at specific sites in mortality events of the 1970s and 1980s. of crustose-coralline algae facilitate The report also indicates that the the British Virgin Islands, remain stable larval settlement and post-settlement number of reefs with A. palmata present at specific sites in Navassa, and increase survival (Ritson-Williams et al., 2010). steadily declined from the 1980s to at specific sites in Jamaica. These Rates of post-settlement mortality after 2000–2004, then remained stable simulations are based on the nine months are high based on between 2000–2004 and 2005–2011. assumption that conditions experienced settlement experiments (Szmant and Acropora palmata was present at about during the monitoring period, ranging Miller, 2005). 20 percent of reefs surveyed in both the from one to seven years depending on The public comments did not provide 5-year period of 2000–2004 and the 7- location, would remain unchanged in new or supplemental information on A. year period of 2005–2011. Acropora the future. We conclude there has been palmata’s life history. Supplemental palmata was dominant on a significant decline of A. palmata information we found on A. palmata’s approximately five to ten percent of throughout its range, with recent life history includes the following. Split hundreds of reef sites surveyed population stability at low percent spawning (spawning over a two month throughout the Caribbean during the coverage. We also conclude that period) has been reported from the four periods of 1990–1994, 1995–1999, absolute abundance is at least hundreds Florida Keys (Fogarty et al., 2012b). 2000–2004, and 2005–2011 (Jackson et of thousands of colonies, but likely to Laboratory experiments have shown al., 2014). decrease in the future with increasing that some individuals (i.e., genotypes) All information on A. palmata’s threats. are sexually incompatible (Baums et al., abundance and population trends is Other Biological Information 2013) and that the proportion of eggs summarized as follows. Based on fertilized increases with higher sperm population estimates there are at least Information on A. palmata’s life concentration (Fogarty et al., 2012b). hundreds of thousands of A. palmata history that we considered in the Experiments using gametes collected in colonies present in both the Florida proposed rule includes the following. Florida had lower fertilization rates than Keys and St. Croix, U.S. Virgin Islands. Growth rates, measured as skeletal those from Belize, possibly due to Absolute abundance is higher than extension of the end of branches, range genotype incompatibilities (Fogarty et estimates from these two locations given from 4 to 11 cm per year (Acropora al., 2012b). the presence of this species in many Biological Review Team, 2005) but in Darling et al. (2012) performed a other locations throughout its range. Curac¸ao have been reported to be slower biological trait-based analysis to

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categorize coral species into four life Genotypic diversity is highly variable. A. palmata’s vulnerability to threats as history strategies: Generalist, weedy, At two sites in the Florida Keys, only follows: High vulnerability to ocean competitive, and stress-tolerant. The one genotype per site was detected out warming, disease, acidification, classifications were primarily separated of 20 colonies sampled at each site sedimentation, and nutrient enrichment; by colony morphology, growth rate, and (Baums et al., 2005b). In contrast, all 15 moderate vulnerability to the trophic reproductive mode. Acropora palmata colonies sampled in Navassa had effects of fishing and predation; and low was classified as a ‘‘competitive’’ unique genotypes (Baums et al., 2006a). vulnerability to sea level rise and species, thus likely more vulnerable to Some sites have relatively high collection and trade. environmental stress. genotypic diversity such as in Los Information on A. palmata’s All information on A. palmata’s life Roques, Venezuela (118 unique susceptibility to disease that we history can be summarized as follows. genotpyes out of 120 samples; Zubillaga considered in the proposed rule The combination of rapid skeletal et al., 2008) and in Bonaire and Curacao includes the following. Disease is growth rates and frequent asexual (18 genotypes of 22 samples and 19 believed to be the primary cause of the reproduction by fragmentation can genotypes of 20 samples, respectively; region-wide decline of A. palmata enable effective competition within, and Baums et al., 2006a). In the Bahamas, beginning in the late 1970s and domination of, reef-building coral about one third of the sampled colonies continues to have a large effect on the communities in high-energy were unique genotypes, and in Panama species. White band disease was environments such as reef crests. Rapid between 24 and 65 percent of the generally associated with the majority of skeletal growth rates and frequent sampled colonies had unique genotypes, disease-related mortalities in A. palmata asexual reproduction by fragmentation depending on the site (Baums et al., from the 1970s to 1990s (Aronson and facilitate potential recovery from 2006a). Precht, 2001). White pox has been disturbances when environmental The public comments did not provide described as having severe impacts on conditions permit (Highsmith, 1982; new or supplemental biological A. palmata, and most monitoring Lirman, 2000). However, low sexual information on A. palmata. information after 2000 indicates that reproduction can lead to reduced Supplemental biological information we lesion patterns resembling white pox genetic diversity and limits the capacity found includes the following. A genetic have higher prevalence than patterns to repopulate sites. study found significant population resembling white band disease Other biological information on A. structure in Puerto Rico locations (Mona (Acropora Biological Review Team, palmata that we considered in the Island, Desecheo Island, La Parguerain, 2005). In the Florida Keys, the causative proposed rule includes the following. La Parguera) both between reefs and agent of white pox was identified as a Genetic samples from 11 locations between locations; population structure bacterium linked to human sewage and throughout the Caribbean indicate that in La Parguera suggests restriction of potential vectors/reservoirs such as A. palmata populations in the eastern gene flow between some reefs in close corallivores (Patterson et al., 2002; Caribbean (St. Vincent and the proximity (Garcia Reyes and Schizas, Sutherland et al., 2011). Grenadines, U.S. Virgin Islands, 2010). A more-recent study provided The effects of white pox appear to be Curac¸ao, and Bonaire) have had little or additional detail on the genetic exacerbated by higher temperatures. In no genetic exchange with populations in structure of A. palmata in Puerto Rico, Hawksnest Bay, U.S. Virgin Islands the western Atlantic and western as compared to Curacao, the Bahamas, during the 2005 bleaching event, the Caribbean (Bahamas, Florida, Mexico, and Guadeloupe that found unique prevalence of white pox had a positive Panama, Navassa, and Puerto Rico) genotypes in 75 percent of the samples linear relationship with temperature, (Baums et al., 2005b). While Puerto Rico with high genetic diversity (Me`ge et al., with mortality increasing with is more closely connected with the 2014). The recent results support two bleaching, indicating a decreased western Caribbean, it is an area of separate populations of A. palmata in resilience to disease when colonies were mixing with contributions from both the eastern Caribbean and western stressed (Muller et al., 2008). regions (Baums et al., 2005b). Models Caribbean; however, there is less Disease is temporally and spatially suggest that the Mona Passage between evidence for separation at Mona variable and is often reported as an the Dominican Republic and Puerto Passage, as found by Baums et al. instantaneous measure of prevalence Rico acts as a filter for larval dispersal (2006b). (percent of colonies affected by disease) and gene flow between the eastern All biological information on A. that provides only a snapshot in time. Caribbean and western Caribbean palmata can be summarized as follows. For instance, in Puerto Rico disease (Baums et al., 2006b). Genotypic diversity is variable across affected an average of 6.7 percent of The western Caribbean is the range with some populations colonies from December 2006 to October characterized by genetically showing evidence of higher input from 2007 (Scha¨rer et al., 2009). In St. Croix depauperate populations with lower sexual recruitment versus others that U.S. Virgin Islands, white band disease densities (0.13 ± 0.08 colonies per m2), rely more heavily on asexual affected three percent of the colonies while denser (0.30 ± 0.21 colonies per recruitment for population surveyed in Buck Island Reef National m2), genotypically rich stands maintenance. There are many areas with Monument between May and June 2004 characterize the eastern Caribbean many unique genotypes. Connectivity (Mayor et al., 2006). (Baums et al., 2006a). Baums et al. and mixing appear limited across larger Studies of permanently marked (2006a) concluded that the western geographic scales with eastern colonies, or monitoring plots, show Caribbean had higher rates of asexual Caribbean populations relatively longer-term trends of disease and recruitment and that the eastern isolated from western Caribbean mortality over time. From January 2003 Caribbean had higher rates of sexual populations, with evidence of to December 2009, 90 percent of the 69 recruitment. They postulated these population structure at a local scale in monitored A. palmata colonies in geographic differences in the some locations. Haulover Bay, St. John, U.S. Virgin contribution of reproductive modes to Islands exhibited signs of disease, and population structure may be related to Susceptibility to Threats the most significant cause of whole habitat characteristics, possibly the Information on threat susceptibilities colony mortality (Rogers and Muller, amount of shelf area available. was interpreted in the proposed rule for 2012). Of colonies monitored in the

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Florida Keys from 2004 to 2011, disease not change their association with Temperature-induced bleaching and was the second highest cause of tissue Symbiodinium type A3 throughout the mortality following bleaching are mortality after physical damage from study period that included the 1997–98 temporally and spatially variable. storms (33 percent of all mortality bleaching event (Thornhill et al., 2006). Bleaching associated with the high attributed to disease, Williams and High water temperatures also affect A. temperatures in 2005 had a large impact Miller, 2012). palmata reproduction. Acropora on A. palmata with 40 to 50 percent of The public comments did not provide palmata embryos and larvae exhibited bleached colonies suffering either new or supplemental information on the more developmental abnormalities, partial or complete mortality in several susceptibility of A. palmata to disease, lower survivorship, and decreased locations. Algal symbionts did not shift and we did not find any new or settlement at 30 degrees and 31.5 in A. palmata after the 1998 bleaching supplemental information. Information degrees C compared to those at 28 event indicating the ability to adapt to on the susceptibility of A. palmata to degrees C (Randall and Szmant, 2009). rising temperatures may not occur disease can be summarized as follows. The public comments did not provide through this mechanism. However, Acropora palmata is highly susceptible new or supplemental information on the Acropora palmata showed evidence of to disease as evidenced by the mass- susceptibility of A. palmata to ocean resistance to bleaching from warmer mortality event in the 1970s and 1980s. warming. Supplemental information we temperatures in some portions of its White pox seems to be more common found includes the following. Acropora range under some circumstances (Little today than white band disease. The palmata larvae exhibited faster Cayman). Through the effects on effects of disease are spatially and development and faster swimming reproduction, high temperatures can temporally (both seasonally and inter- speed at 30 and 31.5 degrees C potentially decrease larval supply and annually) variable. Results from longer- compared to controls at 27 and 28 settlement success, decrease average term monitoring studies in the U.S. degrees C (Baums et al., 2013). The larval dispersal distances, and cause Virgin Islands and the Florida Keys authors suggested these changes could earlier larval settlement, thereby indicate that disease can be a major decrease average larval dispersal affecting gene flow among populations. cause of both partial and total colony distances, and cause earlier larval Therefore, we conclude that A. palmata mortality. Thus, we conclude that A. settlement, thereby affecting gene flow is highly susceptible to ocean warming. palmata is highly susceptible to disease. among populations (Baums et al., 2013). Information on A. palmata’s Information on A. palmata’s A 14-year study was conducted at susceptibility to acidification that we susceptibility to ocean warming that we nine sites around Little Cayman from considered in the proposed rule considered in the proposed rule 1999 to 2012 of live coral cover, juvenile includes the following. Ocean includes the following. High densities, and size structure of coral acidification has a negative impact on temperatures can cause bleaching and colonies to determine response to the early life stages of A. palmata. mortality of A. palmata. In St. Croix, 1998 bleaching event inside versus Compared to controls at 400 matm, U.S. Virgin Islands, colonies outside of marine protected areas. Over carbon dioxide levels of 560 and 800 differentially bleached in Buck Island the first half of the study, bleaching and matm, predicted to occur this century, National Monument during the 2005 disease caused live cover to decrease reduced the rate of fertilization and Caribbean-wide mass bleaching event; from 26 percent to 14 percent in all settlement (combined 52 and 73 colonies in the shallower back reef corals, with full recovery seven years percent, respectively) and post- bleached earlier and suffered greater later with no differences inside versus settlement growth (39 and 50 percent, tissue loss than those located elsewhere outside of marine protected areas. The respectively) of A. palmata in lab (Lundgren and Hillis-Starr, 2008). Data numbers of A. palmata colonies in experiments, and impairment of from two sites in Jamaica, found 100 regularly-observed size-classes did not fertilization was exacerbated at lower percent of A. palmata colonies bleached decrease during this study, which the sperm concentrations (Albright et al., at both sites in 2005, with greater than authors suggested may indicate 2010). 50 percent of the colonies suffering resistance to bleaching and disease. The The public comments did not provide partial mortality (Quinn and Kojis, study concluded that the health of the new or supplemental information on the 2008). At one site, bleached colonies coral assemblage and the similarity of susceptibility of A. palmata to had complete mortality only responses inside and outside the marine acidification. Supplemental information occasionally, and 15 percent of bleached protected area suggested that negligible we found on its susceptibility to this colonies died at the second site (Quinn anthropogenic disturbance at the local threat includes the following. No effects and Kojis, 2008). In Trunk Bay and scale was a key factor underlying the on the progression or timing of larval Saltpond, St. John, U.S. Virgin Islands, observed resilience (Manfrino et al., development, or embryo and larval size almost half of the colonies that bleached 2013). were detected at elevated carbon in 2005 suffered partial or complete Van Woesik et al. (2012) developed a dioxide levels of 700 matm or 1000 matm mortality (44 percent of 27 colonies and coral resiliency index based on (Medina-Rosas et al., 2013). 40 percent of 107 colonies, respectively, biological traits and processes to All information on the susceptibility Rogers et al., 2006). Negligible bleaching evaluate extinction risk due to of A. palmata to acidification can be of A. palmata was observed during a bleaching. Evaluations were performed summarized as follows. Ocean 2006 bleaching event in Navassa that at the genus level, but genera were acidification will likely impact affected corals at deeper depths separated between the Caribbean and fertilization, settlement success, and (between 18 and 37 m) more Indo-Pacific. They indicated that A. post-settlement growth of A. palmata. significantly than at shallower depths palmata is highly vulnerable to Therefore, we conclude that A. palmata (<10 m), likely due to decreased water extinction. is highly susceptible to acidification. motion at the deeper sites (Miller et al., All information on the susceptibility There is no species-specific 2011a). Repeated sampling of the same of A. palmata to ocean warming can be information on the trophic effects of colonies in the Florida Keys and summarized as follows. High water fishing on A. palmata. However, due to Bahamas in 1998 and seasonally temperatures affect A. palmata through the level of reef fishing conducted in the between March 2000 and August 2004 bleaching, lowered resistance to disease, Caribbean, coupled with Diadema die- showed that colonies of A. palmata did and effects on reproduction. off and lack of significant recovery,

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recruitment habitat is limited. sediment and its high reliance on clear (Acropora Biological Review Team, Therefore, the trophic effects of reef water for nutrition, and sedimentation 2005). Predators have been identified as fishing adversely affects A. palmata’s can cause tissue mortality. We conclude potential vectors and reservoirs of recruitment habitat. Thus, we conclude that A. palmata is highly susceptible to disease (Sutherland et al. 2011). that A. palmata has some susceptibility sedimentation. The corallivorous snail C. abbreviata to the trophic effects of reef fishing due Information on A. palmata’s is the main predator, removing up to 16 to low natural recruitment rates. susceptibility to nutrient enrichment cm2 of tissue per day (Brawley and However, the available information does that we considered in the proposed rule Adey 1982), and there is evidence that not support a more precise description includes the following. There are few they concentrate on remnant Acropora of susceptibility to this threat. studies of the effects of nutrients on A. populations following decline Information on A. palmata’s palmata. Field experiments indicate (Acropora Biological Review Team, susceptibility to sedimentation that we that the mean net rate of uptake of 2005). Severity of predation is variable, considered in the proposed rule nitrate by A. palmata exceeds that of and Coralliophila seem to be extremely includes the following. The morphology ammonium by a factor of two and that rare or absent on Acropora spp. in of A. palmata contributes to its A. palmata does not uptake nitrite certain areas such as the Dry Tortugas, sensitivity to sedimentation as it is (Bythell, 1990). Florida and Bocas del Toro, Panama poorer at removing sediment compared The public comments did not provide (Acropora Biological Review Team, to mounding corals such as Orbicella new or supplemental information on the 2005). In St. John, U.S. Virgin Islands, annularis and Diploria strigosa (Abdel- susceptibility of A. palmata to nutrient snail predation affected a total of six Salam et al., 1988). Out of five species enrichment. Supplemental information percent of the colonies across 29 sites, tested, A. palmata was the least tolerant we found on the susceptibility to this but at individual sites, predation of sediment exposure; single threat includes the following. In Vega affected up to 60 percent of the colonies applications of 200 mg per cm2 to Baja, Puerto Rico, A. palmata mortality (Grober-Dunsmore et al., 2006). In Los colonies caused coral tissue death as increased to 52 percent concurrent with Roques, Venezuela snail predation was sediments accumulated on the flattened, pollution and sedimentation associated the most common cause of partial horizontal surfaces (Rogers, 1983). It is with raw sewage and beach mortality (4 to 20 percent), and it generally unable to remove coarser nourishment, respectively, between affected 0.72 to 10.6 percent of the sediments and only weakly able to December 2008 and June 2009 colonies (Zubillaga et al., 2008). Surveys remove finer sediments (Acropora (Hernandez-Delgado et al., 2011). of 235 sites throughout the Florida Keys Biological Review Team, 2005). Water Mortality presented as patchy necrosis- in 2007 revealed that about five percent movement and gravity are probably like and white pox-like conditions that of the A. palmata colonies assessed for more important in removing sediments impacted local reefs following condition were affected via predation by from this species than their capabilities anthropogenic disturbances and was snails and damselfish (Miller et al., of sloughing sediments in stagnant higher inside the shallow platform (52 2008). In Puerto Rico, infestations of water (Acropora Biological Review to 69 percent) and closer to the source corallivorous snails were observed on Team, 2005). Because A. palmata is of pollution (81 to 97 percent) compared three percent of all A. palmata colonies highly dependent on sunlight for to the outer reef (34 to 37 percent; surveyed and ranged from 0.9 to 10.6 nutrition, it is also sensitive to Hernandez-Delgado et al., 2011). percent per site (Scha¨rer et al., 2009). suspended sediments that reduce water All information on the susceptibility The public comments did not provide clarity (Porter, 1976). of A. palmata to nutrient enrichment new or supplemental information on the The public comments did not provide can be summarized as follows. Acropora susceptibility of A. palmata to new or supplemental information on A. palmata is sensitive to nutrients as predation. Supplemental information palmata’s susceptibility to evidenced by increased mortality after we found on the susceptibility of A. sedimentation. Supplemental exposure to raw sewage. We conclude palmata to predation includes the information we found on the that A. palmata is highly susceptible to following. Of the 50 percent tissue loss susceptibility of A. palmata to nutrient enrichment. experienced during monitoring in the sedimentation includes the following. In Information on A. palmata’s Florida Keys between 2004 and 2010, Vega Baja, Puerto Rico, A. palmata susceptibility to predation that we snail predation accounted for 15 percent mortality increased to 52 percent considered in the proposed rule after storm damage (42 percent) and concurrent with pollution and includes the following. There are disease (33 percent; Williams and sedimentation associated with raw several known predators of A. palmata Miller, 2012). The honeycomb cowfish sewage and beach nourishment, including the corallivorous snail Acanthostracion polygonius has been respectively, between December 2008 Coralliophila abbreviata (Baums et al., observed biting A. palmata and causing and June 2009 (Hernandez-Delgado et 2003) and the polychaete worm tissue lesions; it is unknown whether al., 2011). Mortality presented as patchy Hermodice carrunculata. Incidental the fish is actively feeding on the coral necrosis-like and white pox-like corallivores that affect A. palmata tissue or if lesions are a by-product of conditions that impacted local reefs include several species of fish such as its foraging mode (Williams and Bright, following anthropogenic disturbances stoplight parrotfish Sparisoma viride 2013). Lesions healed rapidly (less than and was higher inside the shallow and three-spot damselfish Stegastes six weeks) and did not contribute to platform (52 to 69 percent) and closer to planifrons. Stegastes planifrons does significant losses of live tissue the source of pollution (81 to 97 not directly feed on the coral but (Williams and Bright, 2013). percent) compared to the outer reef (34 removes live tissue to cultivate algal All information on the susceptibility to 37 percent; Hernandez-Delgado et al., gardens. Likewise, parrotfish are of A. palmata to predation can be 2011). primarily herbivores and may be feeding summarized as follows. Predators can All information on the susceptibility on endolithic algae in coral tissue have an impact on A. palmata both of A. palmata to sedimentation can be (Bruckner et al., 2000). Monitoring in through tissue removal and the potential summarized as follows. Acropora the Florida Keys indicates that to spread disease. Predation pressure is palmata is sensitive to sedimentation parrotfish bites on A. palmata usually spatially variable and almost non- due to its poor capability of removing heal in a matter of weeks to months existent in some locations. However, the

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effects of predation can become more Regulatory Mechanisms Additionally, the public comments severe if colonies decrease in abundance suggested that we did not fully consider and density, as predators focus on the In the proposed rule, we relied on the effects that conservation efforts have remaining living colonies. Therefore, we information from the Final Management on the status of A. palmata. Therefore, conclude that A. palmata has high Report for evaluating the existing conservation efforts are described as susceptibility to predation. regulatory mechanisms for controlling follows. Conservation efforts have been threats to all corals. However, we did underway for A. palmata for a number Information on A. palmata’s not provide any species-specific of years. Of 60 Acropora restoration susceptibility to sea level rise that we information on the regulatory efforts identified in 14 Caribbean considered in the proposed rule mechanisms or conservation efforts for countries, 52 percent used A. palmata, includes the following. In-place A. palmata. Public comments were including efforts in Belize, British colonies of A. palmata have been used critical of that approach, and we Virgin Islands, Colombia, Curacao, in the geologic record for reconstructing therefore attempt to analyze regulatory Dominican Republic, Guadalupe, Holocene sea level because this species mechanisms and conservation efforts on Jamaica, Mexico, Puerto Rico, Turks and only develops monospecific thickets in a species basis, where possible, in this Caicos, U.S. Virgin Islands, and Florida waters less than 5 m deep and is final rule. We also incorporate here, the (Young et al., 2012). SECORE, a generally limited to depths of 10 m or evaluation of threats to this species conservation organization comprised of less (Blanchon, 2005; Blanchon et al., conducted in the 2005 status review. public aquariums, zoos, and researchers, 2009). A sustained sea level rise of more Records confirm that A. palmata occurs holds annual workshops to than 14 mm per year is likely to in eight Atlantic ecoregions that accommodate sexual fertilization of A. displace A. palmata from its thicket- encompass 26 kingdom’s and countries’ palmata eggs collected from the wild, forming, framework-building depth EEZs. The 26 kingdoms and countries with the intent of rearing larvae for range (≤5 m) into its remaining habitat are Antigua & Barbuda, Bahamas, development of ex situ populations for range where a mixed framework is Barbados, Belize, Colombia, Costa Rica, conservation (Petersen et al., 2008). likely to develop (Brainard et al., 2011). Cuba, Dominica, Dominican Republic, However, to date, A. palmata colonies In the Yucatan region of Mexico during French Antilles, Grenada, Guatemala, produced through in vitro fertilization the warming that led to the last Haiti, Kingdom of the Netherlands, have rarely been planted into the wild interglacial period, A. palmata was able Honduras, Jamaica, Mexico, Nicaragua, for restoration (but see Roik et al., 2011; to keep up with the first 3 m of rapid Panama, St. Kitts & Nevis, St. Lucia, St. Szmant and Miller, 2005). sea-level rise; continued sea-level rise Vincent & Grenadines, Trinidad and Restoration efforts involving A. led to the demise of the original fore- Tobago, United Kingdom (British palmata more typically re-attach reef crests inhabited by A. palmata, the Caribbean Territories), United States fragments after physical disturbance retreat of A. palmata to a more inland (including U.S. Caribbean Territories), such as storms or ship groundings site, and back-stepping of the reef crest and Venezuela. The regulatory (Bruckner and Bruckner, 2001; Garrison and Ward, 2008) or grow colonies in as sea level rose an additional 2 to 3 m mechanisms relevant to A. palmata, coral nurseries (Becker and Mueller, (total of 6 m over an ecological time described first as a percentage of the 2001; Bowden-Kerby and Carne, 2012; scale; Brainard et al., 2011). above kingdoms and countries that Johnson et al., 2011) to outplant. Fast utilize them to any degree, and second The public comments did not provide growth rates, branching morphology, as the percentages of those kingdoms new or supplemental information on A. and asexual reproduction through palmata’s susceptibility to sea level rise, and countries whose regulatory fragmentation make A. palmata an ideal and we did not find any new or mechanisms may be limited in scope, candidate for active propagation, and supplemental information. All are as follows: General coral protection there are a number of offshore nurseries information on the susceptibility of A. (31 percent with 12 percent limited in that are producing corals for use in palmata to sea level rise can be scope), coral collection (50 percent with restoration and re-establishment of summarized as follows. The fast growth 27 percent limited in scope), pollution degraded populations. High rate of A. palmata could accommodate control (31 percent with 15 percent survivorship (>70 percent) of coral deeper water. We conclude that A. limited in scope), fishing regulations on fragments has been found within coral palmata has a low susceptibility to sea reefs (73 percent with 50 percent nurseries during the first year of level rise. limited in scope), managing areas for propagation (Young et al., 2012). protection and conservation (88 percent Information on A. palmata’s Survival rates after transplanting are with 31 percent limited in scope). The variable, ranging between 43 and 95 susceptibility to collection and trade most common regulatory mechanisms in percent during the first year, and that we considered in the proposed rule place for A. palmata are fishing decreasing in some studies using non- includes the following. Over the last regulations and area management for nursery raised fragments to 0 to 20 decade, collection and trade of this protection and conservation. However, percent after five years (Young et al., species has been low. The public half of the fishing regulations are 2012). comments did not provide new or limited in scope. General coral In conclusion, there are many supplemental information on the protection and collection laws, along conservation efforts aimed at increasing susceptibility of A. palmata to with pollution control laws, are much abundance and genetic diversity of A. collection and trade. Supplemental less common regulatory mechanisms for palmata throughout the Caribbean. information we found includes the the management of A. palmata. The These efforts are important, but not following. Gross exports averaged 2,120 2005 status review and 2006 listing enough to ensure conservation unless pieces of coral per year between 2000 concluded that existing regulatory combined with efforts to reduce the and 2012 and have primarily been for mechanisms are inadequate to control underlying threats and causes of scientific purposes (data available at both global and local threats, and are mortality (Young et al., 2012). While http://trade.cites.org). We conclude that contributing to the threatened status of conservation efforts will likely enhance A. palmata has low susceptibility to the species, and we incorporate that recovery and conservation of A. palmata collection and trade. analysis here. at small spatial scales, they are unlikely

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to affect the status of the species, given things, exposure to high levels of human evidence of synergistic effects of threats the global nature of threats. disturbance that result in pollution and for this species including disease breakage impacts. Also, while asexual outbreaks following bleaching events. Vulnerability to Extinction reproduction (fragmentation) provides a Acropora palmata is highly susceptible In 2006, A. palmata was listed as source for new colonies (albeit clones) to a number of threats, and cumulative threatened, i.e., likely to become in that can buffer natural demographic and effects of multiple threats are likely to danger of extinction within the next 30 environmental variability remains true, exacerbate vulnerability to extinction. years, due to: (1) Recent drastic declines we believed that reliance on asexual Despite the large number of islands and in abundance of the species that have reproduction is not sufficient to prevent environments that are included in the occurred throughout its geographic extinction of the species. Last, the species’ range, geographic distribution range and abundances at historic lows; previous status review and listing in the highly disturbed Caribbean (2) the potential constriction of broad determination underestimated the exacerbates vulnerability to extinction geographic ranges due to local global climate change-associated over the foreseeable future because A. extirpations resulting from a single impacts to A. palmata and A. palmata is limited to an area with high stochastic event (e.g., hurricanes, new cervicornis, based on our current localized human impacts and predicted disease outbreak); (3) limited sexual knowledge of trends in emissions, likely increasing threats. Acropora palmata recruitment in some areas and unknown warming scenarios, and ocean occurs in turbulent water on the back levels in most; and (4) occurrence of the acidification. In particular, in the reef, fore reef, reef crest, and spur and Allee effect (in which fertilization previous determination, we identified groove zone in water ranging from 1 to success declines greatly as adult density ocean acidification only as a factor that 30 m in depth. This moderates declines). ‘‘may be contributing’’ to the status of vulnerability to extinction over the The species was not listed as two species, in comparison to our foreseeable future because the species endangered, i.e., currently in danger of current understanding that ocean occurs in numerous types of reef extinction, because: (1) It was showing acidification is one of the three highest environments that will, on local and limited, localized recovery; (2) range- order threats affecting extinction risk for regional scales, experience highly wide, the rate of decline appeared to corals. variable thermal regimes and ocean have stabilized and was comparatively As explained above in the Risk chemistry at any given point in time. Its slow as evidenced by persistence at Analyses section, a species’ absolute population abundance has reduced abundances for the past two vulnerability to extinction results from been estimated as at least hundreds of decades; (3) it was buffered against the combination of its spatial and thousands of colonies in both Florida major threats by the large number of demographic traits, threat and a portion of the U.S. Virgin Islands colonies, large geographic range, and susceptibilities, and consideration of the and is higher than the estimate from asexual reproduction; and (4) as shown baseline environment and future these two locations due to the by the geologic record, the species has projections of threats. Subsequent to the occurrence of the species in many other persisted through climate cooling and proposed rule, we received and gathered areas throughout its range. Acropora heating fluctuation periods over supplemental species- or genus-specific palmata has low sexual recruitment millions of years, whereas other corals information, described above, that rates, which exacerbates vulnerability to have gone extinct. expands our knowledge regarding the extinction due to decreased ability to In 2012, A. palmata was proposed for species’ abundance, distribution, and recover from mortality events when all listing as endangered because threat susceptibilities. We developed colonies at a site are extirpated. In information available since the original our assessment of the species’ contrast, its fast growth rates and 2006 listing as threatened suggested: (1) vulnerability to extinction using all the propensity for formation of clones Population declines have continued to available information. As explained in through asexual fragmentation enables it occur, with certain populations of both the Risk Analyses section, our to expand between rare events of sexual species decreasing up to an additional assessment in this final rule emphasizes recruitment and increases its potential 50 percent or more since the time of the ability of the species’ spatial and for local recovery from mortality events, listing; (2) there are documented demographic traits to moderate or thus moderating vulnerability to instances of recruitment failure in some exacerbate its vulnerability to extinction. Its abundance and life populations; (3) minimal levels of extinction, as opposed to the approach history characteristics, combined with thermal stress (e.g., 30 degrees C) have we used in the proposed rule, which spatial variability in ocean warming and been shown to impair larval emphasized the species’ susceptibility acidification across the species’ range, development, larval survivorship, and to threats. moderate vulnerability to extinction settlement success of A. palmata; (4) The following characteristics of A. because the threats are non-uniform, near-future levels of acidification have palmata, in conjunction with the and there will likely be a large number been demonstrated to impair information described in the Corals and of colonies that are either not exposed fertilization, settlement success, and Coral Reefs section, Coral Habitat sub- or do not negatively respond to a threat post-settlement growth rates in A. section, and Threats Evaluation section at any given point in time. palmata; (5) on average 50 percent of above, affect its vulnerability to the colonies are clones, meaning the extinction currently and over the Listing Determination effective number of genetic individuals foreseeable future. The species has In the proposed rule, using the is half the total population size; (6) the undergone substantial population determination tool formula approach, A. species’ ranges are not known to have decline and decreases in the extent of palmata was proposed for listing as contracted, but with continued declines occurrence throughout its range due endangered because of: High local extirpations are likely, resulting in mostly to disease. Although localized vulnerability to ocean warming (E), a reduction of absolute range size. mortality events have continued to ocean acidification (E) and disease (C); Furthermore, we took into account that occur, percent benthic cover and high vulnerability to sedimentation (A the BRT identified restriction to the proportion of reefs where A. palmata is and E) and nutrient over-enrichment (A Caribbean as a spatial factor increasing dominant have remained stable over its and E); uncommon abundance (E); extinction risk, though, among other range since the mid-1980s. There is decreasing trend in abundance (E); low

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relative recruitment rate (E); narrow extinction and thus does not warrant persistence of the species in some areas overall distribution (E); restriction to the listing as Endangered because: in the face of continuing threats. Range- Caribbean (E); and inadequacy of (1) While A. palmata’s distribution in wide, a multitude of conservation efforts regulatory mechanisms (D). the Caribbean increases its risk of are already broadly employed In this final rule, we changed the exposure to threats as described above, specifically for A. palmata. However, listing determination for A. palmata its habitat includes back reef considering the global scale of the most from endangered to threatened. We environments and turbulent water on important threats to the species, and the made this determination based on a the fore reef, reef crest, shallow spur ineffectiveness of conservation efforts at more species-specific and holistic and groove zone. It is most commonly addressing the root cause of global approach, including consideration of found in depths of one to 12 m but is threats (i.e., GHG emissions), we do not the buffering capacity of this species’ also found in depths up to 30 m. This believe that any current conservation spatial and demographic traits, and the moderates vulnerability to extinction efforts or conservation efforts planned best available information above on A. currently because the species is not in the future will result in affecting the palmata’s spatial structure, limited to one habitat type but occurs in species’ status to the point at which demography, threat susceptibilities, and numerous types of reef environments listing is not warranted. that will experience highly variable management. The combination of these Indo-Pacific Species Determinations factors indicates that A. palmata is thermal regimes and ocean chemistry on likely to become endangered throughout local and regional scales at any given Absolute abundance is approximated its range within the foreseeable future, point in time, as described in more at a coarse scale in the Demographic and thus warrants listing as threatened detail in the Coral Habitat and Threats Information sections for most of the at this time, because: Evaluation sections; Indo-Pacific species, based on a (1) Acropora palmata is highly (2) Acropora palmata’s absolute comparison of corrected data from susceptible to ocean warming (ESA abundance is at least hundreds of Richards et al. (2008) and the thousands of colonies based on Factor E), disease (C), ocean distribution and abundance results from estimates from two locations in its acidification (E), sedimentation (A, E), Veron (2014). Mean global census sizes range. Absolute abundance is higher nutrients (A, E), and predation (C) and for four species in this final rule than estimates from these locations susceptible to trophic effects of fishing (Acropora jacquelineae, A. lokani, A. since A. palmata occurs in many other (A), depensatory population effects from speciosa, and A. tenella) are provided in locations throughout its range. This rapid, drastic declines and low sexual Richards et al. (2008). An error in the absolute abundance allows for variation recruitment (C), and anthropogenic and global census size formula (Richards et in the responses of individuals to natural abrasion and breakage (A, E). al. 2008, Supplementary Information threats to play a role in moderating _ These threats are expected to continue file Methods S1) resulted in 1,000-fold vulnerability to extinction for the and increase into the future. In addition, under-estimates of global census size in species to some degree, as described in the species is at heightened extinction Richards et al. (2008) for these four more detail in the Corals and Coral risk due to inadequate existing species, as confirmed by NMFS with the Reefs section; regulatory mechanisms to address local author in 2013. Richards et al.’s (2008) (3) Recent information indicates that corrected census results were compared and global threats (D); proportions of Caribbean sites where A. (2) Acropora palmata is with Veron’s ecoregion distribution and palmata is present and dominant have semi-quantitative abundance results to geographically located in the highly stabilized; disturbed Caribbean, where localized derive coarse approximations of (4) Acropora palmata has fast growth absolute abundance. For each species, human impacts are high and threats are rates and high capacity to produce predicted to increase as described in the the resulting absolute abundance is clones through asexual fragmentation, described as either ‘‘at least millions of Threats Evaluation section. A range which can aid in local recovery from constrained to this particular geographic colonies,’’ or ‘‘at least tens of millions mortality events; and of colonies’’ (NMFS, 2014). Although area that is likely to experience severe (5) Acropora palmata shows evidence this comparison produces only very and increasing threats indicates that a of resistance to bleaching from warmer general approximations of abundance, high proportion of the population of this temperatures in some portions of its large scale estimates are sufficient for species is likely to be exposed to those range under some circumstances (e.g. considering whether population size threats over the foreseeable future; and Little Cayman). (3) Acropora palmata’s abundance is The combination of these provides buffering capacity within the still a fraction of what it was before the characteristics indicates that the species context of our listing determinations. mass mortality in the 1970s and 1980s, does not exhibit the characteristics of Genus Millepora and recent population models forecast one that is currently in danger of the extirpation of the species from some extinction, as described previously in Genus Introduction locations over the foreseeable future. the Risk Analyses section and thus does The SRR and SIR provided no genus- The combination of these not warrant listing as endangered at this level introduction information for characteristics and future projections of time. Therefore, we withdraw our Millepora. However, they did provide threats indicates that the species is proposal to list A. palmata as the following information on likely to be in danger of extinction endangered. reproduction in the genus. Millepora within the foreseeable future throughout Progress has been made with A. species are hydrozoans, thus their life its range and warrants listing as palmata-specific conservation and history cycle includes a medusae stage, threatened at this time due to factors A, restoration projects, albeit small-scale, a free-swimming, bell-shaped form C, D, and E. and these projects are likely to increase (‘‘jellyfish’’) that produces gametes. The available information above on A. in the future. Within some countries, A. Reproduction is seasonal. The adult palmata’s spatial structure, palmata-specific conservation and coral colonies produce tiny medusae, demography, threat susceptibilities, and restoration projects show promise for which release gametes within a few management also indicate that the enhancing species recovery at very days after being released from the species is not currently in danger of small spatial scales and facilitating the colony. Medusae are in separate sexes,

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and the milleporid medusae of some die in response to high temperature protected sites there was actually an species live for only a few hours. The events, but they also seem to have a increase in Millepora colonies gametes of some milleporids can high capacity for quickly recovering by (McClanahan et al., 2001). Millepora become mature in 20 to 30 days, more recruiting new colonies. colonies had a bleaching index of 23.06 rapidly than for many scleractinians. Millepora have been observed with a for eight countries in the western Indian Hydrozoan corals of the genus Millepora greater than 20 percent prevalence of Ocean in 1998–2005, which was 12th are the only reef-building corals with skeleton-eroding-band disease in the highest of the 45 genera recorded, and medusae as part of their life history. Red Sea. There are reports of black-band 56 percent of the highest value Branching and columnar forms of disease on Millepora on the Great (McClanahan et al., 2007a). Millepora Millepora are subject to fragmentation Barrier Reef and white plague in had the highest bleaching level of any and may use this mechanism to Florida. Few other reports exist for the genus in Australia, and a moderately reproduce asexually; unlike Pacific, and Caribbean congeners have high level in Kenya in 1998 (Pandolfi et scleractinian corals, the survival of been observed with a small number of al., 2011). Millepora colonies in Millepora fragments may not be size- diseases. Okinawa, Japan, experienced sharp dependent. Millepora species are known to be drops in populations following the 1998 There is only one genus in the Family preyed on by the crown-of-thorns and 2010 mass bleaching episodes Milleporidae, the genus Millepora. seastar Acanthaster planci, although (Hongo and Yamano, 2013). At About 16 species of Millepora are they are less preferred prey than Mauritius in a bleaching event in 2004, currently considered valid. While all acroporids and perhaps most Millepora had a bleaching index of 35, coral species in this final rule are scleractinians. Millepora species are the second highest of the 32 genera ‘‘cnidarians’’ (Phylum Cnidaria), also preyed on by the polychaete recorded (McClanahan et al., 2005a). Millepora are ‘‘hydrozoans’’ (Class Hermodice carunculata, the nudibranch Millepora colonies had the highest level Hydrozoa, which includes jellyfish), mollusk Phyllidia, and filefish of the of bleaching among the corals of the whereas all other species in this rule are genera Alutera and Cantherhines. Socotra islands of Yemen, just outside ‘‘scleractinians’’ (Class Anthozoa, Order Although Millepora species tend to the Red Sea, in 1998 (DeVantier et al., Scleractinia). Like other reef-building favor relatively clear water with low 2005). corals, Millepora species contain rates of sedimentation, they were While Millepora species are among zooxanthellae, produce calcium reported to be among the last 17 out of the most susceptible of all reef-building carbonate skeletons, may grow fast, and 42 genera to drop out along a gradient corals to warming-induced bleaching, are thus major contributors to the of increasing rate of sedimentation. they also often recover more quickly physical structure of coral reefs. Unlike Millepora also showed increased than scleractinians, opportunistically other reef-building corals, the surfaces relative abundance and colony size on over-growing bleached colonies. Such of Millepora colonies are covered with sediment impacted reefs in Kenya. relatively rapid recovery by Millepora tiny polyps that look like hairs, Though little is known about effects of species from bleaching events has been containing stinging cells to capture nutrients on Pacific Millepora, observed in both the Indo-Pacific and prey. Most species can sting humans Caribbean congeners were found to Caribbean, and is facilitated by short with the same stinging cells, hence the decrease in percent cover on eutrophic colony life and ready regeneration of common name ‘‘fire corals.’’ Colonies of reefs in Barbados. fragments (Lewis, 2006). At a forereef Millepora species are encrusting, The genus Millepora has been site in the Marquesas Islands, French branching, foliose (leafy), or involved in international trade from Polynesia, Millepora platyphyllia combinations of these forms. The Indonesia, Solomon Islands, and Fiji overgrew dead scleractinian colonies to biology and ecology of Millepora are with reported exports between 200 and form a large monospecific stand reviewed in Lewis (2006). 3000 pieces per year in the years 2000– (Andre´foue¨t et al., 2014). At a back-reef 2008. Reported exports from Vietnam, site on Ofu Island, American Samoa, Genus Susceptibility to Threats Malaysia, and Tonga were less than following a bleaching event in 2002 that The SRR and SIR provided the 1000 pieces per year in the same time killed almost all Millepora dichotoma, following information on the threat period. colonies appeared and became fairly susceptibilities of the genus Millepora. Public comments did not provide any common within a few years (Doug The genus Millepora has been called a information on the genus Millepora. We Fenner, personal comm.). Following bleaching ‘‘loser.’’ Millepora species are gathered supplemental information on both the 1982–83 and 1997–98 warming ranked as the most susceptible to the susceptibilities of Millepora species events, Millepora intricata was bleaching in response to high seawater to some threats, including the following. extirpated from shallow water in the temperatures of any of the 40 genera or High bleaching and mortality in eastern Pacific, but showed recovery other categories of hermatypic corals in Millepora species has been reported in within several years, likely because of the Great Barrier Reef. The genus has response to warming events. All recolonization from deep water (Smith been reported to be highly susceptible to Millepora colonies on reef flats of two et al., in press). In contrast, a long-term bleaching in the western Indian Ocean islands in the Thousand Islands of study showed that three Millepora and appears to have experienced local Indonesia died in the 1983 El Nino mass species were ‘‘long-term losers’’ (i.e., extirpations in the tropical eastern bleaching (Brown and Suharsono, 1990). populations decreased to zero, and Pacific. Low bleaching occurred in In contrast, Millepora colonies showed remained there) following mass Millepora in Moorea during the 1991 no evidence of bleaching in Moorea, bleaching events in Japan in 1998 and event, but elevated temperatures can French Polynesia in the 1991 bleaching 2010, while two other species of also kill Millepora even in the absence event other than occasional mild paling Millepora were ‘‘neither winners nor of bleaching. At elevated temperatures, (Gleason, 1993). In Palau in 2000, some losers’’ (i.e., changes in their Millepora dichotoma showed decreased mortality was seen among Millepora populations were not significant) (van zooxanthellae density, changes in colonies (Bruno et al., 2001). Almost all Woesik et al., 2011). chlorophyll concentrations, and Millepora colonies in study sites outside Millepora colonies in the Great Barrier decreased calcification. Millepora of marine protected areas in Kenya were Reef had low susceptibility to Skeletal species are among the first to bleach and killed by mass bleaching in 1998, but in Eroding Band (the most prevalent

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disease on the GBR), with a prevalence acidification. The SRR rated the trophic supplemental information on M. of 0.4 percent out of 4,068 colonies effects of fishing as ‘‘medium’’ foveoloata that indicates a very high surveyed (Page and Willis, 2007). importance, the fourth most important level of species identification Several recent studies compare threat to corals overall. This threat was uncertainty, because its distinctive vulnerabilities across genera or species not addressed at the genus or species features are very small and difficult to for a large number of reef-building coral level in the SRR or SIR, because it is an learn. In addition, no pictures of live species, and the results of these studies ecosystem-level process. That is, colonies have been published of this are summarized below with regard to removal of herbivorous fish from coral species. Corals of the World (Veron, Millepora. Foden et al. (2013) developed reef systems by fishing alters trophic 2000) does not include non- a framework for evaluating the interactions by reducing herbivory on scleractinians such Millepora species, vulnerability of corals (and birds and algae, thereby providing a competitive making it very difficult to obtain reliable amphibians) to extinction due to climate advantage for space to algae over coral. reference material. Many coral experts change. They categorized all of the six Thus, the SRR did not discuss this also ignore Millepora species, but even species of Millepora, which they threat in terms of coral taxa, as its those that are interested in them have reported on as having a low effects are difficult to distinguish little opportunity to hone identification vulnerability to climate change. A field between coral genera and species. skills because the species is quite rare study that tracked the responses of 46 Therefore, an unstudied Millepora and not often encountered on surveys. reef-building coral species in southern species is likely to have some Thus, even though M. foveolata is Japan from 1997 to 2010 through two susceptibility to the trophic effects of considered a valid species, and there are bleaching events in 1998 and 2001 rated fishing. The SRR rated sea-level rise as no known taxonomic uncertainty issues, three Millepora species as neither ‘‘low-medium’’ importance to corals the species is so difficult to identify in winners nor losers, and two Millepora overall. This threat was not addressed at the field that there is very little reliable species as long term losers. Three of the the genus or species level in the SRR or information available for this species Millepora species were branching and SIR. Increasing sea levels may increase (Fenner, 2014b). Thus, a high all three branching species were ‘‘long land-based sources of pollution due to proportion of the information on M. term losers,’’ one species is encrusting inundation, resulting in changes to coral foveolata’s distribution and abundance and one produces plates, and those two community structure, most likely to information in the SRR or SIR is likely species were neither long term winners sediment-tolerant assemblages and based on inaccurate field or losers (van Woesik et al., 2011). slower growing species. Because identifications, thus we do not consider There is no information available on the Millepora are not generally sediment- this information to be sufficiently effects of any other threat for Millepora tolerant and are faster growing species, reliable, and are unable to provide a species. an unstudied Millepora species is likely reliable species description for M. Genus Conclusion to have some susceptibility to sea-level foveolata in this final rule. rise. The SRR rated ornamental trade Based on the information from the Listing Determination SRR, SIR, public comments, and (referred to in the proposed rule as Collection and Trade) as ‘‘low’’ In the proposed rule, M. foveolata was supplemental information we can make proposed for listing as endangered the following inferences about the importance to corals overall, and this because of: High vulnerability to ocean susceptibilities of an unstudied threat is addressed at both the genus warming (ESA Factor E); moderate Millepora species to ocean warming, and species levels in the SRR. Because vulnerability to disease (C) and disease, ocean acidification, trophic Millepora species are widely collected acidification (E); uncommon generalized effects of fishing, sedimentation, and traded, an unstudied Millepora range wide abundance (E); narrow nutrients, sea-level rise, predation, or species is likely to have some overall distribution (based on narrow collection and trade. The large majority susceptibility to collection and trade. geographic distribution and shallow of studies report that Millepora species In conclusion, an unstudied Millepora depth distribution (E); and inadequacy are highly susceptible to thermal stress species is likely to be highly susceptible of existing regulatory mechanisms (D). and bleaching, but vulnerability may be to ocean warming (i.e., thermal stress, Based on the lack of information on moderated by the capacity for rapid leading to warming-induced bleaching), M. foveolata’s distribution, abundance, recovery in some species. An unstudied and to have some susceptibility to and threat vulnerabilities due to this species of Millepora such as M. tuberosa disease, ocean acidification, trophic species’ identification uncertainty, we can be predicted in a bleaching event to effects of fishing, sedimentation, believe there is not sufficient evidence not be a ‘‘winner’’ in the long term, but nutrients, sea-level rise, predation, and to support a listing determination of it cannot be predicted whether they will collection and trade. threatened or endangered. Therefore, we be a long term loser, or neither a winner Millepora foveolata find that listing is not warranted at this or loser. Thus, an unstudied species of time. Millepora is likely to be highly Introduction susceptible to ocean warming. Based on The SRR and SIR provided the Millepora tuberosa the above information, an unstudied following information on M. Introduction species of Millepora is likely to have foveoloata’s morphology and taxonomy. some susceptibility to disease, Colonies of Millepora foveolata form The SRR and SIR provided the sedimentation, nutrients, and predation. thin encrusting laminae that adhere following information on M. tuberosa’s The SRR rated ocean acidification as closely to the underlying substrata. morphology and taxonomy. Millepora ‘‘medium-high’’ importance, the third Millepora foveolata is sometimes tuberosa’s colony morphology consists most important threat to corals overall, confused with the similarly encrusting of thin (about 1 mm at encrusting because of the likely effects of Millepora exaesa. peripheral margins) to moderately thick decreasing ocean pH on coral The public comments did not provide (3 cm or more in the central regions of calcification and reproduction. Thus, an any new or supplemental information larger colonies) encrusting laminae that unstudied Millepora species is likely to on M. foveoloata’s morphology and closely adhere to the underlying have some susceptibility to ocean taxonomy. However, we gathered substrata. They are always encrusting

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and so do not make vertical plates or presence of Millepora species, thus the at 59 percent, and the decline in branches, although they can be nodular small number of reliable observations abundance before the 1998 bleaching or lumpy, especially when they encrust for this species likely indicates under- event (‘‘Back-cast Percent Population rubble. Millepora tuberosa is often reporting rather than a reflection of its Reduction’’) was estimated at 22 percent found as small colonies (5 to 30 cm actual distribution or overall (Carpenter et al., 2008). This estimated diameter) but can be greater than one abundance. However, surveys by decline is approximately 50 percent meter in diameter. The SIR reports that Millepora experts have not found the higher than most other Indo-Pacific several authors have commented that species at all coral reef sites surveyed species included in the Carpenter paper, people could inadvertently misidentify within the areas encompassed by its apparently because of the combined M. tuberosa colonies as crustose known locations. Thus we conclude that restricted geographic and depth ranges. coralline algae, and the SIR reports it the available information suggests a However, as summarized above in the can look similar to Psammocora patchy range bounded by east Africa, Inter-basin Comparison sub-section, live nierstrazi if they have similar color. Taiwan, Mariana Islands, Caroline coral cover trends are highly variable There is some taxonomic uncertainty, as Islands, American Samoa, and New both spatially and temporally, M. tuberosa has been synonymized with Caledonia, and that the species’ range producing patterns on small scales that Millepora exaesa in one review. The makes up approximately one third to can be easily taken out of context, thus problem may be that the skeletons are one half of the coral reef areas within quantitative inferences to species- quite similar, but the living colonies the Indo-Pacific. specific trends should be interpreted appear quite different, mainly in color; with caution. At the same time, an Demographic Information M. tuberosa is a wine color, unlike other extensive body of literature documents Millepora species. The SRR and SIR provided the broad declines in live coral cover and The public comments and following information on M. tuberosa’s shifts to reef communities dominated by information we gathered did not abundance. The SRR stated that the hardier coral species or algae over the provide any new or supplemental species is most often reported as past 50 to 100 years (Birkeland, 2004; information on morphology or occasional, but in Guam it is Fenner, 2012; Pandolfi et al., 2003; Sale taxonomy. We gathered supplemental predominant in an area of lagoonal reef and Szmant, 2012). These changes have information, which confirmed that M. south of Agat Boat Harbor. The SIR cited likely occurred, and are occurring, from tuberosa has moderate taxonomic several sources of information not a combination of global and local uncertainty, but is easily identified. available in the SRR, and concluded threats. Given that M. tuberosa probably Millepora tuberosa is distinctive and not that the species’ abundance should be occurs in many areas affected by these difficult to identify by experts, thus the considered common. broad changes, and that it has some distribution and abundance information The public comments did not provide susceptibility to both global and local described below for this species is any new or supplemental information threats, we conclude that it is likely to sufficiently reliable (Fenner, 2014b). on M. tuberosa’s abundance. We have declined in abundance over the gathered supplemental information, Spatial Information past 50 to 100 years, but a precise including abundance results from quantification is not possible based on The SRR and SIR provided the surveys conducted in New Caledonia, the limited species-specific information. following information on M. tuberosa’s American Samoa, and the Northern distribution, habitat, and depth range. Mariana Islands between 2005 and Other Biological Information Millepora tuberosa is known from 2013. In New Caledonia, 87 sites were The public comments and Mauritius, Taiwan, Mariana Islands, surveyed from 2006 to 2009, and only information we gathered did not Caroline Islands, American Samoa, and a single colony of M tuberosa was provide additional biological New Caledonia. The species occurs in a found. At 67 sites surveyed in American information on M. tuberosa. broad range of habitats on the reef slope, Samoa from 2005 to 2010, M. tuberosa reef crest, and back-reef, including but was found at 18 sites (of the sites, 31 Susceptibility to Threats not limited to lower reef crests, upper were on Tutuila, and the species was The SRR and SIR provided species- reef slopes, and lagoons, from 1 to at found at 13 of them). At 22 sites specific information on the least 12 m depth. surveyed in the Northern Mariana susceptibility of M. tuberosa to Public comments and information we Islands in 2013, M. tuberosa was found sedimentation, predation, and gathered provided new or supplemental at three sites (D. Fenner, personal secondary effects of heavy fishing information on M. tuberosa’s comm.). At sites where M. tuberosa has pressure. The relatively high abundance distribution. One public comment stated been actively surveyed (i.e., by coral of this species on Guam suggests it is M. tuberosa has been reported from a abundance monitoring programs that resistant to those threats. Genus-level variety of sources suggesting that its includes Millepora experts), the information is provided for the effects range extends from that shown in the available information shows wide on Millepora of ocean warming, disease, proposed rule westward to Madagascar, variability in the species’ abundance, predation, land-based sources of indicating a broader distribution than from dominant or common (Guam) to pollution (i.e., sedimentation, nutrients, shown in the proposed rule. We uncommon (Tutuila, Northern Mariana toxins, and salinity), and collection and gathered supplemental information, Islands) to rare (New Caledonia). Based trade. The SRR and SIR did not provide including results from surveys carried on the available information, we any other species-specific information out from 2005 to 2014 in New conclude that M. tuberosa’s overall on the effects of these threats on M. Caledonia, American Samoa, the abundance is common or uncommon tuberosa. The threat susceptibility and Northern Mariana Islands, Nauru, overall, but locally rare. exposure information from the SRR and Tonga, and the Chagos Islands, that Carpenter et al. (2008) extrapolated SIR was interpreted in the proposed rule confirmed the occurrence of M. tuberosa species abundance trend estimates from for M. tuberosa’s vulnerabilities to in the first three areas but did not find total live coral cover trends and habitat threats as follows: High vulnerability to it in the latter three areas (D. Fenner, types. For M. tuberosa, the overall ocean warming, moderate personal comm.). Many experts, decline in abundance (‘‘Percent vulnerabilities to disease, acidification, including Veron, do not record the Population Reduction’’) was estimated trophic effects of fishing, nutrients, and

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low vulnerabilities to predation, as the percentage of those countries distribution, based on the available sedimentation, sea-level rise, and whose regulatory mechanisms are information, includes patchy areas from collection and trade. limited in scope, are as follows: General the western Indian Ocean across the Public comments did not provide any coral protection (33 percent with none western and central Pacific, as far east new or supplemental information on M. limited in scope), coral collection (67 as American Samoa. Its geographic tuberosa’s threat susceptibilities. We percent with 17 limited in scope), distribution moderates vulnerability to gathered the following species-specific pollution control (33 percent with 17 extinction because some areas within its and genus-level supplemental percent limited in scope), fishing range are projected to have less than information on this species’ threat regulations on reefs (100 percent with average warming and acidification over susceptibilities. Millepora tuberosa has 17 percent limited in scope), managing the foreseeable future, including the been rated as moderately or highly areas for protection and conservation western Indian Ocean, the central susceptible to bleaching but not coral (100 percent with none limited in Pacific, and other areas, so portions of disease, but these ratings are not based scope). The most common regulatory the population in these areas will be on species-specific data (Carpenter et mechanisms in place for M. tuberosa are less exposed to severe conditions. Its al., 2008). Some colonies in American reef fishing regulations and area depth range is from zero to at least 12 Samoa and Guam have been observed to management for protection and meters. On one hand, its depth range have a discolored yellow area around conservation. Coral collection laws are may moderate vulnerability to part of the perimeter, which appeared to also somewhat utilized. General coral extinction over the foreseeable future be a non-lethal disease (not all colonies protection and pollution control laws because deeper areas of its range will had it, and no mortality was seen. No are much less common regulatory usually have lower irradiance than other disease was seen (Fenner, 2014a). mechanisms for the management of M. surface waters, and acidification is There is no other species-specific tuberosa. generally predicted to accelerate most in information for the exposure or waters that are deeper and cooler than Vulnerability to Extinction susceptibility of M. tuberosa to any those in which the species occurs. On threat. Based on information provided As explained above in the Risk the other hand, its depth range may in the genus description above, M. Analyses section, a species’ exacerbate vulnerability to extinction tuberosa is likely to be highly vulnerability to extinction results from over the foreseeable future if the species susceptible to ocean warming, and has the combination of its spatial and occurs predominantly in the shallower some susceptibilities to disease, ocean demographic characteristics, threat portion of its depth range, since those acidification, trophic effects of fishing, susceptibilities, and consideration of the areas will have higher irradiance and sedimentation, nutrients, sea-level rise, baseline environment and future thus be more severely affected by predation, and collection and trade. projections of threats. The SRR stated warming-induced bleaching. Its habitat that the high bleaching rate, based on Regulatory Mechanisms includes lower reef crests, upper reef genus-level information, is the primary slopes, and lagoons, which moderates In the proposed rule, we did not threat of extinction for M. tuberosa, vulnerability to extinction over the provide any species-specific which was compounded by the disjunct foreseeable future because the species is information on regulatory mechanisms geographic range. The SRR also stated not limited to one habitat type but or conservation efforts for M. tuberosa. that factors that potentially reduce the occurs in numerous types of reef Criticisms of our approach received extinction risk are that M. tuberosa environments that will, on local and during public comment led us to the might be more common than previously regional scales, experience reef following analysis to attempt to analyze observed, and that like other Millepora environments that will, on local and regulatory mechanisms on a species species, it likely has a high capacity for regional scales, experience highly basis. recovering from bleaching. variable thermal regimes and ocean Veron’s updated report on the listed Subsequent to the proposed rule, we chemistry at any given point in time. coral species and their occurrence in received and gathered supplemental While the species is locally rare, its various ecoregions (Veron, 2014) did not species- or genus-specific information, overall abundance is common or include M. tuberosa. To determine what described above, that expands our uncommon. Thus, its overall countries the species occurs in we used knowledge regarding the species abundance, combined with spatial the SRR, IUCN Red List of Threatened abundance, distribution, and threat variability in ocean warming and Species, and other sources where the susceptibilities. We developed our acidification across the species range, species has been confirmed (Fenner, assessment of the species’ vulnerability moderates vulnerability to extinction 2011) and conclude that the species to extinction using all the available because the increasingly severe occurs in a minimum of six countries’ information. As explained in the Risk conditions expected in the foreseeable EEZs. Those six countries are the Analyses section, our assessment in this future will be non-uniform and Federated States of Micronesia, France final rule emphasizes the ability of the therefore will likely be a large number (New Caledonia), Mauritius, Palau, species’ spatial and demographic traits of colonies that are either not exposed Taiwan, and the United States (CNMI, to moderate or exacerbate its or do not negatively respond to a threat Guam, American Samoa). As noted in vulnerability to extinction, as opposed at any given point in time. the Spatial Information paragraph to the approach we used in the above, it is likely the species occurs in proposed rule, which emphasized the Listing Determination a number of other countries, but we species’ susceptibility to threats. In the proposed rule using the cannot determine which ones at this The following characteristics of M. determination tool formula approach, time, thus this management analysis is tuberosa, in conjunction with the M. tuberosa was proposed for listing as limited to the six countries where the information described in the Corals and threatened because of: High species has been confirmed. Coral Reefs section, Coral Habitat sub- vulnerability to ocean warming (ESA The regulatory mechanisms available section, and Threats Evaluation section Factor E); moderate vulnerability to to M. tuberosa, described first as a above, affect its vulnerability to disease (C) and acidification (E); percentage of the above countries that extinction currently and over the common generalized range wide utilize them to any degree, and second foreseeable future. Its geographic abundance (E); narrow overall

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distribution (based on narrow importance threats, the combination of mortality in Seriatopora species in geographic distribution and shallow these biological and environmental response to warming events. In response depth distribution (E); and inadequacy characteristics indicates that the species to the 1998 warming event, Seriatopora of existing regulatory mechanisms (D). possesses significant buffering capacity colonies in Palau had high levels of In this final rule, we changed the to avoid being in danger of extinction bleaching with high mortality (Bruno et listing determination for M. tuberosa within the foreseeable future throughout al., 2001). In response to the same from threatened to not warranted. We its range. It is possible that M. tuberosa’s warming event, over half of Seriatopora made this determination based on a extinction risk may increase in the colonies in study sites within Kenyan more species-specific and holistic future if global threats continue and marine protected areas were killed by assessment of whether this species worsen in severity, likely resulting in mass bleaching (McClanahan et al., meets the definition of either a the continued decline of this species 2001). A large study of the bleaching threatened or endangered coral largely into the future. As the species responses of over 100 coral species on in response to public comments, experiences reduced abundance or the GBR to the 1998 bleaching event including more appropriate range constriction of a certain included one Seriatopora species, consideration of the buffering capacity magnitude, its ability to moderate Seriatopora hystrix. For this species, of this species’ spatial and demographic exposure to threats will diminish. approximately 40 percent of the traits to lessen its vulnerability to However, the species is not likely to observed colonies were bleached, threats. Thus, based on the best become of such low abundance or so resulting in S. hystrix being more available information above on M. spatially fragmented as to be in danger affected than most of the Pocilloporidae tuberosa’s spatial structure, of extinction due to depensatory and Acroporidae species in the study, demography, threat susceptibilities, and processes, the potential effects of and one of the 20 most affected species management, none of the five ESA environmental stochasticity, or the in the entire study (Done et al., 2003b). listing factors, alone or in combination, potential for mortality from catastrophic In response to a 2008 bleaching event are causing this species to be likely to events within the foreseeable future in Papua New Guinea, two become endangered throughout its range throughout its range. Therefore, M. Pocilloporidae species (including S. within the foreseeable future, and thus tuberosa is not warranted for listing at hystrix) and 14 Acroporidae species it is not warranted for listing at this this time under any of the listing factors. were monitored, and each species’ time, because: relative susceptibility to bleaching was (1) Millepora tuberosa’s distribution Genus Seriatopora evaluated in relationship to the other stretches across the Indian Ocean and Genus Introduction species in the study. Nine of the 16 most of the Pacific Ocean and is spread species, including S. hystrix, had over a very large area. While some areas The family Pocilloporidae includes moderate susceptibility to bleaching, within its range are projected to be three genera: Pocillopora, Seriatopora, while five species were rated as severe affected by warming and acidification, and Stylophora. Seriatopora contains or high susceptibilities, and two as low. other areas are projected to have less six species, all occurring in the Indo- Of the 139 S. hystrix colonies monitored than average warming and acidification, Pacific (Veron, 2000). Seriatopora in the study, 126 bleached (Bonin, including the western Indian Ocean, the species have branching colonies. The 2012). In response to a 2004 warming central Pacific, and other areas. This SRR and SIR provided no genus-level event in Mauritius, the genus distribution and the heterogeneous introductory information on Seriatopora was the most bleached of habitats it occupies reduce exposure to Seriatopora. the 32 genera recorded (McClanahan et any given threat event or adverse Genus Susceptibility to Threats al., 2005b). In eight countries in the condition that does not occur uniformly western Indian Ocean in 1998–2005, the throughout the species range. As The SRR and SIR provided the Seriatopora genus had a bleaching explained above in the Threats following information on the threat index of 32, the fourth highest of the 45 Evaluation section, we have not susceptibilities of the genus genera recorded, and 75 percent of the identified any threat that is expected to Seriatopora. Species in the genus highest value (McClanahan et al., occur uniformly throughout the species Seriatopora are highly susceptible to 2007a). range within the foreseeable future; and bleaching across regions, including McClanahan et al. (2007a) calculated (2) Millepora tuberosa’s abundance is Micronesia the GBR, and the western a relative extinction risk score based on described as common or uncommon Indian Ocean. The genus Seriatopora is bleaching for genera of corals in the overall which, in terms of relative known to be susceptible to predation by western Indian Ocean. The index of abundance of corals and in combination snails and the crown-of-thorns seastar, extinction risk was proportional to the with the size of its range, indicates this Acanthaster planci. The genus degree of bleaching and inversely species likely numbers in the tens or Seriatopora has been heavily traded, proportional to the abundance and hundreds of millions of colonies, at primarily from Fiji and Indonesia (and number of reefs on which a taxon was least. This provides buffering capacity occasionally the Philippines and found. The index of extinction risk for in the form of absolute numbers of Taiwan). Many records are at the genus Seriatopora was the eighth highest out colonies and variation in susceptibility level; trade was heavy in the mid-1980s of 47 genera, with a score of 0.46 based between individual colonies. As (exceeding 134,000 pieces in 1987). on a scale of zero to one, with one being discussed in the Corals and Coral Reefs Seriatopora hystrix is the most heavily the score of the highest extinction risk. section above, the more colonies a exploited species, although Seriatopora With regard to disease, two reports species has, the lower the proportion of caliendrum is also exported. from the GBR provide contrasting colonies that are likely to be exposed to The public comments did not provide information regarding the a particular threat at a particular time, any new or supplemental information susceptibilities of Seriatopora species to and all individuals that are exposed will on the threat susceptibilities of the various coral diseases. One study found not have the same response. genus Seriatopora. We gathered that Black Band Disease was nearly Notwithstanding the projections supplemental information, which absent on colonies of Seriatopora through 2100 that indicate increased provided the following. There are species (Page and Willis, 2006). In severity over time of the three high several reports of high bleaching and contrast, colonies of Seriatopora species

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had high susceptibility to Skeletal importance to corals. Thus, we conclude distribution, habitat, and depth range. Eroding Band, with a prevalence of 5.8 that an unstudied Seriatopora species Seriatopora aculeata is distributed from percent. Skeletal Eroding Band is the has some susceptibility to these threats. Australia, Fiji, Indonesia, Japan, Papua most prevalent disease on the GBR (Page Sea-level rise was also rated as ‘‘low- New Guinea, and Madagascar to the and Willis, 2007). Seriatopora in medium’’ importance to corals. Marshall Islands. The SRR and SIR Indonesia was reported to have no Increasing sea levels may increase land- described S. aculeata’s habitat as diseases (Haapkyla et al., 2007). There based sources of pollution due to shallow reef environments, and its is no information available on the inundation, resulting in changes to coral depth range as three to 40 meters. The effects of any other threat for community structure, thus an unstudied SIR reported it in Guam and the Seriatopora species. Seriatopora species is likely to have Northern Marianas. The public comments and Genus Conclusion some susceptibility to sea-level rise. The SRR rated predation and ornamental information we gathered provided Based on the information from the trade (referred to in the proposed rule as supplemental information on the SRR, SIR, public comments, and Collection and Trade) as ‘‘low’’ distribution and habitat of S. aculeata. supplemental information, we can make importance to corals overall. One public comment stated that in the following inferences about the Seriatopora is preyed on by both snails Guam, the few specimens of S. aculeata susceptibilities of an unstudied and crown-of-thorns starfish. Thus we observed since 2004 were found in areas Seriatopora species to ocean warming, conclude that Seriatopora has some with high rates of sedimentation. Thus, disease, ocean acidification, susceptibility to predation. Seriatopora based on all the available information, sedimentation, nutrients, trophic effects is heavily traded, thus we conclude that S. aculeata’s habitat can be summarized of fishing, sea-level rise, predation, and Seriatopora has some susceptibility to as follows: The species occurs in a collection and trade. The SRR rated collection and trade. broad range of habitats on the reef slope ocean warming and disease as ‘‘high’’ In conclusion, an unstudied and back-reef, including but not limited importance to corals. These were rated Seriatopora species is likely to be highly to upper reef slopes, mid-slope terraces, as the three most important threats to susceptible to ocean warming, and to lower reef slopes, reef flats, and lagoons. reef-building corals overall. All studies have some susceptibility to disease, Supplemental information provided the on thermal stress in Seriatopora report ocean acidification, trophic effects of following. Veron (2014) provides an high levels of bleaching in response to fishing, sedimentation, nutrients, sea- updated, much more detailed range map warming events. Thus, we conclude that level rise, predation, and collection and for this species than the maps used in Seriatopora likely has high trade. the SRR. Veron reports that S. aculeata susceptibility to ocean warming. Studies is confirmed in 19 of his 133 Indo- reported that one disease did not infect Seriatopora aculeata Pacific ecoregions, and strongly Seriatopora, but another did at high Introduction predicted to be found in an additional prevalence, and no diseases infected it seven. in Indonesia. Thus, we conclude that The SRR and SIR provided the Seriatopora has some susceptibility to following information on S. aculeata’s Demographic Information disease. Although there is no other morphology and taxonomy. Morphology The SRR and SIR provided the genus-level or species-specific was described as thick, short, tapered following information on S. aculeata’s information on the susceptibilities of branches, usually in fused clumps. The abundance. Seriatopora aculeata has Seriatopora species to ocean taxonomy was described as somewhat been reported as uncommon. acidification, the SRR rated it as uncertain, because genetic studies have The public comments did not provide ‘‘medium-high’’ importance to corals. not corresponded well with morphology any new or supplemental information Thus, we conclude that an unstudied for S. aculeata and other species of on S. aculeata’s abundance, but the Seriatopora species has some Seriatopora. Similar species, supplemental information provided the susceptibility to ocean acidification. Seriatopora stellata and S. hystrix, can following. Veron (2014) reports that S. The SRR rated the trophic effects of have similar branching structures in aculeata occupied 10.3 percent of 2,984 fishing as ‘‘medium’’ importance, the shallow, exposed reef flats. dive sites sampled in 30 ecoregions of fourth most important threat to corals The public comments and the Indo-Pacific, and had a mean overall. This threat was not addressed at information we gathered did not abundance rating of 1.70 on a 1 to 5 the genus or species level in the SRR or provide any new or supplemental rating scale at those sites in which it SIR, because it is an ecosystem-level information on morphology, and was found. Based on this semi- process. That is, removal of herbivorous confirmed that there is a moderate level quantitative system, the species’ fish from coral reef systems by fishing of taxonomic uncertainty for S. abundance was characterized as alters trophic interactions by reducing aculeata, and that there is a moderate ‘‘common,’’ and overall abundance was herbivory on algae, thereby providing a level of species identification described as ‘‘uncommon.’’ Veron did competitive advantage for space to algae uncertainty for this species. Veron not infer trends in abundance from over coral. Thus, the SRR did not (Veron, 2014) states that S. aculeata is these data. As described in the Indo- discuss this threat in terms of coral taxa, sometimes confused with S. stellata, but Pacific Species Determinations as its effects are difficult to distinguish Veron (Veron, 2000; Veron, 2014) introduction above, based on results between coral genera and species. continues to consider it a valid species, from Richards et al. (2008) and Veron Therefore, we conclude that an and we conclude it can be identified by (2014), the absolute abundance of this unstudied Seriatopora species has some experts, and that the distribution and species is likely at least millions of susceptibility to the trophic effects of abundance information described below colonies. fishing. for this species is sufficiently reliable Carpenter et al. (2008) extrapolated Although there is no genus-level or (Fenner, 2014b). species abundance trend estimates from species-specific information on the total live coral cover trends and habitat susceptibilities of Seriatopora species to Spatial Information types. For S. aculeata, the overall sedimentation or nutrients, the SRR The SRR and SIR provided the decline in abundance (‘‘Percent rated both threats as ‘‘low-medium’’ following information on S. aculeata’s Population Reduction’’) was estimated

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at 37 percent, and the decline in aculeata’s threat susceptibilities. One General coral protection and pollution abundance before the 1998 bleaching comment stated that the depth range for control laws are less common regulatory event (‘‘Back-cast Percent Population S. aculeata on the reef slopes of Guam mechanisms for the management of S. Reduction’’) was estimated at 14 are coincident with those of the crown- aculeata. percent. However, as summarized above of-thorns starfish, both of which are Vulnerability to Extinction in the Inter-basin Comparison sub- below 5 to 7 meters depth, exposing S. section, live coral cover trends are aculeata to predation. Seriatopora As explained above in the Risk highly variable both spatially and aculeata has been rated as not Analyses section, a species’ temporally, producing patterns on small moderately or highly susceptible to vulnerability to extinction results from scales that can be easily taken out of bleaching and disease, but this rating is the combination of its spatial and context, thus quantitative inferences to not based on species-specific data demographic characteristics, threat species-specific trends should be (Carpenter et al. 2008). There is no susceptibilities, and consideration of the interpreted with caution. At the same supplemental species-specific baseline environment and future time, an extensive body of literature information for the susceptibility of S. projections of threats. The SRR stated documents broad declines in live coral aculeata to any threat. Based on that the primary factor that increases the cover and shifts to reef communities information provided in the Seriatopora potential extinction risk is its high dominated by hardier coral species or genus description above, S. aculeata is bleaching susceptibility. The genus algae over the past 50 to 100 years likely to be highly susceptible to ocean Seriatopora is heavily traded, but not (Birkeland, 2004; Fenner, 2012; Pandolfi warming, and is likely to have some often identified to species. Heavy use in et al., 2003; Sale and Szmant, 2012). susceptibility to disease, ocean the aquarium trade implies the potential These changes have likely occurred, and acidification, trophic effects of fishing, for local extirpation for this usually are occurring, from a combination of sedimentation, nutrients, sea-level rise, uncommon species. global and local threats. Given that S. predation, and collection and trade. The Subsequent to the proposed rule, we aculeata occurs in many areas affected available information does not support received and gathered supplemental by these broad changes, and that it has more precise ratings of the species- or genus-specific information, some susceptibility to both global and susceptibilities of S. aculeata to the described above, that expands our local threats, we conclude that it is threats. knowledge regarding the species likely to have declined in abundance abundance, distribution, and threat Regulatory Mechanisms. over the past 50 to 100 years, but susceptibilities. We developed our quantification is not possible based on In the proposed rule, we did not assessment of the species’ vulnerability the limited species-specific information. provide any species-specific to extinction using all the available information on the regulatory information. As explained in the Risk Other Biological Information mechanisms or conservation efforts for Analyses section, our assessment in this The SRR and SIR provided the S. aculeata. Criticisms of our approach final rule emphasizes the ability of the following information on S. aculeata’s received during public comment led us species’ spatial and demographic traits life history. Little is known of S. to the following analysis to attempt to to moderate or exacerbate its aculeata’s life history. The much more analyze regulatory mechanisms on a vulnerability to extinction, as opposed common species, S. hystrix, is a species basis. Records confirm that S. to the approach we used in the simultaneous hermaphrodite that aculeata occurs in 19 Indo-Pacific proposed rule, which emphasized the reproduces sexually via brooded larvae. ecoregions that encompass 10 countries’ species’ susceptibility to threats. The public comments and information EEZs. The 10 countries are Federated The following characteristics of S. we gathered provided no additional States of Micronesia, France (French aculeata, in conjunction with the biological information. Pacific Island Territories), Indonesia, information described in the Corals and Japan, Palau, Papua New Guinea, Coral Reefs section, Coral Habitat sub- Susceptibility to Threats Philippines, Solomon Islands, Timor- section, and Threats Evaluation section To describe S. aculeata’s threats, the Leste, and the United States (CNMI, above, affect its vulnerability to SRR and SIR provided genus-level Guam, PRIAs). The regulatory extinction currently and over the information for the effects on mechanisms available to S. aculeata, foreseeable future. Its geographic Seriatopora of o ocean warming, described first as a percentage of the distribution is limited to parts of the disease, acidification, sedimentation, above countries that utilize them to any Coral Triangle and the western nutrients, predation, and collection and degree, and second as the percentage of equatorial Pacific Ocean. Despite the trade. The SRR and SIR did not provide those countries whose regulatory large number of islands and any species-specific information on the mechanisms are limited in scope, are as environments that are included in the effects of these threats on S. aculeata, follows: General coral protection (40 species’ range, this range exacerbates except for a single export record from percent with none limited in scope), vulnerability to extinction over the Indonesia for four pieces of the species coral collection (70 percent with 20 foreseeable future because it is mostly in 2008. We interpreted the threat percent limited in scope), pollution limited to an area projected to have the susceptibility and exposure information control (30 percent with 20 percent most rapid and severe impacts from from the SRR and SIR in the proposed limited in scope), fishing regulations on climate change and localized human rule for S. aculeata’s vulnerabilities as reefs (100 percent with none limited in impacts for coral reefs over the 21st follows. High vulnerability to ocean scope), and managing areas for century. Its depth range of 40 meters warming; moderate vulnerability to protection and conservation (100 moderates vulnerability to extinction disease, ocean acidification, trophic percent with none limited in scope). over the foreseeable future because effects of reef fishing, nutrients, and The most common regulatory deeper areas of its range will usually predation; and low vulnerability to mechanisms in place for S. aculeata are have lower irradiance than surface sedimentation, sea level rise, and reef fishing regulations and area waters, and acidification is generally collection and trade. management for protection and predicted to accelerate most in waters Public comments provided some conservation. Coral collection laws are that are deeper and cooler than those in supplemental information on S. also heavily utilized for the species. which the species occurs. The species

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occurs in a broad range of habitats on (2) Seriatopora aculeata’s distribution play a role in moderating vulnerability the reef slope and back-reef, including is constrained to the Coral Triangle and to extinction for the species to some but not limited to upper reef slopes, western equatorial Pacific, which is degree, as described in more detail in mid-slope terraces, lower reef slopes, projected to have the most rapid and the Corals and Coral Reefs section. reef flats, and lagoons. This moderates severe impacts from climate change and There is no evidence of depensatory vulnerability to extinction over the localized human impacts for coral reefs processes such as reproductive failure foreseeable future because the species is over the 21st century, as described in from low density of reproductive not limited to one habitat type but the Threats Evaluation. Multiple ocean individuals and genetic processes such occurs in numerous types of reef warming events have already occurred as inbreeding affecting this species. environments that will, on local and within the western equatorial Pacific Thus, its absolute abundance indicates regional scales, experience highly that suggest future ocean warming it is currently able to avoid high variable thermal regimes and ocean events may be more severe than average mortality from environmental chemistry at any given point in time. in this part of the world. A range stochasticity, and mortality of a high There is not enough information about constrained to this particular geographic proportion of its population from its abundance to determine if it area that is likely to experience severe catastrophic events. moderates or exacerbates extinction. It and increasing threats indicates that a The combination of these is common and has at least millions of high proportion of the population of this characteristics indicates that the species colonies, but the great majority of the species is likely to be exposed to those does not exhibit the characteristics of population is within an area expected to threats over the foreseeable future. one that is currently in danger of be severely impacted by threats over the The combination of these extinction, as described previously in foreseeable future. While depth characteristics and projections of future the Risk Analyses section, and thus does distribution and habitat variability threats indicates that the species is not warrant listing as endangered at this moderate vulnerability to extinction, the likely to be in danger of extinction time. combination of its geographic within the foreseeable future throughout Range-wide, a multitude of distribution and high susceptibility to its range and warrants listing as conservation efforts are already broadly ocean warming are likely to be more threatened at this time due to factors A, employed that are likely benefiting S. influential to the status of this species C, D, and E. aculeata. However, considering the over the foreseeable future, because of The available information above on S. global scale of the most important the projected severity of ocean warming aculeata’s spatial structure, threats to the species, and the throughout the species’ range in the demography, threat susceptibilities, and ineffectiveness of conservation efforts at foreseeable future, and its high management also indicate that the addressing the root cause of global species is not currently in danger of susceptibility to this threat. threats (i.e., GHG emissions), we do not extinction and thus does not warrant believe that any current conservation Listing Determination listing as Endangered because: efforts or conservation efforts planned (1) While half of S. aculeatas’ range is in the future will result in affecting the In the proposed rule, using the within the Coral Triangle which species status to the point at which determination tool formula approach, S. increases its extinction risk as described listing is not warranted. aculeata was proposed for listing as above, its habitat includes various threatened because of: High shallow reef environments down to 40 Genus Acropora, Indo-Pacific vulnerability to ocean warming (ESA meters. This moderates vulnerability to Genus Introduction Factor E); moderate vulnerability to extinction currently because the species disease (C) and acidification (E); is not limited to one habitat type but The SRR and SIR provided an uncommon generalized range wide occurs in numerous types of reef introduction to Indo-Pacific Acropora, abundance (E); moderate overall environments that will, at local and covering geological history, taxonomy, distribution (based on moderate regional scales, experience highly life history, and threat susceptibilities of geographic distribution and moderate variable thermal regimes and ocean the genus as a whole. Acropora colonies depth distribution (E); and inadequacy chemistry at any given point in time, as are usually branching, bushy, or plate- of existing regulatory mechanisms (D). described in more detail in the Coral like, rarely encrusting or submassive. In this final rule, we maintain the Habitat sub-section and Threats Acropora is by far the largest genus of listing determination for S. aculeata as Evaluation section. There is no evidence corals with over 150 species, and threatened. Based on the best available to suggest that the species is so spatially dominates many reefs, making Acropora information provided above on S. fragmented that depensatory processes, the most important single genus of aculeata’s spatial structure, environmental stochasticity, or the corals in the world. Almost all species demography, threat susceptibilities, and potential for catastrophic events of Acropora are in the Indo-Pacific. management indicate that it is likely to currently pose a high risk to the survival Genus Susceptibility to Threats become endangered throughout its range of the species; within the foreseeable future, and thus (2) Seriatopora aculeata occurs down The SRR and SIR provided the warrants listing as threatened at this to at least 40 m so its depth range will following information on genus-level time, because: provide some refugia from threats threat susceptibilities for Indo-Pacific (1) Seriatopora aculeata is highly because deeper areas of its range will Acropora. Acropora are widely reported susceptible to ocean warming (ESA usually have lower irradiance than to be more sensitive to bleaching in Factor E), and susceptible to disease (C) surface water, and acidification is response to high temperatures than ocean acidification (E), trophic effects of generally predicted to accelerate most in other coral genera. Some studies report fishing (A), nutrients (A, E), and waters that are deeper and cooler than branching species of Acropora to bleach collection and trade (B). In addition, those in which the species occurs; and more than table species, but other existing regulatory mechanisms to (3) Seriatopora aculeata’s absolute studies do not find this. Bleaching address global threats that contribute to abundance is at least millions of mortality in Acropora can be very extinction risk for this species are colonies, which allows for variation in severe. Larval connectivity and survival inadequate (D); and the responses of individuals to threats to of partially-dead colonies are probably

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important in population recovery. reproduction and recruitment. Elevated during mass bleaching in 1998, Bleaching of Acropora has been nutrients have been shown to reduce Acropora had a higher index in Kenya followed by disease outbreaks and by fertilization success, survival, and (80) than in Australia (40); temperatures reduced fecundity for a year or two. settlement of Acropora larvae. Further, were higher in Kenya. Acropora in Fertilization and larval stages of iron-rich ‘‘red’’ soils typical of tropical Mauritius had an index of 39, the fifth Acropora are particularly sensitive to islands, as well as other chemicals in highest of the 32 genera recorded, high temperatures. run-off, interfere with synchronization following a 2004 bleaching event Ocean acidification decreases the rate of spawning among colonies, egg-sperm (McClanahan et al., 2005a). Acropora of calcification in Acropora. For one recognition and interactions, had an index of 28.9 for eight countries species of Acropora in the Caribbean, fertilization, and embryo development. in the western Indian Ocean in 1998– decreases in growth rates on reefs over Acropora species are heavily 2005, which was fifth highest of the 45 decades has been attributed to collected and widely traded genera recorded (McClanahan et al., acidification. Acidification negatively internationally. Trade quotas and 2007a). The abundance of Acropora affects a variety of stages of reports are typically listed only at the after 1998 in the western Indian Ocean reproduction in Acropora. genus level, making any species-specific decreased strongly in proportion to the Acropora are vulnerable to most of inferences with regard to this threat very number of degree heating weeks in 1998 the diseases that infect coral, and are difficult. (McClanahan et al., 2007b). Based on a more commonly affected by acute and The public comments did not provide bleaching index scaled from 0 to 250 lethal diseases (‘‘white diseases’’ or any supplemental information on genus- (with 0 as no bleaching and 250 as tissue loss) than other corals. Such level threat susceptibilities for Indo- complete bleaching), Pandolfi et al. lethal diseases have been the major Pacific Acropora. However, we gathered (2011) report that Acropora bleached cause of the loss of most Acropora in the supplemental information, which heavily in Kenya and moderately in Caribbean. The reduction of coral provides the following genus-level Australia in 1998, with scores of 225 populations by disease leads to negative information on threat susceptibilities of and 120, respectively. Acropora had a synergisms, as it reduces Acropora Indo-Pacific Acropora for ocean moderate percentage of bleaching on reproductive output and can lead to warming, disease, ocean acidification, Howland and Baker islands in the U.S. recruitment failure, making population and predation. With regard to Pacific in early 2010, with 28.7 percent recovery very difficult. susceptibility to ocean warming, Fisk bleached on Baker and 47.7 percent on Acropora are preferred prey for most and Done (1985) report bleaching Howland. Acropora was the fifth most- predators that prey on coral, including patterns on a site on the Great Barrier bleached genus out of 14 genera, and the crown-of-thorns starfish, a variety of Reef in 1982 to 1983. Most species of was 60 percent as bleached as the most snails including Drupella, butterflyfish, Acropora in shallow water had bleached genus (Vargas-Angel et al., and fireworms. Individual territorial significant mortality, but Acropora 2011). butterflyfish can take 400–700 bites per hyacinthus did not. Mortality varied by During a mass-bleaching event in hour, and butterflyfish densities can be species and site. Brown and Suharsono Western Australia in 2010–2011, 50–70 per 1000m2, demonstrating (1990) reported that the 1983 El Nin˜ o Acropora had the highest mortality with possible intense predation on Acropora. caused a mass bleaching event in the 100 percent mortality of colonies larger Acropora have low carbon and protein Thousand Islands, Indonesia. The mass than 10 cm diameter in size, and content in their tissues so a low nutrient bleaching event killed all Acropora (22 Montipora the second highest mortality, value, yet are still preferred prey. This species) in the transects on the reef flats while massive and encrusting corals, suggests that instead of investing in of two islands (Brown and Suharsono, such as Porites and faviids, had much chemical defenses against predation, 1990). Gleason (1993) reported that higher survival rates. Colonies less than Acropora invests its energy in rapid Acropora was the second most affected 10 cm diameter were not killed growth. However, when coral genus by bleaching (Montastraea was (Depczynski et al., 2012). Acropora in populations are greatly reduced, the the most affected) in Moorea, French the turbid waters off Okinawa, Japan, predatory pressure is increased on Polynesia in 1991, and that it had the experienced sharp drops in populations colonies, and can exert a positive- greatest mortality. McClanahan et al. following the 1998 and 2010 mass feedback effect (Allee Effect or (2001) report that almost all Acropora in bleaching episodes (Hongo and Yamano, depensation) that makes populations study sites in Kenya were killed by mass 2013). Sutthacheep et al. (2013) report unstable and can lead to collapse or lack bleaching in 1998. Kayanne et al. (2002) that all colonies of one species of of recovery. reported that in 1998 in the Ryukyu Acropora were completely bleached at In general, Acropora species are Islands of Japan, branching Acropora Laem Set at Samui Island in the western relatively more susceptible to the effects was susceptible to bleaching and Gulf of Thailand in 1998 and 80 percent of sedimentation than many other reef- mortality was high. The branching of the colonies of the other reef-building building corals. Though certain growth species in this study were primarily A. coral species were as well. In 2010, 80 forms (e.g., cylindrical branches) may be formosa (= A. muricata) and also A. percent colonies of one species were more effective at passive sediment pulchra and A. palifera (= Isopora completely bleached and all colonies of rejection than others, Acropora are palifera). Hughes et al. (2003) reported the other species were partly bleached. generally not adept at actively removing that 11 Acropora species ranged from 0 After the 1998 bleaching event, 72 sediment. Acropora have also shown to 100 percent affected by bleaching in percent of colonies had complete particular sensitivity to shading, an Raiatea, French Polynesia, in 2002. mortality, and after the 2010 event, all effect of turbid waters resulting from Done et al. (2003b) reported that 46 bleached colonies had complete sedimentation. In addition, adult Acropora species ranged from 0 to 44 mortality. colonies of Acropora have reportedly percent affected by bleaching on the Bleaching does not always result in shown impacts from sedimentation Great Barrier Reef in 2003. mortality, thus it is important to especially during reproduction. Based on a bleaching index scaled consider bleaching-induced mortality Acropora species are also relatively from 0 to 100 (with 0 as no bleaching and bleaching rates from a single event, more susceptible to the effects of and 100 as complete bleaching), as well as the recovery of a population nutrients, especially with regard to McClanahan et al. (2004) reported that over time to a bleaching event. In Kenya

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in 1998, mortality in Acropora was sixth Barrier Reef, Pocilloporidae and of acidification, as shown by a study of highest of the 18 genera, and 55 percent Acroporidae have the highest A. hyacinthus, which found that natural of the genus with the most mortality prevalence of families, and diseases daily oscillations in CO2 may reduce the (McClanahan, 2004). Three species of have been recorded on at least 23 locally negative effects of increasing Acropora were long-term winners species of Acropora (Willis et al., 2004). ocean acidification (Comeau et al., following mass bleaching events in Black band disease on the Great Barrier 2014). Moderate increases in CO2 may Japan (decreasing from 3.4 percent cover Reef is concentrated in staghorn enhance Acropora growth and to 0 percent then increasing to 3.5 Acropora species with 76 diseased calcification rates in some species, percent; decreasing from 0.2 percent to colonies counted in one study, and however, at higher CO2 levels, growth 0 percent and then increasing to 3.2 Acropora species with other colony and calcification rates drop to zero. percent; decreasing from 1.2 percent morphologies (tables, bushy, corymbose, More consistently across species, cover to 0 percent and then increasing digitate, bottlebrush) had far fewer elevated CO2 tends to decrease to 0.7 percent), and one species was diseased colonies (Page and Willis, Acropora growth and calcification rates neither a winner or a loser (van Woesik 2006). In American Samoa, French (Anthony et al., 2008; Chauvin et al., et al., 2011). Bridge et al. (2013a) report Frigate Shoals (Hawaii) and Johnston 2011; Purkis et al., 2011; Schneider and that Acropora mortality after bleaching Atoll, two species of table Acropora (A. Erez, 2006; Suggett et al., 2013). was higher than for all corals as a hyacinthus and A. cytherea) had larger Acropora species appear to be more whole. Total coral mortality at 0 to 2 m numbers of colonies (13 each) with susceptible to acidification than most depth was 70 percent, while it was 90 growth anomalies in transects than any other genera, as demonstrated by the percent for Acropora, and at 3 to 4 m of 10 other taxa, and much higher than lack of Acropora species in coral depth it was 20 percent for all corals but one other table coral (A. clathrata, with communities existing in naturally low 60 percent for Acropora (Bridge et al., one; Work et al., 2008). In Indonesia, pH waters (Fabricius et al., 2011). 2013a). bushy Acropora had the highest With regard to predation, De’ath and Species or genera that readily bleach prevalence (8%) of disease of any taxon Moran (1998) reported that Acropora but recover quickly are relatively (out of 35 taxa), while corymbose was the most preferred prey of crown- resilient to warming-induced bleaching. Acropora was the eighth highest taxon of-thorns starfish out of the 10 most For example, the genus Acropora and second highest Acropora group common genera on 15 reefs in the Great received a +1 resilience score based on with 0.5 percent disease, and all other Barrier Reef (preferred 14:1 over Porites, trait and process scores assigned to the Acropora groups (tabulate, bottlebrush, the least preferred genus). Pratchett genus (van Woesik et al., 2012). Traits digitate, and staghorn) had 0 percent (2001) reported that in a choice and processes were chosen which were disease (Haapkyla et al., 2007). experiment, crown-of-thorns starfish thought to confer resilience to climate always ate Acropora colonies before change. Resilience scores of 16 Indo- Ocean acidification can have a variety eating colonies of other genera. This was Pacific genera that were evaluated of effects on Indo-Pacific Acropora true of all four of the Acropora species varied between +7 and ¥5. Scores species. While increased CO2 does not tested. When a crown-of-thorns starfish below 0 were correlated with a high appear to affect the survival of has finished eating preferred species, it extinction probability (van Woesik et unidentified Acropora larvae, moves to eating less preferred species, al., 2012). McClanahan et al. (2007a) postsettlement skeletal growth of the and thus in an outbreak, almost all calculated a relative extinction risk polyps of unidentified Acropora species species may be eaten (Pratchett et al., score based on bleaching for genera of (Suwa et al., 2010) and A. digitifera 2001). The snail Drupella rugosa corals in the western Indian Ocean. The (Inoue et al., 2011) are impaired. In preferred to eat Acropora pruinosa over index of extinction risk was addition, increased CO2 impairs the rate Montipora informis, one agaricid and proportional to the degree of bleaching of zooxanthellae acquisition in the four faviid corals in laboratory tests in and inversely proportional to the polyps of A. digitifera (Inoue et al., Hong Kong (Morton et al., 2002). abundance and number of reefs on 2011) and A. millepora (Kaniewska et The public comments did not provide which a taxon was found. The index of al., 2012). In Caribbean Acropora any supplemental information on genus- extinction risk for Acropora was the species, fertilization and settlement are level threat susceptibilities for Indo- ninth lowest out of 47 genera, with a impaired by increased CO2 (Albright et Pacific Acropora. We gathered the score of 0.11 based on a scale of 0 to 1, al., 2010). Elevated CO2 also induces supplemental information above, which with 1 being the score of the highest bleaching in Acropora, even more so provides genus-level information on extinction risk (McClanahan et al., than temperature increases (Anthony et threat susceptibilities of Indo-Pacific 2007a). al., 2008). Carbon dioxide enrichment to Acropora for ocean warming, disease, Diseases have been reported to be 600 to 790 ppm enhanced maximum ocean acidification, and predation. We more common in Acropora than in other photosynthetic rates in A. formosa did not gather any supplemental corals in some areas of the Indo-Pacific, (Crawley et al., 2010), but elevated CO2 information on the other threats (i.e., such as the Northwest Hawaiian Islands levels had no effect on photosynthesis sedimentation, nutrients, trophic effects (Aeby, 2006) and American Samoa or respiration in A. eurystoma of fishing, sea-level rise, or collection (Fenner et al., 2008). However, in the (Schneider and Erez, 2006). A study of and trade). Philippines, Porites was the dominant the effects of near-term ocean host with almost all disease observed in acidification and elevated seawater Genus Conclusion that genus, and only rarely observed on temperature on the physiology of A. Based on the information from the Acropora (Raymundo et al., 2005). In aspera suggested that gene expression of SRR, SIR, public comments, and New Caledonia, Turbinaria had the key metabolic proteins is impacted by supplemental information, we make the highest disease prevalence of any genus the synergistic effects of near term ocean following inferences regarding the with 2.5% infected, while Acropora was acidification (i.e., the conditions susceptibilities of an unstudied tied with Montipora for the least disease expected to result from 50–90 ppm CO2 Acropora species to ocean warming, among the 12 most common genera above current atmospheric levels) and disease, ocean acidification, predation, affected, with less than 0.1% infected ocean warming (Ogawa et al., 2013a). sedimentation, nutrients, trophic effects (Tribollet et al., 2011). On the Great Physical factors may moderate impacts of fishing, sea-level rise, and collection

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and trade. Nearly all the studies cited on reef systems by fishing alters trophic Also, one public comment stated that thermal stress in Acropora report high interactions by reducing herbivory on specimens collected in American Samoa levels of bleaching in response to algae, thereby providing a competitive and identified by the American Samoa warming events. Thus, it is possible to advantage for space to algae over coral. Department of Marine and Water predict that an unstudied Acropora Thus, the SRR did not discuss this Resources as A. jacquelineae appear to species is likely to be highly susceptible threat in terms of coral taxa, as its be A. aculeus, thereby illustrating the to warming-induced bleaching, as long effects are difficult to distinguish species identification uncertainties as some considerations are kept in between coral genera and species. associated with this species. In addition, mind: (1) Despite high overall Accordingly, an unstudied Acropora we gathered supplemental information, susceptibility within the genus to species is likely to have some including Veron (2014), which states warming-induced bleaching, there can susceptibility to the trophic effects of that this species is distinctive. Thus, be high variability between species and fishing. while the public comments and habitats (Done et al., 2003b); (2) colonies The SRR rated sea-level rise as ‘‘low- supplemental information provided that bleach do not necessarily die (in medium’’ importance to corals overall. some information on the taxonomy of A. general, Acropora species have higher This threat was not addressed at the aculeus, we conclude it can be post-bleaching mortality than corals as a genus or species level in the SRR or SIR. identified by experts, and that the whole, but there is high variability in Increasing sea levels may provide new distribution and abundance information response throughout the genus); (3) coral habitats by submergence of hard described below for this species is recovery from bleaching provides the substrates; however sea-level rise is also sufficiently reliable (Fenner, 2014b). mechanism for acclimatization; and (4) likely to increase land-based sources of Spatial Information while most Acropora species readily pollution due to inundation, resulting in bleach in response to warming events, changes to coral community structure, The SRR and SIR provided the most also have the capacity to most likely to sediment-tolerant following information on A. aculeus’ reestablish local populations relatively assemblages and slower-growing distribution, habitat, and depth range: quickly through their rapid growth and species. Because Acropora are not Acropora aculeus is distributed from asexual reproduction capacity. generally sediment-tolerant and are East Africa to the Pitcairn Islands in the The studies cited above suggest that faster growing species, an unstudied eastern Pacific. The SRR and SIR diseases are generally more common in Acropora species is likely to have some reported the species as having the 15th Acropora than other coral genera, susceptibility to sea-level rise. largest range of 114 Acropora species in although there are numerous The SRR rated ornamental trade a large study. Its predominant habitat is documented exceptions, depending on (referred to in the proposed rule as shallow lagoons, and it is also found in location. These studies also demonstrate Collection and Trade) as ‘‘low’’ other habitats protected from direct high variability in disease susceptibility importance to corals overall, and this wave action on back-reefs and reef across Acropora species, depending on threat was addressed at both the genus slopes, and its depth range is low tide growth form, with wide divergence of and species levels in the SRR. Because to at least 20 m. disease susceptibilities among colony Acropora species are some of the most The public comments did not provide morphological groups under the same popular coral species to collect and any new or supplemental information conditions. Thus, it is possible to trade, an unstudied Acropora species is on A. aculeus’ distribution. We gathered predict that an unstudied Acropora likely to have some susceptibility to supplemental information, including species is likely to have some collection and trade. Veron (2014), which reports that this susceptibility to disease. In conclusion, an unstudied Acropora species is confirmed in 68 of his 133 The studies cited above on ocean species is likely to be highly susceptible Indo-Pacific ecoregions, and strongly acidification in Acropora report impacts to ocean warming and to have some predicted to be found in an additional on skeletal growth rates. Thus, it is susceptibility to disease, acidification, 16. Wallace (1999b) reports its possible to predict that an unstudied sedimentation, nutrients, trophic effects occurrence in 24 of her 29 Indo-Pacific Acropora species is likely to have some of fishing, sea-level rise, predation, and areas, many of which are significantly susceptibility to ocean acidification in collection and trade. larger than Veron’s ecoregions. Richards terms of impacts on skeletal growth. The (2009) calculated the geographic range studies cited above on predation in Acropora aculeus of A. aculeus at over 100 million km2. Acropora report that predators such as Introduction The public comments and information crown-of-thorns starfish and Drupella we gathered provided nothing snails prefer to eat Acropora over other The SRR and SIR provided the additional on A. aculeus’ habitat and genera. Thus, it is possible to predict following information on A. aculeus’ depth range. that an unstudied Acropora species is morphology and taxonomy. Morphology likely to have some susceptibility to was described as small bushy colonies Demographic Information predation. Most studies summarized in with flat tops, and taxonomy was The SRR and SIR provided the the SRR on the effects of land-based described as having no taxonomic issues following information on A. aculeus’ sources of pollution suggest that an but being similar in appearance to A. abundance. Acropora aculeus has been unstudied Acropora species is likely to latistella. reported as generally common and have some susceptibility to The public comments and locally abundant, especially in the sedimentation and nutrient enrichment. information we gathered provided central Indo-Pacific, and that it is The SRR rated the trophic effects of information on the morphology or particularly abundant in shallow fishing as ‘‘medium’’ importance, and it taxonomy of A. aculeus. One public lagoons and common in most habitats was the fourth most important threat to comment stated that specimens where it is protected from direct wave corals overall. This threat was not collected in the Mariana Islands and action. addressed at the genus or species level identified by coral expert Richard H. The public comments did not provide in the SRR or SIR, because it is an Randall as A. aculeus appear to be any new or supplemental information ecosystem-level process. That is, different than colonies described as A. on A. aculeus’ abundance. We gathered removal of herbivorous fish from coral aculeus in references used in the SRR. supplemental information, including

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Richards (2009) and Richards et al. Other Biological Information Acropora aculeus has been rated as (2013b), which concluded that this moderately or highly susceptible to species is globally widespread, locally The SRR and SIR provided the disease, but this rating is not based on widespread, and locally common. Based following information on A. aculeus’ species-specific data (Carpenter et al., on these results, the authors concluded life history. Acropora aculeus is a 2008). Page and Willis (2007) reported that A. aculeus is among the most hermaphroditic spawner that is a that Skeletal Eroding Band has been abundant Acropora species, and also participant in mass broadcast spawning found in A. aculeus. Skeletal Eroding among those Acropora species that are in some localities. The public comments Band is the most prevalent disease on most likely to persist in the future. They and information we gathered provided the Great Barrier Reef. They also placed 12 species in this category out of no additional biological information. reported that corymbose Acropora had 85 species of Acropora. Veron (2014) Susceptibility to Threats moderate susceptibility to Skeletal reports that A. aculeus occupied 32.1 Eroding Band in the Great Barrier Reef, percent of 2,984 dive sites sampled in To describe A. aculeus’ threat with a prevalence of 2.4 percent (Page 30 ecoregions of the Indo-Pacific, and susceptibilities, the SRR and SIR and Willis, 2007). No other species- had a mean abundance rating of 1.55 on provided genus-level information for the specific information is available for the a 1 to 5 rating scale at those sites in effects on Acropora of ocean warming, susceptibility of A. aculeus to any other which it was found. Based on this semi- acidification, disease, predation, threat. quantitative system, the species’ sedimentation, nutrients, and collection Based on information from other abundance was characterized as and trade. The SRR and SIR did not Acropora species provided in the genus ‘‘common.’’ Overall abundance was provide any other species-specific description above, A. aculeus may be described as ‘‘usually common in the information on the effects of these susceptible to the effects of ocean central Indo-Pacific, uncommon threats on A. aculeus. We interpreted acidification on skeletal growth. Genus- elsewhere.’’ Veron did not infer the threat susceptibility and exposure level information also suggests that A. abundance trend results from these data. information from the SRR and SIR in the aculeus is susceptible to trophic effects As described in the Indo-Pacific Species proposed rule for A. aculeus’ of fishing, sedimentation, nutrients, Determinations introduction above, vulnerabilities as follows: High predation, sea-level rise, and collection based on results from Richards et al. vulnerability to ocean warming, and trade. Thus, based on the available (2008) and Veron (2014), the absolute moderate vulnerabilities to disease, species-specific and genus information abundance of this species is likely at acidification, trophic effects of fishing, summarized above, A. aculeus is likely least tens of millions of colonies. nutrient over-enrichment, and highly susceptible to ocean warming, predation, and low vulnerabilities to and also likely has some susceptibilities Carpenter et al. (2008) extrapolated to disease, acidification, trophic effects species abundance trend estimates from sedimentation, sea-level rise, and collection and trade. of fishing, sedimentation, nutrients, total live coral cover trends and habitat predation, sea-level rise, and collection types. For A. aculeus, the overall Public comments provided some and trade. The available information decline in abundance (‘‘Percent supplemental information on A. does not support more precise ratings of Population Reduction’’) was estimated aculeus’ threat susceptibilities. One the susceptibilities of A. aculeus to the at 37 percent, and the decline in comment stated that A. aculeus is more threats. abundance before the 1998 bleaching susceptible to predation than indicated event (‘‘Back-cast Percent Population in the proposed rule because of the Regulatory Mechanisms Reduction’’) was estimated at 15 overlap in the depth ranges of this In the proposed rule we did not percent. However, as summarized above species with crown of thorns starfish. In provide any species-specific in the Inter-basin Comparisons sub- addition, we gathered the following information on the regulatory section, live coral cover trends are species-specific and genus-level mechanisms or conservation efforts for highly variable both spatially and supplemental information on this A. aculeus. Public comments were temporally, producing patterns on small species’ threat susceptibilities. Acropora critical of that approach, and we scales that can be easily taken out of aculeus has been rated as moderately or therefore attempt to analyze regulatory context. Thus quantitative inferences to highly susceptible to bleaching, but this mechanisms and conservation efforts on species-specific trends should be rating is not based on species-specific a species basis, where possible, in this interpreted with caution. At the same data (Carpenter et al., 2008). Done et al. final rule. Records confirm that A. time, an extensive body of literature (2003b) report 20 percent of A. aculeus aculeus occurs in 68 Indo-Pacific documents broad declines in live coral colonies were affected by bleaching on ecoregions that encompass 39 countries’ cover and shifts to reef communities the GBR in 2002, and the species ranked EEZs. The 39 countries are Australia, dominated by hardier coral species or 31st in proportion of coral colonies on Bangladesh, Brunei, China, Comoros algae over the past 50 to 100 years the GBR that were bleached and killed Islands, Federated States of Micronesia, (Birkeland, 2004; Fenner, 2012; Pandolfi out of 52 studied Acropora species. That Fiji, France (French Pacific Island et al., 2003; Sale and Szmant, 2012). is, 30 of the 52 species bleached more Territories), India (including Andaman These changes have likely occurred and than A. aculeus, and 21 bleached less. and Nicobar Islands), Indonesia, Japan, are occurring from a combination of Bonin (2012) reported that A. aculeus Kenya, Kiribati, Madagascar, Malaysia, global and local threats. Given that A. had a ‘‘high’’ susceptibility to bleaching Maldives, Marshall Islands, Mauritius, aculeus occurs in many areas affected in Kimbe Bay, Papua New Guinea on a Mozambique, Myanmar, New Zealand by these broad changes, and that it is scale of ‘‘severe,’’ ‘‘high,’’ ‘‘moderate,’’ (Tokelau), Niue, Palau, Papua New likely has some susceptibility to both and ‘‘lowest.’’ Acropora aculeus was Guinea, Philippines, Samoa, Seychelles, global and local threats, we conclude fourth highest out of 16 species, with 50 Solomon Islands, South Africa, Sri that it is likely to have declined in percent of colonies either severely Lanka, Taiwan, Tanzania, Thailand, abundance over the past 50 to 100 years, bleached or dead. The most severely Tonga, Tuvalu, United Kingdom (British but quantification is not possible based affected species had 74 percent of Indian Ocean Territory and Pitcairn on the limited species-specific colonies either severely bleached or Islands), United States (CNMI, Guam, information. dead (Bonin, 2012). American Samoa, PRIAs), Vanuatu, and

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Vietnam. The regulatory mechanisms above, affect its vulnerability to assessment of whether this species relevant to A. aculeus, described first as extinction currently and over the meets the definition of either a the percentage of the above countries foreseeable future. Its geographic threatened or endangered coral largely that utilize them to any degree, and distribution includes most of the coral in response to public comments, second as the percentages of those reef ecoregions in the Indian Ocean and including more appropriate countries whose regulatory mechanisms western and central Pacific Ocean. Its consideration of the buffering capacity may be limited in scope, are as follows: geographic distribution moderates of this species’ spatial and demographic General coral protection (28 percent vulnerability to extinction because some traits to lessen its vulnerability to with 8 percent limited in scope), coral areas within its range are projected to threats. Thus, based on the best collection (56 percent with 31 percent have less than average warming and available information above on A. limited in scope), pollution control (38 acidification over the foreseeable future, aculeus’ spatial structure, demography, percent with 10 percent limited in including the western Indian Ocean, the threat susceptibilities, and management, scope), fishing regulations on reefs (95 central Pacific, and other areas, so none of the five ESA listing factors, percent with 26 percent limited in portions of the population in these areas alone or in combination, are causing scope), and managing areas for will be less exposed to severe this species to be likely to become protection and conservation (97 percent conditions. Its depth range is from low endangered throughout its range within with 8 percent limited in scope). The tide to at least 20 meters. This the foreseeable future, and thus it is not most common regulatory mechanisms in moderates vulnerability to extinction warranted for listing at this time, place for A. aculeus are reef fishing over the foreseeable future because because: regulations and area management for deeper areas of its range will usually (1) Acropora aculeus’ distribution protection and conservation. Coral have lower irradiance than surface across the Indian Ocean and most of the collection laws are also somewhat waters, and acidification is generally Pacific Ocean is spread over a very large common for the species, but 31 percent predicted to accelerate most in waters area. While some areas within its range of coral collection laws are limited in that are deeper and cooler than those in are projected to be affected by warming scope and may not provide substantial which the species occurs. Its and acidification, other areas are protection. General coral protection and predominant habitat is shallow lagoons, projected to have less than average pollution control laws are much less and it is found in other habitats warming and acidification, including common regulatory mechanisms for the protected from direct wave action on the western Indian Ocean, the central management of A. aculeus. back-reefs and reef slopes. This Pacific, and other areas. This moderates vulnerability to extinction distribution and the heterogeneous Vulnerability to Extinction over the foreseeable future because the habitats it occupies reduce exposure to As explained above in the Risk species is not limited to one habitat type any given threat event or adverse Analyses section, a species’ but occurs in numerous types of reef condition that does not occur uniformly vulnerability to extinction results from environments that will, on local and throughout the species range. As the combination of its spatial and regional scales, experience highly explained above in the Threats demographic characteristics, threat variable thermal regimes and ocean Evaluation section, we have not susceptibilities, and consideration of the chemistry at any given point in time. Its identified any threat that is expected to baseline environment and future absolute abundance of at least tens of occur uniformly throughout the species projections of threats. The SRR stated millions of colonies, combined with range within the foreseeable future); that the high bleaching rate of the spatial variability in ocean warming and (2) Acropora aculeus’ total absolute Acropora genus is the primary known acidification across the species range, abundance is at least tens of millions of threat of extinction for A. aculeus. It moderates vulnerability to extinction colonies, providing buffering capacity in listed factors that reduce A. aculeus’ because the increasingly severe the form of absolute numbers of threat of extinction including its conditions expected in the foreseeable colonies and variation in susceptibility geographic range, depth range, future will be non-uniform and between individual colonies. As abundance, and variable habitats. therefore will likely be a large number discussed in the Corals and Coral Reefs Subsequent to the proposed rule, we of colonies that are either not exposed section above, the more colonies a received and gathered supplemental or do not negatively respond to a threat species has, the lower the proportion of species- or genus-specific information, at any given point in time. colonies that are likely to be exposed to described above, that expands our a particular threat at a particular time, knowledge regarding the species Listing Determination and all individuals that are exposed will abundance, distribution, and threat In the proposed rule using the not have the same response; and susceptibilities. We developed our determination tool formula approach, A. (3) It is a broadcast spawner and fast assessment of the species’ vulnerability aculeus was proposed for listing as grower, enhancing recovery potential to extinction using all the available threatened because of: High from mortality events as described in information. As explained in the Risk vulnerability to ocean warming (ESA the Corals and Coral Reefs section Analyses section, our assessment in this Factor E); moderate vulnerability to above. final rule emphasizes the ability of the disease (C) and acidification (E); Notwithstanding the projections species’ spatial and demographic traits common generalized range wide through 2100 that indicate increased to moderate or exacerbate its abundance (E); wide overall distribution severity over time of the three high vulnerability to extinction, as opposed (based on wide geographic distribution importance threats, the combination of to the approach we used in the and moderate depth distribution (E); these biological and environmental proposed rule, which emphasized the and inadequacy of existing regulatory characteristics indicates that the species species’ susceptibility to threats. mechanisms (D). possesses sufficient buffering capacity The following characteristics of A. In this final rule, we changed the to avoid being in danger of extinction aculeus, in conjunction with the listing determination for A. aculeus within the foreseeable future throughout information described in the Corals and from threatened to not warranted. We its range. It is possible that this species’ Coral Reefs section, Coral Habitat sub- made this determination based on a extinction risk may increase in the section, and Threats Evaluation section more species-specific and holistic future if global threats continue and

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worsen in severity and the species’ The public comments and (2014), the absolute abundance of this exposure to the threats increases information we gathered provided species is likely at least tens of millions throughout its range. Should the species information on the distribution and of colonies. experience reduced abundance or range habitat of A. acuminata. One public Carpenter et al. (2008) extrapolated constriction of a certain magnitude, the comment letter stated that A. acuminata species abundance trend estimates from ability of these characteristics to in the Mariana Islands appears to be total live coral cover trends and habitat moderate exposure to threats will restricted to reef flats and upper reef types. For A. acuminata, the overall diminish. However, the species is not slopes in protected to semi-protected decline in abundance (‘‘Percent likely to become of such low abundance areas. Thus, based on all the available Population Reduction’’) was estimated or so spatially fragmented as to be in information, A. acuminata’s habitat can at 35 percent, and the decline in danger of extinction due to depensatory be summarized as follows: Its abundance before the 1998 bleaching processes, the potential effects of predominant habitat is upper reef slopes event (‘‘Back-cast Percent Population environmental stochasticity, or the and mid-slope terraces and shelves in Reduction’’) was estimated at 14 potential for mortality from catastrophic turbid or clear water, and it also occurs percent. However, as summarized above events within the foreseeable future in back-reef habitats including reef flats in the Inter-basin Comparison sub- throughout its range. Therefore, A. and channels. Its depth range is section, live coral cover trends are aculeus is not warranted for listing at approximately two to 20 m depth. We highly variable both spatially and this time under any of the listing factors. gathered supplemental information, temporally, producing patterns on small including Veron (2014), which reports scales that can be easily taken out of Acropora acuminata that A. acuminata is confirmed in 60 of context. Thus, quantitative inferences to Introduction his 133 Indo-Pacific ecoregions and is species-specific trends should be strongly predicted to be found in an interpreted with caution. At the same The SRR and SIR provided the additional 12. Wallace (1999b) reports time, an extensive body of literature following information on A. its occurrence in 23 of her 29 Indo- documents broad declines in live coral acuminata’s morphology and taxonomy. Pacific areas, many of which are cover and shifts to reef communities Morphology was described as typically significantly larger than Veron’s dominated by hardier coral species or forming a tabular base of fused ecoregions. algae over the past 50 to 100 years horizontal branches that turn upward (Birkeland, 2004; Fenner, 2012; Pandolfi Demographic Information and taper to points, and the taxonomy et al., 2003; Sale and Szmant, 2012). was described as having no taxonomic The SRR and SIR provided the These changes have likely occurred, and issues, but colonies turn black when following information on A. are occurring, from a combination of dried. acuminata’s abundance. Acropora global and local threats. Given that A. acuminata has been reported to The public comments and acuminata occurs in many areas occasionally live in extensive clumps information we gathered provided affected by these broad changes, and with dimensions of several meters, and information on the morphology or that it has some susceptibility to both it can be very common in the center of taxonomy of A. acuminata. One public global and local threats, we conclude its range (e.g., Indonesia), but it can be comment letter stated that specimens of that it is likely to have declined in uncommon in the outer parts of its A. acuminata in the Mariana Islands abundance over the past 50 to 100 years, range. The public comments and but a precise quantification is not may be a different species or a distinct information we gathered provided sub-species, based on colony possible based on the limited species- information on the abundance of A. specific information. morphology. We gathered supplemental acuminata. A public comment letter information, including Veron (2014), stated that A. acuminata in the Mariana Other Biological Information which states that this species is Islands is uncommon to rare. We The SRR and SIR provided the distinctive. While the public comments gathered supplemental information, following information on A. and supplemental information provided including Richards (2009) and Richards acuminata’s life history. Like most of its some information on the morphology et al. (2013b), which conclude from congeners, A. acuminata is a broadcast and taxonomy of A. acuminata, it is their data that this species is globally spawner. However, some degree of sufficiently distinctive to be identified widespread, locally restricted, and reproductive isolation probably occurs by experts, thus we conclude that the locally rare, and thus in the second in some locations because the species distribution and abundance information rarest category of Acropora with the does not spawn synchronously with the described below for this species is predicted consequence of persistence. majority of its congeners. The public sufficiently reliable (Fenner, 2014b). They placed 39 species in this category comments and information we gathered Spatial Information out of 85 species of Acropora. Veron provided no additional biological (2014) reports that A. acuminata information. The SRR and SIR provided the occupied 4.7 percent of 2,984 dive sites following information on A. sampled in 30 ecoregions of the Indo- Susceptibility to Threats acuminata’s distribution, habitat, and Pacific, and had a mean abundance To describe A. acuminata’s threat depth range. Acropora acuminata’s rating of 1.21 on a 1 to 5 rating scale at susceptibilities, the SRR and SIR distribution is from the Red Sea to the those sites in which it was found. Based provided genus-level information for the Pitcairn Islands in the eastern Pacific, on this semi-quantitative system, the effects on Acropora of ocean warming, covering 110 million km2, the 5th species’ abundance was characterized as disease, acidification, sedimentation, largest range of 114 Acropora species in ‘‘uncommon.’’ Overall abundance was nutrients, predation, and collection and a large study. In general, its habitat is described as ‘‘sometimes common.’’ trade. The SRR and SIR also stated that upper reef slopes and mid-slope terraces Veron did not infer trends in abundance Acropora acuminata is the only and shelves in turbid or clear water at from these data. As described in the Acropora known to not be preferred as 15–20 m of depth. In Guam, its habitat Indo-Pacific Species Determinations prey by the crown-of-thorns starfish, is deeper reef flat areas and channel introduction above, based on results thus susceptibility to predation appears slopes. from Richards et al. (2008) and Veron to be low. The SRR and SIR did not

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provide any other species-specific Taiwan, Thailand, Tonga, Tuvalu, to the approach we used in the information on the effects of these United Kingdom (British Indian Ocean proposed rule, which emphasized the threats on A. acuminata. The threat Territory, Pitcairn Islands), United species’ susceptibility to threats. susceptibility and exposure information States (CNMI, Guam, American Samoa, The following characteristics of A. from the SRR and SIR was interpreted PRIAs), Vanuatu, Vietnam, and Yemen. acuminata, in conjunction with the in the proposed rule for A. acuminata’s The regulatory mechanisms available to information described in the Corals and vulnerabilities to threats: High A. acuminata, described first as a Coral Reefs section, Coral Habitat sub- vulnerability to ocean warming; percentage of the above countries that section, and Threats Evaluation section moderate vulnerability to disease, utilize them to any degree, and second above, affect its vulnerability to acidification, trophic effects of reef as the percentages of those countries extinction currently and over the fishing, and nutrient over-enrichment; whose regulatory mechanisms may be foreseeable future. Its geographic and low vulnerability to sedimentation, limited in scope, are general coral distribution includes most of the coral sea-level rise, predation, and collection protection (29 percent with 7 percent reef ecoregions in the Indian Ocean and and trade. limited in scope), coral collection (60 western and central Pacific Ocean. Its Public comments did not provide any percent with 29 percent limited in geographic distribution moderates information on A. acuminata’s threat scope), pollution control (45 percent vulnerability to extinction because some susceptibilities. We gathered the with 7 percent limited in scope), fishing areas within its range are projected to following species-specific and genus- regulations on reefs (90 percent with 21 have less than average warming and level supplemental information on this percent limited in scope), and managing acidification over the foreseeable future, species’ threat susceptibilities. Acropora areas for protection and conservation including the western Indian Ocean, the acuminata has been rated as moderately (93 percent with 10 percent limited in central Pacific, and other areas, so or highly susceptible to bleaching and scope). The most common regulatory portions of the population in these areas coral disease, but these ratings are not mechanisms in place for A. acuminata will be less exposed to severe based on species-specific data are reef fishing regulations and area conditions. Its depth range is from 15 to (Carpenter et al., 2008). Based on management for protection and at least 20 meters. This moderates information from other Acropora conservation. Coral collection and vulnerability to extinction over the species provided in the genus pollution control laws are also foreseeable future because deeper areas description above, A. acuminata likely somewhat utilized for the species, but of its range will usually have lower has high susceptibility ocean warming, 29 percent of coral collection laws are irradiance than surface waters, and and also has some susceptibilities to limited in scope and may not provide acidification is generally predicted to coral disease, acidification, trophic substantial protection. General coral accelerate most in waters that are deeper effects of fishing, sedimentation, protection laws are much less and cooler than those in which the nutrients, sea-level rise, predation, and prominent regulatory mechanisms for species occurs. Its habitat includes collection and trade. Thus, based on the the management of A. acuminata. multiple habitat types on both the reef available species-specific and genus slope and back reef. This moderates information summarized above, A. Vulnerability to Extinction vulnerability to extinction over the acuminata is likely highly susceptible As explained above in the Risk foreseeable future because the species is to ocean warming, likely has some Analyses section, a species’ not limited to one habitat type but susceptibilities to disease, acidification, vulnerability to extinction results from occurs in numerous types of reef sedimentation, nutrients, trophic effects the combination of its spatial and environments that will, on local and of fishing, sea-level rise, and collection demographic characteristics, threat regional scales, experience highly and trade, and also has low susceptibilities, and consideration of the variable thermal regimes and ocean susceptibility to predation. baseline environment and future chemistry at any given point in time. In projections of threats. The SRR stated addition, turbidity can mitigate against Regulatory Mechanisms that the high bleaching rate of the the effects of high irradiance by In the proposed rule we did not Acropora genus is the primary known blocking it from the water column in provide any species-specific threat of extinction for A. acuminata. It turbid environments. Its absolute information on the regulatory listed factors that reduce the threat of abundance of at least tens of millions of mechanisms or conservation efforts for extinction including the very wide colonies, combined with spatial A. acuminata. Public comments were geographic range, the broad depth range, variability in ocean warming and ocean critical of that approach, and we the fact that it is often common and acidification across the species’ range, therefore attempt to analyze regulatory sometimes abundant, and the somewhat moderates vulnerability to extinction mechanisms and conservation efforts on broad range of suitable habitats for A. because the increasingly severe a species basis, where possible, in this acuminata. conditions expected in the foreseeable final rule. Records confirm that A. Subsequent to the proposed rule, we future will be non-uniform and acuminata occurs in 60 Indo-Pacific received and gathered supplemental therefore will likely be a large number ecoregions that encompass 42 countries’ species- or genus-specific information, of colonies that are either not exposed EEZs. The 42 countries are Australia, described above, that expands our or do not negatively respond to a threat Brunei, China, Comoros Islands, knowledge regarding the species at any given point in time. Djibouti, Egypt, Eritrea, Federated States abundance, distribution, and threat of Micronesia, Fiji, France (French susceptibilities. We developed our Listing Determination Pacific Island Territories), Indonesia, assessment of the species’ vulnerability In the proposed rule, using the Israel, Japan, Jordan, Kiribati, to extinction using all the available determination tool formula, A. Madagascar, Malaysia, Maldives, information. As explained in the Risk acuminata was proposed for listing as Marshall Islands, Mauritius, Myanmar, Analyses section, our assessment in this threatened because of: High Nauru, New Zealand (Tokelau), Niue, final rule emphasizes the ability of the vulnerability to ocean warming (ESA Palau, Papua New Guinea, Philippines, species’ spatial and demographic traits Factor E); moderate vulnerability to Samoa, Saudi Arabia, Seychelles, to moderate or exacerbate its disease (C) and acidification (E); Solomon Islands, Sri Lanka, Sudan, vulnerability to extinction, as opposed uncommon generalized range wide

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abundance (E); wide overall distribution Notwithstanding the projections species in a large study. It occurs in a (based on wide geographic distribution through 2100 that indicate increased broad range of habitats and its depth and moderate depth distribution (E); severity over time of the three high range as low tide to at least 10 m. and inadequacy of existing regulatory importance threats, the combination of The public comments did not provide mechanisms (D). these biological and environmental supplemental information on A. In this final rule, we changed the characteristics indicates that the species aspera’s distribution. We gathered listing determination for A. acuminata possesses sufficient buffering capacity supplemental information, including from threatened to not warranted. We to avoid being in danger of extinction Veron (2014), which reports that this made this determination based on a within the foreseeable future throughout species is confirmed in 68 of his 133 more species-specific and holistic its range. It is possible that this species’ Indo-Pacific ecoregions, and is strongly assessment of whether this species extinction risk may increase in the predicted to be found in an additional meets the definition of either a future if global threats continue and 17. Wallace (1999b) reports its threatened or endangered coral largely increase in severity and the species occurrence in 21 of her 29 Indo-Pacific in response to public comments, exposure to threats increases throughout areas, many of which are significantly including more appropriate its range. Should the species experience larger than Veron’s ecoregions, and consideration of the buffering capacity reduced abundance or range Richards (2009) calculated the of this species’ spatial and demographic constriction of a certain magnitude, the geographic range of A. aspera at 70 traits to lessen its vulnerability to ability of these characteristics to million km 2. Wallace (1999b) describes threats. Thus, based on the best moderate exposure to threats will its habitat as ‘‘intertidal/shallow available information above on A. diminish. However, the species is not subtidal,’’ and in much of its range the acuminata’s spatial structure, likely to become of such low abundance species is confined to reef flats. Thus, demography, threat susceptibilities, and or so spatially fragmented as to be in based on all the available information, management, none of the five ESA danger of extinction due to depensatory A. aspera’s habitat can be summarized listing factors, alone or in combination, processes, the potential effects of as follows: The species occurs in a are causing this species to become environmental stochasticity, or the broad range of habitats on the reef slope endangered throughout its range within potential for mortality from catastrophic and back-reef, including but not limited the foreseeable future, and thus it is not events within the foreseeable future to lower reef crests, upper reef slopes, warranted for listing at this time, throughout its range. Therefore, A. reef flats, and lagoons. Its depth range because: acuminata is not warranted for listing at is approximately low tide to 20 m depth. (1) Acropora acuminata’s distribution this time under any of the listing factors. across the Indian Ocean and most of the Acropora aspera Demographic Information Pacific Ocean is spread over a very large The SRR and SIR provided the area. While some areas within its range Introduction following information on A. aspera’s are projected to be affected by warming The SRR and SIR provided the abundance. Acropora aspera has been and acidification, other areas are following information on A. aspera’s reported as sometimes locally common projected to have less than average morphology and taxonomy. The and it can occasionally live in extensive warming and acidification, including morphology was described as clumps with dimensions of several the western Indian Ocean, the central arborescent or bushy clumps which may meters. Pacific, and other areas. This have largely vertical branches, and the The public comments and distribution and the heterogeneous taxonomy was described as having no information we gathered provided habitats it occupies reduce exposure to taxonomic issues. information on the abundance of A. any given threat event or adverse The public comments did not provide aspera. One public comment letter condition that does not occur uniformly supplemental information on stated that A. aspera is relatively limited throughout the species’ range. As morphology. We gathered supplemental in abundance in Guam compared to co- explained in the Threats Evaluation information, including van Oppen et al. occurring arborescent species such as section, we have not identified any (2001), which found that A. aspera is Acropora pulchra and Acropora threat that is expected to occur the only genetically distinct member of muricata. We gathered supplemental uniformly throughout the species’ range the A. aspera group of Acropora species, information, including Veron (2014), within the foreseeable future; a group of morphologically similar which reports that A. aspera occupied (2) Acropora acuminata’s total species that hybridize at least 7.5 percent of 2,984 dive sites sampled absolute abundance is at least tens of occasionally. Other supplemental in 30 ecoregions of the Indo-Pacific, and millions of colonies, providing buffering information we gathered was Veron had a mean abundance rating of 1.76 on capacity in the form of absolute (2014), which states that A. aspera is a 1 to 5 rating scale at those sites in numbers of colonies and variation in distinctive, thus we conclude it is which it was found. Based on this semi- susceptibility between individual sufficiently distinctive to be identified quantitative system, the species’ colonies. As discussed in the Corals and by experts, and that the distribution and abundance was characterized as Coral Reefs section above, the more abundance information described below ‘‘common.’’ Overall abundance was colonies a species has, the lower the for this species is sufficiently reliable described as ‘‘sometimes common.’’ proportion of colonies that are likely to (Fenner, 2014b). Veron did not infer trends in abundance be exposed to a particular threat at a from these data. Acropora aspera is a particular time, and all the individuals Spatial Information reef flat species, and reef flats have a that are exposed will not have the same The SRR and SIR provided the larger global area than reef slopes response; and following information on A. aspera’s (Vecsei, 2004). This information is (3) It is a broadcast spawner and fast distribution, habitat, and depth range. relevant because most coral abundance grower, enhancing recovery potential Acropora aspera is distributed from the surveys are carried out only on reef from mortality events as described in Red Sea to the Samoan Islands. The slopes, and thus may significantly the Corals and Coral Reefs section species has a relatively broad range, the underestimate the abundance of species above. 46th largest range of 114 Acropora such as A. aspera that are more common

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on reef-flats than reef slopes. In aborted in years with storm impacts. Band has been found in A. aspera. They American Samoa, A. aspera forms Asexual reproduction can account for also reported that bushy Acropora had clumps on reef flats many meters across, the majority of A. aspera population high susceptibility to Skeletal Eroding as much as about 100 m some places (D. structure in certain areas and can lead Band on the GBR, with a prevalence of Fenner, personal comm.). Richards to local dominance. 3.1 percent. Skeletal Eroding Band is the (2009) and Richards et al. (2013b) The public comments provided no most prevalent disease on the GBR. A conclude from their data that this supplemental biological information. study of the effects of near-term ocean species is globally widespread, locally We gathered the following information. acidification and elevated seawater restricted, and locally common, and In a study of biological traits of coral temperature on the physiology of A. thus in one of the categories of highest species, Darling et al. (2012) found that aspera suggested that gene expression of abundance with the predicted all of over 30 Acropora species studied key metabolic proteins is impacted by consequence of persistence. As were classified as ‘‘competitive’’ species the synergistic effects of near term ocean described in the Indo-Pacific Species which were considered to be less acidification (i.e., the conditions Determinations introduction above, tolerant of environmental stress and expected to result from 50 to 90 ppm based on results from Richards et al. disturbance than those species that were CO2 above current atmospheric levels) (2008) and Veron (2014), the absolute classified as ‘‘stress-tolerant,’’ and ocean warming (Ogawa et al., abundance of this species is likely at ‘‘generalist,’’ or ‘‘weedy’’, because of 2013b). Acropora aspera is a preferred least tens of millions of colonies. documented shifts in coral communities prey of crown-of-thorns seastar (Sonoda Carpenter et al. (2008) extrapolated from ‘‘competitive’’ to the other and Paul, 1993). With regard to species abundance trend estimates from categories. Acropora aspera was one of sedimentation, A. aspera was found to total live coral cover trends and habitat the Acropora species studied, and was be relatively tolerant of silty, turbid types. For A. aspera, the overall decline classified as ‘‘competitive’’ as were all water in the South China Sea (Latypov in abundance (‘‘Percent Population other Acropora species. and Dautova, 2005). No other species- Reduction’’) was estimated at 37 Susceptibility to Threats specific information is available for the percent, and the decline in abundance susceptibility of A. aspera to any other before the 1998 bleaching event (‘‘Back- To describe A. aspera’s threat threat. cast Percent Population Reduction’’) susceptibilities, the SRR and SIR Based on the available genus-level was estimated at 15 percent. However, provided genus-level information for the and species-specific information, A. as summarized above in the Inter-basin effects on Acropora of ocean warming, aspera is likely highly susceptible to Comparison sub-section, live coral cover disease, acidification, sedimentation, ocean warming, and it also likely has trends are highly variable both spatially nutrients, predation, and collection and some susceptibilities to disease, and temporally, producing patterns on trade. The SRR and SIR did not provide acidification, trophic effects of fishing, small scales that can be easily taken out any species-specific information on the sedimentation, nutrients, sea-level rise, of context, thus quantitative inferences effects of these threats on A. aspera. The predation, and collection and trade. The of species-specific trends should be threat exposure and susceptibility available information does not support interpreted with caution. At the same information from the SRR and SIR was more precise ratings of the time, an extensive body of literature interpreted in the proposed rule for A. susceptibilities of A. aspera to the documents broad declines in live coral aspera’s vulnerabilities to threats as threats. cover and shifts to reef communities follows: High vulnerability to ocean Regulatory Mechanisms dominated by hardier coral species or warming, moderate vulnerabilities to algae over the past 50 to 100 years disease, acidification, trophic effects of In the proposed rule we did not (Birkeland, 2004; Fenner, 2012; Pandolfi fishing, nutrients, and predation, and provide any species-specific et al., 2003; Sale and Szmant, 2012). low vulnerabilities to sedimentation, information on the regulatory These changes have likely occurred, and sea-level rise, and collection and trade. mechanisms or conservation efforts for are occurring, from a combination of Public comments did not provide A. aspera. Public comments were global and local threats. Given that A. supplemental information on A. critical of that approach, and we aspera occurs in many areas affected by aspera’s threat susceptibilities. We therefore attempt to analyze regulatory these broad changes, and that it has gathered the following species-specific mechanisms and conservation efforts on some susceptibility to both global and and genus-level supplemental a species basis, where possible, in this local threats, we conclude that it is information on this species’ threat final rule. Records confirm that likely to have declined in abundance susceptibilities. Acropora aspera was Acropora aspera occurs in 68 Indo- over the past 50 to 100 years, but a rated as moderately or highly Pacific ecoregions that encompass 44 precise quantification is not possible susceptible to bleaching and disease, countries’ EEZs. The 44 countries are based on the limited species-specific but this rating is not based on species- Australia (including Cocos-Keeling information. specific data (Carpenter et al., 2008). Islands), Bahrain, Brunei, Cambodia, Done et al. (2003b) reported that 33 China, Federated States of Micronesia, Other Biological Information percent of A. aspera’s colonies on the Fiji, France (French Pacific Island The SRR and SIR provided the GBR were affected by bleaching in 2002, Territories), India (including Andaman following information on A. aspera’s and the species ranked 9th in and Nicobar Islands), Indonesia, Iran, life history. Acropora aspera is a proportion of coral colonies that were Japan, Kiribati, Kuwait, Madagascar, hermaphroditic spawner. While it is a bleached out of 52 studied Acropora Malaysia, Maldives, Marshall Islands, participant in mass broadcast spawning species. That is, eight of the 52 species Mauritius, Myanmar, New Zealand in some localities, asynchronous gamete bleached more than A. aspera, and 43 (Tokelau), Niue, Oman, Palau, Papua development on the Great Barrier Reef bleached less. New Guinea, Philippines, Qatar, Samoa, and New Caledonia may provide a Acropora aspera experiences sub- Saudi Arabia, Seychelles, Singapore, degree of reproductive isolation, acute black-band disease (UNEP, 2010), Solomon Islands, Sri Lanka, Taiwan, although A. aspera has been shown to as well as ciliate infections (Antonius Thailand, Timor-Leste, Tonga, Tuvalu, hybridize with other acroporids. Gamete and Lipscomb, 2000). Page and Willis United Arab Emirates, United Kingdom development in A. aspera may be (2007) reported that Skeletal Eroding (British Indian Ocean Territory), United

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States (CNMI, Guam, American Samoa, The following characteristics of A. this determination based on a more PRIAs), Vanuatu, Vietnam, and Yemen. aspera, in conjunction with the species-specific and holistic assessment The regulatory mechanisms available to information described in the Corals and of whether this species meets the A. aspera, described first as a percentage Coral Reefs section, Coral Habitat sub- definition of either a threatened or of the above countries that utilize them section, and Threats Evaluation section endangered coral largely in response to to any degree, and second as the above, affect its vulnerability to public comments, including more percentage of those countries whose extinction currently and over the appropriate consideration of the regulatory mechanisms are limited in foreseeable future. Its geographic buffering capacity of this species’ spatial scope, are as follows: General coral distribution includes most of the coral and demographic traits to lessen its protection (32 percent with 9 percent reef ecoregions in the Indian Ocean and vulnerability to threats. Thus, based on limited in scope), coral collection (52 western and central Pacific Ocean. Its the best available information above on percent with 25 percent limited in geographic distribution moderates A. aspera’ spatial structure, scope), pollution control (43 percent vulnerability to extinction because some demography, threat susceptibilities, and with 7 percent limited in scope), fishing areas within its range are projected to management, none of the five ESA regulations on reefs (91 percent with 23 have less than average warming and listing factors, alone or in combination, percent limited in scope), and managing acidification over the foreseeable future, are causing this species to be likely to areas for protection and conservation including the western Indian Ocean, the become endangered throughout its range (89 percent with 9 percent limited in central Pacific, and other areas, so within the foreseeable future, and thus scope). The most common regulatory portions of the population in these areas it is not warranted for listing at this mechanisms in place for A. aspera are will be less exposed to severe time, because: reef fishing regulations and area conditions. Its depth range is from low (1) Acropora aspera’s distribution is management for protection and tide to at least 10 meters. Assuming that spread over a very large area. While conservation. Coral collection and the species’ depth distribution is limited some areas within its range are pollution control laws are also to 10 meters, this exacerbates projected to be affected by warming and somewhat utilized for the species, but vulnerability to extinction over the acidification, other areas are projected 25 percent of coral collection laws are foreseeable future because shallow areas to have less than average warming and limited in scope and may not provide are more likely to be affected by acidification, including the western substantial protection. General coral warming-induced bleaching and disease Indian Ocean, the central Pacific, and protection laws are much less common than deeper areas. Its habitat includes other areas. This distribution and the regulatory mechanisms for the lower reef crests, upper reef slopes, reef heterogeneous habitats it occupies management of A. aspera. flats, and lagoons. This moderates reduce exposure to any given threat vulnerability to extinction over the event or adverse condition that does not Vulnerability to Extinction foreseeable future because the species is occur uniformly throughout the species range. As explained above in the As explained above in the Risk not limited to one habitat type but Threats Evaluation section, we have not Analyses section, a species’ occurs in numerous types of reef identified any threat that is expected to vulnerability to extinction results from environments that will, on local and occur uniformly throughout the species the combination of its spatial and regional scales, experience highly range within the foreseeable future; demographic characteristics, threat variable thermal regimes and ocean chemistry at any given point in time. Its (2) Acropora aspera’s absolute susceptibilities, and consideration of the abundance is at least tens of millions of baseline environment and future absolute abundance of at least tens of millions of colonies, combined with colonies, providing buffering capacity in projections of threats. The SRR stated spatial variability in ocean warming and the form of absolute numbers of that the high bleaching rate of the acidification across the species range, colonies and variation in susceptibility Acropora genus is the primary known moderates vulnerability to extinction between individual colonies. As threat of extinction for A. aspera. It because the increasingly severe discussed in the Corals and Coral Reefs listed factors that reduce the threat of conditions expected in the foreseeable section above, the more colonies a extinction including the wide future will be non-uniform and species has, the lower the proportion of geographic range, the fact that it is often therefore will likely be a large number colonies that are likely to be exposed to common and sometimes abundant, and of colonies that are either not exposed a particular threat at a particular time, the somewhat broad range of suitable or do not negatively respond to a threat and all individuals that are exposed will habitats for A. aspera. at any given point in time. not have the same response; and Subsequent to the proposed rule, we (3) It is a broadcast spawner and fast received and gathered supplemental Listing Determination grower, enhancing recovery potential species- or genus-specific information, In the proposed rule using the from mortality events as described in described above, that expands our determination tool formula approach, A. the Corals and Coral Reefs section knowledge regarding the species aspera was proposed for listing as above. abundance, distribution, and threat threatened because of: High Notwithstanding the projections susceptibilities. We developed our vulnerability to ocean warming (ESA through 2100 that indicate increased assessment of the species’ vulnerability Factor E); moderate vulnerability to severity over time of the three high to extinction using all the available disease (C) and acidification (E); importance threats, the combination of information. As explained in the Risk common generalized range wide these biological and environmental Analyses section, our assessment in this abundance (E); narrow overall characteristics indicates that the species final rule emphasizes the ability of the distribution (based on moderate possesses sufficient buffering capacity species’ spatial and demographic traits geographic distribution and shallow to avoid being in danger of extinction to moderate or exacerbate its depth distribution (E); and inadequacy within the foreseeable future throughout vulnerability to extinction, as opposed of existing regulatory mechanisms (D). its range. It is possible that this species’ to the approach we used in the In this final rule, we changed the extinction risk may increase in the proposed rule, which emphasized the listing determination for A. aspera from future if global threats continue and species’ susceptibility to threats. threatened to not warranted. We made worsen in severity and the species’

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exposure to the threats increases complexity, including ridges, furrows, Reduction’’) was estimated at 14 throughout its range. Should the species walls, caves, and other structures, percent. However, as summarized above experience reduced abundance or range collectively providing highly diverse in the Inter-basin Comparison sub- constriction of a certain magnitude, the coral habitats. section, live coral cover trends are ability of these characteristics to The public comments did not provide highly variable both spatially and moderate exposure to threats will supplemental information on A. temporally, producing patterns on small diminish. However, the species is not dendrum’s distribution. We gathered scales that can be easily taken out of likely to become of such low abundance supplemental information, including context, thus quantitative inferences of or so spatially fragmented as to be in Veron (2014), which reports that this species-specific trends should be danger of extinction due to depensatory species is confirmed in 32 of his 133 interpreted with caution. At the same processes, the potential effects of Indo-Pacific ecoregions, and is strongly time, an extensive body of literature environmental stochasticity, or the predicted to be found in an additional documents broad declines in live coral potential for mortality from catastrophic 20. Wallace (1999b) reports its cover and shifts to reef communities events within the foreseeable future occurrence in nine of her 29 Indo- dominated by hardier coral species or throughout its range. Therefore, A. Pacific areas, many of which are algae over the past 50 to 100 years aculeus is not warranted for listing at significantly larger than Veron’s (Birkeland, 2004; Fenner, 2012; Pandolfi this time under any of the listing factors. ecoregions, and Richards (2009) et al., 2003; Sale and Szmant, 2012). reported the species as having the 48th These changes have likely occurred, and Acropora dendrum smallest range of 114 Acropora species are occurring, from a combination of Introduction in a large study and calculated the global and local threats. Given that A. geographic range at over 20 million km2. dendrum occurs in many areas affected The SRR and SIR provided the Acropora dendrum occurs on exposed by these broad changes, and that it has following information on A. dendrum’s reef fronts where Acropora diversity is some susceptibility to both global and morphology and taxonomy. The high (Veron and Wallace, 1984). The local threats, we conclude that it is morphology was described as plates 0.5 public comments and information we likely to have declined in abundance to1 m diameter, with widely spaced gathered provided nothing additional on over the past 50 to 100 years, but a vertical branchlets, and taxonomy was A. dendrum’s habitat and depth range. precise quantification is not possible described as having no taxonomic Demographic Information based on the limited species-specific issues. However, A. dendrum is ‘‘poorly information. characterized and may indeed be a The SRR and SIR provided the ‘phantom’ species, being made up from following information on A. dendrum’s Other Biological Information specimens that cannot be allocated to abundance. Acropora dendrum has been The SRR and SIR provided the other species.’’ However, the BRT treats reported as uncommon or rare. following information on A. dendrum’s it as a nominal species. They stated that The public comments did not provide life history. Like most of its congeners, it is most similar to Heteropora supplemental information on A. A. dendrum is a hermaphroditic appressa and A. microclados. dendrum’s abundance. We gathered spawner (Mezaki et al., 2007; Wallace, The public comments did not provide supplemental information, which 1985) with lecithotrophic (yolk-sac) supplemental information on indicates that there are no locations larvae (Baird et al., 2009). The public morphology or taxonomy. We gathered recorded where A. dendrum is common comments and information we gathered supplemental information, which or even more abundant than a rare provided no supplemental biological confirmed that while there is some species (Wallace, 1999b). Veron (2014) information. taxonomic uncertainty for A. dendrum, provides a much more detailed range it is recognized as valid by experts map for this species than the maps used Susceptibility to Threats (Veron, 2000; Veron, 2014; Wallace, in the SRR, and reports that A. dendrum To describe A. dendrum’s threat 1999b). Veron (2014) states that A. occupied 2.0 percent of 2,984 dive sites susceptibilities, the SRR and SIR dendrum is distinctive, thus we sampled in 30 ecoregions of the Indo- provided genus-level information for the conclude it is sufficiently distinctive to Pacific, and had a mean abundance effects on Acropora of ocean warming, be identified by experts, and that the rating of 1.11 on a 1 to 5 rating scale at disease, acidification, sedimentation, distribution and abundance information those sites in which it was found. Based nutrients, predation, and collection and described below for this species is on this semi-quantitative system, the trade. The SRR and SIR did not provide sufficiently reliable (Fenner, 2014b). species’ abundance was characterized as any other species-specific information ‘‘uncommon.’’ Overall abundance was on the effects of these threats on A. Spatial Information described as ‘‘rare.’’ Veron did not infer dendrum. We interpreted the threat The SRR and SIR provided the trends in abundance from these data. As susceptibility and exposure information following information on A. dendrum’s described in the Indo-Pacific Species from the SRR and SIR in the proposed distribution, habitat, and depth range. Determinations introduction above, rule for A. dendrum’s vulnerabilities as Acropora dendrum is distributed from based on results from Richards et al. follows: High vulnerability to ocean the north-central Indian Ocean to Fiji, (2008) and Veron (2014), the absolute warming, moderate vulnerabilities to and from Japan to the Great Barrier Reef. abundance of this species is likely at disease, acidification, trophic effects of The species’ predominant habitat is least tens of millions of colonies. fishing, nutrients, and predation, and upper reef slopes and mid-slope Carpenter et al. (2008) extrapolated low vulnerabilities to sedimentation, terraces, and its depth range is 5 to 20 species abundance trend estimates from sea-level rise, and collection and trade. m. Upper reef slopes and mid-slope total live coral cover trends and habitat Public comments did not provide terraces extend seaward from the reef types. For A. dendrum, the overall supplemental information on A. crest toward the open ocean, forming decline in abundance (‘‘Percent dendrum’s threat susceptibilities. We one of the most common and Population Reduction’’) was estimated gathered the following species-specific widespread coral reef habitats. They at 35 percent, and the decline in and genus-level supplemental vary in gradient from gentle to steep, abundance before the 1998 bleaching information on this species’ threat and include a great deal of physical event (‘‘Back-cast Percent Population susceptibilities. Acropora dendrum has

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been rated as moderately or highly vulnerability to extinction results from foreseeable future because upper reef susceptible to bleaching and disease, the combination of its spatial and slopes and mid-slope terraces are but these ratings are not based on demographic characteristics, threat physically diverse and widespread, thus species-specific data (Carpenter et al., susceptibilities, and consideration of the the species occurs in reef environments 2008). Based on information from other baseline environment and future that will, on local and regional scales, Acropora species provided in the genus projections of threats. The SRR stated experience highly variable thermal description above, A. dendrum is likely that the high bleaching rate of the regimes and ocean chemistry at any to be highly susceptible to ocean Acropora genus is the primary known given point in time. Its absolute warming, and also has some threat of extinction for A. dendrum. It abundance of at least tens of millions of susceptibilities to disease, acidification, listed factors that reduce the threat of colonies, combined with spatial trophic effects of fishing, sedimentation, extinction, including the fairly wide variability in ocean warming and nutrients, sea-level rise, predation, and geographic range, the depth range, and acidification across the species range, collection and trade. The available the somewhat broad range of suitable moderates vulnerability to extinction information does not support more habitats. because the increasingly severe precise ratings of the susceptibilities of Subsequent to the proposed rule, we conditions expected in the foreseeable A. dendrum to the threats. received and gathered supplemental future will be non-uniform and species- or genus-specific information, therefore will likely be a large number Regulatory Mechanisms described above, that expands our of colonies that are either not exposed In the proposed rule, we did not knowledge regarding the species or do not negatively respond to a threat provide any species-specific abundance, distribution, and threat at any given point in time. information on the regulatory susceptibilities. We developed our mechanisms or conservation efforts for assessment of the species’ vulnerability Listing Determination A. dendrum. Public comments were to extinction using all the available In the proposed rule using the critical of that approach, and we information. As explained in the Risk determination tool formula approach, A. therefore attempt to analyze regulatory Analyses section, our assessment in this dendrum was proposed for listing as mechanisms and conservation efforts on final rule emphasizes the ability of the threatened because of: High a species basis, where possible, in this species’ spatial and demographic traits vulnerability to ocean warming (ESA final rule. Acropora dendrum has to moderate or exacerbate its Factor E); moderate vulnerability to confirmed records of occurrence in 32 vulnerability to extinction, as opposed disease (C) and acidification (E); rare Indo-Pacific ecoregions that encompass to the approach we used in the generalized range wide abundance (E); 14 countries’ EEZs. The 14 countries are proposed rule, which emphasized the moderate overall distribution (based on Australia, Brunei, China, France (French species’ susceptibility to threats. moderate geographic distribution and Pacific Island Territories), Indonesia, The following characteristics of A. moderate depth distribution (E); and Japan, Malaysia, Myanmar, Papua New dendrum, in conjunction with the inadequacy of existing regulatory Guinea, Philippines, Solomon Islands, information described in the Corals and mechanisms (D). Thailand, Vanuatu, and Vietnam. The Coral Reefs section, Coral Habitat sub- In this final rule, we changed the regulatory mechanisms available to A. section, and Threats Evaluation section listing determination for A. dendrum dendrum, described first as a percentage above, affect its vulnerability to from threatened to not warranted. We of the above countries that utilize them extinction currently and over the made this determination based on a to any degree, and second as the foreseeable future. Its geographic range more species-specific and holistic percentage of those countries whose extends from western Malaysia to assessment of whether this species regulatory mechanisms are limited in Vanuatu, and southern Japan to the meets the definition of either a scope, are as follows: General coral GBR. On one hand, this moderates threatened or endangered coral largely protection (36 percent with seven vulnerability to extinction because the in response to public comments, percent limited in scope), coral high latitude areas in the northern and including more appropriate collection (57 percent with 29 percent southern portions of its range are consideration of the buffering capacity limited in scope), pollution control (43 projected to have less than average of this species’ spatial and demographic percent with 21 percent limited in warming over the foreseeable future, traits to lessen its vulnerability to scope), fishing regulations on reefs (100 thus populations in these areas will be threats. Thus, based on the best percent with 21 percent limited in less exposed to severe warming available information above on A. scope), and managing areas for conditions. On the other hand, the dendrum’s spatial structure, protection and conservation (93 percent species’ geographic distribution demography, threat susceptibilities, and with none limited in scope). The most exacerbates vulnerability to extinction management, none of the five ESA common regulatory mechanisms in because much of it lies within the listing factors, alone or in combination, place for A. dendrum are reef fishing western equatorial Pacific, an area are causing this species to be likely to regulations and area management for projected to have the highest seawater become endangered throughout its range protection and conservation. Coral temperatures in the foreseeable future. within the foreseeable future, and thus collection and pollution control laws Its depth range is from 5 to 20 meters. it is not warranted for listing at this are also somewhat utilized for the This moderates vulnerability to time, because: species, but 29 percent of those laws are extinction over the foreseeable future (1) Acropora dendrum’s distribution limited in scope and may not provide because deeper areas of its range will is spread over a very large area. While substantial protection. General coral usually have lower irradiance than some areas within its range are protection laws are much less common surface waters, and acidification is projected to be affected by warming and regulatory mechanisms for the generally predicted to accelerate most in acidification, other areas are projected management of A. dendrum. waters that are deeper and cooler than to have less than average warming and those in which the species occurs. Its acidification, including the central Vulnerability to Extinction habitat includes upper reef slopes and Pacific and other areas. This As explained above in the Risk mid-slope terraces. This moderates distribution and the heterogeneous Analyses section, a species’ vulnerability to extinction over the habitats it occupies reduce exposure to

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any given threat event or adverse The public comments did not provide al., 2012) reported that A. donei was condition that does not occur uniformly any new or supplemental information among the second most abundant group throughout the species range. As on morphology or taxonomy. We of corals on Okinotorishima, Japan, and explained above in the Threats gathered supplemental information, was classified as ‘‘common’’ (paper was Evaluation section, we have not which indicated that there is some provided with the comment). We identified any threat that is expected to taxonomic uncertainty with this species, gathered supplemental information, occur uniformly throughout the species but that it is recognized as valid by which reports that A. donei is a range within the foreseeable future; experts (Fukami et al., 2004; Veron, common species on Indonesian reefs (2) Acropora dendrum’s absolute 2000). Veron (2014) states that A. donei and reefs of the South China Sea and abundance is at least tens of millions of is distinctive, thus we conclude it is Japan (Wallace and Wolstenholme, colonies, providing buffering capacity in sufficiently distinctive to be identified 1998). Veron (2014) reports that A. the form of absolute numbers of by experts, and that the distribution and donei occupied 4.7 percent of 2,984 abundance information described below colonies and variation in susceptibility dive sites sampled in 30 ecoregions of for this species is sufficiently reliable between individual colonies. As the Indo-Pacific, and had a mean discussed in the Corals and Coral Reefs (Fenner, 2014b). abundance rating of 1.16 on a 1 to 5 section above, the more colonies a Spatial Information rating scale at those sites in which it species has, the lower the proportion of was found. Based on this semi- colonies that are likely to be exposed to The SRR and SIR provided the a particular threat at a particular time, following information on A. donei’s quantitative system, the species’ and all individuals that are exposed will distribution, habitat, and depth range. abundance was characterized as not have the same response; and Acropora donei is distributed from the ‘‘uncommon,’’ and overall abundance (3) As with other Acropora species, it northern Indian Ocean to the central was also described as ‘‘uncommon.’’ is a broadcast spawner and fast grower, Indo-Pacific, and from Australia to Veron did not infer trends in abundance enhancing recovery potential from Japan. They reported that it had the 44th from these data. As described in the mortality events. largest range of 114 Acropora species Indo-Pacific Species Determinations Notwithstanding projections through examined. The species’ habitat is upper introduction above, based on results 2100 that indicate increased severity reef slopes and mid-slope terraces. It from Richards et al. (2008) and Veron over time of the three high importance may be restricted habitats where (2014), the absolute abundance of this threats, the combination of these Acropora diversity is high, but this species is likely at least tens of millions biological and environmental includes a large proportion of the Indo- of colonies. Pacific’s reef slopes. Its depth range is characteristics indicates that the species Carpenter et al. (2008) extrapolated possesses sufficient buffering capacity 5 to 20 m. The public comments did not provide species abundance trend estimates from to avoid being in danger of extinction total live coral cover trends and habitat within the foreseeable future throughout any new or supplemental information on A. donei’s distribution. We gathered types. For A. donei, the overall decline its range. It is possible that this species’ in abundance (‘‘Percent Population extinction risk may increase in the supplemental information, including Veron (2014), which provides an Reduction’’) was estimated at 37 future if global threats continue and updated, much more detailed range map percent, and the decline in abundance worsen in severity and the species’ for this species than the maps used in before the 1998 bleaching event (‘‘Back- exposure to the threats increases the SRR. Veron reports that A. donei is cast Percent Population Reduction’’) throughout its range. Should the species confirmed in 50 of his 133 Indo-Pacific experience reduced abundance or range was estimated at 15 percent. However, ecoregions, and is strongly predicted to constriction of a certain magnitude, the as summarized above in the Inter-basin be found in an additional 17. Wallace ability of these characteristics to Comparison sub-section, live coral cover (1999b) reports its occurrence in 20 of moderate exposure to threats will trends are highly variable both spatially her 29 Indo-Pacific areas, many of diminish. However, the species is not and temporally, producing patterns on which are significantly larger than likely to become of such low abundance small scales that can be easily taken out Veron’s ecoregions. Acropora donei has or so spatially fragmented as to be in of context, thus quantitative inferences a relatively broad range overall, danger of extinction due to depensatory to species-specific trends should be estimated at 75 million km2 processes, the potential effects of (Richards, interpreted with caution. At the same environmental stochasticity, or the 2009). The public comments and time, an extensive body of literature potential for mortality from catastrophic information we gathered provided documents broad declines in live coral events within the foreseeable future nothing additional on A. donei’s habitat cover and shifts to reef communities throughout its range. Therefore, A. and depth range. dominated by hardier coral species or dendrum is not warranted for listing at Demographic Information algae over the past 50 to 100 years this time under any of the listing factors. The SRR and SIR provided the (Birkeland, 2004; Fenner, 2012; Pandolfi et al., 2003; Sale and Szmant, 2012). Acropora donei following information on A. donei’s abundance. Acropora donei has been These changes have likely occurred, and Introduction reported to be uncommon. Richards are occurring, from a combination of The SRR and SIR provided the (2009) concluded that A. donei is global and local threats. Given that A. following information on A. donei’s globally widespread, locally restricted, donei occurs in many areas affected by morphology and taxonomy. Morphology and locally rare, and thus in the second these broad changes, and that it has was described as table-like, up to 2 m rarest category of Acropora with the some susceptibility to both global and diameter, with branchlets that are predicted consequence of local local threats, we conclude that it is horizontal near the edge but upturned in extinction. The public comments and likely to have declined in abundance the middle, and taxonomy was information we gathered provided over the past 50 to 100 years, but a described as having no taxonomic information on A. donei’s abundance. precise quantification is not possible issues, but being similar in appearance One public comment stated that a based on the limited species-specific to A. yongei. recently published paper (Kayanne et information.

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Other Biological Information Brunei, China, Comoros Islands, species’ spatial and demographic traits The SRR and SIR provided the Djibouti, Eritrea, Federated States of to moderate or exacerbate its following information on A. donei’s life Micronesia, Fiji, France (French Pacific vulnerability to extinction, as opposed history. Acropora donei is a Island Territories), Indonesia, Japan, to the approach we used in the hermaphroditic spawner with Kiribati, Madagascar, Malaysia, proposed rule, which emphasized the Maldives, Marshall Islands, Myanmar, species’ susceptibility to threats. lecithotrophic (yolk-sac) larvae. The New Zealand (Tokelau), Niue, Palau, The following characteristics of A. public comments and information we Papua New Guinea, Philippines, Samoa, donei, in conjunction with the gathered provided no additional Saudi Arabia, Solomon Islands, Sri information described in the Corals and biological information. Lanka, Taiwan, Thailand, Tonga, Coral Reefs section, Coral Habitat sub- Susceptibility to Threats Tuvalu, United States (American section, and Threats Evaluation section above, affect its vulnerability to To describe A. donei’s threat Samoa, PRIAs), Vanuatu, Vietnam, and extinction currently and over the susceptibilities, the SRR and SIR Yemen. The regulatory mechanisms foreseeable future. Its geographic provided genus-level information for the relevant to A. donei, described first as distribution includes most of the coral effects on Acropora of ocean warming, the percentage of the above countries that utilize them to any degree, and reef ecoregions in the Indian Ocean and disease, acidification, sedimentation, second as the percentages of those western and central Pacific Ocean. Its nutrients, predation, and collection and countries whose regulatory mechanisms geographic distribution moderates trade. The SRR and SIR did not provide may be limited in scope, are as follows: vulnerability to extinction because some any other species-specific information General coral protection (32 percent areas within its range are projected to on the effects of these threats on A. with 6 percent limited in scope), coral have less than average warming and donei. We interpreted the threat collection (59 percent with 29 percent acidification over the foreseeable future, susceptibility and exposure information limited in scope), pollution control (44 including the western Indian Ocean, the from the SRR and SIR in the proposed percent with 9 percent limited in central Pacific, and other areas, so rule for A. donei’s vulnerabilities as scope), fishing regulations on reefs (97 portions of the population in these areas follows: High vulnerability to ocean percent with 15 percent limited in will be less exposed to severe warming, moderate vulnerabilities to scope), and managing areas for conditions. Its depth range is from five disease, ocean acidification, trophic protection and conservation (94 percent to at least 20 meters. This moderates effects of fishing, nutrients, and with 3 percent limited in scope). The vulnerability to extinction over the predation, and low vulnerabilities to most common regulatory mechanisms in foreseeable future because deeper areas sedimentation, sea-level rise, and place for A. donei are reef fishing of its range will usually have lower collection and trade. regulations and area management for irradiance than surface, and Public comments did not provide any protection and conservation. Coral acidification is generally predicted to new or supplemental information on A. collection and pollution control laws accelerate most in waters that are deeper donei’s threat susceptibilities. We are also somewhat utilized for the and cooler than those in which the gathered the following species-specific species, but 29 percent of coral species occurs. Its habitat includes and genus-level supplemental collection laws are limited in scope and upper reef slopes and mid-slope information on this species’ threat may not provide substantial protection. terraces. This moderates vulnerability to susceptibilities. Acropora donei has General coral protection laws are much extinction over the foreseeable future been rated as moderately or highly less common regulatory mechanisms for because the species is not limited to one susceptible to bleaching and disease, the management of A. donei. habitat type but occurs in numerous but these ratings are not based on types of reef environments that will, on species-specific data (Carpenter et al., Vulnerability to Extinction local and regional scales, experience 2008). Based on information from other As explained above in the Risk highly variable thermal regimes and Acropora species provided in the genus Analyses section, a species’ ocean chemistry at any given point in description above, A. donei is likely vulnerability to extinction results from time. Its absolute abundance of at least highly susceptible to ocean warming, the combination of its spatial and tens of millions of colonies, combined and likely has some susceptibilities to demographic characteristics, threat with spatial variability in ocean disease, ocean acidification, trophic susceptibilities, and consideration of the warming and acidification across the effects of fishing, sedimentation, baseline environment and future species range, moderates vulnerability nutrients, sea-level rise, predation, and projections of threats. The SRR stated to extinction because the increasingly collection and trade. The available that the high bleaching rate of the severe conditions expected in the information does not support more Acropora genus is the primary known foreseeable future will be non-uniform precise ratings of the susceptibilities of threat of extinction for A. donei. It listed and therefore will likely be a large A. donei to the threats. factors that reduce the threat of number of colonies that are either not extinction including the moderate Regulatory Mechanisms exposed or do not negatively respond to geographic and depth ranges. a threat at any given point in time. In the proposed rule, we did not Subsequent to the proposed rule, we provide any species-specific received and gathered supplemental Listing Determination information on the regulatory species- or genus-specific information, In the proposed rule using the mechanisms or conservation efforts for described above, that expands our determination tool formula, A. donei A. donei. Criticisms of our approach knowledge regarding the species was proposed for listing as threatened received during public comment led us abundance, distribution, and threat because of: High vulnerability to ocean to the following analysis to attempt to susceptibilities. We developed our warming (ESA Factor E); moderate analyze regulatory mechanisms on a assessment of the species’ vulnerability vulnerability to disease (C) and species basis. Records confirm that A. to extinction using all the available acidification (E); uncommon generalized donei occurs in 68 Indo-Pacific information. As explained in the Risk range wide abundance (E); moderate ecoregions that encompass 34 countries’ Analyses section, our assessment in this overall distribution (based on moderate EEZs. The 34 countries are Australia, final rule emphasizes the ability of the geographic distribution and moderate

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depth distribution (E); and inadequacy possesses sufficient buffering capacity reef flats, and adjacent habitats in of existing regulatory mechanisms (D). to avoid being in danger of extinction depths ranging from 0 to 8 m. In this final rule, we changed the within the foreseeable future throughout The public comments did not provide listing determination for A. donei from its range. It is possible that this species’ any new or supplemental information threatened to not warranted. We made extinction risk may increase in the on A. globiceps’ distribution. We this decision based on a more species- future if global threats continue and gathered supplemental information, specific and holistic assessment of worsen in severity and the species’ including Veron (2014), which reports whether this species meets the exposure to the threats increases that A. globiceps is confirmed in 22 of definition of either a threatened or throughout its range. Should the species his 133 Indo-Pacific ecoregions, and endangered coral largely in response to experience reduced abundance or range strongly predicted to be found in an public comments, including more constriction of a certain magnitude, the additional 16. Wallace (1999b) reports appropriate consideration of the ability of these characteristics to its occurrence in seven of her 29 Indo- buffering capacity of this species’ spatial moderate exposure to threats will Pacific areas, many of which are and demographic traits to lessen its diminish. However, the species is not significantly larger than Veron’s vulnerability to threats. Thus, based on likely to become of such low abundance ecoregions. Wallace’s (1999b) map the best available information above on or so spatially fragmented as to be in shows it from a smaller area than Veron A. donei’s spatial structure, danger of extinction due to depensatory (Veron, 2000; Veron, 2014). Based on demography, threat susceptibilities, and processes, the potential effects of the Wallace (1999b) range, A. globiceps management none of the five ESA environmental stochasticity, or the has a relatively small range, estimated at factors, alone or in combination, are potential for mortality from catastrophic 5 million km2 (Richards, 2009). The causing this species to be endangered events within the foreseeable future public comments and information we throughout its range within the throughout its range. Therefore, A. gathered provided nothing additional on foreseeable future, and thus it is not donei is not warranted for listing at this A. globiceps’ habitat and depth range. warranted for listing at this time, time under any of the listing factors. Demographic Information because: (1) Acropora donei’s distribution Acropora globiceps The SRR and SIR provided the following information on A. globiceps’ across the Indian Ocean and most of the Introduction Pacific Ocean is spread over a very large abundance. Acropora globiceps has area. While some areas within its range The SRR and SIR provided the been reported as common (Veron, 2000). are projected to be affected by warming following information on A. globiceps’ The public comments did not provide and acidification, other areas are morphology and taxonomy. Morphology any new or supplemental information projected to have less than average was described as digitate and usually on A. globiceps’ abundance. We warming and acidification, including small, and taxonomy was described as gathered supplemental information, the western Indian Ocean, the central having no taxonomic issues, but radial including Veron (2014), which reports Pacific, and other areas. This corallites were reported similar to that A. globiceps occupied 3.2 percent distribution and the heterogeneous Acropora secale and Acropora retusa. It of 2,984 dive sites sampled in 30 habitats it occupies reduce exposure to appears similar to Acropora gemmifera, ecoregions of the Indo-Pacific, and had any given threat event or adverse but in strong wave action is similar to a mean abundance rating of 1.95 on a 1 condition that does not occur uniformly Acropora monticulosa. to 5 rating scale at those sites in which throughout the species range. As it was found. Based on this semi- The public comments did not provide explained above in the Threats quantitative system, the species’ any new or supplemental information Evaluation section, we have not abundance was characterized as identified any threat that is expected to on morphology and taxonomy. We ‘‘uncommon.’’ Overall abundance was occur uniformly throughout the species gathered supplemental information, described as ‘‘sometimes common.’’ range within the foreseeable future); including Wallace (1999b), which states Veron did not infer trends in abundance (2) Acropora donei’s total absolute that A. globiceps’ branch thickness and from these data. As described in the abundance is at least tens of millions of colony shape is similar to that of Indo-Pacific Species Determinations colonies, providing buffering capacity in Acropora humilis, and its branch shape introduction above, based on results the form of absolute numbers of and radial corallite morphology is from Richards et al. (2008) and Veron colonies and variation in susceptibility similar to that of Acropora samoensis. It (2014), the absolute abundance of this between individual colonies. As appears that this species has often been species is likely at least tens of millions discussed in the Corals and Coral Reefs mistaken for A. humilis (Fenner, 2014b). of colonies. section above, the more colonies a Veron (2014) states that A. globiceps is Carpenter et al. (2008) extrapolated species has, the lower the proportion of distinctive, thus we conclude it can be species abundance trend estimates from colonies that are likely to be exposed to identified by experts, and that the total live coral cover trends and habitat a particular threat at a particular time, distribution and abundance information types. For A. globiceps, the overall and all individuals that are exposed will described below for this species is decline in abundance (‘‘Percent not have the same response; and sufficiently reliable (Fenner, 2014b). Population Reduction’’) was estimated (3) It is a broadcast spawner and fast Spatial Information at 35 percent, and the decline in grower, enhancing recovery potential abundance before the 1998 bleaching from mortality events as described in The SRR and SIR provided the event (‘‘Back-cast Percent Population the Corals and Coral Reefs section following information on A. globiceps’ Reduction’’) was estimated at 14 percent above. distribution, habitat, and depth range. (Carpenter et al., 2008). However, as Notwithstanding the projections Acropora globiceps is distributed from summarized above in the Inter-basin through 2100 that indicate increased the oceanic west Pacific to the central Comparison sub-section, live coral cover severity over time of the three high Pacific as far east as the Pitcairn Islands. trends are highly variable both spatially importance threats, the combination of The species has the 27th smallest range and temporally, producing patterns on these biological and environmental of 114 Acropora species in a large study. small scales that can be easily taken out characteristics indicates that the species The species occurs on upper reef slopes, of context, thus quantitative inferences

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to species-specific trends should be to disease, acidification, trophic effects that the high bleaching rate of the interpreted with caution. At the same of fishing, sedimentation, nutrients, sea- Acropora genus is the primary known time, an extensive body of literature level rise, predation, and collection and threat of extinction for A. globiceps, but documents broad declines in live coral trade. The available information does the narrow depth range also increases cover and shifts to reef communities not support more precise ratings of the the risk of extinction. It listed factors dominated by hardier coral species or susceptibilities of A. globiceps to the that reduce the threat of extinction algae over the past 50 to 100 years threats. including common abundance and (Birkeland, 2004; Fenner, 2012; Pandolfi persistence in intertidal habitats. Regulatory Mechanisms et al., 2003; Sale and Szmant, 2012). Subsequent to the proposed rule, we These changes have likely occurred, and In the proposed rule, we did not received and gathered supplemental are occurring, from a combination of provide any species-specific species- or genus-specific information, global and local threats. Given that A. information on the regulatory described above, that expands our globiceps occurs in many areas affected mechanisms or conservation efforts for knowledge regarding the species by these broad changes, and that it has A. globiceps. Criticisms of our approach abundance, distribution, and threat some susceptibility to both global and received during public comment led us susceptibilities. We developed our local threats, we conclude that it is to the following analysis to attempt to assessment of the species’ vulnerability likely to have declined in abundance analyze regulatory mechanisms on a to extinction using all the available over the past 50 to 100 years, but a species basis. Records confirm that A. information. As explained in the Risk precise quantification is not possible globiceps occurs in 22 Indo-Pacific Analyses section, our assessment in this due to the limited species-specific ecoregions that encompass 19 countries’ final rule emphasizes the ability of the information. EEZs. The 19 countries are Australia, species’ spatial and demographic traits Federated States of Micronesia, Fiji, to moderate or exacerbate its Other Biological Information France (French Pacific Island vulnerability to extinction, as opposed The SRR and SIR provided the Territories), Indonesia, Japan, New to the approach we used in the following information on A. globiceps’ Zealand (Cook Islands, Tokelau), Niue, proposed rule, which emphasized the life history. Acropora globiceps is a Palau, Papua New Guinea, Philippines, species’ susceptibility to threats. hermaphroditic spawner with Samoa, Solomon Islands, Timor-Leste, The following characteristics of A. lecithotrophic (yolk-sac) larvae. The Tonga, Tuvalu, United Kingdom globiceps, in conjunction with the public comments and information we (Pitcairn Islands), United States (CNMI, information described in the Corals and gathered did not provide additional Guam, American Samoa), and Vietnam. Coral Reefs section, Coral Habitat sub- biological information. The regulatory mechanisms relevant to section, and Threats Evaluation section A. globiceps, described first as the above, affect its vulnerability to Susceptibility to Threats percentage of the above countries that extinction currently and over the To describe A. globiceps’ threat utilize them to any degree and second, foreseeable future. Its geographic susceptibilities, the SRR and SIR as the percentages of those countries distribution includes the Coral Triangle, provided genus-level information for the whose regulatory mechanisms may be but also includes many coral reef effects on Acropora of ocean warming, limited in scope, are as follows: General ecoregions in the western and central acidification, disease, predation, coral protection (32 percent with none Pacific Ocean, as far east as the Pitcairn sedimentation, and nutrients. The SRR limited in scope), coral collection (74 Islands. Some areas within its range are and SIR did not provide any other percent with 37 percent limited in projected to have less than average species-specific information on the scope), pollution control (42 percent warming and acidification over the effects of these threats on A. globiceps. with 16 percent limited in scope), foreseeable future, including the central The exposure and susceptibility threat fishing regulations on reefs (100 percent Pacific, so portions of the population in information from the SRR and SIR was with 11 percent limited in scope), and these areas will be less exposed to interpreted in the proposed rule for A. managing areas for protection and severe conditions. On the other hand, globiceps’ vulnerabilities to threats as conservation (100 percent with 5 the Coral Triangle area is projected to follows: High vulnerability to ocean percent limited in scope). The most have the most rapid and severe impacts warming, moderate vulnerabilities to common regulatory mechanisms in from climate change and localized disease, ocean acidification, trophic place for A. globiceps are reef fishing human impacts for coral reefs over the effects of fishing, nutrients, and regulations, area management for 21st century. As such, its geographic predation, and low vulnerabilities to protection and conservation, and coral distribution has the ability to both sedimentation, sea-level rise, and collection laws. However, 37 percent of moderate and exacerbate vulnerability collection and trade. coral collection laws are limited in to extinction. Its depth range of zero to Public comments did not provide any scope and may not provide substantial 8 meters exacerbates vulnerability to new or supplemental information on A. protection. Pollution control laws are extinction over the foreseeable future globiceps’ threat susceptibilities. We also somewhat utilized for the species. because a large proportion of the gathered the following species-specific General coral protection laws are much population is restricted to shallow areas. and genus-level supplemental less common regulatory mechanisms for Shallow reef areas can be physically information on this species’ threat the management of A. globiceps. diverse, but are often subjected to susceptibilities. Acropora globiceps has frequent changes in environmental been rated as moderately or highly Vulnerability to Extinction conditions, extremes, high irradiance, susceptible to bleaching and disease, As explained above in the Risk and simultaneous effects from multiple but these ratings are not based on Analyses section, a species’ stressors, both local and global in species-specific data (Carpenter et al., vulnerability to extinction results from nature. Its habitat includes upper reef 2008). Based on information from other the combination of its spatial and slopes, reef flats, and adjacent habitats. Acropora species provided in the genus demographic characteristics, threat This moderates vulnerability to description above, A. globiceps is likely susceptibilities, and consideration of the extinction over the foreseeable future highly susceptible to ocean warming, baseline environment and future because the species is not limited to one and also likely has some susceptibilities projections of threats. The SRR stated habitat type but occurs in numerous

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types of reef environments that will, on be exposed to threats that are worse in believe that any current conservation local and regional scales, experience shallow habitats, such as efforts or conservation efforts planned highly variable thermal regimes and simultaneously elevated irradiance and in the future will result in affecting the ocean chemistry at any given point in seawater temperatures, as well as species status to the point at which time. Its absolute abundance of at least localized impacts. listing is not warranted. tens of millions of colonies combined The combination of these with spatial variability in ocean characteristics and future projections of Acropora horrida warming and acidification across the threats indicates that the species is Introduction species range, moderates vulnerability likely to be in danger of extinction The SRR and SIR provided the to extinction because the increasingly within the foreseeable future throughout following information on A. horrida’s severe conditions expected in the its range and warrants listing as morphology and taxonomy. Morphology foreseeable future will be non-uniform threatened at this time due to factors A, was described as usually open and therefore will likely be a large C, D, and E. branched, becoming bushy on upper number of colonies that are either not The available information above on A. reef slopes and in shallow lagoons. No exposed or do not negatively respond to globiceps’ spatial structure, taxonomic issues were raised, but A. a threat at any given point in time. demography, threat susceptibilities, and management also indicate that the horrida was stated to be similar to Listing Determination species is not currently in danger of Acropora tortuosa, and Acropora In the proposed rule using the extinction and thus does not warrant vaughani. determination tool formula approach, A. listing as Endangered because: The public comments did not provide globiceps was proposed for listing as (1) While A. globiceps’ distribution any new or supplemental information threatened because of: High includes the Coral Triangle area, it also on morphology or taxonomy. We vulnerability to ocean warming (ESA includes many ecoregions throughout gathered supplemental information, Factor E); moderate vulnerability to the central Pacific from Japan down to including Veron (2014), which states disease (C) and acidification (E); New Caledonia and as far east as the that A. horrida is distinctive, thus we common generalized range wide Pitcairn Islands. This distribution conclude it can be identified by experts, abundance (E); narrow overall includes some areas within its range and that the distribution and abundance distribution (based on moderate that are projected to have less than information described below for this geographic distribution and narrow average warming and acidification over species is sufficiently reliable (Fenner, depth distribution (E); and inadequacy the foreseeable future, including the 2014b). of existing regulatory mechanisms (D). central Pacific, so portions of the Spatial Information In this final rule, we maintain the population in these areas will be less listing determination for A. globiceps. exposed to severe conditions. The SRR and SIR provided the Based on the best available information (2) Acropora globiceps’ absolute following information on A. horrida’s provided above on A. globicep’s spatial abundance is at least tens of millions of distribution, habitat, and depth range. structure, demography, threat colonies which allows for variation in Acropora horrida is distributed from the susceptibilities, and management the responses of individuals to threats to Red Sea to French Polynesia. The indicate that it is likely to become play a role in moderating vulnerability species has a very broad range overall, endangered throughout its range within to extinction for the species to some having the 14th largest range of 114 the foreseeable future, and thus degree, as described in more detail in Acropora species examined. It is found warrants listing as threatened at this the Corals and Coral Reefs section. in numerous reef slope and back-reef time, because: There is no evidence of depensatory habitats with turbid water, including (1) Acropora globiceps is highly processes such as reproductive failure but not limited to, upper reef slopes, susceptible to ocean warming (ESA from low density of reproductive mid-slope terraces, lagoons, and Factor E), and susceptible to disease (C), individuals and genetic processes such adjacent habitats. The SRR described its ocean acidification (E), trophic effects of as inbreeding affecting this species. depth range as 5 to 20 m. fishing (A, E), nutrients (A, E), and Thus, its absolute abundance indicates The public comments did not provide predation (C). These threats are it is currently able to avoid high any new or supplemental information expected to continue and increase into mortality from environmental on A. horrida’s distribution. We the future. In addition, existing stochasticity, and mortality of a high gathered supplemental information, regulatory mechanisms to address global proportion of its population from including Veron (2014), which reports threats that contribute to extinction risk catastrophic events. that this species is confirmed in 61 of for this species are inadequate (D); and The combination of these his 133 Indo-Pacific ecoregions, and (2) Acropora globiceps occurs characteristics indicates that the species strongly predicted to be found in an primarily in depths of zero to eight does not exhibit the characteristics of additional 22. Wallace (1999b) reports meters which can be considered a one that is currently in danger of its occurrence in 24 of her 29 Indo- shallow depth range compared to the extinction, as described previously in Pacific areas, many of which are overall depth of occurrence for reef the Risk Analyses section, and thus does significantly larger than Veron’s building corals in general. Shallow reef not warrant listing as endangered at this ecoregions. Richards (2009) calculated areas are often subjected to highly time. the geographic range of A. horrida at variable environmental conditions, Range-wide, a multitude of over 100 million km2. Wallace (1999b) extremes, high irradiance, and conservation efforts are already broadly reports the depths from which A. simultaneous effects from multiple employed that are likely benefiting A. horrida specimens were collected stressors, both local and global in globiceps. However, considering the ranged from 17 to 39 m. nature. A limited depth range reduces global scale of the most important the absolute area in which the species threats to the species, and the Demographic Information may occur throughout its geographic ineffectiveness of conservation efforts at The SRR and SIR provided the range and indicates that a large addressing the root cause of global following information on A. horrida’s proportion of the population is likely to threats (i.e., GHG emissions), we do not abundance. Acropora horrida has been

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reported as usually uncommon. This is Other Biological Information susceptible to bleaching and disease, a species that is globally widespread, The SRR and SIR provided the but these ratings are not based on locally restricted, and locally rare, and following information on A. horrida’s species-specific data (Carpenter et al., thus in the second rarest category of life history. Acropora horrida is a 2008). Done et al. (2003b) reported that Acropora with the predicted hermaphroditic spawner with 20 percent of A. horrida colonies on the consequence of local extinction. The lecithotrophic (yolk-sac) larvae. Mean Great Barrier Reef were affected by public comments did not provide any egg size for A. horrida has been bleaching in 2002, and the species new or supplemental information on A. recorded as 0.64 mm and mean polyp ranked 29th in proportion of coral colonies that were bleached and killed horrida’s abundance. We gathered fecundity has been recorded as 9.0 eggs out of 52 studied Acropora species. That supplemental information, including per polyp. This species did synchronize is, 28 of the 52 species bleached more Veron (2014), which reports that A. its spawning with other Acropora than A. horrida, and 23 bleached less. horrida occupied 8.9 percent of 2,984 species on the central GBR during the No other species-specific information dive sites sampled in 30 ecoregions of major multispecies spawning events in is available for the susceptibility of A. the Indo-Pacific, and had a mean early summer 1981–1983. horrida to any other threat. Based on abundance rating of 1.70 on a 1 to 5 Public comments provided no information from other Acropora rating scale at those sites in which it additional biological information. We species provided in the genus was found. Based on this semi- gathered the following supplemental description above, A. horrida may be quantitative system, the species’ information on the life history of A. susceptible to the effects of disease, abundance was characterized as horrida. Darling et al. (2012) found that ocean acidification, trophic effects of ‘‘common.’’ Overall abundance was all of over 30 Acropora species studied fishing, sedimentation, nutrients, sea- described as ‘‘uncommon.’’ Veron did were classified as ‘‘competitive’’ species level rise, predation, and collection and not infer trends in abundance from which were considered to be less trade. Thus, based on the available these data. As described in the Indo- tolerant of environmental stress and species-specific and genus information Pacific Species Determinations disturbance than those species that were summarized above, A. horrida is likely introduction above, based on results classified as ‘‘stress-tolerant,’’ highly susceptible to ocean warming, from Richards et al. (2008) and Veron ‘‘generalist,’’ or ‘‘weedy,’’ because of and also likely has some susceptibilities documented shifts in coral communities (2014), the absolute abundance of this to disease, ocean acidification, trophic from ‘‘competitive’’ to the other species is likely at least tens of millions effects of fishing, predation, categories. Acropora horrida was one of of colonies. sedimentation, nutrients, sea-level rise, the Acropora species studied. and collection and trade. The available Carpenter et al. (2008) extrapolated Susceptibility to Threats information does not support more species abundance trend estimates from precise ratings of the susceptibilities of total live coral cover trends and habitat To describe A. horrida’ threat A. horrida to the threats. types. For A. horrida, the overall decline susceptibilities, the SRR and SIR in abundance (‘‘Percent Population provided genus-level information for the Regulatory Mechanisms Reduction’’) was estimated at 36 effects on Acropora of ocean warming, In the proposed rule, we did not percent, and the decline in abundance acidification, disease, predation, provide any species-specific before the 1998 bleaching event (‘‘Back- sedimentation, nutrients, and collection information on the regulatory cast Percent Population Reduction’’) and trade. The SRR and SIR also mechanisms or conservation efforts for was estimated at 15 percent. However, provided the following species-specific A. horrida. Criticisms of our approach as summarized above in the Inter-basin information on A. horrida’s threats. received during public comment led us Comparison sub-section, live coral cover With regard to ocean warming, A. to the following analysis to attempt to trends are highly variable both spatially horrida is thought to have been locally analyze regulatory mechanisms on a and temporally, producing patterns on extirpated in the Arabian Gulf after the species basis. Records confirm that A. small scales that can be easily taken out 1996 and 1998 bleaching events, but the horrida occurs in 61 Indo-Pacific of context, thus quantitative inferences species is considered less susceptible to ecoregions that encompass 45 countries’ to species-specific trends should be bleaching than other Acropora spp. The EEZs. The 45 countries are Australia, SRR and SIR did not provide any interpreted with caution. At the same Bahrain, China, Djibouti, Egypt, Eritrea, species-specific information on the time, an extensive body of literature Federated States of Micronesia, Fiji, effects of these threats on A. horrida. We France (French Pacific Island documents broad declines in live coral interpreted the threat susceptibility and Territories), Indonesia, Iran, Israel, cover and shifts to reef communities exposure information from the SRR and Japan, Jordan, Kenya, Kiribati, Kuwait, dominated by hardier coral species or SIR in the proposed rule for A. horrida’s Madagascar, Malaysia, Maldives, algae over the past 50 to 100 years vulnerabilities as follows: High Marshall Islands, Mauritius, (Birkeland, 2004; Fenner, 2012; Pandolfi vulnerability to ocean warming, Mozambique, Myanmar, New Zealand et al., 2003; Sale and Szmant, 2012). moderate vulnerabilities to disease, (Tokelau), Niue, Palau, Papua New These changes have likely occurred, and acidification, trophic effects of fishing, Guinea, Philippines, Qatar, Samoa, are occurring, from a combination of nutrients, and predation, and low Saudi Arabia, Seychelles, Solomon global and local threats. Given that A. vulnerabilities to sedimentation, sea- Islands, Sudan, Taiwan, Tanzania, horrida occurs in many areas affected by level rise, and collection and trade. Thailand, Tonga, Tuvalu, United Arab these broad changes, and that it has Public comments did not provide any Emirates, United Kingdom (British some susceptibility to both global and new or supplemental information on A. Indian Ocean Territory), United States local threats, we conclude that it is lokani’s threat susceptibilities. We (American Samoa, PRIAs), Vietnam, and likely to have declined in abundance gathered the following species-specific Yemen. The regulatory mechanisms over the past 50 to 100 years, but a and genus-level supplemental relevant to A. horrida, described first as precise quantification is not possible information on this species’ threat the percentage of the above countries based on the limited species-specific susceptibilities. Acropora horrida has that utilize them to any degree and information. been rated as moderately or highly second, as the percentages of those

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countries whose regulatory mechanisms reef ecoregions in the Indian Ocean and of whether this species meets the may be limited in scope, are as follows: western and central Pacific Ocean. Its definition of either a threatened or General coral protection (24 percent geographic distribution moderates endangered coral largely in response to with 2 percent limited in scope), coral vulnerability to extinction because some public comments, including more collection (58 percent with 24 percent areas within its range are projected to appropriate consideration of the limited in scope), pollution control (44 have less than average warming and buffering capacity of this species’ spatial percent with 7 percent limited in acidification over the foreseeable future, and demographic traits to lessen its scope), fishing regulations on reefs (87 including the western Indian Ocean, the vulnerability to threats. Thus, based on percent with 24 percent limited in central Pacific, and other areas, so the best available information above on scope), and managing areas for portions of the population in these areas A. horrida’s spatial structure, protection and conservation (87 percent will be less exposed to severe demography, threat susceptibilities, and with 11 percent limited in scope). The conditions. Its depth range is from five management, none of the five ESA most common regulatory mechanisms in to 39 meters. This moderates listing factors, alone or in combination, place for A. horrida are reef fishing vulnerability to extinction over the are causing this species to be likely to regulations and area management for foreseeable future because deeper areas become endangered throughout its range protection and conservation. Coral of its range will usually have lower within the foreseeable future, and thus collection and pollution control laws irradiance than surface waters, and it is not warranted for listing at this are also somewhat utilized for the acidification is generally predicted to time, because: species, but 24 percent of coral accelerate most in waters that are deeper (1) Acropora horrida’s distribution collection laws are limited in scope and and cooler than those in which the from the Red Sea across the Indian may not provide substantial protection. species occurs. Its habitat includes Ocean and most of the Pacific Ocean is General coral protection laws are much numerous reef slope and back-reef spread over a very large area. While less common regulatory mechanisms for habitats with turbid water, including some areas within its range are the management of A. horrida. but not limited to, upper reef slopes, projected to be affected by warming and mid-slope terraces, lagoons, and acidification, other areas are projected Vulnerability to Extinction adjacent habitats. This moderates to have less than average warming and As explained above in the Risk vulnerability to extinction over the acidification, including the western Analyses section, a species’ foreseeable future because the species is Indian Ocean, the central Pacific, and vulnerability to extinction results from not limited to one habitat type but other areas. This distribution and the the combination of its spatial and occurs in numerous types of reef heterogeneous habitats it occupies demographic characteristics, threat environments that will, on local and reduce exposure to any given threat susceptibilities, and consideration of the regional scales, experience highly event or adverse condition that does not baseline environment and future variable thermal regimes and ocean occur uniformly throughout the species projections of threats. The SRR stated chemistry at any given point in time. In range. As explained above in the that the high bleaching rate of the addition, turbidity can mitigate the Threats Evaluation section, we have not Acropora genus is the primary known effects of high irradiance by blocking it identified any threat that is expected to threat of extinction for A. horrida. It from the water column. Its absolute occur uniformly throughout the species listed factors that reduce the threat of abundance of at least tens of millions of range within the foreseeable future; extinction including the very wide colonies, combined with spatial (2) Acropora horrida’s total absolute geographic range, with large local variability in ocean warming and abundance is at least tens of millions of distributions, and tolerance for turbid acidification across the species range, colonies, providing buffering capacity in water. moderates vulnerability to extinction the form of absolute numbers of Subsequent to the proposed rule, we because the increasingly severe colonies and variation in susceptibility received and gathered supplemental conditions expected in the foreseeable between individual colonies. As species- or genus-specific information, future will be non-uniform and discussed in the Corals and Coral Reefs described above, that expands our therefore will likely be a large number section above, the more colonies a knowledge regarding the species of colonies that are either not exposed species has, the lower the proportion of abundance, distribution, and threat or do not negatively respond to a threat colonies that are likely to be exposed to susceptibilities. We developed our at any given point in time. a particular threat at a particular time, assessment of the species’ vulnerability and all individuals that are exposed will to extinction using all the available Listing Determination not have the same response; and information. As explained in the Risk In the proposed rule using the (3) It is a broadcast spawner and fast Analyses section, our assessment in this determination tool formula approach, A. grower, enhancing recovery potential final rule emphasizes the ability of the horrida was proposed for listing as from mortality events as described in species’ spatial and demographic traits threatened because of: High the Corals and Coral Reefs section to moderate or exacerbate its vulnerability to ocean warming (ESA above. vulnerability to extinction, as opposed Factor E); moderate vulnerability to Notwithstanding the projections to the approach we used in the disease (C) and acidification (E); through 2100 that indicate increased proposed rule, which emphasized the uncommon generalized range wide severity over time of the three high species’ susceptibility to threats. abundance (E); wide overall distribution importance threats, the combination of The following characteristics of A. (based on wide geographic distribution these biological and environmental horrida, in conjunction with the and moderate depth distribution (E); characteristics indicates that the species information described in the Corals and and inadequacy of existing regulatory possesses sufficient buffering capacity Coral Reefs section, Coral Habitat sub- mechanisms (D). to avoid being in danger of extinction section, and Threats Evaluation section In this final rule, we changed the within the foreseeable future throughout above, affect its vulnerability to listing determination for A. horrida from its range. It is possible that this species’ extinction currently and over the threatened to not warranted. We made extinction risk may increase in the foreseeable future. Its geographic this determination based on a more future if global threats continue and distribution includes most of the coral species-specific and holistic assessment increase in severity and the species

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exposure to threats increases throughout lower reef slopes, walls and ledges, mid- colonies. The calculation of the total its range. Should the species experience slopes, and upper reef slopes protected world population of this species was reduced abundance or range from wave action, and its depth range is flawed, since the area of 1 km2 was constriction of a certain magnitude, the 10 to 35 m. given as 1,000 m2 (Richards et al., 2008: ability of these characteristics to The public comments did not provide Appendix 1), when it is actually moderate exposure to threats will any new or supplemental information 1,000,000 m2. Thus, the correct diminish. However, the species is not on A. jacquelineae’s distribution, population estimate is 1,000 times likely to become of such low abundance habitat, or depth range. We gathered greater than stated, or a total population or so spatially fragmented as to be in supplemental information on its size of 31,599,000 colonies, and an danger of extinction due to depensatory distribution, including Veron (2014), effective population size of 3,476,000 processes, the potential effects of which reports that A. jacquelineae is colonies. environmental stochasticity, or the confirmed in 12 of his 133 Indo-Pacific Carpenter et al. (2008) extrapolated potential for mortality from catastrophic ecoregions, and strongly predicted to be species abundance trend estimates from events within the foreseeable future found in an additional five. Wallace total live coral cover trends and habitat throughout its range. Therefore, A. (1999b) reports its occurrence in seven types. For A. jacquelineae, the overall horrida is not warranted for listing at of her 29 Indo-Pacific areas, many of decline in abundance (‘‘Percent this time under any of the listing factors. which are larger than Veron’s Population Reduction’’) was estimated ecoregions. Richards (2009) calculated at 37 percent, and the decline in Acropora jacquelineae the geographic range of this species at abundance before the 1998 bleaching Introduction 2 million km2, which was 1.8 percent of event (‘‘Back-cast Percent Population the size of the largest range for any Reduction’’) was estimated at 14 The SRR and SIR provided the species. percent. However, as summarized above following information on A. in the Inter-basin Comparison sub- Demographic Information jacquelineae’s morphology and section, live coral cover trends are taxonomy. The morphology was The SRR and SIR provided the highly variable both spatially and described as flat plates up to 1 m in following information on A. temporally, producing patterns on small diameter. Viewed from above, plates are jacquelineae’s abundance. Acropora scales that can be easily taken out of covered with a mass of fine delicately- jacquelineae has been reported as context, thus quantitative inferences to curved axial corallites giving an almost uncommon. species-specific trends should be moss-like appearance. Evidence from The public comments did not provide interpreted with caution. At the same genetics indicates it is not a hybrid, and any new or supplemental information time, an extensive body of literature so the SRR considered it a valid species. on A. jacquelineae’s abundance. We documents broad declines in live coral The public comments and gathered supplemental information, cover and shifts to reef communities information we gathered provided including Richards (2009) and Richards dominated by hardier coral species or supplemental information on the et al. (2013b), which conclude from algae over the past 50 to 100 years morphology or taxonomy of A. their data that A. jacquelineae is (Birkeland, 2004; Fenner, 2012; Pandolfi jacquelineae. One public comment globally restricted, locally restricted, et al., 2003; Sale and Szmant, 2012). stated that specimens collected in and locally rare, and thus in the rarest These changes have likely occurred, and American Samoa and identified by the category of Acropora with the predicted are occurring, from a combination of American Samoa Department of Marine consequence of global extinction. They global and local threats. Given that A. and Water Resources as A. jacquelineae placed 15 species in this category out of jacquelineae occurs in many areas appear to be A. aculeus, thereby 85 species of Acropora. Bonin (2012) affected by these broad changes, and has illustrating the species identification reported that A. jacquelineae was the some susceptibility to both global and uncertainties associated with this 19th most abundant species of Acropora local threats, we conclude that it is species. We gathered supplemental in Kimbe Bay, Papua New Guinea, with likely to have declined in abundance information, including Veron (2014), about 18 percent of the abundance of over the past 50 to 100 years, but a which states that A. jacquelineae is the most abundant species of Acropora. precise quantification is not possible distinctive when compared with other Veron (2014) reports that A. based on the limited species-specific species but not on its own. We conclude jacquelineae occupied 1.6 percent of information. the species can be identified by experts 2,984 dive sites sampled in 30 (Fenner, 2014b). Thus, we conclude that ecoregions of the Indo-Pacific, and had Other Biological Information the distribution and abundance a mean abundance rating of 1.44 on a 1 The SRR and SIR provided the information described below for this to 5 rating scale at those sites in which following information on A. species is sufficiently reliable (Fenner, it was found. Based on this semi- jacquelineae’s life history. Acropora 2014b). quantitative system, the species’ jacquelineae is a hermaphroditic abundance was characterized as Spatial Information spawner with lecithotrophic (yolk-sac) ‘‘uncommon.’’ Overall abundance was larvae. The public comments and The SRR and SIR provided the also described as ‘‘uncommon.’’ Veron information we gathered did not following information on A. did not infer trends in abundance from provide anything additional to the jacquelineae’s distribution, habitat, and these data. above-described biological information. depth range. Acropora jacquelineae is Richards et al. (2008) reported that A. distributed within the Coral Triangle jacquelineae had the 14th lowest Susceptibility to Threats including Papua New Guinea, and is population of the 15 rare Acropora To describe A. jacquelineae’s threat reported from American Samoa. The species they studied. Richards et al. susceptibilities, the SRR and SIR species has a limited range overall, the (2008) gave the total world population provided genus-level information for the 22nd smallest range of 114 Acropora of this species as 31,599 +/-17,358 effects on Acropora of ocean warming, species. It is found in numerous colonies, and the effective population acidification, disease, predation, subtidal reef slope and back-reef size (i.e., a mathematical estimate of the sedimentation, nutrients, and collection habitats, including but not limited to, size of the breeding population) as 3,476 and trade. The SRR and SIR did not

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provide any species-specific with none limited in scope), and moderates vulnerability to extinction information on the effects of these managing areas for protection and over the foreseeable future because threats on A. jacquelineae. We conservation (100 percent with none deeper areas of its range will usually interpreted the threat susceptibility and limited in scope). The most common have lower irradiance than surface exposure information from the SRR and regulatory mechanisms in place for A. waters, and acidification is generally SIR in the proposed rule for A. jacquelineae are reef fishing regulations predicted to accelerate most in waters jacquelineae’s vulnerabilities as follows: and area management for protection and that are deeper and cooler than those in High vulnerability to ocean warming, conservation. General coral protection, which the species occurs. Its habitat moderate vulnerability to disease, ocean coral collection, and pollution control includes lower reef slopes, walls and acidification, trophic effects of fishing, laws are much less common regulatory ledges, mid-slopes, and upper reef nutrients, and predation, and low mechanisms for the management of A. slopes protected from wave action. This vulnerability to sedimentation, sea-level jacquelineae. moderates vulnerability to extinction rise, and collection and trade. over the foreseeable future because the Vulnerability to Extinction Public comments did not provide any species is not limited to one habitat type new or supplemental information on A. As explained above in the Risk but occurs in numerous types of reef jacquelineae’s threat susceptibilities. Analyses section, a species’ environments that will, on local and We gathered the following species- vulnerability to extinction results from regional scales, experience highly specific and genus-level supplemental the combination of its spatial and variable thermal regimes and ocean information on this species’ threat demographic characteristics, threat chemistry at any given point in time. Its susceptibilities. Acropora jacquelineae susceptibilities, and consideration of the effective population size estimate of has been rated as moderately or highly baseline environment and future approximately 3.5 million colonies, susceptible to bleaching and disease, projections of threats. The SRR stated combined with the location of its range, but this rating is not based on species- that the high bleaching rate of the exacerbates vulnerability to extinction specific data (Carpenter et al., 2008). Acropora genus is the primary known because increasingly severe conditions There is no species-specific information threat of extinction for A. jacquelineae. within the limited species range are for the exposure or susceptibility of A. It listed factors that contribute to the likely to affect a high proportion of its jacquelineae to any threat. Thus, based threat of extinction including limited effective population at any given point on the available genus information range, small local distribution and small in time. summarized above, A. jacquelineae is local abundance, as well as the likely highly susceptible to ocean possibility of genetic introgression. Listing Determination warming, and also likely has some Subsequent to the proposed rule, we In the proposed rule using the susceptibility to disease, ocean received and gathered supplemental determination tool formula approach, A. acidification, sedimentation, nutrients, species- or genus-specific information, jacquelineae was proposed for listing as trophic effects of fishing, sea-level rise, described above, that expands our endangered because of: High predation, and collection and trade. The knowledge regarding the species vulnerability to ocean warming (ESA available information does not support abundance, distribution, and threat Factor E); moderate vulnerability to more precise ratings of the susceptibilities. We developed our disease (C) and acidification (E); rare susceptibilities of A. jacquelineae to the assessment of the species’ vulnerability generalized range wide abundance (E); threats. to extinction using all the available narrow overall distribution (based on information. As explained in the Risk narrow geographic distribution and Regulatory Mechanisms Analyses section, our assessment in this moderate depth distribution (E); and In the proposed rule, we did not final rule emphasizes the ability of the inadequacy of existing regulatory provide any species-specific species’ spatial and demographic traits mechanisms (D). information on the regulatory to moderate or exacerbate its In this final rule, we changed the mechanisms or conservation efforts for vulnerability to extinction, as opposed listing determination for A. jacquelineae A. jacquelineae. Criticisms of our to the approach we used in the from endangered to threatened. We approach received during public proposed rule, which emphasized the made this determination based on a comment led us to the following species’ susceptibility to threats. more species-specific and holistic analysis to attempt to analyze regulatory The following characteristics of A. assessment of whether this species mechanisms on a species basis. Records jacquelineae, in conjunction with the meets the definition of either a confirm that A. jacquelineae occurs in information described in the Corals and threatened or endangered coral largely 12 Indo-Pacific ecoregions that Coral Reefs section, Coral Habitat sub- in response to public comments, encompass five countries’ EEZs. The section, and Threats Evaluation section including adequate consideration of the five countries are Federated States of above, affect its vulnerability to buffering capacity of this species’ spatial Micronesia, Indonesia, Papua New extinction currently and over the and demographic traits to lessen its Guinea, Solomon Islands, and Timor- foreseeable future. Its geographic vulnerability to threats. Thus, based on Leste. The regulatory mechanisms distribution is limited almost the best available information provided relevant to A. jacquelineae, described exclusively to the Coral Triangle in the above on A. jacquelineae’s spatial first as the percentage of the above western equatorial Pacific Ocean. structure, demography, threat countries that utilize them to any degree Despite the large number of islands and susceptibilities, and management and second, as the percentages of those environments that are included in the indicate that it is likely to become countries whose regulatory mechanisms species range, this range exacerbates endangered throughout its range within may be limited in scope, are as follows: vulnerability to extinction over the the foreseeable future, and thus General coral protection (20 percent foreseeable future because it is limited warrants listing as threatened at this with none limited in scope), coral to the area projected to have the most time, because: collection (40 percent with none limited rapid and severe impacts from climate (1) Acropora jacquelineae is highly in scope), pollution control (20 percent change and localized human impacts for susceptible to ocean warming (ESA with 20 percent limited in scope), coral reefs over the 21st century. Its Factor E), and susceptible to disease (C), fishing regulations on reefs (100 percent depth range of ten to 35 meters ocean acidification (E), trophic effects of

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fishing (A), predation (C), and nutrient numerous types of reef environments plates with thick branches of highly enrichment (A, E). These threats are that will, on local and regional scales, irregular length and shape, and the expected to continue and increase into experience highly variable thermal taxonomy was described as having no the future. In addition existing regimes and ocean chemistry at any taxonomic issues but this species was regulatory mechanisms to address global given point in time, as described in reported to be similar to Acropora threats that contribute to extinction risk more detail in the Coral Habitat sub- polystoma and Acropora lutkeni, and is for this species are inadequate (D). section and Threats Evaluation section. not easily identified in the field. (2) Acropora jacquelineae’s There is no evidence to suggest the The public comments did not provide distribution is constrained mostly to the species is so spatially fragmented that any new or supplemental information Coral Triangle and western equatorial depensatory processes, environmental on morphology or taxonomy. We Pacific, which is projected to have the stochasticity, or the potential for gathered supplemental information, most rapid and severe impacts from catastrophic events currently pose a including Veron (2014), which states climate change and localized human high risk to the survival of the species; that A. listeri is distinctive, thus we impacts for coral reefs over the 21st (2) Acropora jacquelineae’s absolute conclude the distribution and century, as described in the Threats abundance is tens of millions of abundance information described below Evaluation. Multiple ocean warming colonies and effective population size is for this species is sufficiently reliable events have already occurred within the still millions of colonies which allows (Fenner, 2014b). western equatorial Pacific that suggest for variation in the responses of Spatial Information future ocean warming events may be individuals to threats to play a role in more severe than average in this part of moderating vulnerability to extinction The SRR and SIR provided the the world. A range constrained to this for the species to some degree, as following information on A. listeri’s particular geographic area that is likely described in more detail in the Corals distribution, habitat, and depth range. to experience severe and increasing and Coral Reefs section. There is no Acropora listeri is distributed from the threats indicates that a high proportion evidence of depensatory processes such Red Sea through the Indian Ocean to the of the population of this species is likely as reproductive failure from low density southeast Pacific. The species has a very to be exposed to those threats over the of reproductive individuals and genetic broad range overall, the 13th largest foreseeable future; and processes such as inbreeding affecting range of 114 Acropora species. Its (3) Acropora jacquelineae’s absolute this species. Thus, its absolute predominant habitat is lower reef crests abundance is estimated to be 31 million abundance indicates it is currently able and upper reef slopes in strong wave colonies, however its estimated effective to avoid high mortality from action, and adjacent or similar habitats. population size is much lower at environmental stochasticity, and Its depth range is from near the surface approximately 3.5 million genetically mortality of a high proportion of its to 15 m deep. The public comments did not provide distinct individuals. Considering the population from catastrophic events; any new or supplemental information limited range of this species in an area and where severe and increasing impacts are (3) It is a broadcast spawner and fast on A. listeri’s distribution, habitat, or predicted, this level of abundance grower, enhancing recovery potential depth range. We gathered supplemental leaves the species vulnerable to from mortality events, as described in information, including Veron (2014), becoming of such low abundance within the Corals and Coral Reefs section which reports that this species is the foreseeable future that it may be at above. confirmed in 54 of his 133 Indo-Pacific risk from depensatory processes, The combination of these ecoregions, and strongly predicted to be environmental stochasticity, or characteristics indicates that the species found in an additional 14. Wallace catastrophic events, as explained in does not exhibit the characteristics of (1999b) reports its occurrence in 21 of more detail in the Corals and Coral one that is currently in danger of her 29 Indo-Pacific areas (Wallace, Reefs and Risk Analyses sections. extinction, as described previously in 1999b), many of which are larger than The combination of these the Risk Analyses section, and thus does Veron’s ecoregions. Richards (2009) characteristics and projections of future not warrant listing as endangered at this calculated the geographic range of A. threats indicates that the species is 2 time. listeri at 105 million km . likely to be in danger of extinction Range-wide, a multitude of within the foreseeable future throughout Demographic Information conservation efforts are already broadly its range and warrants listing as The SRR and SIR provided the employed that are likely benefiting A. threatened at this time due to factors A, following information on A. listeri’s jacquelineae. However, considering the C, D, and E. abundance. Acropora listeri has been The available information above on A. global scale of the most important reported as uncommon. This species is jacquelineae’s spatial structure, threats to the species, and the globally widespread, locally restricted, demography, threat susceptibilities, and ineffectiveness of conservation efforts at and locally rare, and thus in the second management also indicate that the addressing the root cause of global rarest category of Acropora with the species the species is not currently in threats (i.e., GHG emissions), we do not predicted consequence of local danger of extinction and thus does not believe that any current conservation extinction. warrant listing as Endangered because: efforts or conservation efforts planned The public comments did not provide (1) While A. jacquelineae’s in the future will result in affecting the any new or supplemental information distribution is constrained mostly to the species status to the point at which on A. listeri’s abundance. We gathered Coral Triangle which increases it listing is not warranted. supplemental information, including extinction risk as described above, its Acropora listeri Veron (2014), which reports that A. habitat includes sub-tidal walls, ledges listeri occupied 5.5 percent of 2,984 on walls, and shallow reef slopes Introduction dive sites sampled in 30 ecoregions of protected from wave action. This The SRR and SIR provided the the Indo-Pacific, and had a mean moderates vulnerability to extinction following information on A. listeri’s abundance rating of 1.35 on a 1 to 5 currently because the species is not morphology and taxonomy. Morphology rating scale at those sites in which it limited to one habitat type but occurs in was described as irregular clumps or was found. Based on this semi-

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quantitative system, the species’ information on the effects of these received during public comment led us abundance was characterized as threats on A. listeri. We interpreted the to the following analysis to attempt to ‘‘uncommon.’’ and overall abundance threat susceptibility and exposure analyze regulatory mechanisms on a was also described as ‘‘uncommon.’’ information from the SRR and SIR in the species basis. Records confirm that A. Veron did not infer trends in abundance proposed rule for A. listeri’s listeri occurs in 54 Indo-Pacific from these data. As described in the vulnerabilities as follows: High ecoregions that encompass 40 countries’ Indo-Pacific Species Determinations vulnerability to ocean warming, EEZs. The 40 countries are Australia, introduction above, based on results moderate vulnerability to disease, ocean Brunei, China, Djibouti, Egypt, Eritrea, from Richards et al. (2008) and Veron acidification, trophic effects of fishing, Federated States of Micronesia, Fiji, (2014), the absolute abundance of this nutrients, and predation, and low France (French Pacific Island species is likely at least tens of millions vulnerability to sedimentation, sea-level Territories), India (Andaman and of colonies. rise, and collection and trade. Nicobar Islands), Indonesia, Israel, Carpenter et al. (2008) extrapolated Public comments did not provide any Japan, Jordan, Kiribati, Malaysia, species abundance trend estimates from new or supplemental information on A. Marshall Islands, Mauritius, Myanmar, total live coral cover trends and habitat listeri’s threat susceptibilities. We New Zealand (Tokelau), Niue, Palau, types. For A. listeri, the overall decline gathered the following species-specific Papua New Guinea, Philippines, Samoa, in abundance (‘‘Percent Population and genus-level supplemental Saudi Arabia, Seychelles, Solomon Reduction’’) was estimated at 35 information on this species’ threat Islands, Sri Lanka, Sudan, Taiwan, percent, and the decline in abundance susceptibilities. Acropora listeri has Tanzania, Timor-Leste, Tonga, Tuvalu, before the 1998 bleaching event (‘‘Back- been rated as moderately or highly United Kingdom (British Indian Ocean cast Percent Population Reduction’’) susceptible to bleaching and disease, Territory, Pitcairn Islands), United was estimated at 14 percent. However, but this rating is not based on species- States (CNMI, Guam, American Samoa, as summarized above in the Inter-basin specific data (Carpenter et al., 2008). PRIAs), Vanuatu, Vietnam, and Yemen. Comparison sub-section, live coral cover Done et al. (2003b) report 20 percent of The regulatory mechanisms relevant to trends are highly variable both spatially A. listeri colonies were affected by A. listeri, described first as the and temporally, producing patterns on bleaching on the Great Barrier Reef in percentage of the above countries that small scales that can be easily taken out 2002, which was 47 percent as much as utilize them to any degree and second, of context, thus quantitative inferences the most affected species (Brown and as the percentages of those countries to species-specific trends should be Cossins, 2011). whose regulatory mechanisms may be interpreted with caution. At the same With regard to disease, A. listeri has limited in scope, are as follows: General time, an extensive body of literature been rated as moderately or highly coral protection (30 percent with 8 documents broad declines in live coral susceptible to bleaching and disease, percent limited in scope), coral cover and shifts to reef communities but this rating is not based on species- collection (63 percent with 30 percent dominated by hardier coral species or specific data (Carpenter et al., 2008). limited in scope), pollution control (45 algae over the past 50 to 100 years Skeletal Eroding Band is the most percent with 8 percent limited in (Birkeland, 2004; Fenner, 2012; Pandolfi prevalent disease on the GBR, and it has scope), fishing regulations on reefs (90 et al., 2003; Sale and Szmant, 2012). been found in A. listeri. Acropora percent with 23 percent limited in These changes have likely occurred, and species with similar morphology to A. scope), and managing areas for are occurring, from a combination of listeri had moderate susceptibility to protection and conservation (95 percent global and local threats. Given that A. this disease on the GBR, with a with 10 percent limited in scope). The listeri occurs in many areas affected by prevalence of 2.4 percent (Page and most common regulatory mechanisms in these broad changes, and has some Willis, 2007). No other species-specific place for A. listeri are reef fishing susceptibility to both global and local information is available for the regulations and area management for threats, we conclude that it is likely to susceptibility of A. listeri to any other protection and conservation. Coral have declined in abundance over the threat. Based on information from other collection and pollution control laws past 50 to 100 years, but a precise Acropora species provided in the genus are also somewhat common for the quantification is not possible based on description above, A. listeri may be species, but 30 percent of coral the limited species-specific information. susceptible to the effects of ocean collection laws are limited in scope and acidification, sedimentation, and may not provide substantial protection. Other Biological Information nutrients, and predation. Thus, based on General coral protection laws are much The SRR and SIR provided the the available species-specific and genus less prominent regulatory mechanisms following information on A. listeri’s life information summarized above, A. for the management of A. listeri. history. Acropora listeri is a listeri likely is highly susceptible to hermaphroditic spawner with ocean warming, and also likely has Vulnerability to Extinction lecithotrophic (yolk-sac) larvae. The some susceptibility to disease, ocean As explained above in the Risk public comments and information we acidification, trophic effects of fishing, Analyses section, a species’ gathered did not provide anything sedimentation, nutrients, sea-level rise, vulnerability to extinction results from additional to the above-described predation, and collection and trade. The the combination of its spatial and biological information. available information does not support demographic characteristics, threat more precise ratings of the susceptibilities, and consideration of the Susceptibility to Threats susceptibilities of A. listeri to the baseline environment and future To describe A. listeri’s threat threats. projections of threats. The SRR stated susceptibilities, the SRR and SIR that the high bleaching rate of the provided genus-level information for the Regulatory Mechanisms Acropora genus is the primary known effects on Acropora of ocean warming, In the proposed rule, we did not threat of extinction for A. listeri. Its acidification, disease, predation, provide any species-specific limited local distribution was also listed sedimentation, nutrients, and collection information on the regulatory as a contributing factor to its threat of and trade. The SRR and SIR did not mechanisms or conservation efforts for extinction. The SRR also listed factors provide any species-specific A. listeri. Criticisms of our approach that reduce the threat of extinction

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including its broad geographic range local and regional scales, experience habitats it occupies reduce exposure to and tolerance for high-energy highly variable thermal regimes and any given threat event or adverse environments. ocean chemistry at any given point in condition that does not occur uniformly Subsequent to the proposed rule, we time. In addition, reef zones with strong throughout the species range. As received and gathered supplemental wave action experience high levels of explained above in the Threats species- or genus-specific information, mixing which can dilute adverse Evaluation section, we have not described above, that expands our environmental conditions. Its absolute identified any threat that is expected to knowledge regarding the species abundance of at least tens of millions of occur uniformly throughout the species abundance, distribution, and threat colonies, combined with spatial range within the foreseeable future; susceptibilities. We developed our variability in ocean warming and (2) Acropora listeri’s absolute assessment of the species’ vulnerability acidification across the species range, abundance is at least tens of millions of to extinction using all the available moderates vulnerability to extinction colonies, providing buffering capacity in information. As explained in the Risk because the increasingly severe the form of absolute numbers of Analyses section, our assessment in this conditions expected in the foreseeable colonies and variation in susceptibility final rule emphasizes the ability of the future will be non-uniform and between individual colonies. As species’ spatial and demographic traits therefore will likely be a large number discussed in the Corals and Coral Reefs to moderate or exacerbate its of colonies that are either not exposed section above, the more colonies a vulnerability to extinction, as opposed or do not negatively respond to a threat species has, the lower the proportion of to the approach we used in the at any given point in time. colonies that are likely to be exposed to proposed rule, which emphasized the Listing Determination a particular threat at a particular time, species’ susceptibility to threats. and all individuals that are exposed will The following characteristics of A. In the proposed rule using the not have the same response; and listeri, in conjunction with the determination tool formula approach, A. (3) It is a broadcast spawner and fast information described in the Corals and listeri was proposed for listing as grower, enhancing recovery potential Coral Reefs section, Coral Habitat sub- threatened because of: High from mortality events, as described in section, and Threats Evaluation section vulnerability to ocean warming (ESA the Corals and Coral Reefs section above, affect its vulnerability to Factor E); moderate vulnerability to above. extinction currently and over the disease (C) and acidification (E); Notwithstanding the projections foreseeable future. Its geographic uncommon generalized range wide through 2100 that indicate increased distribution stretches from the Red Sea abundance (E); moderate overall severity over time of the three high and east coast of Africa, across the distribution (based on wide geographic importance threats, the combination of Indian Ocean and over to the southeast distribution and shallow depth these biological and environmental Pacific Ocean. Its geographic distribution (E); and inadequacy of characteristics indicates that the species distribution moderates vulnerability to existing regulatory mechanisms (D). possesses sufficient buffering capacity extinction because some areas within its In this final rule, we changed the to avoid being in danger of extinction range are projected to have less than listing determination for A. aculeus within the foreseeable future throughout average warming and acidification over from threatened to not warranted. We its range. It is possible that this species’ made this determination based on a the foreseeable future, including the extinction risk may increase in the more species-specific and holistic western Indian Ocean, the central future if global threats continue and assessment of whether this species Pacific, and other areas, so portions of increase in severity and the species meets the definition of either a the population in these areas will be exposure to threats increases throughout threatened or endangered coral largely less exposed to severe conditions. Its its range. Should the species experience in response to public comments, depth range is from near the surface to reduced abundance or range including more appropriate 15 meters. On one hand, its depth range constriction of a certain magnitude, the consideration of the buffering capacity may moderate vulnerability to ability of these characteristics to of this species’ spatial and demographic extinction over the foreseeable future moderate exposure to threats will traits to lessen its vulnerability to because deeper areas of its range will diminish. However, the species is not usually have lower irradiance than threats. Thus, based on the best likely to become of such low abundance surface waters, and acidification is available information provided on A. or so spatially fragmented as to be in generally predicted to accelerate most in listeri’s spatial structure, demography, danger of extinction due to depensatory waters that are deeper and cooler than threat susceptibilities, and management, processes, the potential effects of those in which the species occurs. On none of the five ESA listing factors, environmental stochasticity, or the the other hand, its depth range may alone or in combination, are causing potential for mortality from catastrophic exacerbate vulnerability to extinction this species to be likely to become events within the foreseeable future over the foreseeable future if the species endangered throughout its range within throughout its range. Therefore, A. occurs predominantly in the shallower the foreseeable future, and thus is not listeri is not warranted for listing at this portion of its depth range, since those warranted for listing at this time, areas will have higher irradiance and because: time under any of the listing factors. thus be more severely affected by (1) Acropora listeri’s distribution from Acropora lokani warming-induced bleaching. Its habitat the Red Sea across the Indian Ocean and includes lower reef crests, upper reef most of the Pacific Ocean is spread over Introduction slopes, and other habitats exposed to a very large area. While some areas The SRR and SIR provided the strong wave action, and its depth range within its range are projected to be following information on A. lokani’s is from near the surface to 15 m deep. affected by warming and acidification, morphology and taxonomy. Morphology This moderates vulnerability to other areas are projected to have less was described as small bushy colonies extinction over the foreseeable future than average warming and acidification, of forked branches, and taxonomy was because the species is not limited to one including the western Indian Ocean, the described as having no taxonomic issues habitat type but occurs in numerous central Pacific, and other areas. This but being similar in appearance to some types of reef environments that will, on distribution and the heterogeneous other Acropora species.

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The public comments did not provide abundance. We gathered supplemental a combination of global and local supplemental information on information, including Richards et al. threats. Given that A. lokani occurs in morphology or taxonomy. We gathered (2013b), which concludes that this many areas affected by these broad supplemental information, including species is globally restricted, locally changes, and that it has some Veron (2014), which states that A. restricted, and locally rare, and thus in susceptibility to both global and local lokani is distinctive, thus we conclude the rarest category of Acropora with the threats, we conclude that it is likely to it can be identified by experts, and that predicted consequence of global have declined in abundance over the the distribution and abundance extinction. They placed 15 species in past 50 to 100 years, but a precise information described below for this this category out of 85 species of quantification is not possible based on species is sufficiently reliable (Fenner, Acropora (Richards et al., 2013b). Veron the limited species-specific information. 2014b). (2014) reports that A. lokani occupied 2.75 percent of 2,984 dive sites sampled Other Biological Information Spatial Information in 30 ecoregions of the Indo-Pacific, and The SRR and SIR provided the had a mean abundance rating of 1.44 on The SRR and SIR provided the following information on A. lokani’s a 1 to 5 rating scale at those sites in following information on A. lokani’s life distribution, habitat, and depth range. which it was found. Based on this semi- history. Acropora lokani is assumed to Acropora lokani occurs from central quantitative system, the species’ be a hermaphroditic spawner with Indonesia to Fiji. The species has the abundance was characterized as lecithotrophic (yolk-sac) larvae. The 33rd smallest range of 114 Acropora ‘‘uncommon.’’ Overall abundance was public comments and information we species in a large study. However, as described as ‘‘sometimes common.’’ gathered did not provide anything described below, this was an error, as A. Veron did not infer trends in abundance additional to the above-described lokani actually had the 30th smallest from these data. biological information. range in the study. A. lokani occurs in Richards et al. (2008) reported that A. reef slope and back-reef habitats, lokani had the eleventh lowest Susceptibility to Threats including at least upper reef-slopes, population of the 15 rare Acropora To describe A. lokani’s threat mid-slopes, and lagoon patch reefs, and species they studied. Richards et al. susceptibilities, the SRR and SIR its depth range as 8 to 25 m. (2008) gave the total world population provided genus-level information for the The public comments and of this species as about 18,960 +/-9480 effects on Acropora of ocean warming, information we gathered provided colonies, and the effective population acidification, disease, predation, information on the distribution of A. size (i.e., a mathematical estimate of the sedimentation, nutrients, and collection lokani. One public comment letter size of the breeding population) as about indicated that the range map for A. 2,086 colonies. The calculation of the and trade. The SRR and SIR did not lokani mistakenly included American total world population of this species provide any species-specific Samoa. We gathered supplemental was flawed, since the area of 1 km2 was information on the effects of these information, including Veron (2014), given as 1,000 m2 (Richards et al., 2008: threats on A. lokani. We interpreted the which provides an much more detailed Appendix 1), when it is actually threat susceptibility and exposure range map for this species than the 1,000,000 m2. Thus, the correct information from the SRR and SIR in the maps used in the SRR. Veron reports population estimate is 1,000 times proposed rule for A. lokani’s that this species is confirmed in 14 of greater than stated, or a total population vulnerabilities as follows: High his 133 Indo-Pacific ecoregions is size of 18,960,000 colonies, and an vulnerability to ocean warming, strongly predicted to be found in an effective population size of 2,086,000 moderate vulnerabilities to disease, additional six, and confirms that the colonies. acidification, trophic effects of fishing, species is not known to occur in Carpenter et al. (2008) extrapolated nutrients, and predation, and low American Samoa. Wallace (1999) species abundance trend estimates from vulnerabilities to sedimentation, sea- reports its occurrence in four of her 29 total live coral cover trends and habitat level rise, and collection and trade. Indo-Pacific areas, many of which are types. For A. lokani, the overall decline Public comments did not provide any significantly larger than Veron’s in abundance (‘‘Percent Population new or supplemental information on A. ecoregions. Richards (2009) calculated Reduction’’) was estimated at 36 lokani’s threat susceptibilities. We the geographic range of this species at percent, and the decline in abundance gathered the following species-specific 2 before the 1998 bleaching event (‘‘Back- over 5 million km , which was the 30th and genus-level supplemental cast Percent Population Reduction’’) smallest among the 114 Acropora information on this species’ threat was estimated at 14 percent. However, species for which ranges were susceptibilities. Acropora lokani has as summarized above in the Inter-basin calculated, and 3.6 percent of the size of been rated as moderately or highly the largest range for any species. Comparisons sub-section, live coral cover trends are highly variable both susceptible to thermal bleaching and Richards et al. (Richards et al., 2013a) disease, but these ratings are not based calculate the range of this species as 8.5 spatially and temporally, producing on species-specific data (Carpenter et million km2. The public comments and patterns on small scales that can be al., 2008). Based on information from information we gathered provided easily taken out of context. Thus other Acropora species provided in the nothing additional on A. lokani’s habitat quantitative inferences to species- genus description above, A. lokani is and depth range. specific trends should be interpreted with caution. At the same time, an likely highly susceptible to ocean Demographic Information extensive body of literature documents warming, and likely has some The SRR and SIR provided the broad declines in live coral cover and susceptibility to disease, acidification, following information on A. lokani’s shifts to reef communities dominated by trophic effects of fishing, sedimentation, abundance. Acropora lokani has been hardier coral species or algae over the nutrients, sea-level rise, predation, and reported as uncommon, but sometimes past 50 to 100 years (Birkeland, 2004; collection and trade. The available common. Fenner, 2012; Pandolfi et al., 2003; Sale information does not support more The public comments did not provide and Szmant, 2012). These changes have precise ratings of the susceptibilities of supplemental information on A. lokani’s likely occurred, and are occurring, from A. lokani to the threats.

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Regulatory Mechanisms abundance, distribution, and threat generalized range wide abundance (E); In the proposed rule we did not susceptibilities. We developed our overall narrow distribution (based on provide any species-specific assessment of the species’ vulnerability narrow geographic distribution and information on the regulatory to extinction using all the available moderate depth distribution (E); and mechanisms or conservation efforts for information. As explained in the Risk inadequacy of existing regulatory A. lokani. Criticisms of our approach Analyses section, our assessment in this mechanisms (D). In this final rule, we changed the received during public comment led us final rule emphasizes the ability of the listing determination for A. lokani from to the following analysis to attempt to species’ spatial and demographic traits endangered to threatened. No analyze regulatory mechanisms on a to moderate or exacerbate its vulnerability to extinction, as opposed supplemental information or public species basis. Records confirm that A. to the approach we used in the comments changed our assessment of lokani occurs in 14 Indo-Pacific proposed rule, which emphasized the the type and severity of threats affecting ecoregions that encompass nine species’ susceptibility to threats. A. lokani. Rather, we made this countries’ EEZs. The nine countries are The following characteristics of A. determination based on a more species- Federated States of Micronesia, Fiji, lokani, in conjunction with the specific and holistic assessment of France (French Pacific Island information described in the Corals and whether this species meets the Territories), Indonesia, Palau, Papua Coral Reefs section, Coral Habitat sub- definition of either a threatened or New Guinea, Philippines, Solomon section, and Threats Evaluation section endangered coral largely in response to Islands, and Timor-Leste. The regulatory above, affect its vulnerability to public comments, including more mechanisms relevant to A. lokani, extinction currently and over the appropriate consideration of the described first as a percentage of the foreseeable future. Its geographic buffering capacity of this species’ spatial above countries that utilize them to any distribution is limited to parts of the and demographic traits to lessen its degree, and second as the percentage of Coral Triangle and the western vulnerability to threats. Thus, based on those countries whose regulatory equatorial Pacific Ocean. Despite the the best available information provided mechanisms are limited in scope, are as large number of islands and above on A. lokani’s spatial structure, follows: General coral protection (33 environments that are included in the demography, threat susceptibilities, and percent with none limited in scope), species’ range, this range exacerbates management indicate that it is likely to coral collection (67 percent with 22 vulnerability to extinction over the become endangered throughout its range percent limited in scope), pollution foreseeable future because it is mostly within the foreseeable future, and thus control (33 percent with 22 percent limited to an area projected to have the warrants listing as threatened at this limited in scope), fishing regulations on most rapid and severe impacts from time, because: reefs (100 percent with none limited in climate change and localized human (1) Acropora lokani is highly scope), and managing areas for impacts for coral reefs over the 21st susceptible to ocean warming (ESA protection and conservation (100 century. Its depth range of eight to 25 Factor E), and susceptible to disease (C) percent with none limited in scope). meters moderates vulnerability to ocean acidification (E), trophic effects of The most common regulatory extinction over the foreseeable future fishing (A), nutrients (A, E), and mechanisms in place for A. lokani are because deeper areas of its range will predation (C). These threats are coral collection laws, reef fishing usually have lower irradiance than expected to continue and increase into regulations, and area management for surface waters, and acidification is the future. In addition, existing protection and conservation. General generally predicted to accelerate most in regulatory mechanisms to address global coral protection and pollution control waters that are deeper and cooler than threats that contribute to extinction risk laws are much less common regulatory those in which the species occurs. Its for this species are inadequate (D). mechanisms for the management of A. habitat includes at least upper reef- (2) Acropora lokani’s distribution is lokani. slopes, mid-slopes, and lagoon patch mostly constrained to the Coral Triangle and western equatorial Pacific, which is Vulnerability to Extinction reefs. This moderates vulnerability to extinction over the foreseeable future projected to have the most rapid and As explained above in the Risk because the species is not limited to one severe impacts from climate change and Analyses section, a species’ habitat type but occurs in numerous localized human impacts for coral reefs vulnerability to extinction results from types of reef environments that will, on over the 21st century, as described in the combination of its spatial and local and regional scales, experience the Threats Evaluation. Multiple ocean demographic characteristics, threat highly variable thermal regimes and warming events have already occurred susceptibilities, and consideration of the ocean chemistry at any given point in within the western equatorial Pacific baseline environment and future time. Its effective population size of two that suggest future ocean warming projections of threats. The SRR stated million colonies, combined with the events may be more severe than average that the high bleaching rate of the location of its range, exacerbates in this part of the world. A range Acropora genus is the primary known vulnerability to extinction because constrained to this particular geographic threat of extinction for A. lokani, with increasingly severe conditions within area that is likely to experience severe the potential for extinction increased by the limited species range are likely to and increasing threats indicates that a the smallest effective population size of affect a high proportion of its effective high proportion of the population of this species with actual data, limited population at any given point in time. species is likely to be exposed to those geographic and restricted latitudinal threats over the foreseeable future; and range, and also the small global Listing Determination (3) Acropora lokani’s absolute distribution, small local distributions, In the proposed rule using the abundance is estimated to be 19 million and small local abundances. determination tool formula approach, A. colonies, however its estimated effective Subsequent to the proposed rule, we lokani was proposed for listing as population size is much lower at around received and gathered supplemental endangered because of: High two million genetically distinct species- or genus-specific information, vulnerability to ocean warming (ESA colonies. Considering the limited range described above, that expands our Factor E); moderate vulnerability to of this species in an area where severe knowledge regarding the species disease (C) and acidification (E); rare and increasing impacts are predicted,

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this level of abundance leaves the one that is currently in danger of Indo-Pacific ecoregions, and strongly species vulnerable to becoming of such extinction, as described previously in predicted to be found in an additional low abundance within the foreseeable the Risk Analyses section, and thus does 18. Wallace (1999b) reports its future that it may be at risk from not warrant listing as endangered at this occurrence in 21 of her 29 Indo-Pacific depensatory processes, environmental time. areas, many of which are larger than stochasticity, or catastrophic events, as Range-wide, a multitude of Veron’s ecoregions. Richards (2009) explained in more detail in the Corals conservation efforts are already broadly calculated the geographic range of A. and Coral Reefs and Risk Analyses employed that are likely benefiting A. microclados at 100 million km2. The sections. lokani. However, considering the global public comments and information we The combination of these scale of the most important threats to gathered provided nothing additional on characteristics and projections of future the species, and the ineffectiveness of A. microclados’ habitat and depth range. threats indicates that the species is conservation efforts at addressing the Demographic Information likely to be in danger of extinction root cause of global threats (i.e., GHG within the foreseeable future throughout emissions), we do not believe that any The SRR and SIR provided the its range and warrants listing as current conservation efforts or following information on A. threatened at this time due to factors A, conservation efforts planned in the microclados’ abundance. Acropora C, D, and E. future will result in affecting the species microclados has been reported as The available information above on A. status to the point at which listing is not uncommon. This species is globally lokani’s spatial structure, demography, warranted. widespread, locally restricted, and threat susceptibilities, and management locally rare, and thus in the second also indicate that the species is not Acropora microclados rarest category of Acropora with the currently in danger of extinction and Introduction predicted consequence of local thus does not warrant listing as extinction. The public comments did Endangered because: The SRR and SIR provided the not provide any new or supplemental (1) While A. lokani’s distribution is following information on A. information on A. microclados’ constrained mostly to the Coral Triangle microclados’ morphology and abundance. We gathered supplemental which increases it extinction risk as taxonomy. Morphology was described information, including Veron (2014), described above, its habitat includes as plates up to 1 m diameter, with short, which reports that A. microclados sheltered lagoon patch reefs and other uniform, evenly spaced, tapered occupied 15.2 percent of 2,984 dive shallow reef environments. This branchlets up to 10 mm thick at the sites sampled in 30 ecoregions of the moderates vulnerability to extinction base, and taxonomy was described as Indo-Pacific, and had a mean abundance currently because the species is not having no taxonomic issues but that it rating of 1.51 on a 1 to 5 rating scale at limited to one habitat type but occurs in is most similar to A. massawensis, A. those sites in which it was found. Based numerous types of reef environments lamarcki, and A. macrostoma. on this semi-quantitative system, the that will, on local and regional scales, The public comments did not provide species’ abundance was characterized as experience highly variable thermal any new or supplemental information ‘‘common.’’ Overall abundance was also regimes and ocean chemistry at any on morphology or taxonomy. We described as ‘‘usually uncommon.’’ given point in time, as described in gathered supplemental information, Veron did not infer trends in abundance more detail in the Coral Habitat and including Veron (2014), which states from these data. As described in the Threats Evaluation sections. There is no that A. microclados is distinctive, thus Indo-Pacific Species Determinations evidence to suggest that the species is so we conclude it can be identified by introduction above, based on results spatially fragmented that depensatory experts, and that the distribution and from Richards et al. (2008) and Veron processes, environmental stochasticity, abundance information described below (2014), the absolute abundance of this or the potential for catastrophic events for this species is sufficiently reliable species is likely at least tens of millions currently pose a high risk to the survival (Fenner, 2014b). of colonies. of the species; and Carpenter et al. (2008) extrapolated Spatial Information (2) Acropora lokani’s absolute species abundance trend estimates from abundance is tens of millions of The SRR and SIR provided the total live coral cover trends and habitat colonies, and effective population size following information on A. types. For A. microclados, the overall is still millions of colonies which allows microclados’ distribution, habitat, and decline in abundance (‘‘Percent for variation in the responses of depth range. Acropora microclados is Population Reduction’’) was estimated individuals to threats to play a role in distributed from the Red Sea, to the at 33 percent, and the decline in moderating vulnerability to extinction central Pacific. The species has a broad abundance before the 1998 bleaching for the species to some degree, as range overall with the 20th largest range event (‘‘Back-cast Percent Population described in more detail in the Corals of 114 Acropora species. Its habitat is Reduction’’) was estimated at 14 and Coral Reefs section. There is no predominantly lower reef crests, upper percent. However, as summarized above evidence of depensatory processes such reef slopes, and mid-slope terraces, and in the Inter-basin Comparison sub- as reproductive failure from low density its depth range is from five to 20 m. section, live coral cover trends are of reproductive individuals and genetic The public comments provided the highly variable both spatially and processes such as inbreeding affecting following supplemental information on temporally, producing patterns on small this species. Thus, its absolute A. microclados’ distribution. One public scales that can be easily taken out of abundance indicates it is currently able comment stated that the species has not context, thus quantitative inferences to to avoid high mortality from been confirmed in the Commonwealth species-specific trends should be environmental stochasticity, and of the Northern Mariana Islands by interpreted with caution. At the same mortality of a high proportion of its expert Richard H. Randall, in time, an extensive body of literature population from catastrophic events. contradiction to the SRR. We gathered documents broad declines in live coral The combination of these supplemental information, including cover and shifts to reef communities characteristics indicates that the species Veron (2014), which reports that this dominated by hardier coral species or does not exhibit the characteristics of species is confirmed in 56 of his 133 algae over the past 50 to 100 years

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(Birkeland, 2004; Fenner, 2012; Pandolfi susceptibility: of 48 Acropora species, as the percentages of those countries et al., 2003; Sale and Szmant, 2012). only three species had no bleaching, whose regulatory mechanisms may be These changes have likely occurred, and including A. microclados (Done et al., limited in scope, are as follows: General are occurring, from a combination of 2003b). In a study of ocean warming of coral protection (27 percent with 5 global and local threats. Given that A. Acropora species in Kimbe Bay, Papua percent limited in scope), coral microclados occurs in many areas New Guinea, A. microclados had collection (62 percent with 30 percent affected by these broad changes, and moderate bleaching susceptibility: of 16 limited in scope), pollution control (46 that it has some susceptibility to both Acropora species, A. microclados had percent with 8 percent limited in global and local threats, we conclude the sixth highest level of bleaching, with scope), fishing regulations on reefs (89 that it is likely to have declined in seven percent mortality compared to 40 percent with 16 percent limited in abundance over the past 50 to 100 years, percent for the highest species, and was scope), and managing areas for but a precise quantification is not rated ‘‘moderate’’ on a scale of severe, protection and conservation (95 percent possible based on the limited species- high, moderate, and least (Bonin, 2012). with 11 percent limited in scope). The specific information. No other species-specific information is most common regulatory mechanisms in available for the susceptibility of A. place for A. microclados are reef fishing Other Biological Information microclados to any other threat. Based regulations and area management for The SRR and SIR provided the on information from other Acropora protection and conservation. Coral following information on A. species provided in the genus collection and pollution control laws microclados’ life history. Acropora description above, A. microclados may are also somewhat common for the microclados is a hermaphroditic be susceptible to ocean warming, species, but 30 percent of coral spawner with lecithotrophic (yolk-sac) disease, ocean acidification, trophic collection laws are limited in scope and larvae. The public comments and effects of fishing, sedimentation, may not provide substantial protection. information we gathered did not nutrients, sea-level rise, predation, and General coral protection laws are much provide anything additional to the collection and trade. Thus, based on the less prominent regulatory mechanisms above-described biological information. available species-specific and genus for the management of A. microclados. information summarized above, A. Susceptibility to Threats Vulnerability to Extinction microclados likely has some To describe A. microclados’ threat susceptibility to ocean warming, As explained above in the Risk susceptibilities, the SRR and SIR disease, ocean acidification, trophic Analyses section, a species’ provided genus-level information for the effects of fishing, sedimentation, vulnerability to extinction results from effects on Acropora of ocean warming, nutrients, sea-level rise, predation, and the combination of its spatial and acidification, disease, predation, collection and trade. The available demographic characteristics, threat sedimentation, nutrients, and collection information does not support more susceptibilities, and consideration of the and trade. The SRR and SIR did not precise ratings of the susceptibilities of baseline environment and future provide any species-specific A. microclados to the threats. projections of threats. The SRR stated information on the effects of these that the high bleaching rate of the threats on A. microclados. We Regulatory Mechanisms Acropora genus is the primary known interpreted the threat susceptibility and In the proposed rule, we did not threat of extinction for A. microclados. exposure information from the SRR and provide any species-specific The threat of extinction may be SIR in the proposed rule for A. information on the regulatory increased to by its limited local microclados’ vulnerabilities as follows: mechanisms or conservation efforts for distribution and uncommon local High vulnerability to ocean warming, A. microclados. Criticisms of our abundance. The SRR also listed factors moderate vulnerabilities to disease, approach received during public that reduce the threat of extinction ocean acidification, trophic effects of comment led us to the following including the species’ geographic and fishing, nutrients, and predation, and analysis to attempt to analyze regulatory depth ranges. low vulnerabilities to sedimentation, mechanisms on a species basis. Records Subsequent to the proposed rule, we sea-level rise, and collection and trade. confirm that A. microclados occurs in received and gathered supplemental Public comments provided some 56 Indo-Pacific ecoregions that species- or genus-specific information, supplemental information on A. encompass 37 countries’ EEZs. The 37 described above, that expands our microclados’ threat susceptibilities. One countries are Australia, China, Comoros knowledge regarding the species comment stated that A. microclados is Islands, Djibouti, Egypt, Eritrea, abundance, distribution, and threat more susceptible to predation than Federated States of Micronesia, Fiji, susceptibilities. We developed our indicated in the proposed rule because France (French Pacific Island assessment of the species’ vulnerability of the overlap in the depth ranges of this Territories), Indonesia, Israel, Japan, to extinction using all the available species with crown of thorns starfish. Jordan, Malaysia, Maldives, Marshall information. As explained in the Risk We gathered the following species- Islands, Mauritius, Myanmar, New Analyses section, our assessment in this specific and genus-level supplemental Zealand (Cook Islands, Tokelau), Niue, final rule emphasizes the ability of the information on this species’ threat Palau, Papua New Guinea, Philippines, species’ spatial and demographic traits susceptibilities. Acropora microclados Samoa, Saudi Arabia, Seychelles, to moderate or exacerbate its has been rated as moderately or highly Solomon Islands, Sudan, Taiwan, vulnerability to extinction, as opposed susceptible to bleaching and disease, Thailand, Tonga, Tuvalu, United to the approach we used in the but this rating is not based on species- Kingdom (British Indian Ocean proposed rule, which emphasized the specific data (Carpenter et al., 2008). Territory, Pitcairn Islands), United species’ susceptibility to threats. Supplemental species-specific States (CNMI, Guam, American Samoa, The following characteristics of A. information is available on the PRIAs), Vanuatu, Vietnam, and Yemen. microclados, in conjunction with the susceptibility of A. microclados to The regulatory mechanisms relevant to information described in the Corals and ocean warming. In a study of ocean A. microclados, described first as the Coral Reefs section, Coral Habitat sub- warming of Acropora species on the percentage of the above countries that section, and Threats Evaluation section GBR, A. microclados had low bleaching utilize them to any degree and second, above, affect its vulnerability to

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extinction currently and over the from threatened to not warranted. We severity over time of the three high foreseeable future. Its geographic made this determination based on a importance threats, the combination of distribution includes most of the coral more species-specific and holistic these biological and environmental reef ecoregions in the Indian Ocean and assessment of whether this species characteristics indicates that the species western and central Pacific Ocean. Its meets the definition of either a possesses sufficient buffering capacity geographic distribution moderates threatened or endangered coral largely to avoid being in danger of extinction vulnerability to extinction because some in response to public comments, within the foreseeable future throughout areas within its range are projected to including more appropriate its range. It is possible that this species’ have less than average warming and consideration of the buffering capacity extinction risk may increase in the acidification over the foreseeable future, of this species’ spatial and demographic future if global threats continue and including the western Indian Ocean, the traits to lessen its vulnerability to increase in severity and the species central Pacific, and other areas, so threats. Thus, based on the best exposure to threats increases throughout portions of the population in these areas available information above on A. its range. Should the species experience will be less exposed to severe microclados’ spatial structure, reduced abundance or range conditions. Its depth range is from five demography, threat susceptibilities, and constriction of a certain magnitude, the to 20 meters. This moderates management, none of the five ESA ability of these characteristics to vulnerability to extinction over the listing factors, alone or in combination, moderate exposure to threats will foreseeable future because deeper areas are causing this species to be likely to diminish. However, the species is not of its range will usually have lower become endangered throughout its range likely to become of such low abundance irradiance than surface waters, and within the foreseeable future, and thus or so spatially fragmented as to be in acidification is generally predicted to it is not warranted for listing at this danger of extinction due to depensatory accelerate most in waters that are deeper time, because: processes, the potential effects of and cooler than those in which the (1) While the species has some environmental stochasticity, or the species occurs. Its habitat is susceptibility to bleaching, unlike most potential for mortality from catastrophic predominantly lower reef crests, upper other Acropora species, it does not events within the foreseeable future reef slopes, and mid-slope terraces. This appear to be highly susceptible to this throughout its range. Therefore, A. moderates vulnerability to extinction threat, as shown by two newly available microclados is not warranted for listing over the foreseeable future because the species-specific studies; at this time under any of the listing species is not limited to one habitat type (2) Acropora microclados’ factors. but occurs in numerous types of reef distribution from the Red Sea across the environments that will, on local and Indian Ocean and most of the Pacific Acropora palmerae regional scales, experience highly Ocean includes is spread over a very Introduction variable thermal regimes and ocean large area. While some areas within its chemistry at any given point in time. Its range are projected to be affected by The SRR and SIR provided the absolute abundance of at least tens of warming and acidification, other areas following information on A. palmerae’s millions of colonies, combined with are projected to have less than average morphology and taxonomy. Morphology spatial variability in ocean warming and warming and acidification, including was described as encrusting with or acidification across the species range, the western Indian Ocean, the central without short, irregularly shaped moderates vulnerability to extinction Pacific, and other areas. This branches. Colonies seldom exceed 1 m because the increasingly severe distribution and the heterogeneous across. There is doubt as to whether A. conditions expected in the foreseeable habitats it occupies reduce exposure to palmerae is a separate species or a future will be non-uniform and any given threat event or adverse strong-water form of A. robusta; therefore will likely be a large number condition that does not occur uniformly however, in the absence of genetic of colonies that are either not exposed throughout the species range. As information, the BRT considered it a or do not negatively respond to a threat explained above in the Threats valid species. A. palmerae is like the at any given point in time. In addition, Evaluation section, we have not encrusting base of A. robusta, but it has two species-specific studies indicate identified any threat that is expected to smaller branches, if any. that, unlike many other Acropora occur uniformly throughout the species The public comments did not provide species, A. microclados is not highly range within the foreseeable future; any new or supplemental information susceptible to warming-induced (3) Acropora microclados’ absolute on morphology or taxonomy. We bleaching, one of the primary threats abundance is at least tens of millions of gathered supplemental information, identified for corals. colonies, providing buffering capacity in including Wallace (1999b) and Veron the form of absolute numbers of (Veron, 2000), who both considered it a Listing Determination colonies and variation in susceptibility valid species. In addition, Veron (2014) In the proposed rule using the between individual colonies. As states that A. palmerae is distinctive, determination tool formula approach, A. discussed in the Corals and Coral Reefs thus we conclude it can be identified by microclados was proposed for listing as section above, the more colonies a experts, and that the distribution and threatened because of: High species has, the lower the proportion of abundance information described below vulnerability to ocean warming (ESA colonies that are likely to be exposed to for this species is sufficiently reliable Factor E); moderate vulnerability to a particular threat at a particular time, (Fenner, 2014b). disease (C) and acidification (E); and all individuals that are exposed will Spatial Information uncommon generalized range wide not have the same response; and abundance (E); wide overall distribution (4) It is a broadcast spawner and fast The SRR and SIR provided the (based on wide geographic distribution grower, enhancing recovery potential following information on A. palmerae’s and moderate depth distribution (E); from mortality events, as described in distribution, habitat, and depth range. and inadequacy of existing regulatory the Corals and Coral Reefs section Acropora palmerae is distributed from mechanisms (D). above. the northern Indian Ocean to the central In this final rule, we changed the Notwithstanding the projections Indo-Pacific and central Pacific. The listing determination for A. microclados through 2100 that indicate increased species has a moderate range overall,

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with the 52nd largest range of 114 abundance of this species is likely at information from the SRR and SIR in the Acropora species. The SRR and SIR least tens of millions of colonies. proposed rule for A. palmerae’s reported that it occurs in most reef slope Carpenter et al. (2008) extrapolated vulnerabilities as follows: High and back-reef habitats, including upper species abundance trend estimates from vulnerability to ocean warming, reef slopes, lower reef crests, and reef total live coral cover trends and habitat moderate vulnerabilities to disease, flats, with a depth range of five to 20 m. types. For A. palmerae, the overall ocean acidification, trophic effects of The public comments and information decline in abundance (‘‘Percent fishing, nutrients, and predation, and we gathered provided the following Population Reduction’’) was estimated low vulnerabilities to sedimentation, information on A. palmerae’s at 39 percent, and the decline in sea-level rise, and collection and trade. distribution. One public comment stated abundance before the 1998 bleaching Public comments did not provide any that the depth distribution appears to be event (‘‘Back-cast Percent Population new or supplemental information on A. restricted to depths of less than 12 m, Reduction’’) was estimated at 15 palmerae’s threat susceptibilities. We based on observations in Guam and percent. However, as summarized above gathered the following species-specific reports from elsewhere. We gathered in the Inter-basin Comparison sub- and genus-level supplemental supplemental information, including section, live coral cover trends are information on this species’ threat observations that the depth range of A. highly variable both spatially and susceptibilities. Acropora palmerae has palmerae in American Samoa is low temporally, producing patterns on small been rated as moderately or highly tide to about 5 m deep, and on Tinian scales that can be easily taken out of susceptible to thermal bleaching and Island in the Marianas it is from about context, thus quantitative inferences to coral disease, but these ratings are not 2 to 5 m (D. Fenner, pers. species-specific trends should be based on species-specific data communication). Thus, based on all the interpreted with caution. At the same (Carpenter et al., 2008). No other available information, A. palmerae’s time, an extensive body of literature species-specific information is available habitat includes upper reef slopes, mid- documents broad declines in live coral for the susceptibility of A. palmerae to slope terraces, lower reef crests, and reef cover and shifts to reef communities any other threat. Based on information flats. Based on all the information from dominated by hardier coral species or from other Acropora species provided across its range, we consider its depth algae over the past 50 to 100 years in the genus description above, A. range to be from two to 20 m depth. (Birkeland, 2004; Fenner, 2012; Pandolfi palmerae is likely highly susceptible to Veron (2014) reports that A. palmerae is et al., 2003; Sale and Szmant, 2012). ocean warming, and also has some confirmed in 42 of his 133 Indo-Pacific These changes have likely occurred, and susceptibilities to disease, ocean ecoregions, and strongly predicted to be are occurring, from a combination of acidification, trophic effects of fishing, found in an additional 17. Wallace global and local threats. Given that A. sedimentation, nutrients, sea-level rise, (1999b) reports its occurrence in seven palmerae occurs in many areas affected predation, and collection and trade. The of her 29 Indo-Pacific areas, many of by these broad changes, and that it has available information does not support which are larger than Veron’s some susceptibility to both global and more precise ratings of the ecoregions. Richards (2009) calculated local threats, we conclude that it is susceptibilities of A. palmerae to the the geographic range at over 60 million likely to have declined in abundance threats. 2 over the past 50 to 100 years, but a km . Regulatory Mechanisms precise quantification is not possible Demographic Information based on the limited species-specific In the proposed rule, we did not The SRR and SIR provided the information. provide any species-specific following information on A. palmerae’s information on the regulatory abundance. Acropora palmerae has Other Biological Information mechanisms or conservation efforts for been reported as uncommon. The SRR and SIR provided the A. palmerae. Criticisms of our approach The public comments did not provide following information on A. palmerae’s received during public comment led us any new or supplemental information life history. Like most other Acropora to the following analysis to attempt to on A. palmerae’s abundance. We species, A. palmerae is a analyze regulatory mechanisms on a gathered supplemental information, hermaphroditic spawner with species basis. Records confirm that A. including Veron (2014), which reports lecithotrophic (yolk-sac) larvae. Unlike palmerae occurs in 42 Indo-Pacific that A. palmerae occupied 2.7 percent most other Acropora species, colonies of ecoregions that encompass 28 countries’ of 2,984 dive sites sampled in 30 A. palmerae can be entirely encrusting EEZs. The 28 countries are Australia, ecoregions of the Indo-Pacific, and had with no branches (or colonies may have China, Federated States of Micronesia, a mean abundance rating of 1.81 on a 1 short, irregularly-shaped branches). The Fiji, France (French Pacific Island to 5 rating scale at those sites in which public comments and information we Territories), India (including Andaman it was found. Based on this semi- gathered did not provide anything and Nicobar Islands), Indonesia, Japan, quantitative system, the species’ additional to the above-described Marshall Islands, Mauritius, Myanmar, abundance was characterized as biological information. New Zealand (Cook Islands, Tokelau), ‘‘uncommon,’’ and overall abundance Niue, Palau, Papua New Guinea, was also described as ‘‘uncommon.’’ Susceptibility to Threats Philippines, Samoa, Seychelles, Veron did not infer trends in abundance To describe A. palmerae’s threat Solomon Islands, Sri Lanka, Taiwan, from these data. Acropora palmerae can susceptibilities, the SRR and SIR Thailand, Timor-Leste, Tonga, Tuvalu, be abundant within a very narrow depth provided genus-level information for the United States (CNMI, Guam, American range in shallow water (as it is on the effects on Acropora of ocean warming, Samoa, PRIAs), Vanuatu, and Vietnam. west coast of Tinian in the Marianas), acidification, disease, predation, The regulatory mechanisms relevant to which may be missed in some surveys sedimentation, nutrients, and collection A. palmerae, described first as the (D. Fenner, personal comm.). As and trade. The SRR and SIR did not percentage of the above countries that described in the Indo-Pacific Species provide any species-specific utilize them, to any degree and second, Determinations introduction above, information on the effects of these as the percentages of those countries based on results from Richards et al. threats on A. palmerae. We interpreted whose regulatory mechanisms may be (2008) and Veron (2014), the absolute the threat susceptibility and exposure limited in scope, are as follows: General

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coral protection (36 percent with 11 western and central Pacific Ocean. Its threatened or endangered coral largely percent limited in scope), coral geographic distribution moderates in response to public comments, collection (57 percent with 29 percent vulnerability to extinction because some including more appropriate limited in scope), pollution control (39 areas within its range are projected to consideration of the buffering capacity percent with 11 percent limited in have less than average warming and of this species’ spatial and demographic scope), fishing regulations on reefs (96 acidification over the foreseeable future, traits to lessen its vulnerability to percent with 11 percent limited in including the western Indian Ocean, the threats. Thus, based on the best scope), and managing areas for central Pacific, and other areas, so available information above on A. protection and conservation (96 percent portions of the population in these areas palmerae’s spatial structure, with 4 percent limited in scope). The will be less exposed to severe demography, threat susceptibilities, and most common regulatory mechanisms in conditions. Its depth range is from the management, none of the five ESA place for A. palmerae are reef fishing surface to as much as 20 meters. This listing factors, alone or in combination, regulations and area management for moderates vulnerability to extinction are causing this species to be likely to protection and conservation. Coral over the foreseeable future because become endangered throughout its range collection and pollution control laws deeper areas of its range will usually within the foreseeable future, and thus are also somewhat common for the have lower irradiance than surface is not warranted for listing at this time, species, but 29 percent of coral waters, and acidification is generally because: collection laws are limited in scope and predicted to accelerate most in waters (1) Acropora palmerae’s distribution may not provide substantial protection. that are deeper and cooler than those in across the Indian Ocean and most of the General coral protection laws are much which the species occurs. Its habitat Pacific Ocean is spread over a very large less prominent regulatory mechanisms includes upper reef slopes, mid-slope area. While some areas within its range for the management of A. palmerae. terraces, lower reef crests, and reef flats are projected to be affected by warming in depth ranging from two to 20 m and acidification, other areas are Vulnerability to Extinction depth. This moderates vulnerability to projected to have less than average As explained above in the Risk extinction over the foreseeable future warming and acidification, including Analyses section, a species’ because the species is not limited to one the western Indian Ocean, the central vulnerability to extinction results from habitat type but occurs in numerous Pacific, and other areas. This the combination of its spatial and types of reef environments that will, on distribution and the wide variety of demographic characteristics, threat local and regional scales, experience habitat types it occupies reduce susceptibilities, and consideration of the highly variable thermal regimes and exposure to any given threat event or baseline environment and future ocean chemistry at any given point in adverse condition that does not occur projections of threats. The SRR stated time. Reef zones subject to high wave uniformly throughout the species range. that the high bleaching rate of the action also experience high levels of As explained above in the Threats Acropora genus is the primary known mixing which can dilute adverse Evaluation section, we have not threat of extinction for A. palmerae. It environmental conditions. Its absolute identified any threat that is expected to listed factors that reduce the threat of abundance of at least tens of millions of occur uniformly throughout the species extinction including its very broad colonies, combined with spatial range within the foreseeable future; geographic range, the fact that it is often variability in ocean warming and (2) Acropora palmerae’s absolute common and sometimes abundant, and acidification across the species range, abundance is at least tens of millions of the broad range of suitable habitat types moderates vulnerability to extinction colonies, providing buffering capacity in for A. palmerae. because the increasingly severe the form of absolute numbers of Subsequent to the proposed rule, we conditions expected in the foreseeable colonies and variation in susceptibility received and gathered supplemental future will be non-uniform and between individual colonies. As species- or genus-specific information, therefore will likely be a large number discussed in the Corals and Coral Reefs described above, that expands our of colonies that are either not exposed section above, the more colonies a knowledge regarding the species or do not negatively respond to a threat species has, the lower the proportion of abundance, distribution, and threat at any given point in time. colonies that are likely to be exposed to susceptibilities. We developed our a particular threat at a particular time, assessment of the species’ vulnerability Listing Determination and all individuals that are exposed will to extinction using all the available In the proposed rule using the not have the same response; and information. As explained in the Risk determination tool formula approach, A. (3) It is a broadcast spawner and fast Analyses section, our assessment in this palmerae was proposed for listing as grower, enhancing recovery potential final rule emphasizes the ability of the threatened because of: High from mortality events, as described in species’ spatial and demographic traits vulnerability to ocean warming (ESA the Corals and Coral Reefs section to moderate or exacerbate its Factor E); moderate vulnerability to above. vulnerability to extinction, as opposed disease (C) and acidification (E); Notwithstanding the projections to the approach we used in the uncommon generalized range wide through 2100 that indicate increased proposed rule, which emphasized the abundance (E); moderately wide severity over time of the three high species’ susceptibility to threats. distribution (based on moderate importance threats, the combination of The following characteristics of A. geographic distribution and moderate these biological and environmental palmerae, in conjunction with the depth distribution (E); and inadequacy characteristics indicates that the species information described in the Corals and of existing regulatory mechanisms (D). possesses sufficient buffering capacity Coral Reefs section, Coral Habitat sub- In this final rule, we changed the to avoid being in danger of extinction section, and Threats Evaluation section listing determination for A. palmerae within the foreseeable future throughout above, affect its vulnerability to from threatened to not warranted. We its range. It is possible that this species’ extinction currently and over the made this determination based on a extinction risk may increase in the foreseeable future. Its geographic more species-specific and holistic future if global threats continue and distribution includes most of the coral assessment of whether this species increase in severity and the species reef ecoregions in the Indian Ocean and meets the definition of either a exposure to threats increases throughout

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its range. Should the species experience paniculata’s distribution. One public Carpenter et al. (2008) extrapolated reduced abundance or range comment stated that occurrence of A. species abundance trend estimates from constriction of a certain magnitude, the paniculata within the Mariana Islands total live coral cover trends and habitat ability of these characteristics to has not been confirmed by expert types. For A. paniculata, the overall moderate exposure to threats will Richard H. Randall, in contradiction to decline in abundance (‘‘Percent diminish. However, the species is not the SRR. We gathered supplemental Population Reduction’’) was estimated likely to become of such low abundance information, including Veron (2014), at 35 percent, and the decline in or so spatially fragmented as to be in which reports that A. paniculata is abundance before the 1998 bleaching danger of extinction due to depensatory confirmed in 51 of his 133 Indo-Pacific event (‘‘Back-cast Percent Population processes, the potential effects of ecoregions, and strongly predicted to be Reduction’’) was estimated at 14 percent environmental stochasticity, or the found in an additional 15. Wallace in the study. However, as summarized potential for mortality from catastrophic (1999b) reports its occurrence in 19 of above in the Inter-basin Comparison events within the foreseeable future her 29 Indo-Pacific areas, many of sub-section, live coral cover trends are throughout its range. Therefore, A. which are larger than Veron’s highly variable both spatially and palmerae is not warranted for listing at ecoregions. Richards (2009) calculated temporally, producing patterns on small this time under any of the listing factors. the geographic range at 80 million km2. scales that can be easily taken out of The public comments and information context, thus quantitative inferences to Acropora paniculata we gathered provided nothing species-specific trends should be Introduction additional on A. paniculata’s habitat interpreted with caution. At the same and depth range. time, an extensive body of literature The SRR and SIR provided the documents broad declines in live coral following information on A. Demographic Information cover and shifts to reef communities paniculata’s morphology and taxonomy. The SRR and SIR provided the dominated by hardier coral species or Morphology was described as large algae over the past 50 to 100 years plates or tables that are 25 mm thick and following information on A. paniculata’s abundance. Acropora (Birkeland, 2004; Fenner, 2012; Pandolfi frequently greater than 1 m across, and et al., 2003; Sale and Szmant, 2012). taxonomy was described as having no paniculata has been reported as uncommon to rare (Veron, 2000). These changes have likely occurred, and taxonomic issues, but it is quite similar are occurring, from a combination of to A. cytherea and similar to A. Richards (2009) concluded that this species is globally widespread, locally global and local threats. Given that A. jacquelineae. paniculata occurs in many areas The public comments and restricted, and locally rare, and thus in the second rarest category of Acropora affected by these broad changes, and information we gathered provided that it has some susceptibility to both information on morphology and with the predicted consequence of local extinction. global and local threats, we conclude taxonomy of A. paniculata. One public that it is likely to have declined in The public comments and comment stated that in Hawaii, colony abundance over the past 50 to 100 years, morphology of A. paniculata resembles information we gathered provided the but a precise quantification is not that of A. cytherea, but that A. following information on A. possible based on the limited species- paniculata occurs at greater depths than paniculata’s abundance. One public specific information. A. cytherea, which opens the possibility comment stated that Fenner’s 2005 book of them being the same species that Corals of Hawaii notes that in the Other Biological Information changes growth forms at different Hawaiian Islands, A. paniculata is ‘‘not The SRR and SIR provided the depths. We gathered supplemental common,’’ which the commenter argued following information on A. information, including Veron (2014), demonstrates that the species is not rare, paniculata’s life history. Like most other which states that A. paniculata is at least in Hawaii. We gathered Acropora species, A. paniculata is a distinctive, thus we conclude it can be supplemental information, including hermaphroditic spawner with identified by experts, and that the observations made in 2014 that A. lecithotrophic (yolk-sac) larvae. The distribution and abundance information paniculata is one of the most common public comments and information we described below for this species is corals in the Chagos Islands in the gathered did not provide anything sufficiently reliable (Fenner, 2014b). Indian Ocean, where it has recovered additional to the above-described rapidly from the 1998 mass bleaching biological information. Spatial Information event (D. Fenner, personal comm.). The SRR and SIR provided the Veron (2014) reports that A. paniculata Susceptibility to Threats following information on A. occupied 14.3 percent of 2,984 dive To describe A. paniculata’s threat paniculata’s distribution, habitat, and sites sampled in 30 ecoregions of the susceptibilities, the SRR and SIR depth range. Acropora paniculata is Indo-Pacific, and had a mean abundance provided genus-level information for the distributed from the Red Sea and Indian rating of 1.43 on a 1 to 5 rating scale at effects on Acropora of ocean warming, Ocean to the west and central Pacific, those sites in which it was found. Based acidification, disease, predation, including within the Mariana Islands. on this semi-quantitative system, the sedimentation, nutrients, and collection The species has a moderately broad species’ abundance was characterized as and trade. The SRR and SIR did not range, the 40th largest range of 114 ‘‘common,’’ and overall abundance was provide any species-specific Acropora species. Its habitat includes described as ‘‘uncommon.’’ Veron did information on the effects of these numerous reef slope and back-reef not infer trends in abundance from threats on A. paniculata. We interpreted habitats, including at least upper reef these data. As described in the Indo- the threat susceptibility and exposure slopes, mid-slope terraces, lower reef Pacific Species Determinations information from the SRR and SIR in the slopes, and sheltered lagoons, and its introduction above, based on results proposed rule for A. paniculata’s depth range is 10 to 35 m. from Richards et al. (2008) and Veron vulnerabilities as follows: High The public comments and the (2014), the absolute abundance of this vulnerability to ocean warming, supplemental information provided the species is likely at least tens of millions moderate vulnerabilities to disease, following information on A. of colonies. ocean acidification, trophic effects of

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fishing, nutrients, and predation, and collection (59 percent with 30 percent areas within its range are projected to low vulnerabilities to sedimentation, limited in scope), pollution control (43 have less than average warming and sea-level rise, and collection and trade. percent with 8 percent limited in acidification over the foreseeable future, Public comments did not provide any scope), fishing regulations on reefs (89 including the western Indian Ocean, the new or supplemental information on A. percent with 22 percent limited in central Pacific, and other areas, so paniculata’s threat susceptibilities. We scope), and managing areas for portions of the population in these areas gathered the following species-specific protection and conservation (95 percent will be less exposed to severe and genus-level supplemental with 11 percent limited in scope). The conditions. Its depth range is from 10 to information on this species’ threat most common regulatory mechanisms in 35 meters. This moderates vulnerability susceptibilities. Acropora paniculata place for A. paniculata are reef fishing to extinction over the foreseeable future has been rated as moderately or highly regulations and area management for because deeper areas of its range will susceptible to bleaching and disease, protection and conservation. Coral usually have lower irradiance than but these ratings are not based on collection and pollution control laws surface waters, and acidification is species-specific data (Carpenter et al., are also somewhat common for the generally predicted to accelerate most in 2008). No other species-specific species, but 30 percent of coral waters that are deeper and cooler than information is available for the collection laws are limited in scope and those in which the species occurs. Its susceptibility of A. paniculata to any may not provide substantial protection. habitat includes at least upper reef other threat. Based on information from General coral protection laws are much slopes, mid-slope terraces, lower reef other Acropora species provided in the less prominent regulatory mechanisms slopes, and sheltered lagoons. This genus description above, A. paniculata for the management of A. paniculata. moderates vulnerability to extinction likely is highly susceptible to ocean over the foreseeable future because the Vulnerability to Extinction warming, and also has some species is not limited to one habitat type susceptibility to disease, ocean As explained above in the Risk but occurs in numerous types of reef acidification, trophic effects of fishing, Analyses section, a species’ environments that will, on local and sedimentation, nutrients, sea-level rise, vulnerability to extinction results from regional scales, experience highly predation, and collection and trade. The the combination of its spatial and variable thermal regimes and ocean available information does not support demographic characteristics, threat chemistry at any given point in time. Its more precise ratings of the susceptibilities, and consideration of the absolute abundance of at least tens of susceptibilities of A. paniculata to the baseline environment and future millions of colonies, combined with threats. projections of threats. The SRR stated spatial variability in ocean warming and that the high bleaching rate of the Regulatory Mechanisms acidification across the species range, Acropora genus is the primary known moderates vulnerability to extinction In the proposed rule, we did not threat of extinction for A. paniculata. It because the increasingly severe provide any species-specific listed factors that reduce the threat of conditions expected in the foreseeable information on the regulatory extinction including the moderately future will be non-uniform and mechanisms or conservation efforts for wide geographic range, presence in therefore will likely be a large number A. paniculata. Criticisms of our deeper habitats, and being common in of colonies that are either not exposed approach received during public New Guinea though rare elsewhere. or do not negatively respond to a threat comment led us to the following Subsequent to the proposed rule, we at any given point in time. analysis to attempt to analyze regulatory received and gathered supplemental mechanisms on a species basis. Records species- or genus-specific information, Listing Determination confirm that A. paniculata occurs in 51 described above, that expands our In the proposed rule using the Indo-Pacific ecoregions that encompass knowledge regarding the species determination tool formula approach, A. 37 countries’ EEZs. The 37 countries are abundance, distribution, and threat paniculata was proposed for listing as Australia (including Cocos-Keeling susceptibilities. We developed our threatened because of: High Islands), China, Comoros Islands, Egypt, assessment of the species’ vulnerability vulnerability to ocean warming (ESA Federated States of Micronesia, Fiji, to extinction using all the available Factor E); moderate vulnerability to France (French Pacific Island information. As explained in the Risk disease (C) and acidification (E); Territories), India (Andaman and Analyses section, our assessment in this uncommon generalized range wide Nicobar Islands), Indonesia, Israel, final rule emphasizes the ability of the abundance (E); wide overall distribution Japan, Jordan, Kiribati, Madagascar, species’ spatial and demographic traits (based on wide geographic distribution Malaysia, Maldives, Marshall Islands, to moderate or exacerbate its and moderate depth distribution (E); Mauritius, Myanmar, Nauru, New vulnerability to extinction, as opposed and inadequacy of existing regulatory Zealand (Tokelau), Niue, Palau, Papua to the approach we used in the mechanisms (D). New Guinea, Philippines, Samoa, Saudi proposed rule, which emphasized the In this final rule, we changed the Arabia, Solomon Islands, Sudan, species’ susceptibility to threats. listing determination for A. paniculata Taiwan, Thailand, Tonga, Tuvalu, The following characteristics of A. from threatened to not warranted. We United Kingdom (British Indian Ocean paniculata, in conjunction with the made this determination based on a Territory), United States (Hawaii, information described in the Corals and more species-specific and holistic American Samoa, PRIAs), Vanuatu, and Coral Reefs section, Coral Habitat sub- assessment of whether this species Vietnam. The regulatory mechanisms section, and Threats Evaluation section meets the definition of either a relevant to A. paniculata, described first above, affect its vulnerability to threatened or endangered coral largely as the percentage of the above countries extinction currently and over the in response to public comments, that utilize them to any degree and foreseeable future. Its geographic including more appropriate second, as the percentages of those distribution includes most of the coral consideration of the buffering capacity countries whose regulatory mechanisms reef ecoregions in the Indian Ocean and of this species’ spatial and demographic may be limited in scope, are as follows: western and central Pacific Ocean. Its traits to lessen its vulnerability to General coral protection (24 percent geographic distribution moderates threats. Thus, based on the best with 3 percent limited in scope), coral vulnerability to extinction because some available information above on A.

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paniculata’s spatial structure, danger of extinction due to depensatory (2009) estimated its range at 1.4 million demography, threat susceptibilities, and processes, the potential effects of km2. The public comments and management, none of the five ESA environmental stochasticity, or the information we gathered provided listing factors, alone or in combination, potential for mortality from catastrophic nothing additional on A. pharaonis’ are causing this species to be likely to events within the foreseeable future habitat and depth range. become endangered throughout its range throughout its range. Therefore, A. Demographic Information within the foreseeable future, and thus paniculata is not warranted for listing at is not warranted for listing at this time, this time under any of the listing factors. The SRR and SIR provided the because: following information on A. pharaonis’ (1) Acropora paniculata’s distribution Acropora pharaonis abundance. Acropora pharaonis has from the Red Sea across the Indian Introduction been reported as common. The public Ocean and most of the Pacific Ocean is comments did not provide spread over a very large area. While The SRR and SIR provided the supplemental information on A. some areas within its range are following information on A. pharaonis’ pharaonis’ abundance. We gathered projected to be affected by warming and morphology and taxonomy. Morphology supplemental information, including acidification, other areas are projected was described as large horizontal tables Veron (2014), which reports that A. to have less than average warming and or irregular clusters of horizontal or pharaonis occupied 3.6 percent of 2,984 acidification, including the western upright interlinked contorted branches, dive sites sampled in 30 ecoregions of Indian Ocean, the central Pacific, and and taxonomy was described as having the Indo-Pacific, and had a mean other areas. This distribution and the no taxonomic issues but being similar in abundance rating of 1.80 on a 1 to 5 heterogeneous habitats it occupies appearance to Acropora clathrata and rating scale at those sites in which it reduce exposure to any given threat Acropora plumosa. was found. Based on this semi- event or adverse condition that does not The public comments did not provide quantitative system, the species’ occur uniformly throughout the species supplemental information on abundance was characterized as range. As explained above in the morphology or taxonomy. We gathered ‘‘uncommon.’’ Overall abundance was Threats Evaluation section, we have not supplemental information, including described as ‘‘common in the Red Sea, identified any threat that is expected to that A. pharaonis is recognized as valid uncommon elsewhere.’’ Veron did not occur uniformly throughout the species by experts (Veron, 2000; Veron, 2014; infer trends in abundance from these range within the foreseeable future; Wallace, 1999a). Veron (2014) also data. As described in the Indo-Pacific (2) Acropora paniculata’s absolute states that records of this species in the Species Determinations introduction abundance is at least tens of millions of Pacific by other authors are likely to be above, based on results from Richards et colonies, providing buffering capacity in another, probably undescribed species. al. (2008) and Veron (2014), the absolute the form of absolute numbers of However, we conclude the species can abundance of this species is likely at colonies and variation in susceptibility be identified by experts, thus the least millions of colonies. between individual colonies. As distribution and abundance information Carpenter et al. (2008) extrapolated discussed in the Corals and Coral Reefs described below for this species is species abundance trend estimates from section above, the more colonies a sufficiently reliable (Fenner, 2014b). total live coral cover trends and habitat species has, the lower the proportion of Spatial Information types. For A. pharaonis, the overall colonies that are likely to be exposed to decline in abundance (‘‘Percent a particular threat at a particular time, The SRR and SIR provided the Population Reduction’’) was estimated and all individuals that are exposed will following information on A. pharaonis’ at 30 percent, and the decline in not have the same response; and distribution, habitat, and depth range. abundance before the 1998 bleaching (3) It is a broadcast spawner and fast Acropora pharaonis has a disjoint event (‘‘Back-cast Percent Population grower, enhancing recovery potential distribution, being present in the Red Reduction’’) was estimated at 14 from mortality events as described in Sea and western/northern Indian Ocean, percent. However, as summarized above the Corals and Coral Reefs section and areas in the Pacific Ocean. It notes in the Inter-basin Comparison sub- above. that IUCN stated that there are doubts section, live coral cover trends are Notwithstanding the projections about the Pacific records. The species highly variable both spatially and through 2100 that indicate increased has the 14th smallest range of 114 temporally, producing patterns on small severity over time of the three high Acropora species. Its habitat includes scales that can be easily taken out of importance threats, the combination of reef slope and back-reef habitats, context, thus quantitative inferences to these biological and environmental including at least upper reef slopes, species-specific trends should be characteristics indicates that the species mid-slope terraces, and lagoons, and its interpreted with caution. At the same possesses sufficient buffering capacity depth range is 5 to 25 meters. time, an extensive body of literature to avoid being in danger of extinction The public comments did not provide documents broad declines in live coral within the foreseeable future throughout supplemental information on A. cover and shifts to reef communities its range. It is possible that this species’ pharaonis’ distribution. We gathered dominated by hardier coral species or extinction risk may increase in the supplemental information, including algae over the past 50 to 100 years future if global threats continue and Veron (2014), which reports that A. (Birkeland, 2004; Fenner, 2012; Pandolfi increase in severity and the species pharaonis is confirmed in 11 of his 133 et al., 2003; Sale and Szmant, 2012). exposure to threats increases throughout Indo-Pacific ecoregions, and strongly These changes have likely occurred, and its range. Should the species experience predicted to be found in an additional are occurring, from a combination of reduced abundance or range eight. All 19 of these ecoregions are in global and local threats. Given that A. constriction of a certain magnitude, the the Indian Ocean. Wallace (1999b) pharaonis occurs in areas affected by ability of these characteristics to reports its occurrence in six of her 29 these broad changes, and has some moderate exposure to threats will Indo-Pacific areas, many of which are susceptibility to both global and local diminish. However, the species is not larger than Veron’s ecoregions, stating threats, we conclude that it is likely to likely to become of such low abundance that, ‘‘This unusual species appears to have declined in abundance over the or so spatially fragmented as to be in be restricted to the Red Sea.’’ Richards past 50 to 100 years, but a precise

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quantification is not possible based on Regulatory Mechanisms species- or genus-specific information, the limited species-specific information. In the proposed rule, we did not described above, that expands our knowledge regarding the species Other Biological Information provide any species-specific abundance, distribution, and threat The SRR and SIR provided the information on the regulatory mechanisms or conservation efforts for susceptibilities. We developed our following information on A. pharaonis’ assessment of the species’ vulnerability life history. Acropora pharaonis is a A. pharaonis. Criticisms of our approach received during public to extinction using all the available hermaphroditic spawner with information. As explained in the Risk lecithotrophic (yolk-sac) larvae. The comment led us to the following analysis to attempt to analyze regulatory Analyses section, our assessment in this public comments and information we final rule emphasizes the ability of the gathered did not provide anything mechanisms on a species basis. Records confirm that A. pharaonis occurs in 11 species’ spatial and demographic traits additional to the above-described to moderate or exacerbate its biological information. Indo-Pacific ecoregions that encompass 21 countries’ EEZs. The 21 countries are vulnerability to extinction, as opposed Susceptibility to Threats Bahrain, Djibouti, Egypt, Eritrea, France to the approach we used in the proposed rule, which emphasized the To describe A. pharaonis’ threat (French Pacific Island Territories), species’ susceptibility to threats. susceptibilities, the SRR and SIR India, Iran, Israel, Jordan, Kuwait, provided genus-level information for the Madagascar, Maldives, Mauritius, Qatar, The following characteristics of A. effects on Acropora of ocean warming, Saudi Arabia, Seychelles, Somalia, Sri pharaonis, in conjunction with the acidification, disease, predation, Lanka, Sudan, United Arab Emirates, information described in the Corals and sedimentation, nutrients, and collection and Yemen. The regulatory mechanisms Coral Reefs section, Coral Habitat sub- and trade. The SRR also reported that A. relevant to A. pharaonis, described first section, and Threats Evaluation section pharaonis was locally extirpated in the as the percentage of the above countries above, affect its vulnerability to SE Arabian Gulf after the combined that utilize them to any degree and extinction currently and over the impacts of the 1996 and 1998 bleaching second, as the percentages of those foreseeable future. Its geographic events, and that the species is countries whose regulatory mechanisms distribution includes the Red Sea and susceptible to several diseases that may be limited in scope, are as follows: Arabian Gulf, but relatively few islands. affect reproduction including reduced General coral protection (29 percent This exacerbates vulnerability to fecundity. We interpreted the threat with 10 percent limited in scope), coral extinction over the foreseeable future susceptibility and exposure information collection (43 percent with five percent because it is restricted a portion of the from the SRR and SIR in the proposed limited in scope), pollution control (52 Indian Ocean with a limited amount of rule for A. pharaonis’ vulnerabilities as percent with five percent limited in island and offshore habitat, and follows: High vulnerability to ocean scope), fishing regulations on reefs (76 includes areas projected to have the warming and disease, moderate percent with 24 percent limited in most rapid and severe impacts from vulnerabilities to ocean acidification, scope), and managing areas for climate change and localized human trophic effects of fishing, nutrients, and protection and conservation (71 percent impacts for coral reefs over the 21st predation, and low vulnerabilities to with 14 percent limited in scope). The century (i.e., the Red Sea and the sedimentation, sea-level rise, and most common regulatory mechanisms in Arabian Gulf). Its depth range of five to collection and trade. place for A. pharaonis are reef fishing 25 meters moderates vulnerability to Public comments did not provide regulations and area management for extinction over the foreseeable future supplemental information on A. protection and conservation. Coral because deeper areas of its range will pharaonis’ threat susceptibilities. We collection and pollution control laws usually have lower irradiance than gathered the following species-specific are also somewhat common for the surface waters, and acidification is and genus-level supplemental species. General coral protection laws generally predicted to accelerate most in information on this species’ threat are much less prominent regulatory waters that are deeper and cooler than susceptibilities. Acropora pharaonis has mechanisms for the management of A. those in which the species occurs. Its been rated as moderately or highly pharaonis. habitat includes reef slope and back-reef susceptible to bleaching and disease, habitats, including at least upper reef but these ratings are not based on Vulnerability to Extinction slopes, mid-slope terraces, and lagoons. species-specific data (Carpenter et al., As explained above in the Risk This moderates vulnerability to 2008). No other species-specific Analyses section, a species’ extinction over the foreseeable future information is available for the vulnerability to extinction results from because the species is not limited to one susceptibility of A. pharaonis to any the combination of its spatial and habitat type but occurs in numerous other threat. Based on information from demographic characteristics, threat types of reef environments that will, on other Acropora species provided in the susceptibilities, and consideration of the local and regional scales, experience genus description above, A. pharaonis baseline environment and future highly variable thermal regimes and likely has high susceptibility ocean projections of threats. The SRR stated ocean chemistry at any given point in warming, and also likely has some that the high bleaching rate of the time. There is not enough information susceptibility to disease, ocean Acropora genus is the primary known about its abundance to determine if it acidification, trophic effects of fishing, threat of extinction for A. pharaonis. moderates or exacerbates extinction: It sedimentation, nutrients, sea-level rise, This is exacerbated by its restricted is common in the Red Sea, uncommon and collection and trade. Based on the range and the need for protected elsewhere, and has at least millions of available information, high habitats. The SRR also listed factors that colonies, but the Red Sea and Arabian susceptibility to disease (as stated in the reduce the threat of extinction including Gulf portions of the population are proposed rule for this species) is not its moderate depth range (5 m to 25 m) expected to be severely impacted by supported. The available information and its common abundance levels in the threats over the foreseeable future. does not support more precise ratings of Red Sea. While depth distribution and habitat the susceptibilities of A. pharaonis to Subsequent to the proposed rule, we variability moderate vulnerability to the threats. received and gathered supplemental extinction, the combination of its

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geographic distribution and high The combination of these pharaonis. However, considering the susceptibility to ocean warming are characteristics and future projections of global scale of the most important likely to be more influential to the status threats indicates that the species is threats to the species, and the of this species over the foreseeable likely to be in danger of extinction ineffectiveness of conservation efforts at future, because of the projected severity within the foreseeable future throughout addressing the root cause of global of ocean warming in much of the its range and warrants listing as threats (i.e., GHG emissions), we do not species’ range in the foreseeable future, threatened at this time due to factors A, believe that any current conservation and its high susceptibility to this threat. C, D, and E. efforts or conservation efforts planned The available information above on A. in the future will result in affecting the Listing Determination pharaonis’ spatial structure, species status to the point at which In the proposed rule using the demography, threat susceptibilities, and listing is not warranted. determination tool formula approach, A. management also indicate that the Acropora polystoma pharaonis was proposed for listing as species the species is not currently in threatened because of: High danger of extinction and thus does not Introduction vulnerability to ocean warming (ESA warrant listing as Endangered because: (1) While A. pharaonis’ distribution The SRR and SIR provided the Factor E) and disease (C); moderate following information on A. polystoma’s vulnerability to acidification (E); in only the Indian Ocean and the Middle East, which increases it morphology and taxonomy. Morphology common generalized range wide was described as irregular clumps or abundance (E); narrow overall extinction risk as described above, its habitat includes sheltered lagoon patch plates with tapered branches of similar distribution (based on narrow length and shape, and being similar to geographic distribution and moderate reefs and other shallow reef environments. This moderates A. massawensis and A. polystoma. The depth distribution (E); and inadequacy taxonomy was described as not having of existing regulatory mechanisms (D). vulnerability to extinction currently because the species is not limited to one much uncertainty, except in the In this final rule, we confirmed the Mariana Islands where specimens species’ proposed listing determination habitat type but occurs in numerous types of reef environments that will, on previously identified as A. polystoma as threatened. Based on the best may be a different species. available information provided above on local and regional scales, experience highly variable thermal regimes and The public comments and A. pharaonis’ spatial structure, information we gathered provided demography, threat susceptibilities, and ocean chemistry at any given point in time, as described in more detail in the information on morphology or management indicate that it is likely to Coral Habitat and Threats Evaluation taxonomy of A. polystoma. One public become endangered throughout its range sections. There is no evidence that the comment stated that specimens of A. within the foreseeable future, and thus species is so spatially fragmented or polystoma in Guam may represent a still warrants listing as threatened at geographically constrained that different species. We gathered this time, because: depensatory processes, environmental supplemental information, including (1) Acropora pharaonis is highly stochasticity, or the potential for Veron (2014), which states that A. susceptible to ocean warming (ESA catastrophic events currently pose a polystoma is distinctive, thus we Factor E), and susceptible to disease (C), high risk to the survival of the species; conclude it can be identified by experts, ocean acidification (E), trophic effects of and and that the distribution and abundance fishing (A), predation (C), and nutrients (2) Acropora pharaonis absolute information described below for this (A, E). These threats are expected to abundance is at least millions of species is sufficiently reliable (Fenner, continue and increase into the future. In colonies, which allows for variation in 2014b). addition, existing regulatory the responses of individuals to threats to Spatial Information mechanisms to address global threats play a role in moderating vulnerability that contribute to extinction risk for this to extinction for the species to some The SRR and SIR provided the species are inadequate (D). degree, as described in more detail in following information on A. polystoma’s (2) Acropora pharaonis’ distribution the Corals and Coral Reefs section. distribution, habitat, and depth range. is constrained entirely to the Red Sea, There is no evidence of depensatory Acropora polystoma is distributed from Arabian Gulf, and western and central processes such as reproductive failure the Red Sea to the Indian Ocean to the Indian Ocean where projections of from low density of reproductive central Pacific. The species has the 28th ocean warming and local threats (e.g., individuals and genetic processes such largest range of 114 Acropora species. land-based sources of pollution) are as inbreeding affecting this species. Its habitat includes areas exposed to both frequent and severe over the Thus, its absolute abundance indicates strong wave action, including upper reef foreseeable future compared to other it is currently able to avoid high slopes, lower reef crests, reef flats, and areas of the Indo-Pacific. A range mortality from environmental other habitats, and its depth range is constrained to a particular geographic stochasticity, and mortality of a high three to 10 meters. area that is likely to experience severe proportion of its population from The public comments did not provide and worsening threats indicates that a catastrophic events. any new or supplemental information high proportion of the population of this The combination of these on A. polystoma’s distribution. We species is likely to be exposed to those characteristics indicates that the species gathered supplemental information, threats over the foreseeable future; and does not exhibit the characteristics of including Veron (2014), which reports (3) Acropora pharaonis suffered one that is currently in danger of that this species is confirmed in 48 of documented local extirpation in the extinction, as described previously in his 133 Indo-Pacific ecoregions, and southeast Arabian Gulf after the the Risk Analyses section, and thus does strongly predicted to be found in an combined impacts of the 1996 and 1998 not warrant listing as endangered at this additional 19. Wallace (1999b) reports bleaching events, providing evidence time. its occurrence in 19 of her 29 Indo- that this species has already been Range-wide, a multitude of Pacific areas, many of which are severely impacted by ocean warming in conservation efforts are already broadly significantly larger than Veron’s some parts of its range. employed that are likely benefiting A. ecoregions. Richards (2009) calculated

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the geographic range of A. polystoma at precise quantification is not possible Regulatory Mechanisms 2 85 million km . The public comments based on the limited species-specific In the proposed rule, we did not and information we gathered provided information. provide any species-specific nothing additional on A. polystoma’s Other Biological Information information on the regulatory habitat and depth range. mechanisms or conservation efforts for Demographic Information The SRR and SIR provided the A. polystoma. Criticisms of our The SRR and SIR provided the following information on A. polystoma’s approach received during public following information on A. polystoma’s life history. Acropora polystoma is a comment led us to the following abundance. Acropora polystoma has hermaphroditic spawner with analysis to attempt to analyze regulatory been reported as uncommon. lecithotrophic (yolk-sac) larvae. The mechanisms on a species basis. Records The public comments did not provide public comments and information we confirm that A. polystoma occurs in 48 any new or supplemental information gathered did not provide anything Indo-Pacific ecoregions that encompass on A. polystoma’s abundance. We additional to the above-described 41 countries’ EEZs. The 41 countries are gathered supplemental information, biological information. Australia, Brunei, China, Djibouti, including Veron (2014), which reports Egypt, Eritrea, Federated States of that A. polystoma occupied 6.7 percent Susceptibility to Threats Micronesia, Fiji, France (French Pacific Island Territories), India (Andaman and of 2,984 dive sites sampled in 30 To describe A. polystoma’s threat ecoregions of the Indo-Pacific, and had Nicobar Islands), Indonesia, Israel, susceptibilities, the SRR and SIR Japan, Jordan, Kenya, Madagascar, a mean abundance rating of 1.74 on a 1 provided genus-level information for the to 5 rating scale at those sites in which Malaysia, Maldives, Marshall Islands, effects on Acropora of ocean warming, Mauritius, Myanmar, New Zealand it was found. Based on this semi- acidification, disease, predation, quantitative system, the species’ (Tokelau), Niue, Palau, Papua New sedimentation, nutrients, and collection abundance was characterized as Guinea, Philippines, Samoa, Saudi and trade. The SRR and SIR did not ‘‘common.’’ Overall abundance was Arabia, Solomon Islands, Sudan, provide any species-specific described as ‘‘uncommon.’’ Veron did Taiwan, Tanzania, Thailand, Timor- not infer trends in abundance from information on the effects of these Leste, Tonga, Tuvalu, United Kingdom these data. As described in the Indo- threats on A. polystoma. We interpreted (British Indian Ocean Territory), United Pacific Species Determinations the threat susceptibility and exposure States (CNMI, Guam, American Samoa, introduction above, based on results information from the SRR and SIR in the PRIAs), Vanuatu, Vietnam, and Yemen. from Richards et al. (2008) and Veron proposed rule for A. polystoma’s The regulatory mechanisms relevant to (2014), the absolute abundance of this vulnerabilities as follows: High A. polystoma, described first as the species is likely at least tens of millions vulnerability to ocean warming and percentage of the above countries that of colonies. disease, moderate vulnerabilities to utilize them to any degree and second, Carpenter et al. (2008) extrapolated ocean acidification, trophic effects of the percentages of those countries species abundance trend estimates from fishing, nutrients, and predation, and whose regulatory mechanisms may be total live coral cover trends and habitat low vulnerabilities to sedimentation, limited in scope, are as follows: General types. For A. polystoma, the overall sea-level rise, and collection and trade. coral protection (24 percent with two decline in abundance (‘‘Percent Public comments did not provide any percent limited in scope), coral Population Reduction’’) was estimated new or supplemental information on A. collection (63 percent with 32 percent at 35 percent, and the decline in polystoma’s threat susceptibilities. We limited in scope), pollution control (39 abundance before the 1998 bleaching gathered the following species-specific percent with seven percent limited in event (‘‘Back-cast Percent Population and genus-level supplemental scope), fishing regulations on reefs (90 Reduction’’) was estimated at 14 information on this species’ threat percent with 20 percent limited in percent. However, as summarized above susceptibilities. A. polystoma has been scope), and managing areas for in in the Inter-basin Comparison sub- rated as moderately or highly protection and conservation (95 percent section, live coral cover trends are susceptible to bleaching and warming- with 10 percent limited in scope). The highly variable both spatially and most common regulatory mechanisms in induced disease, but these ratings are temporally, producing patterns on small place for A. polystoma are reef fishing not based on species-specific data scales that can be easily taken out of regulations and area management for (Carpenter et al., 2008). No other context, thus quantitative inferences to protection and conservation. Coral species-specific information is available species-specific trends should be collection and pollution control laws for the susceptibility of A. polystoma to interpreted with caution. At the same are also somewhat common for the time, an extensive body of literature any other threat. Based on information species, but 32 percent of coral documents broad declines in live coral from other Acropora species provided collection laws are limited in scope and cover and shifts to reef communities in the genus description above, A. may not provide substantial protection. dominated by hardier coral species or polystoma likely has high susceptibility General coral protection laws are much algae over the past 50 to 100 years ocean warming, and also likely has less prominent regulatory mechanisms (Birkeland, 2004; Fenner, 2012; Pandolfi some susceptibilities to disease, ocean for the management of A. polystoma. et al., 2003; Sale and Szmant, 2012). acidification, trophic effects of fishing, These changes have likely occurred, and sedimentation, nutrients, sea-level rise, Vulnerability to Extinction are occurring, from a combination of and collection and trade. Based on the As explained above in the Risk global and local threats. Given that A. available information, high Analyses section, a species’ polystoma occurs in many areas affected susceptibility to disease, as stated in the vulnerability to extinction results from by these broad changes, and that it has proposed rule for this species, is not the combination of its spatial and some susceptibility to both global and supported. The available information demographic characteristics, threat local threats, we conclude that it is does not support more precise ratings of susceptibilities, and consideration of the likely to have declined in abundance the susceptibilities of A. polystoma to baseline environment and future over the past 50 to 100 years, but a the threats. projections of threats. The SRR stated

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that the high bleaching rate of the wave action experience high levels of explained above in the Threats Acropora genus is the primary known mixing which can dilute adverse Evaluation section, we have not threat of extinction for A. polystoma, environmental conditions. Its absolute identified any threat that is expected to which is exacerbated by the relatively abundance of at least tens of millions of occur uniformly throughout the species restricted depth range and the colonies, combined with spatial range within the foreseeable future; uncommon abundance. It listed factors variability in ocean warming and (2) Acropora polystoma’s absolute that reduce the threat of extinction acidification across the species range, abundance is at least tens of millions of including the wide geographic range, moderates vulnerability to extinction colonies, providing buffering capacity in and the intertidal habitat which may because the increasingly severe the form of absolute numbers of indicate potentially increased tolerance. conditions expected in the foreseeable colonies and variation in susceptibility Subsequent to the proposed rule, we future will be non-uniform and between individual colonies. As received and gathered supplemental therefore will likely be a large number discussed in the Corals and Coral Reefs species- or genus-specific information, of colonies that are either not exposed section above, the more colonies a described above, that expands our or do not negatively respond to a threat species has, the lower the proportion of knowledge regarding the species at any given point in time. colonies that are likely to be exposed to abundance, distribution, and threat Listing Determination a particular threat at a particular time, susceptibilities. We developed our and all individuals that are exposed will assessment of the species’ vulnerability In the proposed rule using the not have the same response; and to extinction using all the available determination tool formula approach, A. (3) A. polystoma is a broadcast information. As explained in the Risk polystoma was proposed for listing as spawner and fast grower, enhancing Analyses section, our assessment in this threatened because of: High recovery potential from mortality events final rule emphasizes the ability of the vulnerability to ocean warming (ESA as described in the Corals and Coral species’ spatial and demographic traits Factor E); moderate vulnerability to Reefs section above. to moderate or exacerbate its disease (C) and acidification (E); Notwithstanding the projections vulnerability to extinction, as opposed uncommon generalized range wide through 2100 that indicate increased to the approach we used in the abundance (E); moderate overall severity over time of the three high proposed rule, which emphasized the distribution (based on wide geographic importance threats, the combination of species’ susceptibility to threats. distribution and shallow depth these biological and environmental The following characteristics of A. distribution (E); and inadequacy of characteristics indicates that the species polystoma, in conjunction with the existing regulatory mechanisms (D). possesses sufficient buffering capacity information described in the Corals and In this final rule, we changed the to avoid being in danger of extinction Coral Reefs section, Coral Habitat sub- listing determination for A. polystoma within the foreseeable future throughout section, and Threats Evaluation section from threatened to not warranted. We its range. It is possible that this species’ above, affect its vulnerability to made this determination based on a extinction risk may increase in the more species-specific and holistic extinction currently and over the future as global threats continue and assessment of whether this species foreseeable future. Its geographic increase in severity and the species meets the definition of either a distribution includes most of the coral exposure to threats increases throughout threatened or endangered coral largely reef ecoregions in the Indian Ocean and its range. Should the species experience in response to public comments, western and central Pacific Ocean. Its reduced abundance or range including more appropriate geographic distribution moderates constriction of a certain magnitude, the consideration of the buffering capacity vulnerability to extinction because some ability of these characteristics to of this species’ spatial and demographic areas within its range are projected to moderate exposure to threats will traits to lessen its vulnerability to have less than average warming and diminish. However, the species is not threats. Thus, based on the best acidification over the foreseeable future, likely to become of such low abundance including the western Indian Ocean, the available information above on A. or so spatially fragmented as to be in central Pacific, and other areas, so polystoma’s spatial structure, danger of extinction due to depensatory portions of the population in these areas demography, threat susceptibilities, and processes, the potential effects of will be less exposed to severe management, none of the five ESA environmental stochasticity, or the conditions. Its depth distribution down listing factors, alone or in combination, potential for mortality from catastrophic to 10 meters may exacerbate the species are causing this species to be likely to events within the foreseeable future exposure to some threats that are more become endangered throughout its range throughout its range. Therefore, A. severe in shallower water. Shallow reef within the foreseeable future, and thus polystoma is not warranted for listing at environments can experience frequent is not warranted for listing at this time, this time under any of the listing factors. changes in environmental conditions, because: extremes, high irradiance, and multiple (1) Acropora polystoma’s distribution Acropora retusa stressors simultaneously. However, its across the Red Sea, Indian Ocean and habitat includes areas exposed to strong most of the Pacific Ocean is spread over Introduction wave action, including upper reef a very large area. While some areas The SRR and SIR provided the slopes, lower reef crests, reef flats, and within its range are projected to be following information on A. retusa’s other high energy habitats. This affected by warming and acidification, morphology and taxonomy. The moderates vulnerability to extinction other areas are projected to have less morphology was described as flat plates over the foreseeable future because the than average warming and acidification, with short thick digitate branchlets and species is not limited to one habitat type including the western Indian Ocean, the taxonomy was described as having no but occurs in numerous types of reef central Pacific, and other areas. This taxonomic issues, but it is similar to environments that will, on local and distribution and the heterogeneous Acropora branchi, Acropora gemmifera, regional scales, experience highly habitats it occupies reduce exposure to and Acropora monticulosa. variable thermal regimes and ocean any given threat event or adverse The public comments did not provide chemistry at any given point in time. In condition that does not occur uniformly any new or supplemental information addition, areas of high currents and/or throughout the species range. As on morphology or taxonomy of A.

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retusa. We gathered supplemental abundance of this species is likely at fishing, nutrients, and predation, and information, which indicated that while least millions of colonies. low vulnerabilities to sedimentation, there is some taxonomic uncertainty for Carpenter et al. (2008) extrapolated sea-level rise, and collection and trade. this species, it is recognized as valid by species abundance trend estimates from Public comments did not provide any experts (Veron, 2000; Wallace, 1999a). total live coral cover trends and habitat new or supplemental information on A. Veron (2014) states that A. retusa is types. For A. retusa, the overall decline retusa’s threat susceptibilities. We readily confused with other Acropora, in abundance (‘‘Percent Population gathered the following species-specific but we conclude it can be identified by Reduction’’) was estimated at 49 and genus-level supplemental experts, and that the distribution and percent, and the decline in abundance information on this species’ threat abundance information described below before the 1998 bleaching event (‘‘Back- susceptibilities. Acropora retusa has for this species is sufficiently reliable cast Percent Population Reduction’’) been rated as moderately or highly (Fenner, 2014b). was estimated at 18 percent. However, susceptible to bleaching and disease, as summarized above in the Inter-basin but these ratings are not based on Spatial Information Comparison sub-section, live coral cover species-specific data (Carpenter et al., The SRR and SIR provided the trends are highly variable both spatially 2008). No other species-specific following information on A. retusa’s and temporally, producing patterns on information is available for the distribution, habitat, and depth range. small scales that can be easily taken out susceptibility of A. retusa to any other Acropora retusa is distributed from the of context, thus quantitative inferences threat. Based on information from other Red Sea and the Indian Ocean to the to species-specific trends should be Acropora species provided in the genus central Pacific. The species has the 52nd interpreted with caution. At the same description above, A. retusa is likely largest range of 114 Acropora species. time, an extensive body of literature highly susceptible to ocean warming, Its habitat includes shallow reef slope documents broad declines in live coral and also likely has some susceptibilities and back-reef areas, such as upper reef cover and shifts to reef communities to disease, ocean acidification, trophic slopes, reef flats, shallow lagoons, and dominated by hardier coral species or effects of fishing, sedimentation, its depth range is one to five meters. algae over the past 50 to 100 years nutrients, sea-level rise, predation, and The public comments did not provide (Birkeland, 2004; Fenner, 2012; Pandolfi collection and trade. The available any new or supplemental information et al., 2003; Sale and Szmant, 2012). information does not support more on A. retusa’s distribution. We gathered These changes have likely occurred, and precise ratings of the susceptibilities of supplemental information, including are occurring, from a combination of A. retusa to the threats. Veron (2014), which reports that this global and local threats. Given that A. Regulatory Mechanisms species is confirmed in 23 of his 133 retusa occurs in many areas affected by Indo-Pacific ecoregions, and strongly these broad changes, and that it has In the proposed rule, we did not predicted to be found in an additional some susceptibility to both global and provide any species-specific 21. Wallace (1999b) reports its local threats, we conclude that it is information on the regulatory occurrence in five of her 29 Indo-Pacific likely to have declined in abundance mechanisms or conservation efforts for areas, many of which are larger than over the past 50 to 100 years, but a A. retusa. Criticisms of our approach Veron’s ecoregions. Richards (2009) precise quantification is not possible received during public comment led us estimated its range at 68 million km2. due to the limited amount of species- to the following analysis to attempt to The public comments and information specific information. analyze regulatory mechanisms on a we gathered provided nothing species basis. Records confirm that A. additional on A. retusa’s habitat and Other Biological Information retusa occurs in 23 Indo-Pacific depth range. The SRR and SIR provided the ecoregions that encompass 26 countries’ following information on A. retusa’s life EEZs. The 26 countries are Brunei, Demographic Information history. Acropora retusa is a Federated States of Micronesia, Fiji, The SRR and SIR provided the hermaphroditic spawner with France (French Pacific Island following information on A. retusa’s lecithotrophic (yolk-sac) larvae. The Territories), India, Indonesia, Japan, abundance. Acropora retusa has been public comments and information we Kenya, Madagascar, Malaysia, reported as common in South Africa gathered did not provide anything Mauritius, Mozambique, New Zealand and uncommon elsewhere. The public additional to the above-described (Cook Islands, Tokelau), Niue, Palau, comments did not provide any new or biological information. Papua New Guinea, Samoa, Seychelles, supplemental information on A. retusa’s Solomon Islands, South Africa, Sri abundance. We gathered supplemental Susceptibility to Threats Lanka, Tanzania, Tonga, Tuvalu, United information, including Veron (2014), To describe A. retusa’ threat States (CNMI, Guam, American Samoa), which reports that A. retusa occupied susceptibilities, the SRR and SIR and Vietnam. The regulatory 0.5 percent of 2,984 dive sites sampled provided genus-level information for the mechanisms relevant to A. retusa, in 30 ecoregions of the Indo-Pacific, and effects on Acropora of ocean warming, described first as the percentage of the had a mean abundance rating of 1.21 on acidification, disease, predation, above countries that utilize them to any a 1 to 5 rating scale at those sites in sedimentation, nutrients, and collection degree and second, as the percentages of which it was found. Based on this semi- and trade. The SRR and SIR did not those countries whose regulatory quantitative system, the species’ provide any other species-specific mechanisms may be limited in scope, abundance was characterized as ‘‘rare.’’ information on the effects of these are as follows: General coral protection Overall abundance was described as threats on A. retusa. We interpreted the (19 percent with eight percent limited in ‘‘common in South Africa, rare threat susceptibility and exposure scope), coral collection (58 percent with elsewhere.’’ Veron did not infer trends information from the SRR and SIR in the 35 percent limited in scope), pollution in abundance from these data. As proposed rule for A. retusa’s control (38 percent with 12 percent described in the Indo-Pacific Species vulnerabilities as follows: High limited in scope), fishing regulations on Determinations introduction above, vulnerability to ocean warming, reefs (96 percent with 23 percent based on results from Richards et al. moderate vulnerabilities to disease, limited in scope), and managing areas (2008) and Veron (2014), the absolute ocean acidification, trophic effects of for protection and conservation (100

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percent with none limited in scope). portions of the population in these areas warrants listing as threatened at this The most common regulatory will be less exposed to severe time, because: mechanisms in place for A. retusa are conditions. Its depth range of zero to (1) Acropora retusa is highly reef fishing regulations and area five meters exacerbates vulnerability to susceptible to ocean warming (ESA management for protection and extinction over the foreseeable future. Factor E), and susceptible to disease (C), conservation. Coral collection and Shallow reef areas are often subjected to ocean acidification (E), trophic effects of pollution control laws are also highly variable environmental fishing (A), predation (C), and nutrients somewhat common for the species, but conditions, extremes, high irradiance, (A, E). These threats are expected to 35 percent of coral collection laws are and simultaneous effects from multiple continue and increase into the future. In limited in scope and may not provide stressors, both local and global in addition, existing regulatory substantial protection. General coral nature. A species restricted to such mechanisms addressing global threats protection laws are much less shallow depths is likely to have a high that contribute to extinction risk for this prominent regulatory mechanisms for proportion of individuals exposed to species inadequate (D); the management of A. retusa. higher levels of irradiance and other (2) Acropora retusa is restricted to shallow habitat (zero to five meters), Vulnerability to Extinction threats that are more severe in shallow habitats. Its habitat includes shallow where many global and local threats As explained above in the Risk reef slope and back-reef areas, such as may be more severe, especially near Analyses section, a species’ upper reef slopes, reef flats, and shallow populated areas. Shallow reef areas are vulnerability to extinction results from lagoons. While this generally moderates often subjected to highly variable the combination of its spatial and vulnerability to extinction for most environmental conditions, extremes, demographic characteristics, threat species that can occupy a diverse set of high irradiance, and simultaneous susceptibilities, and consideration of the habitat types, in this case, habitat effects from multiple stressors, both baseline environment and future heterogeneity likely does not provide local and global in nature. A limited projections of threats. The SRR stated much moderation of exposure to threats depth range also reduces the absolute that the high bleaching rate of the because of the shallow depth restriction area in which the species may occur Acropora genus is the primary known for this species. Its absolute abundance throughout its geographic range, and threat of extinction for A. retusa. The of at least millions of colonies, indicates that a large proportion of the species’ rarity adds to its risk of combined with spatial variability in population is likely to be exposed to extinction. The SRR also listed factors ocean warming and acidification across threats that are worse in shallow that reduce the threat of extinction the species range, moderates habitats, such as simultaneously including its geographic range and its vulnerability to extinction because the elevated irradiance and seawater occurrence in tidal pools (suggesting temperatures, as well as localized increasingly severe conditions expected high physiological stress tolerance). impacts; and in the foreseeable future will be non- Subsequent to the proposed rule, we (3) Acropora retusa’s abundance is received and gathered supplemental uniform and therefore will likely be a considered rare overall. This level of species- or genus-specific information, large number of colonies that are either abundance, combined with its restricted described above, that expands our not exposed or do not negatively depth distribution where impacts are knowledge regarding the species respond to a threat at any given point more severe, leaves the species abundance, distribution, and threat in time. However, its qualitative vulnerable to becoming of such low susceptibilities. We developed our abundance is described as rare, which abundance within the foreseeable future assessment of the species’ vulnerability combined with its restricted depth that it may be at risk from depensatory to extinction using all the available distribution indicates it is likely that a processes, environmental stochasticity, information. As explained in the Risk high proportion of individuals will be or catastrophic events, as explained in Analyses section, our assessment in this affected by threats that are typically more detail in the Corals and Coral final rule emphasizes the ability of the more severe in shallow habitats at any Reefs and Risk Analyses sections. species’ spatial and demographic traits given point in time. The combination of these to moderate or exacerbate its Listing Determination characteristics and future projections of vulnerability to extinction, as opposed threats indicates that the species is to the approach we used in the In the proposed rule using the listing likely to be in danger of extinction proposed rule, which emphasized the determination tool approach, A. retusa within the foreseeable future throughout species’ susceptibility to threats. was proposed for listing as threatened its range and warrants listing as The following characteristics of A. because of: High vulnerability to ocean threatened at this time due to factors A, retusa, in conjunction with the warming (ESA Factor E); moderate C, D, and E. information described in the Corals and vulnerability to disease (C) and The available information above on A. Coral Reefs section, Coral Habitat sub- acidification (E); uncommon generalized retusa’s spatial structure, demography, section, and Threats Evaluation section range wide abundance (E); moderate threat susceptibilities, and management above, affect its vulnerability to overall distribution (based on wide also indicate that the species is not extinction currently and over the geographic distribution and shallow currently in danger of extinction and foreseeable future. Its geographic depth distribution (E); and inadequacy thus does not warrant listing as distribution includes many coral reef of existing regulatory mechanisms (D). Endangered because: ecoregions in the Indian Ocean and In this final rule, we maintain the (1) Acropora retusa’s distribution western and central Pacific Ocean. Its species’ proposed listing determination from South Africa to the Pitcairn Islands geographic distribution moderates as threatened. Based on the best is spread over a very large area. While vulnerability to extinction because some available information provided above on some areas within its range are areas within its range are projected to A. retusa’s spatial structure, projected to be affected by warming and have less than average warming and demography, threat susceptibilities, and acidification, other areas are projected acidification over the foreseeable future, management indicate that it is likely to to have less than average warming and including the western Indian Ocean, the become endangered throughout its range acidification, including the western central Pacific, and other areas, so within the foreseeable future, and thus Indian Ocean, the central Pacific, and

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other areas. This distribution reduces was described as arborescent with large, Demographic Information exposure to any given threat event or tapered, prostate branches, reaching a The SRR and SIR provided the adverse condition that does not occur maximum size of 50 cm and taxonomy following information on A. rudis’ uniformly throughout the species range. was described as having no taxonomic abundance. Acropora rudis has been As explained above in the Threats issues but being similar in appearance reported as uncommon, however, it has Evaluation section, we have not to A. hemprichii and A. variolosa. been noted to comprise as much as half identified any threat that is expected to The public comments and of the Acropora in some areas. occur uniformly throughout the species information we gathered provided The public comments did not provide range within the foreseeable future; information on morphology or supplemental information on A. rudis’ (2) While Acropora retusa is limited taxonomy. One public comment stated abundance. We gathered supplemental to shallow depths, which increases its that specimens collected in American information, including Veron (2014), extinction risk as described above, its Samoa and identified by the American which reports that A. rudis occupied 0.1 geographic range encompasses Samoa Department of Marine and Water percent of 2,984 dive sites sampled in heterogeneous habitat, the benefits of Resources as A. rudis appear to be A. 30 ecoregions of the Indo-Pacific, and which are explained in detail in the aculeus, thereby illustrating the species had a mean abundance rating of 1.25 on Coral Habitat sub-section above, across identification uncertainties associated a 1 to 5 rating scale at those sites in almost half of the coral reef area in the with this species. We gathered which it was found. Based on this semi- Indo-Pacific, and there is no evidence to supplemental information, including quantitative system, the species’ suggest that it is so spatially fragmented Veron (2014), which states that A. rudis abundance was characterized as ‘‘rare.’’ that depensatory processes, is readily confused with Acropora Overall abundance was described as environmental stochasticity, or the schmitti in shallow habitats, but is very ‘‘uncommon.’’ Veron did not infer potential for catastrophic events distinctive otherwise, thus we conclude trends in abundance from these data. currently pose a high risk to the survival it can be identified by experts, and that Other information indicates that A. of the species; and the distribution and abundance rudis can be locally common, as it has (3) While Acropora retusa’s information described below for this been reported to comprise as much as qualitative abundance is characterized species is sufficiently reliable (Fenner, half of the Acropora in the area south as rare, its absolute abundance is at least 2014b). of the Hikkaduwa Nature Reserve in Sri millions of colonies. Additionally, A. Spatial Information Lanka (Rajasuriya, 2002). As described retusa is considered common in a in the Indo-Pacific Species portion of its range (South Africa), The SRR and SIR provided the Determinations introduction above, indicating it is not of such low following information on A. rudis’ based on results from Richards et al. abundance that depensatory processes, distribution, habitat, and depth range. (2008) and Veron (2014), the absolute environmental stochasticity, or the Acropora rudis’ distribution has long abundance of this species is likely at potential for catastrophic events been thought by Veron and others to be least millions of colonies. currently pose a high risk to the survival restricted to the northeastern Indian Carpenter et al. (2008) extrapolated of the species. Ocean, with recent reports by Fenner species abundance trend estimates from Notwithstanding the projections suggesting it may also occur in New total live coral cover trends and habitat through 2100 that indicate increased Caledonia and the Samoas. The species types. For A. rudis, the overall decline severity over time of the three high has the 24th smallest range of 114 in abundance (‘‘Percent Population importance threats, the combination of Acropora species. Its predominant Reduction’’) was estimated at 59 these biological and environmental habitat is lower reef crests and upper percent, and the decline in abundance characteristics indicates that the species reef slopes in three to 15 m of depth. before the 1998 bleaching event (‘‘Back- does not exhibit the characteristics of The public comments did not provide cast Percent Population Reduction’’) one that is currently in danger of supplemental information on A. rudis’ was estimated at 22 percent. This extinction, as described previously in distribution. We gathered supplemental estimated decline is approximately 50 the Risk Analyses section, and thus does information, including Veron (2014), percent higher than most other Indo- not warrant listing as endangered at this which provides much more detailed Pacific Acropora species included in the time. range map for this species than the paper, apparently because of the Range-wide, a multitude of maps used in the SRR. Veron reports combined restricted geographic and conservation efforts are already broadly that this species is confirmed in seven depth ranges (Carpenter et al., 2008). employed that are likely benefiting A. of his 133 Indo-Pacific ecoregions, and However, as summarized above in the retusa. However, considering the global strongly predicted to be found in an Inter-basin Comparison sub-section, live scale of the most important threats to additional two. Veron (2014) does not coral cover trends are highly variable the species, and the ineffectiveness of show it in New Caledonia and the both spatially and temporally, conservation efforts at addressing the Samoas, apparently because he does not producing patterns on small scales that root cause of global threats (i.e., GHG believe there is enough information can be easily taken out of context, thus emissions), we do not believe that any available to strongly predict its quantitative inferences to species- current conservation efforts or occurrence there. Wallace (1999b) specific trends should be interpreted conservation efforts planned in the reports its occurrence in four of her 29 with caution. At the same time, an future will result in affecting the species Indo-Pacific areas, many of which are extensive body of literature documents status to the point at which listing is not larger than Veron’s ecoregions. Richards broad declines in live coral cover and warranted. (2009) calculated the geographic range shifts to reef communities dominated by Acropora rudis of A. rudis at two million km2, which hardier coral species or algae over the was the 24th smallest range of the 114 past 50 to 100 years (Birkeland, 2004; Introduction Acropora species examined. The public Fenner, 2012; Pandolfi et al., 2003; Sale The SRR and SIR provided the comments and information we gathered and Szmant, 2012). These changes have following information on A. rudis’ provided nothing additional on A. rudis’ likely occurred, and are occurring, from morphology and taxonomy. Morphology habitat and depth range. a combination of global and local

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threats. Given that A. rudis occurs in Regulatory Mechanisms susceptibilities. We developed our many areas affected by these broad In the proposed rule, we did not assessment of the species’ vulnerability changes, and that it has some provide any species-specific to extinction using all the available susceptibility to both global and local information on the regulatory information. As explained in the Risk threats, we conclude that it is likely to mechanisms or conservation efforts for Analyses section, our assessment in this have declined in abundance over the A. rudis. Criticisms of our approach final rule emphasizes the ability of the past 50 to 100 years, but a precise received during public comment led us species’ spatial and demographic traits quantification is not possible based on to the following analysis to attempt to to moderate or exacerbate its the limited species-specific information. analyze regulatory mechanisms on a vulnerability to extinction, as opposed to the approach we used in the Other Biological Information species basis. Records confirm that A. rudis occurs in seven Indo-Pacific proposed rule, which emphasized the The SRR and SIR provided the ecoregions that encompass eight species’ susceptibility to threats. following information on A. rudis’ life countries’ EEZs. The eight countries are The following characteristics of A. history. There is no information Bangladesh, India (Andaman and rudis, in conjunction with the available on the reproductive biology of Nicobar Islands), Indonesia, Malaysia, information described in the Corals and A. rudis, but all other Acropora studied Maldives, Myanmar, Sri Lanka, and Coral Reefs section, Coral Habitat sub- to date are hermaphroditic broadcast Thailand. The regulatory mechanisms section, and Threats Evaluation section spawners. The public comments and relevant to A. rudis, described first as above, affect its vulnerability to information we gathered did not the percentage of the above countries extinction currently and over the provide anything additional to the that utilize them to any degree and foreseeable future. Its geographic above-described biological information. second, as the percentages of those distribution includes the Maldives and countries whose regulatory mechanisms parts of the northeastern Indian Ocean. Susceptibility to Threats may be limited in scope, are as follows: This range exacerbates vulnerability to General coral protection (25 percent extinction over the foreseeable future To describe A. rudis’ threat because it is restricted to an area susceptibilities, the SRR and SIR with 13 percent limited in scope), coral collection (38 percent with 13 percent projected to experience severe climate provided genus-level information for the change and localized impacts within the effects on Acropora of ocean warming, limited in scope), pollution control (50 percent with 13 percent limited in foreseeable future. Its depth range is acidification, disease, predation, scope), fishing regulations on reefs (100 three to 15 meters. On one hand, its sedimentation, and nutrients. The SRR percent with 25 percent limited in depth range may moderate vulnerability and SIR did not provide any species- scope), and managing areas for to extinction over the foreseeable future specific information on the effects of protection and conservation (88 percent because deeper areas of its range will these threats on A. rudis. We interpreted with 13 percent limited in scope). The usually have lower irradiance than the threat susceptibility and exposure most common regulatory mechanisms in surface waters, and acidification is information from the SRR and SIR in the place for A. rudis are reef fishing generally predicted to accelerate most in proposed rule for A. rudis’ regulations and area management for waters that are deeper and cooler than vulnerabilities as follows: High protection and conservation. Coral those in which the species occurs. On vulnerability to ocean warming, collection and pollution control laws the other hand, its depth range may moderate vulnerabilities to disease, are also somewhat common for the exacerbate vulnerability to extinction ocean acidification, trophic effects of species. General coral protection laws over the foreseeable future if the species fishing, nutrients, and predation, and are much less common regulatory occurs predominantly in the shallower low vulnerabilities to sedimentation, mechanisms for the management of A. portion of its depth range, since those sea-level rise, and collection and trade. rudis. areas will have higher irradiance and Public comments did not provide thus will be more severely affected by supplemental information on A. rudis’ Vulnerability to Extinction warming-induced bleaching. Its habitat threat susceptibilities. We gathered the As explained above in the Risk includes lower reef crests and upper following species-specific and genus- Analyses section, a species’ reef slopes. This moderates level supplemental information on this vulnerability to extinction results from vulnerability to extinction over the species’ threat susceptibilities. Acropora the combination of its spatial and foreseeable future because upper reef rudis has been rated as moderately or demographic characteristics, threat slopes are physically diverse and highly susceptible to bleaching and susceptibilities, and consideration of the widespread reef areas, thus the species disease, but these ratings are not based baseline environment and future occurs in reef environments that will, on species-specific data (Carpenter et projections of threats. The SRR stated on local and regional scales, experience al., 2008). No other species-specific that factors that increase the potential highly variable thermal regimes and information is available for the extinction risk of A. rudis include the ocean chemistry at any given point in susceptibility of A. rudis to any other relatively high susceptibility of the time. It is rare, but has at least millions threat. Based on information from other genus Acropora to common threats, and of colonies. On one hand, its depth Acropora species provided in the genus a particularly narrow and somewhat range may moderate vulnerability to description above, A. rudis is likely disjointed biogeographic range with extinction over the foreseeable future highly susceptible to ocean warming, limited latitudinal extent. They stated because deeper areas of its range will and also likely has some susceptibilities that there are no factors that notably usually have lower irradiance than to disease, ocean acidification, trophic reduce the threat of extinction. surface waters, and acidification is effects of fishing, sedimentation, Subsequent to the proposed rule, we generally predicted to accelerate most in nutrients, sea-level rise, predation, and received and gathered supplemental waters that are deeper and cooler than collection and trade. The available species- or genus-specific information, those in which the species occurs. On information does not support more described above, that expands our the other hand, its depth range may precise ratings of the susceptibilities of knowledge regarding the species exacerbate vulnerability to extinction A. rudis to the threats. abundance, distribution, and threat over the foreseeable future if the species

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occurs predominantly in the shallower that contribute to extinction risk for this currently pose a high risk to the survival portion of its depth range, since those species are inadequate (D); of the species; and areas will have higher irradiance and (2) Acropora rudis’ geographic (2) Acropora rudis’ abundance is thus will be more severely affected by distribution is restricted to the Maldives locally common in portions of its range, warming-induced bleaching. Its absolute and northeastern Indian Ocean. While it has at least millions of colonies, and abundance of at least millions of coral reefs in this area are projected to there is no evidence of depensatory colonies, combined with spatial experience climate change effects later processes such as reproductive failure variability in ocean warming and than the average predictions of severe from low density of reproductive acidification across the species range, conditions, it is nevertheless projected individuals and genetic processes such moderates vulnerability to extinction to experience severe impacts from as inbreeding affecting this species. because the increasingly severe combined climate change and localized Thus, its abundance indicates it is conditions expected in the foreseeable human impacts for coral reefs within currently able to avoid high mortality future will be non-uniform and the foreseeable future. In addition, its from environmental stochasticity, and therefore will likely be a large number range is constrained to a particular mortality of a high proportion of its of colonies that are either not exposed geographic area such that a high population from catastrophic events; or do not negatively respond to a threat proportion of the population of this The combination of these at any given point in time. However, its species is likely to be exposed to threats characteristics indicates that the species qualitative abundance is described as that occur throughout this range over does not exhibit the characteristics of rare, which combined with its restricted the foreseeable future; and one that is currently in danger of depth distribution indicates it is likely (3) While A. rudis’ abundance can be extinction, as described previously in that a high proportion of individuals locally common, overall it is considered the Risk Analyses section, and thus does will be affected by threats that are uncommon or rare, which means it does not warrant listing as endangered at this typically more severe in shallow not possess as much buffering capacity time. habitats at any given point in time. in the form of variability in response Range-wide, a multitude of between individuals or absolute Listing Determination conservation efforts are already broadly abundance that would be afforded to a employed that are likely benefiting A. In the proposed rule using the more abundant or common species. rudis. However, considering the global determination tool formula approach, A. Considering the limited range of this scale of the most important threats to rudis was proposed for listing as species, this level of abundance leaves the species, and the ineffectiveness of endangered because of: High the species vulnerable to becoming of conservation efforts at addressing the vulnerability to ocean warming (ESA such low abundance within the root cause of global threats (i.e., GHG Factor E); moderate vulnerability to foreseeable future that it may be at risk emissions), we do not believe that any disease (C) and acidification (E); from depensatory processes, current conservation efforts or uncommon generalized range wide environmental stochasticity, or conservation efforts planned in the abundance (E); narrow overall catastrophic events, as explained in future will result in affecting the species distribution (based on narrow more detail in the Corals and Coral status to the point at which listing is not geographic distribution and shallow Reefs and Risk Analyses sections. warranted. depth distribution (E); and inadequacy The combination of these of existing regulatory mechanisms (D). characteristics and future projections of Acropora speciosa In this final rule, we changed the threats indicates that the species is Introduction listing determination for A. rudis from likely to be in danger of extinction endangered to threatened. We made this within the foreseeable future throughout The SRR and SIR provided the determination based on a more species- its range and warrants listing as following information on A. speciosa’s specific and holistic assessment of threatened at this time due to factors A, morphology and taxonomy. Morphology whether this species meets the C, D, and E. was described as thick cushions or definition of either a threatened or The available information above on A. bottlebrush branches and taxonomy was endangered coral largely in response to rudis’ spatial structure, demography, described as having no taxonomic issues public comments, including more threat susceptibilities, and management but being similar in appearance to A. appropriate consideration of the also indicate that the species is not echinata and A. granulosa. buffering capacity of this species’ spatial currently in danger of extinction and The public comments did not provide and demographic traits to lessen its thus does not warrant listing as supplemental information on vulnerability to threats. Thus, based on Endangered because: morphology or taxonomy. We gathered the best available information provided (1) While A. rudis’ distribution is supplemental information, including by above on A. rudis’s spatial structure, restricted to the Maldives and Wallace (1999b), indicating species demography, threat susceptibilities, and northeastern Indian Ocean, its habitat is identification uncertainty for A. management indicate that it is likely to upper reef slopes of fringing reefs. This speciosa. However, Veron (2014) states become endangered throughout its range moderates vulnerability to extinction that A. speciosa is distinctive so we within the foreseeable future, and thus currently because the species occurs in conclude it can be identified by experts warrants listing as threatened at this common and variable habitats that are and that the distribution and abundance time, because: predicted, on local and regional scales, information described below for this (1) Acropora rudis is highly to experience highly variable thermal species is sufficiently reliable (Fenner, susceptible to ocean warming (ESA regimes and ocean chemistry at any 2014b). Factor E), and susceptible to disease (C), given point in time, as described in ocean acidification (E), trophic effects of more detail in the Coral Habitat and Spatial Information fishing (A), predation (C), and nutrients Threats Evaluation sections. There is no The SRR and SIR provided the (A, E). These threats are expected to evidence to suggest it is so spatially following information on A. speciosa’s continue and increase into the future. In fragmented that depensatory processes, distribution, habitat, and depth range. addition, existing regulatory environmental stochasticity, or the Acropora speciosa is distributed from mechanisms to address global threats potential for catastrophic events Indonesia to French Polynesia. The

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species has the 51st smallest range of population) as 1,204 colonies. The specific information on the effects of 114 Acropora species. It occurs on calculation of the total world population these threats on A. speciosa. We lower reef slopes and walls, especially of this species was flawed, since the interpreted the threat susceptibility and those characterized by clear water and area of 1 km2 was given as 1,000 m2, exposure information from the SRR and high Acropora diversity on steep slopes. when it is actually 1,000,000 m2. Thus, SIR in the proposed rule for A. Its depth range is 12 to 40 meters, and the correct population estimate is 1,000 speciosa’s vulnerabilities as follows: it has been found in mesophotic times greater than stated, or a total High vulnerability to ocean warming, habitats. population size of 10,942,000 colonies, moderate vulnerabilities to disease, The public comments did not provide and an effective population size of ocean acidification, trophic effects of supplemental information on A. 1,204,000 colonies. fishing, nutrients, and predation, and speciosa’s distribution. We gathered Carpenter et al. (2008) extrapolated low vulnerabilities to sedimentation, supplemental information, including species abundance trend estimates from sea-level rise, and collection and trade. Veron (2014), which reports that A. total live coral cover trends and habitat Public comments did not provide speciosa is confirmed in 26 of his 133 types. For A. speciosa, the overall supplemental information on A. Indo-Pacific ecoregions, and strongly decline in abundance (‘‘Percent speciosa’s threat susceptibilities. We predicted to be found in an additional Population Reduction’’) was estimated gathered the following species-specific 12. Wallace (1999b) reports its at 35 percent, and the decline in and genus-level supplemental occurrence in 10 of her 29 Indo-Pacific abundance before the 1998 bleaching information on this species’ threat areas, many of which are larger than event (‘‘Back-cast Percent Population susceptibilities. Acropora speciosa has Veron’s ecoregions. Richards (2009) Reduction’’) was estimated at 14 been rated as moderately or highly estimated its range at 20 million km2. percent. However, as summarized above susceptible to bleaching and coral The species was tentatively identified in in the Inter-basin Comparison sub- disease, but these ratings are not based mesophotic assemblages in American section, live coral cover trends are on species-specific data (Carpenter et Samoa: ‘‘Shallow, plate-like reefs (more highly variable both spatially and al., 2008). No other species-specific than 50 m) were comprised mostly of temporally, producing patterns on small information is available for the Acropora spp., possibly A. clathrata, A. scales that can be easily taken out of susceptibility of A. speciosa to any other speciosa, and A. crateriformis’’ (Bare et context, thus quantitative inferences to threat. Based on information from other al., 2010). The public comments and species-specific trends should be Acropora species provided in the genus information we gathered provided interpreted with caution. At the same description above, A. speciosa likely is nothing additional on A. speciosa’s time, an extensive body of literature highly susceptible to ocean warming, habitat and depth range. documents broad declines in live coral and also likely has some susceptibility cover and shifts to reef communities to disease, ocean acidification, trophic Demographic Information dominated by hardier coral species or effects of fishing, sedimentation, The SRR and SIR provided the algae over the past 50 to 100 years nutrients, sea-level rise, predation, and following information on A. speciosa’s (Birkeland, 2004; Fenner, 2012; Pandolfi collection and trade. The available abundance. Acropora speciosa has been et al., 2003; Sale and Szmant, 2012). information does not support more reported as uncommon. These changes have likely occurred, and precise ratings of the susceptibilities of The public comments did not provide are occurring, from a combination of A. speciosa to the threats. supplemental information on A. global and local threats. Given that A. Regulatory Mechanisms speciosa’s abundance. We gathered speciosa occurs in many areas affected supplemental information, including by these broad changes, and likely has In the proposed rule, we did not Richards et al. (2013b), which some susceptibility to both global and provide any species-specific concludes that this species is globally local threats, we conclude that it is information on the regulatory widespread, locally restricted, and likely to have declined in abundance mechanisms or conservation efforts for locally rare, and thus in the second over the past 50 to 100 years, but a A. speciosa. Criticisms of our approach rarest category of Acropora with the precise quantification is not possible received during public comment led us predicted consequence of local based on the limited species-specific to the following analysis to attempt to extinction. Veron (2014) reports that A. information. analyze regulatory mechanisms on a speciosa occupied 8.3 percent of 2,984 species basis. Records confirm that A. dive sites sampled in 30 ecoregions of Other Biological Information speciosa occurs in 26 Indo-Pacific the Indo-Pacific, and had a mean The SRR and SIR provided the ecoregions that encompass 18 countries’ abundance rating of 1.60 on a 1 to 5 following information on A. speciosa’s EEZs. The 18 countries are Australia, rating scale at those sites in which it life history. Based on information from Brunei, China, Federated States of was found. Based on this semi- other Acropora species, A. speciosa is Micronesia, Fiji, France (French Pacific quantitative system, the species’ most likely a hermaphroditic spawner Island Territories), Indonesia, Malaysia, abundance was characterized as with lecithotrophic (yolk-sac) larvae. Maldives, Marshall Islands, Palau, ‘‘common.’’ Overall abundance was The public comments and information Papua New Guinea, Philippines, described as ‘‘usually uncommon.’’ we gathered did not provide anything Solomon Islands, Taiwan, Timor-Leste, Veron did not infer trends in abundance additional to the above-described United States (PRIAs), and Vietnam. from these data. biological information. The regulatory mechanisms relevant to Richards et al. (2008) reported that A. A. speciosa, described first as the speciosa had the ninth smallest Susceptibility to Threats percentage of the above countries that population of the 15 rare Acropora To describe A. speciosa’s threat utilize them to any degree and second, species they studied. Richards et al. susceptibilities, the SRR and SIR as the percentages of those countries (2008: Appendix 1) gave the total world provided genus-level information for the whose regulatory mechanisms may be population of this species as 10,942 ± effects on Acropora of ocean warming, limited in scope, are as follows: General 5,471 colonies, and the effective acidification, disease, predation, coral protection (39 percent with none population size (i.e., a mathematical sedimentation, and nutrients. The SRR limited in scope), coral collection (67 estimate of the size of the breeding and SIR did not provide any species- percent with 28 percent limited in

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scope), pollution control (50 percent because some areas within its range are fishing (A), predation (C), and nutrient with 17 percent limited in scope), projected to have less than average enrichment (A, E). These threats are fishing regulations on reefs (94 percent warming and acidification over the expected to continue and increase into with 17 percent limited in scope), and foreseeable future, including the central the future. In addition, existing managing areas for protection and Pacific, so portions of the population in regulatory mechanisms to address global conservation (100 percent with six these areas will be less exposed to threats that contribute to extinction risk percent limited in scope). The most severe conditions. Its depth range of 12 for this species are inadequate (D); common regulatory mechanisms in to 40 moderates vulnerability to (2) Although A. speciosa’s habitat place for A. speciosa are reef fishing extinction over the foreseeable future includes mesophotic depths which may regulations and area management for because deeper areas of its range will provide some buffering capacity against protection and conservation. Coral usually have lower irradiance than threats that are more severe in shallower collection and pollution control laws surface waters. However, while reef environments such as warming, its are also common for the species, but 28 acidification is generally predicted to habitat is quite specialized, which may percent of coral collection laws are accelerate more quickly in waters that limit buffering capacity if threats are limited in scope and may not provide are deeper and cooler than those in more pronounced within the type of substantial protection. General coral which the species occurs, the lower habitat where the species occurs within; protection laws are less common portion of its depth range may be and regulatory mechanisms for the affected by acidification over the (3) Acropora speciosa’s effective management of A. speciosa. foreseeable future. Its habitat is lower population size of 1.2 million reef slopes and walls, especially those Vulnerability to Extinction genetically distinct colonies could characterized by clear water and high increase vulnerability to extinction if a As explained above in the Risk Acropora diversity on steep slopes. This high proportion of the effective Analyses section, a species’ specialized habitat may exacerbate population occurs within the parts of its vulnerability to extinction results from vulnerability to extinction over the range most affected by threats, the combination of its spatial and foreseeable future because the species is potentially causing the species to demographic characteristics, threat somewhat limited in its habitat, decline to such low abundance within susceptibilities, and consideration of the reducing the buffering capacity of the foreseeable future that it may be at baseline environment and future habitat heterogeneity. While the risk from depensatory processes, projections of threats. The SRR stated geographic distribution, depth environmental stochasticity, or that factors that increase the potential distribution, and habitat of A. speciosa catastrophic events. extinction risk for A. speciosa include all may moderate extinction risk over The combination of these the relatively high susceptibility of the the foreseeable future, its effective genus Acropora to common threats. It characteristics and projections of future population size of 1.2 million colonies threats indicates that the species is listed factors that reduce the threat of substantially exacerbate extinction risk extinction for this species including likely to be in danger of extinction over the foreseeable future, because within the foreseeable future throughout high local abundance and broad depth increasingly severe conditions are likely range. its range and warrants listing as to affect a high proportion of its threatened at this time due to factors A, Subsequent to the proposed rule, we effective population at any given point C, D, and E. received and gathered supplemental in time. species- or genus-specific information, The available information above on A. described above, that expands our Listing Determination speciosa’s spatial structure, knowledge regarding the species In the proposed rule, using the demography, threat susceptibilities, and abundance, distribution, and threat determination tool formula approach, A. management also indicate that the susceptibilities. We developed our speciosa was proposed for listing as species is not currently in danger of assessment of the species’ vulnerability threatened because of: High extinction and thus does not warrant to extinction using all the available vulnerability to ocean warming (ESA listing as Endangered because: information. As explained in the Risk Factor E); moderate vulnerability to (1) Acropora speciosa lives at depths Analyses section, our assessment in this disease (C) and acidification (E); of at least 40 m, providing some final rule emphasizes the ability of the uncommon generalized range wide buffering capacity against threat- species’ spatial and demographic traits abundance (E); moderate overall induced mortality events that may be to moderate or exacerbate its distribution (based on moderate more severe in shallow habitats; and vulnerability to extinction, as opposed geographic distribution and moderate (2) Acropora speciosa’s total to the approach we used in the depth distribution (E); and inadequacy population size is estimated at 10.9 proposed rule, which emphasized the of existing regulatory mechanisms (D). million colonies, approximately ten species’ susceptibility to threats. In this final rule, we maintain the times the size of its effective population, The following characteristics of A. species’ proposed listing determination providing a buffer against the species speciosa, in conjunction with the as threatened. Based on the best declining to such low abundance that information described in the Corals and available information provided above on depensatory processes, environmental Coral Reefs section, Coral Habitat sub- A. speciosa’s spatial structure, stochasticity, or the potential for section, and Threats Evaluation section demography, threat susceptibilities, and catastrophic events currently pose a above, affect its vulnerability to management indicate that it is likely to high risk to the survival of the species. extinction currently and over the become endangered throughout its range The combination of these foreseeable future. Its geographic within the foreseeable future, and thus characteristics indicates that the species distribution includes most of the warrants listing as threatened at this does not exhibit the characteristics of ecoregions in the Coral Triangle, the time, because: one that is currently in danger of western Pacific, and the GBR, as well as (1) Acropora speciosa is highly extinction, as described previously in parts of the Indian Ocean and central susceptible to ocean warming (ESA the Risk Analyses section, and thus does Pacific. Its geographic distribution Factor E), and susceptible to disease (C), not warrant listing as endangered at this moderates vulnerability to extinction ocean acidification (E), trophic effects of time.

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Range-wide, a multitude of Indo-Pacific ecoregions, and strongly et al., 2003; Sale and Szmant, 2012). conservation efforts are already broadly predicted to be found in an additional These changes have likely occurred, and employed that are likely benefiting A. 17. Wallace (1999b) reports its are occurring, from a combination of speciosa. However, considering the occurrence in 16 of her 29 Indo-Pacific global and local threats. Given that A. global scale of the most important areas, many of which are larger than striata occurs in many areas affected by threats to the species, and the Veron’s ecoregions. Richards (2009) these broad changes, and that it has ineffectiveness of conservation efforts at estimated its range at 50 million km2. some susceptibility to both global and addressing the root cause of global The public comments and information local threats, we conclude that it is threats (i.e., GHG emissions), we do not we gathered provided nothing likely to have declined in abundance believe that any current conservation additional on A. striata’s habitat and over the past 50 to 100 years but a efforts or conservation efforts planned depth range. precise quantification is not possible due to the limited amount of species- in the future will result in affecting the Demographic Information species status to the point at which specific information. listing is not warranted. The SRR and SIR provided the following information on A. striata’s Other Biological Information Acropora striata abundance. Acropora striata has rare The SRR and SIR provided the Introduction overall abundance but may be locally following information on A. striata’s life dominant in some areas in Japan. history. Acropora striata is a The SRR and SIR provided the The public comments did not provide hermaphroditic spawner, with larval following information on A. striata’s any new or supplemental information development and settlement taking five morphology and taxonomy. Morphology on A. striata’s abundance. We gathered to 10 days, and larvae remaining was described as dense thickets with supplemental information, including competent for 31 days. The public short cylindrical branches, and Richards et al. (2013b), which comments and information we gathered taxonomy was described as having no concludes that this species is globally did not provide anything additional to taxonomic issues but being similar in widespread, locally widespread, and the above-described biological appearance to A. tumida, A. sekesiensis, locally rare. Veron (2014) reports that A. information. and A. parahemprichii. striata occupied 3.2 percent of 2,984 The public comments and dive sites sampled in 30 ecoregions of Susceptibility to Threats information we gathered provided the Indo-Pacific, and had a mean To describe A. striata’s threat supplemental information on abundance rating of 1.38 on a 1 to 5 susceptibilities, the SRR and SIR morphology or taxonomy. One public rating scale at those sites in which it provided genus-level information for the comment stated that specimens reported was found. Based on this semi- effects on Acropora of ocean warming, as A. striata in Guam differ in colony quantitative system, the species’ acidification, disease, predation, form and in other characteristics from abundance was characterized as sedimentation, nutrients, and collection the species described as A. striata in ‘‘uncommon.’’ Overall abundance was and trade. The SRR and SIR did not Veron (2000). We gathered described as ‘‘may be locally dominant provide any species-specific supplemental information, including in Japan, uncommon elsewhere.’’ Veron information on the effects of these Wallace (1999b), which provide did not infer trends in abundance from threats on A. striata. We interpreted the contradictory information to Veron these data. As described in the Indo- threat susceptibility and exposure (2000) regarding the morphology of this Pacific Species Determinations information from the SRR and SIR in the species. Veron (2014) states that A. introduction above, based on results proposed rule for A. striata’s striata is easily confused with other from Richards et al. (2008) and Veron vulnerabilities as follows: High Acropora with a bushy growth form. (2014), the absolute abundance of this vulnerability to ocean warming, Although there is uncertainty, we species is likely at least tens of millions moderate vulnerabilities to disease, conclude that A. striata can be of colonies. ocean acidification, trophic effects of identified by experts, and that the Carpenter et al. (2008) extrapolated fishing, nutrients, and predation, and distribution and abundance information species abundance trend estimates from low vulnerabilities to sedimentation, described below for this species is total live coral cover trends and habitat sea-level rise, and collection and trade. sufficiently reliable (Fenner, 2014b). types. For A. striata, the overall decline Public comments did not provide any in abundance (‘‘Percent Population new or supplemental information on A. Spatial Information Reduction’’) was estimated at 36 striata’s threat susceptibilities. We The SRR and SIR provided the percent, and the decline in abundance gathered the following species-specific following information on A. striata’s before the 1998 bleaching event (‘‘Back- and genus-level supplemental distribution, habitat, and depth range. cast Percent Population Reduction’’) information on this species’ threat Acropora striata is distributed from was estimated at 14 percent. However, susceptibilities. Acropora striata has Indonesia to French Polynesia, and as summarized above in the Inter-basin been rated as moderately or highly possibly to Japan. The species has the Comparison sub-section, live coral cover susceptible to bleaching and disease, 54th largest range of 114 Acropora trends are highly variable both spatially but these ratings are not based on species. Its predominant habitat is and temporally, producing patterns on species-specific data (Carpenter et al., upper reef slopes, and it occurs in other small scales that can be easily taken out 2008). There is no species-specific shallow habitats such as mid-slopes and of context, thus quantitative inferences information for the susceptibility of A. lagoons, and its depth range is at 10 to to species-specific trends should be striata to any threat. Based on 25 m. interpreted with caution. At the same information from other Acropora The public comments did not provide time, an extensive body of literature species provided in the genus any new or supplemental information documents broad declines in live coral description above, A. striata is likely on A. striata’s distribution. We gathered cover and shifts to reef communities highly susceptible to ocean warming, supplemental information, including dominated by hardier coral species or and also likely has some susceptibility Veron (2014), which reports that A. algae over the past 50 to 100 years to disease, ocean acidification, trophic striata is confirmed in 36 of his 133 (Birkeland, 2004; Fenner, 2012; Pandolfi effects of fishing, sedimentation,

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nutrients, sea-level rise, predation, and demographic characteristics, threat ocean chemistry at any given point in collection and trade. The available susceptibilities, and consideration of the time. Its absolute abundance of at least information does not support more baseline environment and future tens of millions of colonies, combined precise ratings of the susceptibilities of projections of threats. The SRR stated with spatial variability in ocean A. striata to the threats. that factors that increase the potential warming and acidification across the species range, moderates vulnerability Regulatory Mechanisms extinction risk for A. striata include its locally rare abundance. Factors that to extinction because the increasingly In the proposed rule, we did not reduce the potential extinction risk A. severe conditions expected in the provide any species-specific striata include its relatively broad global foreseeable future will be non-uniform information on the regulatory distribution. Subsequent to the and therefore will likely be a large mechanisms or conservation efforts for proposed rule, we received and gathered number of colonies that are either not A. striata. Criticisms of our approach supplemental species- or genus-specific exposed or do not negatively respond to received during public comment led us information, described above, that a threat at any given point in time. to the following analysis to attempt to expands our knowledge regarding the Listing Determination analyze regulatory mechanisms on a species abundance, distribution, and species basis. Records confirm that A. threat susceptibilities. We developed In the proposed rule using the striata occurs in 36 Indo-Pacific our assessment of the species’ determination tool formula approach, A. ecoregions that encompass 38 countries’ vulnerability to extinction using all the striata was proposed for listing as EEZs. The 38 countries are Australia, available information. As explained in threatened because of: High China, Comoros Islands, Egypt, the Risk Analyses section, our vulnerability to ocean warming (ESA Federated States of Micronesia, Fiji, assessment in this final rule emphasizes Factor E); moderate vulnerability to France (French Pacific Island the ability of the species’ spatial and disease (C) and acidification (E); Territories), Indonesia, Israel, Japan, demographic traits to moderate or uncommon generalized range wide Jordan, Kenya, Kiribati, Madagascar, exacerbate its vulnerability to abundance (E); moderate overall Malaysia, Maldives, Marshall Islands, extinction, as opposed to the approach distribution (based on moderate Mauritius, Myanmar, Nauru, New we used in the proposed rule, which geographic distribution and moderate Zealand (Cook Islands, Tokelau), Niue, emphasized the species’ susceptibility depth distribution (E); and inadequacy Palau, Papua New Guinea, Philippines, to threats. of existing regulatory mechanisms (D). Samoa, Saudi Arabia, Seychelles, In this final rule, we changed the Solomon Islands, Sudan, Taiwan, The following characteristics of A. Tanzania, Thailand, Timor-Leste, striata, in conjunction with the listing determination for A. striata from Tonga, Tuvalu, United States (CNMI, information described in the Corals and threatened to not warranted. We made Guam, American Samoa, PRIAs), and Coral Reefs section, Coral Habitat sub- this determination based on a more Vietnam. The regulatory mechanisms section, and Threats Evaluation section species-specific and holistic assessment relevant to A. striata, described first as above, affect its vulnerability to of whether this species meets the the percentage of the above countries extinction currently and over the definition of either a threatened or that utilize them to any degree and foreseeable future. Its geographic endangered coral largely in response to second, as the percentages of those distribution includes most of the coral public comments, including more countries whose regulatory mechanisms reef ecoregions in the Indian Ocean and appropriate consideration of the may be limited in scope, are as follows: western and central Pacific Ocean. Its buffering capacity of this species’ spatial General coral protection (26 percent geographic distribution moderates and demographic traits to lessen its with 3 percent limited in scope), coral vulnerability to extinction because some vulnerability to threats. Thus, based on collection (58 percent with 26 percent areas within its range are projected to the best available information above on limited in scope), pollution control (45 have less than average warming and A. striata’s spatial structure, percent with eight percent limited in acidification over the foreseeable future, demography, threat susceptibilities, and scope), fishing regulations on reefs (89 including the western Indian Ocean, the management, none of the five ESA percent with 21 percent limited in central Pacific, and other areas, so listing factors, alone or in combination, scope), and managing areas for portions of the population in these areas are causing this species to be likely to protection and conservation (95 percent will be less exposed to severe become endangered throughout its range with eight percent limited in scope). conditions. Its depth range is from ten within the foreseeable future, and thus The most common regulatory to 25 meters. This moderates it is not warranted for listing at this mechanisms in place for A. striata are vulnerability to extinction over the time, because: reef fishing regulations and area foreseeable future because deeper areas (1) Acropora striata’s distribution management for protection and of its range will usually have lower across most of the Pacific Ocean is conservation. Coral collection and temperatures than surface waters due to spread over a very large area. While pollution control laws are also local and micro-habitat variability in some areas within its range are somewhat common for the species, but environmental conditions, and projected to be affected by warming and 26 percent of coral collection laws are acidification is generally predicted to acidification, other areas are projected limited in scope and may not provide accelerate most in waters that are deeper to have less than average warming and substantial protection. General coral and cooler than those in which the acidification, including the western protection laws are much less species occurs. Its habitat includes Indian Ocean, the central Pacific, and prominent regulatory mechanisms for upper reef slopes, mid-slopes and other areas. This distribution and the the management of A. striata. lagoons. This moderates vulnerability to heterogeneous habitats it occupies extinction over the foreseeable future reduce exposure to any given threat Vulnerability to Extinction because the species is not limited to one event or adverse condition that does not As explained above in the Risk habitat type but occurs in numerous occur uniformly throughout the species Analyses section, a species’ types of reef environments that will, on range. As explained above in the vulnerability to extinction results from local and regional scales, experience Threats Evaluation section, we have not the combination of its spatial and highly variable thermal regimes and identified any threat that is expected to

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occur uniformly throughout the species However, the species is recognized as Richards et al. (2008) reported that A. range within the foreseeable future); valid and distinct by experts (Veron, tenella had the seventh lowest (2) Acropora striata’s total absolute 2000; Wallace, 1999a), so we conclude population of the 15 rare Acropora abundance is at least tens of millions of it can be identified by experts and that species they studied. Richards et al. colonies, providing buffering capacity in the distribution and abundance (2008) gave the total world population the form of absolute numbers of information described below for this of this species as about 5207 +/-1606 colonies and variation in susceptibility species is sufficiently reliable (Fenner, colonies, and the effective population between individual colonies. As 2014b). size (i.e., a mathematical estimate of the discussed in the Corals and Coral Reefs size of the breeding population) as about Spatial Information section above, the more colonies a 573 colonies (Richards et al., 2008). The species has, the lower the proportion of The SRR and SIR provided the calculation of the total world population colonies that are likely to be exposed to following information on A. tenella’s of this species was flawed, since the a particular threat at a particular time, distribution, habitat, and depth range. area of 1 km2 was given as 1,000 m2 and all individuals that are exposed will Acropora tenella is distributed from (Richards et al., 2008: Appendix 1), not have the same response; and Japan to Indonesia to New Guinea and when it is actually 1,000,000 m2. Thus, (3) It is a broadcast spawner and fast the Marshall Islands. The species has the correct population estimate is 1,000 grower, enhancing recovery potential the 43rd smallest range of 114 Acropora times greater than stated, or a total from mortality events as described in species. Its habitat is lower reef slopes population size of 5,207,000 colonies, the Corals and Coral Reefs section and shelves between 40 and 70 meters, and an effective population size of above. and it apparently is specialized for 573,000 colonies. Notwithstanding the projections calm, deep conditions. Carpenter et al. (2008) extrapolated through 2100 that indicate increased The public comments did not provide species abundance trend estimates from severity over time of the three high supplemental information on A. total live coral cover trends and habitat importance threats, the combination of tenella’s distribution. We gathered types. For A. tenella, the overall decline these biological and environmental supplemental information, including in abundance (‘‘Percent Population characteristics indicates that the species Veron (2014), which reports that A. Reduction’’) was estimated at 39 possesses sufficient buffering capacity tenella is confirmed in 18 of his 133 percent, and the decline in abundance to avoid being in danger of extinction Indo-Pacific ecoregions, and strongly before the 1998 bleaching event (‘‘Back- within the foreseeable future throughout predicted to be found in an additional cast Percent Population Reduction’’) was estimated at 15 percent. However, its range. It is possible that this species’ six. Wallace (1999b) reports its as summarized above in the Inter-basin extinction risk may increase in the occurrence in six of her 29 Indo-Pacific Comparison sub-section, live coral cover future if global threats continue and areas, many of which are larger than trends are highly variable both spatially increase in severity and the species Veron’s ecoregions. Richards (2009) and temporally, producing patterns on exposure to threats increases throughout estimated its range at 15 million km2, small scales that can be easily taken out its range. Should the species experience which was the 43rd smallest range of of context, thus quantitative inferences reduced abundance or range 114 Acropora species examined. to species-specific trends should be constriction of a certain magnitude, the Acropora tenella was one of three interpreted with caution. At the same ability of these characteristics to species that dominated mesophotic reef moderate exposure to threats will time, an extensive body of literature habitat in Okinawa between 35 and 47 documents broad declines in live coral diminish. However, the species is not m depth (Sinniger et al., 2013). likely to become of such low abundance cover and shifts to reef communities or so spatially fragmented as to be in Demographic Information dominated by hardier coral species or algae over the past 50 to 100 years danger of extinction due to depensatory The SRR and SIR provided the processes, the potential effects of (Birkeland, 2004; Fenner, 2012; Pandolfi following information on A. tenella’s et al., 2003; Sale and Szmant, 2012). environmental stochasticity, or the abundance. Acropora tenella has been potential for mortality from catastrophic These changes have likely occurred, and reported as locally common in some are occurring, from a combination of events within the foreseeable future locations. throughout its range. Therefore, A. global and local threats. Given that A. The public comments did not provide tenella occurs in many areas affected by striata is not warranted for listing at this supplemental information on A. time under any of the listing factors. these broad changes, and that it has tenella’s abundance. We gathered some susceptibility to both global and Acropora tenella supplemental information, including local threats, we conclude that it is Richards (2013b), which concludes that likely to have declined in abundance Introduction this species is globally widespread, over the past 50 to 100 years, but a The SRR and SIR provided the locally restricted, and locally rare, and precise quantification is not possible following information on A. tenella’s thus in the second rarest category of based on the limited species-specific morphology and taxonomy. Morphology Acropora with the predicted information. was described as horizontal, platy consequence of local extinction. Veron colonies with flattened branches, and (2014) reports that A. tenella occupied Other Biological Information taxonomy was described as having no 0.4 percent of 2,984 dive sites sampled The SRR and SIR provided the taxonomic issues but being similar in in 30 ecoregions of the Indo-Pacific, and following information on A. tenella’s appearance to Acropora pichoni. had a mean abundance rating of 1.25 on life history. Based on information from The public comments did not provide a 1 to 5 rating scale at those sites in other Acropora species, A. tenella is supplemental information on which it was found. Based on this semi- most likely a hermaphroditic spawner morphology or taxonomy. We gathered quantitative system, the species’ with lecithotrophic (yolk-sac) larvae. supplemental information, including abundance was characterized as ‘‘rare,’’ The public comments and information Veron (2014), which states that A. and its overall abundance was also we gathered did not provide anything tenella is readily confused with other described as ‘‘rare.’’ Veron did not infer additional to the above-described flattened, finely branched Acropora. trends in abundance from these data. biological information.

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Susceptibility to Threats that utilize them to any degree and equatorial Pacific Ocean. Despite the To describe A. tenella’s threat second, as the percentages of those large number of islands and susceptibilities, the SRR and SIR countries whose regulatory mechanisms environments that are included in the provided genus-level information for the may be limited in scope, are as follows: species’ range, this range exacerbates effects on Acropora of ocean warming, General coral protection (25 percent vulnerability to extinction over the acidification, disease, predation, with none limited in scope), coral foreseeable future because it is mostly sedimentation, nutrients, and collection collection (58 percent with 33 percent limited to an area projected to have the and trade. The SRR and SIR did not limited in scope), pollution control (33 most rapid and severe impacts from provide any species-specific percent with 17 percent limited in climate change and localized human scope), fishing regulations on reefs (92 impacts for coral reefs over the 21st information on the effects of these percent with 17 percent limited in century. Its mesophotic depth range of threats on A. tenella. We interpreted the scope), and managing areas for 40 to 70 meters moderates vulnerability threat susceptibility and exposure protection and conservation (100 to extinction over the foreseeable future information from the SRR and SIR in the percent with eight percent limited in because of lower irradiance, sharply proposed rule for A. tenella’s scope). The most common regulatory reducing warming-induced bleaching. vulnerabilities as follows: High mechanisms in place for A. tenella are In addition, other threats usually occur vulnerability to ocean warming, reef fishing regulations and area at lower levels at such depths, such as moderate vulnerabilities to disease, management for protection and sedimentation resulting from land-based ocean acidification, trophic effects of conservation. Coral collection laws are sources of pollution. However, unlike fishing, nutrients, and predation, and also somewhat common for the species, the other Acropora species in this final low vulnerabilities to sedimentation, but 33 percent of coral collection laws rule, A. tenella’s mesophotic habitat sea-level rise, and collection and trade. are limited in scope and may not may often have substantially cooler Public comments did not provide provide substantial protection. General temperatures than the shallower photic supplemental information on A. coral protection and pollution control zone, and thus more likely to be affected tenella’s threat susceptibilities. We laws are much less prominent by increasing acidification over the gathered the following species-specific regulatory mechanisms for the foreseeable future. Its habitat consists of and genus-level supplemental management of A. tenella. lower reef slopes and shelves spanning information on this species’ threat 40 to 70 meters of depth, a much Vulnerability to Extinction susceptibilities. Acropora tenella has different habitat than the surface and been rated as moderately or highly As explained above in the Risk shallow reef habitats occupied by the susceptible to bleaching and disease, Analyses section, a species’ other Acropora species in this final rule. but these ratings are not based on vulnerability to extinction results from Its habitat may moderate vulnerability species-specific data (Carpenter et al., the combination of its spatial and to extinction over the foreseeable future 2008). No other species-specific demographic characteristics, threat because of variable conditions at any information is available for the susceptibilities, and consideration of the given point in time. However, its habitat susceptibility of A. tenella to any other baseline environment and future may exacerbate extinction risk over the threat. Based on information from other projections of threats. The SRR stated foreseeable future because increasing Acropora species provided in the genus that one factor that reduces the potential acidification is expected to vary less description above, A. tenella is likely extinction risk for this species is its spatially at these depths on coral reefs highly susceptible to ocean warming, deep depth range, which reduces than in shallower areas on coral reefs. and also likely has some susceptibilities exposure to surface-based threats. Its effective population size of to disease, ocean acidification, trophic Subsequent to the proposed rule, we approximately half a million colonies, effects of fishing, sedimentation, received and gathered supplemental combined with the location of its range, nutrients, sea-level rise, predation, and species- or genus-specific information, exacerbates vulnerability to extinction collection and trade. The available described above, that expands our because increasingly severe conditions information does not support more knowledge regarding the species within the limited species range are precise ratings of the susceptibilities of abundance, distribution, and threat likely to affect a high proportion of its A. tenella to the threats. susceptibilities. We developed our effective population at any given point assessment of the species’ vulnerability Regulatory Mechanisms in time. to extinction using all the available In the proposed rule, we did not information. As explained in the Risk Listing Determination provide any species-specific Analyses section, our assessment in this In the proposed rule, using the information on the regulatory final rule emphasizes the ability of the determination tool formula approach, A. mechanisms or conservation efforts for species’ spatial and demographic traits tenella was proposed for listing as A. tenella. Criticisms of our approach to moderate or exacerbate its threatened because of: High received during public comment led us vulnerability to extinction, as opposed vulnerability to ocean warming (ESA to the following analysis to attempt to to the approach we used in the Factor E); moderate vulnerability to analyze regulatory mechanisms on a proposed rule, which emphasized the disease (C) and acidification (E); species basis. Records confirm that A. species’ susceptibility to threats. uncommon generalized range wide tenella occurs in 18 Indo-Pacific The following characteristics of A. abundance (E); wide overall distribution ecoregions that encompass 12 countries’ tenella, in conjunction with the (based on moderate geographic EEZs. The 12 countries are Brunei, information described in the Corals and distribution and wide depth China, Federated States of Micronesia, Coral Reefs section, Coral Habitat sub- distribution, E); and inadequacy of Indonesia, Japan, Marshall Islands, section, and Threats Evaluation section existing regulatory mechanisms (D). Palau, Papua New Guinea, Philippines, above, affect its vulnerability to In this final rule, we maintain the Taiwan, United States (PRIAs), and extinction currently and over the species’ proposed listing determination Vietnam. The regulatory mechanisms foreseeable future. Its geographic as threatened. Based on the best relevant to A. tenella, described first as distribution is limited to the Coral available information provided above on the percentage of the above countries Triangle and parts of the western A. tenella’s spatial structure,

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demography, threat susceptibilities, and also indicate that the species is not The public comments did not provide management indicate that it is likely to currently in danger of extinction and supplemental information on become endangered throughout its range thus does not warrant listing as morphology or taxonomy. We gathered within the foreseeable future, and thus Endangered because: supplemental information, including warrants listing as threatened at this (1) While Acropora tenella’s range is Veron (2014), which indicates that A. time, because: constrained to mesophotic habitat in the vaughani is distinctive, thus we (1) Acropora tenella is highly Coral Triangle and western Pacific, its conclude it can be identified by experts, susceptible to ocean warming (ESA habitat heterogeneity moderates and that the distribution and abundance Factor E), and susceptible to disease (C), vulnerability to extinction currently information described below for this ocean acidification (E), trophic effects of because of variable conditions at any species is sufficiently reliable (Fenner, fishing (A), predation (C), and nutrient given point in time. There is no 2014b). enrichment (A, E). These threats are evidence to suggest that the species is Spatial Information expected to continue and increase into not so spatially fragmented or the future. Although its mesophotic geographically constrained that The SRR and SIR provided the depth distribution may provide some depensatory processes, environmental following information on A. vaughani’s buffering capacity against threats that stochasticity, or the potential for distribution, habitat, and depth range. are more severe in shallower reef catastrophic events currently pose a Acropora vaughani is distributed from environments, it may not provide high risk to the survival of the species; the Red Sea to Fiji. The species has the buffering capacity against other threats and 34th largest range of 114 Acropora for which depth is a less influential (2) Acropora tenella’s mesophotic species. It is found in numerous reef factor, like acidification and disease. In depth distribution provides some slope and back-reef habitats with turbid addition, existing regulatory buffering capacity against threats that water, including but not limited to, mechanisms to address global threats are more severe in shallower upper reef slopes, mid-slope terraces, that contribute to extinction risk for this environments such as nutrient lagoons, and adjacent habitats, and the species are inadequate (D); enrichment, sedimentation, and ocean depth range is from low tide to 20 or 30 (2) Acropora tenella’s distribution is warming; meters. constrained mostly within the Coral (3) Acropora tenella’s total population The public comments did not provide Triangle and western equatorial Pacific, size is estimated at five million supplemental information on A. which is projected to have the most colonies, approximately ten times the vaughani’s distribution. We gathered rapid and severe impacts from climate size of its effective population, supplemental information, including change and localized human impacts for providing a buffer against the species Veron (2014), who reports that A. coral reefs over the 21st century, as declining to such low abundance that vaughani is confirmed in 59 of his 133 described in the Threats Evaluation. depensatory processes, environmental Indo-Pacific ecoregions, and strongly predicted to be found in an additional Multiple ocean warming events have stochasticity, or the potential for 13. Wallace (1999b) reports its already occurred within the western catastrophic events currently pose a occurrence in 24 of her 29 Indo-Pacific equatorial Pacific that suggest future high risk to the survival of the species. ocean warming events may be more The combination of these areas, many of which are larger than severe than average in this part of the characteristics indicates that the species Veron’s ecoregions. Richards (2009) world. Although the mesophotic range calculated the geographic range of A. does not exhibit the characteristics of 2 of the species reduces the impacts of one that is currently in danger of vaughani at over 80 million km . The warming, disease, and localized human extinction, as described previously in public comments and information we impacts, the species occurs at the Risk Analyses section, and thus does gathered provided nothing additional on mesophotic depths where the effects of not warrant listing as endangered at this A. vaughani’s habitat and depth range. acidification are expected to be greater time. Range-wide, a multitude of Demographic Information over the foreseeable future than in conservation efforts are already broadly The SRR and SIR provided the shallower areas; and employed that are likely benefiting A. (3) Acropora tenella’s effective following information on A. vaughani’s tenella. However, considering the global population size of 0.5 million colonies abundance. Acropora vaughani is scale of the most important threats to could increase vulnerability to reported to be uncommon. The public the species, and the ineffectiveness of extinction if a high proportion of the comments did not provide conservation efforts at addressing the effective population occurs within the supplemental information on A. root cause of global threats (i.e., GHG parts of its range most affected by vaughani’s abundance. We gathered emissions), we do not believe that any threats, potentially causing the species supplemental information, including current conservation efforts or to decline to such low abundance Richards et al. (2013b), which conclude conservation efforts planned in the within the foreseeable future that it may from their data that this species is future will result in affecting the species be at risk from depensatory processes, globally widespread, locally restricted, status to the point at which listing is not environmental stochasticity, or and locally rare, and thus in the second warranted. catastrophic events. rarest category of Acropora with the The combination of these Acropora vaughani predicted consequence of local characteristics and projections of future extinction. Veron (2014) reports that A. threats indicates that the species is Introduction vaughani occupied 7.5 percent of 2,984 likely to be in danger of extinction The SRR and SIR provided the dive sites sampled in 30 ecoregions of within the foreseeable future throughout following information on A. vaughani’s the Indo-Pacific, and had a mean its range and warrants listing as morphology and taxonomy. Morphology abundance rating of 1.69 on a 1 to 5 threatened at this time due to factors A, was described as open-branched, bushy, rating scale at those sites in which it C, D, and E. arborescent colonies, and the taxonomy was found. Based on this semi- The available information above on A. was described as having no taxonomic quantitative system, the species’ tenella’s spatial structure, demography, issues but being similar to A. horrida, A. abundance was characterized as threat susceptibilities, and management tortuosa, A. rufus and A. austera. ‘‘common.’’ Overall abundance was

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described as ‘‘uncommon.’’ Veron did and trade. The SRR and SIR also susceptibilities of A. vaughani to the not infer trends in abundance from provided species-specific information threats. these data. As described in the Indo- reporting that Acropora species Regulatory Mechanisms Pacific Species Determinations including A. vaughani suffered greater introduction above, based on results than 90 percent mortality during the In the proposed rule, we did not from Richards et al. (2008) and Veron 1996 and 1998 bleaching events in the provide any species-specific (2014), the absolute abundance of this southeastern Arabian Gulf, but that information on the regulatory species is likely at least tens of millions portions of some A. vaughani survived, mechanisms or conservation efforts for of colonies. contributing to potentially accelerated A. vaughani. Criticisms of our approach received during public comment led us Carpenter et al. (2008) extrapolated recovery. The SRR and SIR did not to the following analysis to attempt to species abundance trend estimates from provide any other species-specific analyze regulatory mechanisms on a total live coral cover trends and habitat information on the effects of these species basis. Records confirm that A. types. For A. vaughani, the overall threats on A. vaughani. We interpreted decline in abundance (‘‘Percent vaughani occurs in 59 Indo-Pacific the threat susceptibility and exposure Population Reduction’’) was estimated ecoregions that encompass 43 countries’ information from the SRR and SIR in the at 35 percent, and the decline in EEZs. The 43 countries are Australia, proposed rule for A. vaughani’s abundance before the 1998 bleaching Cambodia, China, Comoros Islands, event (‘‘Back-cast Percent Population vulnerabilities as follows: High Djibouti, Egypt, Eritrea, Federated States Reduction’’) was estimated at 14 vulnerability to ocean warming, of Micronesia, Fiji, France (French percent. However, as summarized above moderate vulnerabilities to disease, Pacific Island Territories), India in the Inter-basin Comparison sub- ocean acidification, trophic effects of (Andaman and Nicobar Islands), section, live coral cover trends are fishing, nutrients, and predation, and Indonesia, Israel, Japan, Jordan, Kenya, highly variable both spatially and low vulnerabilities to sedimentation, Kiribati, Malaysia, Maldives, Marshall temporally, producing patterns on small sea-level rise, and collection and trade. Islands, Mauritius, Myanmar, New scales that can be easily taken out of Public comments provided some Zealand (Tokelau), Niue, Palau, Papua context, thus quantitative inferences to supplemental information on A. New Guinea, Philippines, Samoa, Saudi species-specific trends should be vaughani’s threat susceptibilities. One Arabia, Seychelles, Solomon Islands, Sri interpreted with caution. At the same comment stated that A. vaughani is Lanka, Sudan, Taiwan, Tanzania, time, an extensive body of literature more susceptible to predation than Thailand, Timor-Leste, Tonga, Tuvalu, documents broad declines in live coral indicated in the proposed rule because United Kingdom (British Indian Ocean cover and shifts to reef communities of the overlap in the depth ranges of this Territory), United States (CNMI, Guam, dominated by hardier coral species or species with crown of thorns starfish. American Samoa, PRIAs), Vietnam, and algae over the past 50 to 100 years We gathered the following species- Yemen. The regulatory mechanisms (Birkeland, 2004; Fenner, 2012; Pandolfi specific and genus-level supplemental relevant to A. vaughani, described first et al., 2003; Sale and Szmant, 2012). information on this species’ threat as the percentage of the above countries These changes have likely occurred, and susceptibilities. Acropora vaughani has that utilize them to any degree and are occurring, from a combination of been rated as moderately or highly second, as the percentages of those global and local threats. Given that A. susceptible to bleaching, but this rating countries whose regulatory mechanisms may be limited in scope, are as follows: vaughani occurs in many areas affected is not based on species-specific data General coral protection (28 percent by these broad changes, and that it has (Carpenter et al., 2008). All Acropora with five percent limited in scope), some susceptibility to both global and species in the southeastern Arabian coral collection (58 percent with 26 local threats, we conclude that it is Gulf, including A. vaughani, suffered likely to have declined in abundance percent limited in scope), pollution nearly complete mortality during the control (44 percent with seven percent over the past 50 to 100 years, but a 1996 bleaching event (Riegl, 1999), but precise quantification is not possible limited in scope), fishing regulations on some A. vaughani colonies survived the reefs (91 percent with 19 percent based on the limited species-specific 1998 mass bleaching event (Riegl and information. limited in scope), and managing areas Piller, 2001). No other species-specific for protection and conservation (95 Other Biological Information information is available for the percent with nine percent limited in The SRR and SIR provided the susceptibility of A. vaughani to any scope). The most common regulatory following information on A. vaughani’s other threat. For the other threats, based mechanisms in place for A. vaughani life history. Acropora vaughani is a on information from other Acropora are reef fishing regulations and area hermaphroditic spawner with species provided in the genus management for protection and lecithotrophic (yolk-sac) larvae. It is one description above, A. vaughani may be conservation. Coral collection and of several Acropora that achieve susceptible to the effects of coral pollution control laws are also reproductive isolation by spawning disease, ocean acidification, predation, somewhat common for the species, but earlier in the evening than other species. sedimentation, nutrient enrichment, 26 percent of coral collection laws are The public comments and information trophic effects of fishing, sea-level rise, limited in scope and may not provide we gathered did not provide anything and collection and trade. Thus, based on substantial protection. General coral additional to the above-described the available species-specific and genus protection laws are much less biological information. information summarized above, A. prominent regulatory mechanisms for vaughani is likely highly susceptible to the management of A. vaughani. Susceptibility to Threats ocean warming, and also likely has To describe A. vaughani’s threat some susceptibilities to disease, ocean Vulnerability to Extinction susceptibilities, the SRR and SIR acidification, trophic effects of fishing, As explained above in the Risk provided genus-level information for the sedimentation, nutrients, sea-level rise, Analyses section, a species’ effects on Acropora of ocean warming, predation, and collection and trade. The vulnerability to extinction results from acidification, disease, predation, available information does not support the combination of its spatial and sedimentation, nutrients, and collection more precise ratings of the demographic characteristics, threat

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susceptibilities, and consideration of the regional scales, experience highly identified any threat that is expected to baseline environment and future variable thermal regimes and ocean occur uniformly throughout the species projections of threats. The SRR stated chemistry at any given point in time. Its range within the foreseeable future; that factors that reduce the potential absolute abundance of at least tens of (2) Acropora vaughani’s total extinction risk for this species include millions of colonies, combined with abundance is at least tens of millions of the broad global distribution, the wide spatial variability in ocean warming and colonies, providing buffering capacity in range of habitats occupied by A. acidification across the species range, the form of absolute numbers of vaughani, its use in restoration and moderates vulnerability to extinction colonies and variation in susceptibility replantation, and its known recovery because the increasingly severe between individual colonies. As after bleaching events via tissue conditions expected in the foreseeable discussed in the Corals and Coral Reefs remnants from within the reef future will be non-uniform and section above, the more colonies a framework. therefore will likely be a large number species has, the lower the proportion of Subsequent to the proposed rule, we of colonies that are either not exposed colonies that are likely to be exposed to received and gathered supplemental or do not negatively respond to a threat a particular threat at a particular time, species- or genus-specific information, at any given point in time. and all individuals that are exposed will described above, that expands our Listing Determination not have the same response; and knowledge regarding the species (3) It is a broadcast spawner and fast abundance, distribution, and threat In the proposed rule, using the grower, enhancing recovery potential susceptibilities. We developed our determination tool formula approach, A. from mortality events as described in assessment of the species’ vulnerability vaughani was proposed for listing as the Corals and Coral Reefs section to extinction using all the available threatened because of: High above. information. As explained in the Risk vulnerability to ocean warming (ESA Notwithstanding the projections Analyses section, our assessment in this Factor E); moderate vulnerability to through 2100 that indicate increased final rule emphasizes the ability of the disease (C) and acidification (E); severity over time of the three high species’ spatial and demographic traits uncommon generalized range wide importance threats, the combination of to moderate or exacerbate its abundance (E); wide overall distribution these biological and environmental vulnerability to extinction, as opposed (based on wide geographic distribution characteristics indicates that the species to the approach we used in the and moderate depth distribution (E); possesses sufficient buffering capacity proposed rule, which emphasized the and inadequacy of existing regulatory to avoid being in danger of extinction species’ susceptibility to threats. mechanisms (D). within the foreseeable future throughout The following characteristics of A. In this final rule, we changed the its range. It is possible that this species’ vaughani, in conjunction with the listing determination for A. vaughani extinction risk may increase in the information described in the Corals and from threatened to not warranted. We future if global threats continue and Coral Reefs section, Coral Habitat sub- made this determination based on a worsen in severity and the species’ more species-specific and holistic section, and Threats Evaluation section exposure to the threats increases assessment of whether this species above, affect its vulnerability to throughout its range. Should the species meets the definition of either a extinction currently and over the experience reduced abundance or range threatened or endangered coral largely foreseeable future. Its geographic constriction of a certain magnitude, the in response to public comments, distribution includes about half of the ability of these characteristics to including more appropriate coral reef ecoregions in the Indian moderate exposure to threats will consideration of the buffering capacity Ocean and western and central Pacific diminish. However, the species is not of this species’ spatial and demographic Ocean. Its geographic distribution likely to become of such low abundance traits to lessen its vulnerability to moderates vulnerability to extinction or so spatially fragmented as to be in threats. Thus, based on the best because some areas within its range are danger of extinction due to depensatory projected to have less than average available information above on A. processes, the potential effects of warming and acidification over the vaughani’s spatial structure, environmental stochasticity, or the foreseeable future, including the demography, threat susceptibilities, and potential for mortality from catastrophic western Indian Ocean, the central management, none of the five ESA events within the foreseeable future Pacific, and other areas, so portions of listing factors, alone or in combination, throughout its range. Therefore, A. the population in these areas will be are causing this species to be likely to vaughani is not warranted for listing at less exposed to severe conditions. Its become endangered throughout its range this time under any of the listing factors. depth range is from low tide to 20 or 30 within the foreseeable future, and thus meters. This moderates vulnerability to it is not warranted for listing at this Acropora verweyi extinction over the foreseeable future time, because: because deeper areas of its range will (1) Acropora vaughani’s distribution Introduction usually have lower irradiance than is spread over a very large area. While The SRR and SIR provided the surface waters, and acidification is some areas within its range are following information on A. verweyi’s generally predicted to accelerate most in projected to be affected by warming and morphology and taxonomy. Morphology waters that are deeper and cooler than acidification, other areas are projected was described as clumps with those in which the species occurs. Its to have less than average warming and noticeably rounded or bulb-like habitat includes turbid upper reef acidification, including the western corallites, and taxonomy was described slopes, mid-slope terraces, lagoons, and Indian Ocean, the central Pacific, and as having no taxonomic issues. adjacent habitats, and the depth range is other areas. This distribution and the The public comments did not provide from low tide to 20 or 30 meters. This heterogeneous habitats it occupies any new or supplemental information moderates vulnerability to extinction reduce exposure to any given threat on morphology or taxonomy. We over the foreseeable future because the event or adverse condition that does not gathered supplemental information, species is not limited to one habitat type occur uniformly throughout the species including Veron (2014) which states but occurs in numerous types of reef range. As explained above in the that A. verweyi is distinctive, thus we environments that will, on local and Threats Evaluation section, we have not conclude it can be identified by experts

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and that the distribution and abundance Pacific Species Determinations proposed rule for A. verweyi’s information described below for this introduction above, based on results vulnerabilities as follows: High species is sufficiently reliable (Fenner, from Richards et al. (2008) and Veron vulnerability to ocean warming, 2014b). (2014), the absolute abundance of this moderate vulnerabilities to disease, species is likely at least tens of millions ocean acidification, trophic effects of Spatial Information of colonies. fishing, nutrients, and predation, and The SRR and SIR provided the Carpenter et al. (2008) extrapolated low vulnerabilities to sedimentation, following information on A. verweyi’s species abundance trend estimates from sea-level rise, and collection and trade. distribution, habitat, and depth range. total live coral cover trends and habitat Public comments did not provide any Acropora verweyi is distributed from the types. For A. verweyi, the overall new or supplemental information on A. western Indian Ocean to the central decline in abundance (‘‘Percent verweyi’s threat susceptibilities. We Pacific. The species has the 16th largest Population Reduction’’) was estimated gathered the following species-specific range of 114 Acropora species. Its at 37 percent, and the decline in and genus-level supplemental habitat is predominantly lower reef abundance before the 1998 bleaching information on this species’ threat crests, upper reef slopes and other high event (‘‘Back-cast Percent Population susceptibilities. Acropora verweyi has energy habitats and its depth range is to Reduction’’) was estimated at 15 been rated as moderately or highly at least 15 m. percent. However, as summarized above susceptible to bleaching and disease, The public comments did not provide in the Inter-basin Comparison sub- but these ratings are not based on any new or supplemental information section, live coral cover trends are species-specific data (Carpenter et al., on A. verweyi’s distribution. We highly variable both spatially and 2008). Acropora verweyi tolerates high gathered supplemental information, temporally, producing patterns on small temperatures in back-reef pools on Ofu, including Veron (2014), which reports scales that can be easily taken out of American Samoa where corals are more that A. verweyi is confirmed in 63 of his context, thus quantitative inferences to tolerant than elsewhere due to repeated 133 Indo-Pacific ecoregions, and species-specific trends should be brief exposure to high temperatures strongly predicted to be found in an interpreted with caution. At the same (Craig et al., 2001), although A. verweyi additional 17. Wallace (1999b) reports it time, an extensive body of literature is not abundant and acroporids still from 17 of her 29 Indo-Pacific areas, documents broad declines in live coral bleach some in these pools (Fenner and many of which are larger than Veron’s cover and shifts to reef communities Heron, 2008). Acropora verweyi was ecoregions. Richards (2009) calculated dominated by hardier coral species or relatively resistant to bleaching in the geographic range of A. verweyi at algae over the past 50 to 100 years Moorea during the 1991 warming event over 100 million km2. Acropora verweyi (Birkeland, 2004; Fenner, 2012; Pandolfi (Gleason, 1993). Reduced carbonate occurs in many different habitats, et al., 2003; Sale and Szmant, 2012). concentrations decrease calcification including fringing reefs with turbid These changes have likely occurred, and rates in A. verweyi (Marubini et al., water (Veron, 2000), and shallow reef are occurring, from a combination of 2003). While the overall magnitude of top and reef edge habitats (Wallace, global and local threats. Given that A. calcification was similar to the other 1999b). Acropora verweyi occurs on verweyi occurs in many areas affected coral species tested, A. verweyi showed upper reef slopes, especially those by these broad changes, and that it has reductions in mineral density that other exposed to wave action or currents some susceptibility to both global and species did not, potentially making it (Veron, 2014). Carpenter et al. (2008) local threats, we conclude that it is more susceptible to bioerosion or give the depth range for A. verweyi as likely to have declined in abundance breaking from wave action (Marubini et 2 to 15 meters. over the past 50 to 100 years, but a al., 2003). No other species-specific Demographic Information precise quantification is not possible. information is available for the susceptibility of A. verweyi to any other The SRR and SIR provided the Other Biological Information threat. For the other threats, based on following information on A. verweyi’s The SRR and SIR provided the information from other Acropora abundance. Acropora verweyi is following information on A. verweyi’s species provided in the genus generally common, but can be locally life history. Acropora verweyi is a description above, A. verweyi may be abundant, especially in the western hermaphroditic spawner that is a susceptible to the effects of disease, Indian Ocean. The public comments did participant in mass broadcast spawning trophic effects of fishing, sedimentation, not provide any new or supplemental in some localities. The public comments nutrients, sea-level rise, predation, and information on A. verweyi’s abundance. and information we gathered did not collection and trade. Thus, based on the We gathered supplemental information, provide anything additional to the available species-specific and genus including Richards et al. (2013b), which above-described biological information information summarized above, A. concludes that the species is globally based on the limited species-specific verweyi is likely to have some widespread, locally widespread, and information. susceptibility to ocean warming, locally rare. Veron (2014) reports that A. disease, acidification, trophic effects of Susceptibility to Threats verweyi occupied 4.7 percent of 2,984 fishing, sedimentation, nutrients, sea- dive sites sampled in 30 ecoregions of To describe A. verweyi’s threat level rise, predation, and collection and the Indo-Pacific, and had a mean susceptibilities, the SRR and SIR trade. The available information does abundance rating of 1.59 on a 1 to 5 provided genus-level information for the not support more precise ratings of the rating scale at those sites in which it effects on Acropora of ocean warming, susceptibilities of A. verweyi to the was found. Based on this semi- acidification, disease, predation, threats. quantitative system, the species’ sedimentation, nutrients, and collection abundance was characterized as and trade. The SRR and SIR did not Regulatory Mechanisms ‘‘uncommon.’’ Overall abundance was provide any other species-specific In the proposed rule, we did not described as ‘‘occasionally common in information on the effects of these provide any species-specific the western Indian Ocean.’’ Veron did threats on A. verweyi. We interpreted information on the regulatory not infer trends in abundance from the threat susceptibility and exposure mechanisms or conservation efforts for these data. As described in the Indo- information from the SRR and SIR in the A. verweyi. Criticisms of our approach

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received during public comment led us longitudinal geographic range, variable thermal regimes and ocean to the following analysis to attempt to observations of occasional resistance to chemistry at any given point in time. In analyze regulatory mechanisms on a thermal stress in shallow backreef pools, addition, areas with good circulation species basis. Records confirm that A. and its relatively common abundance. experience high levels of mixing which verweyi occurs in 63 Indo-Pacific Subsequent to the proposed rule, we can dilute adverse environmental ecoregions that encompass 41 countries’ received and gathered supplemental conditions. Its absolute abundance of at EEZs. The 41 countries are Australia, species- or genus-specific information, least tens to hundreds of millions of Cambodia, China, Comoros Islands, described above, that expands our colonies, combined with spatial Egypt, Federated States of Micronesia, knowledge regarding the species variability in ocean warming and Fiji, France (French Pacific Island abundance, distribution, and threat acidification across the species range, Territories), Indonesia, Israel, Japan, susceptibilities. We developed our moderates vulnerability to extinction Jordan, Kenya, Kiribati, Madagascar, assessment of the species’ vulnerability because the increasingly severe Malaysia, Maldives, Marshall Islands, to extinction using all the available conditions expected in the foreseeable Mauritius, Myanmar, Nauru, New information. As explained in the Risk future will be non-uniform and Zealand (Cook Islands, Tokelau), Niue, Analyses section, our assessment in this therefore will likely be a large number Palau, Papua New Guinea, Philippines, final rule emphasizes the ability of the of colonies that are either not exposed Samoa, Saudi Arabia, Seychelles, species’ spatial and demographic traits or do not negatively respond to a threat Solomon Islands, Sri Lanka, Sudan, to moderate or exacerbate its at any given point in time. Taiwan, Tanzania, Thailand, Tonga, vulnerability to extinction, as opposed Listing Determination Tuvalu, United Kingdom (Pitcairn to the approach we used in the Islands), United States (CNMI, Guam, proposed rule, which emphasized the In the proposed rule using the American Samoa, PRIAs), Vanuatu, and species’ susceptibility to threats. determination tool formula approach, A. Vietnam. The regulatory mechanisms The following characteristics of A. verweyi was proposed for listing as relevant to A. verweyi, described first as verweyi, in conjunction with the threatened because of: High the percentage of the above countries information described in the Corals and vulnerability to ocean warming (ESA that utilize them to any degree and Coral Reefs section, Coral Habitat sub- Factor E); moderate vulnerability to second, as the percentages of those section, and Threats Evaluation section disease (C) and acidification (E); countries whose regulatory mechanisms above, affect its vulnerability to common generalized range wide may be limited in scope, are as follows: extinction currently and over the abundance (E); moderate overall General coral protection (27 percent foreseeable future. Its geographic distribution (based on wide geographic with seven percent limited in scope), distribution includes most of the coral distribution and shallow depth coral collection (56 percent with 29 reef ecoregions in the Indian Ocean and distribution (E); and inadequacy of percent limited in scope), pollution western and central Pacific Ocean. Its existing regulatory mechanisms (D). control (44 percent with seven percent geographic distribution moderates In this final rule, we changed the limited in scope), fishing regulations on vulnerability to extinction because some listing determination for A. verweyi reefs (90 percent with 22 percent areas within its range are projected to from threatened to not warranted. No limited in scope), and managing areas have less than average warming and supplemental information or public for protection and conservation (95 acidification over the foreseeable future, comments changed our assessment of percent with 10 percent limited in including the western Indian Ocean, the the type and severity of threats affecting scope). The most common regulatory central Pacific, and other areas, so A. verweyi. Rather, we made this mechanisms in place for A. verweyi are portions of the population in these areas determination based on a more species- reef fishing regulations and area will be less exposed to severe specific and holistic assessment of management for protection and conditions. Its depth range is from low whether this species meets the conservation. Coral collection and tide to at least 15 meters. On one hand, definition of either a threatened or pollution control laws are also its depth range may moderate endangered coral largely in response to somewhat common for the species, but vulnerability to extinction over the public comments, including more 29 percent of coral collection laws are foreseeable future because deeper areas appropriate consideration of the limited in scope and may not provide of its range will usually have lower buffering capacity of this species’ spatial substantial protection. General coral irradiance than surface waters, and and demographic traits to lessen its protection laws are much less acidification is generally predicted to vulnerability to threats. Thus, based on prominent regulatory mechanisms for accelerate most in waters that are deeper the best available information above on the management of A. verweyi. and cooler than those in which the A. verweyi’s spatial structure, species occurs. On the other hand, its demography, threat susceptibilities, and Vulnerability to Extinction depth range may exacerbate management, none of the five ESA As explained above in the Risk vulnerability to extinction over the listing factors, alone or in combination, Analyses section, a species’ foreseeable future if the species occurs are causing this species to be likely to vulnerability to extinction results from predominantly in the shallower portion become endangered throughout its range the combination of its spatial and of its depth range, since those areas will within the foreseeable future, and thus demographic characteristics, threat have higher irradiance and thus be more it is not warranted for listing at this susceptibilities, and consideration of the severely affected by warming-induced time, because: baseline environment and future bleaching. Its habitat includes lower reef (1) Acropora verweyi’s distribution projections of threats. The SRR stated crests, upper reef slopes and other high across the Indian Ocean and most of the that the factors that increase the energy habitats. This moderates Pacific Ocean is spread over a very large potential extinction risk for A. verweyi vulnerability to extinction over the area. While some areas within its range include the relatively high susceptibility foreseeable future because the species is are projected to be affected by warming of the genus Acropora to common not limited to one habitat type but and acidification, other areas are threats. It listed factors that reduce the occurs in numerous types of reef projected to have less than average potential extinction risk for A. verweyi environments that will, on local and warming and acidification, including including its very wide latitudinal and regional scales, experience highly the western Indian Ocean, the central

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Pacific, and other areas. This verweyi is not warranted for listing at the highest prevalence out of 25 taxa distribution and the heterogeneous this time under any of the listing factors. had 8 percent prevalence of disease habitats it occupies reduce exposure to (Haapkyla et al., 2007). Genus Anacropora any given threat event or adverse Genus Conclusion condition that does not occur uniformly Genus Introduction throughout the species range. As The family Acroporidae includes five Based on the information from the explained above in the Threats genera, Acropora, Montipora, SRR, SIR, public comments, and Evaluation section, we have not Astreopora, Isopora, and Anacropora. information we gathered, we can make identified any threat that is expected to Anacropora contains seven species, all the following inferences about the occur uniformly throughout the species occurring in the Indo-Pacific. Like most susceptibilities of an unstudied range within the foreseeable future; Acropora species, colonies of Anacropora species to ocean warming, (2) Acropora verweyi’s absolute Anacropora species are branching. disease, acidification, sedimentation, abundance is at least tens of millions of Unlike Acropora, there is no corallite on nutrients, trophic effects of fishing, sea- colonies, providing buffering capacity in the tip of the branches of Anacropora level rise, predation, and collection and the form of absolute numbers of colonies, a diagnostic characteristic of trade. The SRR rated ocean warming colonies and variation in susceptibility Acropora (Veron, 2000). Anacropora is and disease as ‘‘high’’ importance, and between individual colonies. As morphologically like branching ocean acidification as ‘‘medium-high’’ discussed in the Corals and Coral Reefs Montipora without an encrusting base importance, to corals. These were rated section above, the more colonies a (Veron and Wallace, 1985). The SRR as the three most important threats to species has, the lower the proportion of and SIR provided the following genus- reef-building corals overall. The one colonies that are likely to be exposed to level introductory information on available study on the effects of ocean a particular threat at a particular time, Anacropora. Morphologic taxonomy has warming on Anacropora reported and all individuals that are exposed will been unable to resolve whether variable thermal-induced bleaching not have the same response; and Anacropora are recently derived from within the genus (Bruno et al., 2001). (3) It is a broadcast spawner and fast Montipora or from Acropora, but genetic While there is no other genus-level or grower, enhancing recovery potential evidence supports the former view. species-specific information on the from mortality events as described in susceptibilities of Anacropora species to the Corals and Coral Reefs section Genus Susceptibility to Threats ocean warming, the SRR rated it as above. The SRR and SIR provided the ‘‘high’’ importance to corals. Thus, we Notwithstanding the projections following information on the threat conclude that an unstudied Anacropora through 2100 that indicate increased susceptibilities of the genus species has some susceptibility to ocean severity over time of the three high Anacropora. The bleaching warming. Similarly for ocean importance threats, the combination of susceptibility in the genus Anacropora acidification, while there is no genus- these biological and environmental is not well known. In the 1998 level or species-specific information on characteristics indicates that the species bleaching event in Palau, Anacropora the susceptibilities of Anacropora possesses sufficient buffering capacity colonies (not identified to species) were species to ocean acidification, the SRR to avoid being in danger of extinction moderately affected relative to other rated it as ‘‘medium-high’’ importance within the foreseeable future throughout coral genera, with total mortality of to corals. Thus, we conclude that an its range. It is possible that this species’ some Anacropora colonies in some unstudied Anacropora species has some extinction risk may increase in the limited areas, while those in other areas susceptibility to ocean acidification. future if global threats continue and were unaffected. This was a major The one available study on the effects of increase in severity and the species bleaching event, with 48 percent disease on Anacropora reported no exposure to threats increases throughout bleaching overall (all coral species disease on Anacropora colonies its range. Despite its current combined), and bleaching and mortality (Haapkyla et al., 2007). However, this distribution, A. verweyi is characterized of different genera and species ranging single study is inadequate to imply as uncommon overall, thus its from zero to nearly 100 percent (Bruno susceptibility level for all Anacropora abundance may not provide much et al., 2001). With regard to predation, species, thus we conclude that buffering capacity in terms of overall A. puertogalerae have been reported to Anacropora has some susceptibility to numbers. In addition, A. verweyi be only preyed on by wrasses in disease. showed reductions in mineral density in proportion to its availability (Cole et al., The SRR rated the trophic effects of response to reduced carbonate 2010). With regard to sedimentation and fishing as ‘‘medium’’ importance, the concentrations, potentially making it nutrients, some Anacropora species fourth most important threat to corals more susceptible to bioerosion or appear resistant to both these threats overall. This threat was not addressed at breaking from wave action as ocean while others appear susceptible the genus or species level in the SRR or acidification increases. Should the (Mohammed and Mohammed, 2005). SIR, because it is an ecosystem-level species experience reduced abundance Collection and trade in the genus process. That is, removal of herbivorous or range constriction of a certain Anacropora has been reported to be fish from coral reef systems by fishing magnitude, the ability of its range to negligible, with only 14 pieces reported alters trophic interactions by reducing moderate exposure to threats will in export over the last decade (CITES, herbivory on algae, thereby providing a diminish. However, the species is not 2010). competitive advantage for space to algae likely to become of such low abundance The public comments did not provide over coral. Thus, the SRR did not or so spatially fragmented as to be in any new or supplemental information discuss this threat in terms of coral taxa, danger of extinction due to depensatory on the threat susceptibilities of the as its effects are difficult to distinguish processes, the potential effects of genus Anacropora. We gathered between coral genera and species. environmental stochasticity, or the supplemental information that provided Therefore, an unstudied Anacropora potential for mortality from catastrophic the following. One study reported that species is likely to have some events within the foreseeable future disease was not found on Anacropora at susceptibility to the trophic effects of throughout its range. Therefore, A. a site in Indonesia, while the taxon with fishing.

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The SRR rated sedimentation, information described below for this Reduction’’) was estimated at 15 nutrients, and sea-level rise as ‘‘low- species is sufficiently reliable (Fenner, percent. However, as summarized above medium’’ importance to corals overall. 2014b). in the Inter-basin Comparison sub- The one available study on the effects of section, live coral cover trends are Spatial Information sedimentation and nutrients highly variable both spatially and (Mohammed and Mohammed, 2005) on The SRR and SIR provided the temporally, producing patterns on small Anacropora species suggest either following information on A. scales that can be easily taken out of intermediate or variable susceptibilities. puertogalerae’s distribution, habitat, context, thus quantitative inferences to Thus we conclude that an unstudied and depth range. Anacropora species-specific trends should be Anacropora species has some puertogalerae’s distribution is the Coral interpreted with caution. At the same susceptibility to sedimentation and Triangle and western equatorial Pacific, time, an extensive body of literature nutrients. Sea-level rise was not plus southern Japan to the GBR. Its documents broad declines in live coral addressed at the genus or species level habitat includes both coral reef and non- cover and shifts to reef communities in the SRR or SIR. Increasing sea levels reefal environments, including upper dominated by hardier coral species or may increase land-based sources of reef slopes, mid-slopes, and lagoons on algae over the past 50 to 100 years pollution due to inundation, resulting in reefs, and various substrates in non- (Birkeland, 2004; Fenner, 2012; Pandolfi changes to coral community structure, reefal areas. Its depth range as five to at et al., 2003; Sale and Szmant, 2012). thus an unstudied Anacropora species least 20 meters depth. These changes have likely occurred, and is likely to have some susceptibility to The public comments did not provide are occurring, from a combination of sea-level rise. The SRR rated predation any new or supplemental information global and local threats. Given that A. and ornamental trade (referred to in the on A. puertogalerae’s distribution. We puertogalerae occurs in many areas proposed rule as Collection and Trade) gathered supplemental information, affected by these broad changes, and as ‘‘low’’ importance to corals overall. including Veron (2014), which reports that it has some susceptibility to both The one available study on the effects of that A. puertogalerae is confirmed in 26 global and local threats, we conclude predation (Cole et al., 2010) on of his 133 Indo-Pacific ecoregions, and that it is likely to have declined in Anacropora species suggest either strongly predicted to be found in an abundance over the past 50 to 100 years, intermediate or variable susceptibility, additional seven. but a precise quantification is not thus we conclude that an unstudied Demographic Information possible based on the limited species- specific information. Anacropora species has some The SRR and SIR provided the susceptibility to predation. Because the following information on A. Other Biological Information available information suggests that puertogalerae’s abundance. Anacropora The SRR and SIR provided the Anacropora species are lightly collected puertogalerae is reported to be following information on A. and traded, an unstudied Anacropora uncommon but can form large thickets puertogalerae’s life history. Anacropora species is likely to have low in the Philippines. puertogalerae has been reported to be a susceptibility to collection and trade. The public comments did not provide simultaneous hermaphrodite and a In conclusion, an unstudied any new or supplemental information broadcast spawner. Clonal structure Anacropora species is likely to have on A. puertogalerae’s abundance. We suggests the species also reproduces by some susceptibility to ocean warming, gathered supplemental information, fragmentation. Larvae contain disease, ocean acidification, including Veron (2014), which states zooxanthellae that can supplement sedimentation, nutrients, trophic effects that it is sometimes a dominant species maternal provisioning with energy of fishing, sea-level rise, predation, and where it occurs. Veron (2014) reports sources provided by their low susceptibility to collection and that A. puertogalerae occupied 4.6 photosynthesis. The public comments trade. percent of 2,984 dive sites sampled in and information we gathered provided Anacropora puertogalerae 30 ecoregions of the Indo-Pacific, and no additional biological information. had a mean abundance rating of 2.02 on Introduction a 1 to 5 rating scale at those sites in Susceptibility to Threats The SRR and SIR provided the which it was found. Based on this semi- To describe A. puertogalerae’s threat following information on A. quantitative system, the species’ susceptibilities, the SRR and SIR puertogalerae’s morphology and abundance was characterized as provided genus-level information for the taxonomy. Morphology was described ‘‘uncommon.’’ Overall abundance was effects on Acropora of ocean warming, as compact branches, typically less than also described as ‘‘uncommon.’’ Veron acidification, disease, predation, 13 mm in diameter and tapering, with did not infer trends in abundance from sedimentation, nutrients, and collection thin spines under corallites, and these data. As described in the Indo- and trade. The SRR and SIR provided taxonomy was described as having no Pacific Species Determinations the following species-specific taxonomic issues but being similar in introduction above, based on results information on A. puertogalerae’s appearance to A. spinosa and A. forbesi. from Richards et al. (2008) and Veron threats. In a two month study in Kimbe The public comments and (2014), the absolute abundance of this Bay, PNG, it was observed that A. information we gathered did not species is likely at least tens of millions puertogalerae was only preyed on by provide any new or supplemental of colonies. wrasses in proportion to its availability information on morphology, and Carpenter et al. (2008) extrapolated (Cole et al., 2010). The SRR and SIR did confirmed that there are no known species abundance trend estimates from not provide any other species-specific taxonomic problems for A. total live coral cover trends and habitat information on the effects of these puertogalerae, but that there is a types. For A. puertogalerae, the overall threats on A. puertogalerae. We moderate level of species identification decline in abundance (‘‘Percent interpreted the threat susceptibility and uncertainty for this species. However, Population Reduction’’) was estimated exposure information from the SRR and the species can be identified by experts at 38 percent, and the decline in SIR in the proposed rule for A. (Fenner, 2014b), thus we conclude that abundance before the 1998 bleaching puertogalerae’s vulnerabilities as the distribution and abundance event (‘‘Back-cast Percent Population follows: High vulnerability to ocean

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warming, moderate vulnerability to regulations and area management for severe warming conditions. On the disease, ocean acidification, trophic protection and conservation. Coral other hand, the species’ geographic effects of fishing, nutrients and collection and pollution control laws distribution exacerbates vulnerability to predation, and low vulnerability to are also somewhat common for the extinction because much of it lies sedimentation, sea level rise, predation, species, but 38 percent of coral within the western equatorial Pacific, an and collection and trade. collection laws are limited in scope and area projected to have the highest Public comments did not provide any may not provide substantial protection. seawater temperatures in the foreseeable new or supplemental information on A. General coral protection laws are much future. Its depth range is from five to at puertogalerae’s threat susceptibilities. less common regulatory mechanisms for least 20 meters. This moderates We gathered the following species- the management of A. puertogalerae. vulnerability to extinction over the specific and genus-level supplemental foreseeable future because deeper areas Vulnerability to Extinction information on this species’ threat of its range will usually have lower susceptibilities. Anacropora As explained above in the Risk irradiance than surface waters, and puertogalerae has been rated as Analyses section, a species’ acidification is generally predicted to moderately or highly susceptible to vulnerability to extinction results from accelerate most in waters that are deeper bleaching and disease, but these ratings the combination of its spatial and and cooler than those in which the are not based on species-specific data demographic characteristics, threat species occurs. Its habitat includes both (Carpenter et al., 2008). Based on the susceptibilities, and consideration of the coral reef and non-reefal environments, genus and species-specific information baseline environment and future including upper reef slopes, mid-slopes, described above, A. puertogalerae likely projections of threats. The SRR stated and lagoons on reefs, and various has some susceptibility to ocean that ‘‘factors that increase the potential substrates in non-reefal areas. This is warming, disease, acidification, trophic extinction risk for A. puertogalerae are particularly important for moderating effects of fishing, sedimentation, that the high susceptibility to threats vulnerability to extinction over the nutrients, sea-level rise, and predation, common to members of the genus foreseeable future because the species is and low susceptibility to collection and Acropora (bleaching, disease, and not limited to one habitat type but trade. The available information does predation) are generally considered occurs in numerous types of reef and not support more precise ratings of the appropriate to species in the confamilial non-reef environments that will, on susceptibilities of A. puertogalerae to genus Anacropora as well.’’ It noted that local and regional scales, experience the threats. a factor that reduces potential extinction highly variable thermal regimes and risk is that A. puertogalerae has a Regulatory Mechanisms ocean chemistry at any given point in somewhat broad range. time. Its absolute abundance of at least In the proposed rule, we did not Subsequent to the proposed rule, we tens of millions of colonies, combined provide any species-specific received and gathered supplemental with spatial variability in ocean information on the regulatory species- or genus-specific information, warming and acidification across the mechanisms or conservation efforts for described above, that expands our species range, moderates vulnerability A. puertogalerae. Criticisms of our knowledge regarding the species to extinction because the increasingly approach received during public abundance, distribution, and threat severe conditions expected in the comment led us to the following susceptibilities. We developed our foreseeable future will be non-uniform analysis to attempt to analyze regulatory assessment of the species’ vulnerability and therefore will likely be a large mechanisms on a species basis. Records to extinction using all the available number of colonies that are either not confirm that A. puertogalerae occurs in information. As explained in the Risk exposed or do not negatively respond to 26 Indo-Pacific ecoregions that Analyses section, our assessment in this a threat at any given point in time. encompass 16 countries’ EEZs. The 16 final rule emphasizes the ability of the countries are Australia, Brunei, China, species’ spatial and demographic traits Listing Determination Fiji, France (French Pacific Island to moderate or exacerbate its In the proposed rule using the Territories), Indonesia, Japan, Malaysia, vulnerability to extinction, as opposed determination tool formula approach, A. Palau, Papua New Guinea, Philippines, to the approach we used in the puertogalerae was proposed for listing Solomon Islands, Taiwan, Timor-Leste, proposed rule, which emphasized the as threatened because of: High Vanuatu, and Vietnam. The regulatory species’ susceptibility to threats. vulnerability to ocean warming (ESA mechanisms relevant to A. The following characteristics of A. Factor E); moderate vulnerability to puertogalerae, described first as the puertogalerae, in conjunction with the disease (C) and acidification (E); percentage of the above countries that information described in the Corals and uncommon generalized range wide utilize them, to any degree and second, Coral Reefs section, Coral Habitat sub- abundance (E); moderate overall as the percentages of those countries section, and Threats Evaluation section distribution (based on moderate whose regulatory mechanisms may be above, affect its vulnerability to geographic distribution and moderate limited in scope, are as follows: General extinction currently and over the depth distribution (E); and inadequacy coral protection (38 percent with 6 foreseeable future. Its geographic of existing regulatory mechanisms (D). percent limited in scope), coral distribution includes many of the coral In this final rule, we changed the collection (69 percent with 38 percent reef ecoregions in the western and listing determination for A. limited in scope), pollution control (44 central Pacific Ocean; the Coral Triangle puertogalerae from threatened to not percent with 19 percent limited in and western equatorial Pacific, plus warranted. We made this determination scope), fishing regulations on reefs (100 southern Japan to the GBR. On one based on a more species-specific and percent with 19 percent limited in hand, this moderates vulnerability to holistic assessment of whether this scope), and managing areas for extinction because the high latitude species meets the definition of either a protection and conservation (100 areas in the northern and southern threatened or endangered coral largely percent with none limited in scope). portions of its range are projected to in response to public comments, The most common regulatory have less than average warming over the including more appropriate mechanisms in place for A. foreseeable future, thus populations in consideration of the buffering capacity puertogalerae are reef fishing these areas will be less exposed to of this species’ spatial and demographic

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traits to lessen its vulnerability to moderate exposure to threats will Demographic Information threats. Thus, based on the best diminish. However, the species is not available information above on A. likely to become of such low abundance The SRR and SIR provided the puertogalerae’s spatial structure, or so spatially fragmented as to be in following information on A. spinosa’s demography, threat susceptibilities, and danger of extinction due to depensatory abundance. Its abundance is reported to management, none of the five ESA processes, the potential effects of be uncommon, but it may occur in listing factors, alone or in combination, environmental stochasticity, or the extensive tracts in certain areas. are causing this species to be likely to potential for mortality from catastrophic The public comments did not provide become endangered throughout its range events within the foreseeable future. any new or supplemental information within the foreseeable future, and thus Therefore, A. puertogalerae is not on A. spinosa’s abundance. We gathered is not warranted for listing at this time, warranted for listing at this time under supplemental information, including because: any of the listing factors. Veron (2014), which reports that A. (1) Anacropora puertogalerae’s spinosa occupied 1.5 percent of 2,984 distribution is spread over a very large Anacropora spinosa dive sites sampled in 30 ecoregions of area. While some areas within its range Introduction the Indo-Pacific, and had a mean are projected to be affected by warming abundance rating of 1.84 on a 1 to 5 and acidification, other areas are The SRR and SIR provided the rating scale at those sites in which it projected to have less than average following information on A. spinosa’s was found. Based on this semi- warming, including high latitude areas morphology and taxonomy. Morphology quantitative system, the species’ in both the northern and southern was described as compact branches, less abundance was characterized as portions of the species’ range. This than 10 mm in diameter and tapering. ‘‘uncommon,’’ and overall abundance distribution and the heterogeneous They have elongate, crowded, irregular was described as ‘‘usually uncommon.’’ habitats it occupies reduce exposure to spines that are not strongly tapered, and Veron did not infer trends in abundance any given threat event or adverse taxonomy was described as having no from these data. As described in the condition that does not occur uniformly taxonomic issues but being similar in Indo-Pacific Species Determinations throughout the species range. As appearance to Anacropora introduction above, based on results explained above in the Threats puertogalerae. from Richards et al. (2008) and Veron Evaluation section, we have not (2014), the absolute abundance of this The public comments and identified any threat that is expected to species is likely at least millions of information we gathered did not occur uniformly throughout the species colonies. range within the foreseeable future; provide information on morphology, (2) Anacropora puertogalerae occurs and confirmed that there are no known Carpenter et al. (2008) extrapolated in very diverse habitats, including both taxonomic problems for A. spinosa and species abundance trend estimates from coral reef and non-reefal habitats so the that there is a moderate level of species total live coral cover trends and habitat species will experience a variety of identification uncertainty for this types. For A. spinosa, the overall environmental conditions at any given species. Veron (2014) states that A. decline in abundance (‘‘Percent time; and spinosa is easily confused with Population Reduction’’) was estimated (3) Anacropora puertogalerae’s Anacropora puertogalerae. However, at 58 percent, and the decline in absolute abundance is at least tens of the species can be identified by experts abundance before the 1998 bleaching millions of colonies, providing buffering (Fenner, 2014b), thus we conclude that event (‘‘Back-cast Percent Population capacity in the form of absolute the distribution and abundance Reduction’’) was estimated at 22 percent numbers of colonies and variation in information described below for this in the study. However, as summarized susceptibility between individual species is sufficiently reliable (Fenner, above in the Inter-basin Comparison colonies. As discussed in the Corals and 2014b). sub-section, live coral cover trends are Coral Reefs section above, the more highly variable both spatially and colonies a species has, the lower the Spatial Information temporally, producing patterns on small proportion of colonies that are likely to scales that can be easily taken out of The SRR and SIR provided the be exposed to a particular threat at a context, thus quantitative inferences to particular time, and all individuals that following information on A. spinosa’s species-specific trends should be are exposed will not have the same distribution, habitat, and depth range. interpreted with caution. At the same response. Anacropora spinosa’s distribution is the time, an extensive body of literature Notwithstanding the projections Coral Triangle and southern Japan. Its documents broad declines in live coral through 2100 that indicate increased habitat includes both coral reef and non- cover and shifts to reef communities severity over time of the three high reefal environments, including upper dominated by hardier coral species or importance threats, the combination of reef slopes, mid-slopes, and lagoons on algae over the past 50 to 100 years these biological and environmental reefs, and various substrates in non- (Birkeland, 2004; Fenner, 2012; Pandolfi characteristics indicates that the species reefal areas. Its depth range is five to 15 et al., 2003; Sale and Szmant, 2012). possesses sufficient buffering capacity meters deep. These changes have likely occurred, and to avoid being in danger of extinction The public comments provided the are occurring, from a combination of within the foreseeable future throughout following information that a photograph global and local threats. Given that A. its range. It is possible that this species’ of A. spinosa that appeared in Veron spinosa occurs in many areas affected extinction risk may increase in the (2000) was erroneously attributed to by these broad changes, and that it has future if global threats continue and Guam but was actually taken in Palau. some susceptibility to both global and increase in severity and the species We gathered supplemental information, local threats, we conclude that it is exposure to threats increases throughout including Veron (2014), which reports likely to have declined in abundance its range. Should the species experience that A. spinosa is confirmed in 13 of his over the past 50 to 100 years, but a reduced abundance or range 133 Indo-Pacific ecoregions, and precise quantification is not possible constriction of a certain magnitude, the strongly predicted to be found in an based on the limited species-specific ability of these characteristics to additional six. information.

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Other Biological Information A. spinosa. Criticisms of our approach species’ spatial and demographic traits The SRR and SIR provided the received during public comment led us to moderate or exacerbate its following information on A. spinosa’s to the following analysis to attempt to vulnerability to extinction, as opposed life history: Anacropora spinosa has analyze regulatory mechanisms on a to the approach we used in the been reported to be a simultaneous species basis. Records confirm that A. proposed rule, which emphasized the spinosa occurs in 13 Indo-Pacific species’ susceptibility to threats. hermaphrodite that broadcast spawns ecoregions that encompass six The following characteristics of A. mature gametes. Planula larvae contain countries’ EEZs. The six countries are spinosa, in conjunction with the zooxanthellae that can supplement Indonesia, Japan, Palau, Papua New information described in the Corals and maternal provisioning with energy Guinea, Philippines, and the Solomon Coral Reefs section, Coral Habitat sub- sources provided by their Islands. The regulatory mechanisms section, and Threats Evaluation section photosynthesis. The public comments relevant to A. spinosa, described first as above, affect its vulnerability to and information we gathered did not the percentage of the above countries extinction currently and over the provide anything additional to the that utilize them to any degree and foreseeable future. Its geographic above-described biological information. second, as the percentages of those distribution is limited to the Coral Susceptibility to Threats countries whose regulatory mechanisms Triangle and southern Japan. Despite may be limited in scope, are as follows: the large number of islands and To describe A. spinosa’s threat General coral protection (17 percent environments that are included in the susceptibilities, the SRR and SIR with none limited in scope), coral species’ range, this range exacerbates provided genus-level information for the collection (67 percent with 33 percent vulnerability to extinction over the effects on Anacropora of ocean limited in scope), pollution control (17 foreseeable future because it is mostly warming, acidification, disease, percent with 17 percent limited in limited to an area projected to have the predation, sedimentation, nutrients, and scope), fishing regulations on reefs (100 most rapid and severe impacts from collection and trade. The SRR and SIR percent with none limited in scope), climate change and localized human provided the following species-specific and managing areas for protection and impacts for coral reefs over the 21st information on A. spinosa’s threats. The conservation (100 percent with none century. Its depth range is five to 15 only known export of A. spinosa was a limited in scope). The most common meters On one hand, its depth range single specimen from Indonesia in 2005. regulatory mechanisms in place for A. may moderate vulnerability to We interpreted the threat susceptibility spinosa are reef fishing regulations and extinction over the foreseeable future and exposure information from the SRR area management for protection and because deeper areas of its range will and SIR in the proposed rule for A. conservation. Coral collection laws are usually have lower irradiance than spinosa’s vulnerabilities as follows: also somewhat common for the species, surface waters, and acidification is High vulnerability to ocean warming; but 33 percent of coral collection laws generally predicted to accelerate most in moderate vulnerability to disease, ocean are limited in scope and may not waters that are deeper and cooler than acidification, trophic effects of reef provide substantial protection. General those in which the species occurs. On fishing, nutrients, and predation, and coral protection and pollution control the other hand, its depth range may low vulnerability to sedimentation, sea laws are much less common regulatory exacerbate vulnerability to extinction level rise, and collection and trade. mechanisms for the management of A. over the foreseeable future if the species Public comments did not provide any spinosa. occurs predominantly in the shallower new or supplemental information on A. portion of its depth range, since those spinosa’s threat susceptibilities, but we Vulnerability to Extinction areas will have higher irradiance and gathered species-specific and genus- As explained above in the Risk thus be more severely affected by level supplemental information on this Analyses section, a species’ warming-induced bleaching. Its habitat species’ threat exposures. Anacropora vulnerability to extinction results from includes upper reef slopes, mid-slopes, spinosa has been rated as moderately or the combination of its spatial and and lagoons on reefs, and various highly susceptible to bleaching and demographic characteristics, threat substrates in non-reefal areas. This disease, but these ratings are not based susceptibilities, and consideration of the moderates vulnerability to extinction on species-specific data (Carpenter et baseline environment and future over the foreseeable future because the al., 2008). No other species-specific projections of threats. The SRR stated species is not limited to one habitat type information is available for the factors that increase the potential but occurs in numerous types of reef susceptibility of A. spinosa to any other extinction risk for A. spinosa are that and non-reef environments that will, on threat. the high susceptibility to threats local and regional scales, experience Based on information provided in the common to members of the genus highly variable thermal regimes and genus description above, A. spinosa Acropora (bleaching, disease, and ocean chemistry at any given point in likely has some susceptibilities to ocean predation) are generally considered time. There is not enough information warming, disease, acidification, trophic appropriate to species in the confamilial about its abundance to determine if it effects of fishing, sedimentation, genus Anacropora as well. moderates or exacerbates extinction: It nutrients, sea-level rise, predation, and Subsequent to the proposed rule, we is uncommon and has at least millions low susceptibility to collection and received and gathered supplemental of colonies, but the great majority of the trade. The available information does species- or genus-specific information, population is within an area expected to not support more precise ratings of the described above, that expands our be severely impacted by threats over the susceptibilities of A. spinosa to the knowledge regarding the species foreseeable future. threats. abundance, distribution, and threat susceptibilities. We developed our Listing Determination Regulatory Mechanisms assessment of the species’ vulnerability In the proposed rule using the In the proposed rule, we did not to extinction using all the available determination tool formula approach, A. provide any species-specific information. As explained in the Risk spinosa was proposed for listing as information on the regulatory Analyses section, our assessment in this endangered because of: High mechanisms or conservation efforts for final rule emphasizes the ability of the vulnerability to ocean warming (ESA

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Factor E); moderate vulnerability to also indicate that the species is not species status to the point at which disease (C) and acidification (E); currently in danger of extinction and listing is not warranted. uncommon generalized range wide thus does not warrant listing as Genus Astreopora abundance (E); narrow overall Endangered because: distribution (based on narrow (1) While A. spinosa’s distribution is Genus Introduction constrained almost entirely to the Coral geographic distribution and shallow The family Acroporidae includes five Triangle which increases it extinction depth distribution (E); and inadequacy genera, Acropora, Montipora, risk as described above, its habitat of existing regulatory mechanisms (D). Astreopora, Isopora, and Anacropora. In this final rule, we changed the includes shallow reef environments, Astreopora contains 15 species, all listing determination for A. spinosa generally in clear or slightly turbid occurring in the Indo-Pacific (Veron, from endangered to threatened. We water and on soft substrates of lower 2000; Wallace et al., 2011). Unlike made this determination based on a reef slopes, and it has also been found Acropora and Anacropora species, more species-specific and holistic in non-reef environments. This assessment of whether this species moderates vulnerability to extinction Astreopora colonies are massive, meets the definition of either a currently because the species is not laminar, or encrusting. The SRR and SIR threatened or endangered coral largely limited to one habitat type but occurs in provided no genus-level introductory in response to public comments, numerous types of reef and non-reef information on Astreopora. including more appropriate environments that will, on local and Genus Susceptibility to Threats consideration of the buffering capacity regional scales, experience highly The SRR and SIR provided the of this species’ spatial and demographic variable thermal regimes and ocean following information on the threat traits to lessen its vulnerability to chemistry at any given point in time, as susceptibilities of the genus Astreopora. threats. Thus, based on the best described in more detail in the Coral Astreopora species can be susceptible to available information provided above on Habitat and Threats Evaluation sections. bleaching, although overall Astreopora A. spinosa’s spatial structure, There is no evidence to suggest that the species are less susceptible to bleaching demography, threat susceptibilities, and species is so spatially fragmented that than other genera within the family management indicate that it is likely to depensatory processes, environmental become endangered throughout its range stochasticity, or the potential for Acroporidae, and often survive when within the foreseeable future, and thus catastrophic events currently pose a they do bleach. Congeners have warrants listing as threatened at this high risk to the survival of the species; contracted a fungal disease in Kenya, time, because: and and Astreopora myriophthalma was (1) Anacropora spinosa is likely to be (2) Anacropora spinosa’s absolute infected with black-band disease at a susceptible to ocean warming (ESA abundance is at least millions of polluted site in Jordan. Trade in the Factor E), disease (C), ocean colonies which allows for variation in genus Astreopora has been reported to acidification (E), trophic effects of the responses of individuals to threats to be light and sporadic. fishing (A), nutrients (A, E), and play a role in moderating vulnerability The public comments did not provide predation (C). In addition, existing to extinction for the species to some any new or supplemental information regulatory mechanisms to address global degree, as described in more detail in on the threat susceptibilities of the threats that contribute to extinction risk the Corals and Coral Reefs section. genus Astreopora, but the supplemental for this species are inadequate (D); and There is no evidence of depensatory information provided the following. In (2) Anacropora spinosa’s distribution processes such as reproductive failure Palau in 1998, Astreopora species had is constrained almost entirely within the from low density of reproductive moderate levels of bleaching and Coral Triangle, which is projected to individuals and genetic processes such moderate mortality (Bruno et al., 2001). have the most rapid and severe impacts as inbreeding affecting this species. In Kenya in 1998, three quarters of from climate change and localized Thus, its absolute abundance indicates Astreopora species within marine human impacts for coral reefs over the it is currently able to avoid high protected areas were affected by mass 21st century, as described in the Threats mortality from environmental bleaching. Although many Astreopora Evaluation. Multiple ocean warming stochasticity, and mortality of a high colonies bleached, none died. Of the 18 events have already occurred within the proportion of its population from genera included in the study, five western equatorial Pacific that suggest catastrophic events. genera including Astreopora had some future ocean warming events may be The combination of these bleaching but no mortality, and the more severe than average in this part of characteristics indicates that the species bleaching index for Astreopora was the the world. A range constrained to this does not exhibit the characteristics of fifth lowest of the 18 genera particular geographic area that is likely one that is currently in danger of (McClanahan et al., 2004; McClanahan to experience severe and increasing extinction, as described previously in et al., 2001). In Thailand in 1998 and threats indicates that a high proportion the Risk Analyses section, and thus does 2010, all colonies of Astreopora of the population of this species is likely not warrant listing as endangered at this myriophthalma completely bleached, to be exposed to those threats over the time. but in both events, all colonies foreseeable future. Range-wide, a multitude of completely recovered (Sutthacheep et The combination of these conservation efforts are already broadly al., 2013). In Mauritius in 2004, the characteristics and projections of future employed that are likely benefiting A. Astreopora genus had the 23rd highest threats indicates that the species is spinosa. However, considering the bleaching rate of the 32 genera recorded, likely to be in danger of extinction global scale of the most important and 12 percent of the highest value within the foreseeable future throughout threats to the species, and the (McClanahan et al., 2005a). In eight its range and warrants listing as ineffectiveness of conservation efforts at countries in the western Indian Ocean threatened at this time due to factors A, addressing the root cause of global in 1998–2005, the Astreopora genus had C, D, and E. threats (i.e., GHG emissions), we do not the 21st highest bleaching rate of the 45 The available information above on A. believe that any current conservation genera recorded, and 39 percent of the spinosa’s spatial structure, demography, efforts or conservation efforts planned highest value (McClanahan et al., threat susceptibilities, and management in the future will result in affecting the 2007a).

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On the GBR, Astreopora species had the genus or species level in the SRR or Astreopora cucullata a very low level of Black Band Disease SIR, because it is an ecosystem-level occurrence, just two percent the level of process. That is, removal of herbivorous Introduction this disease found in Acropora species fish from coral reef systems by fishing The SRR and SIR provided the at the same sites (Page and Willis, 2006). alters trophic interactions by reducing following information on A. cucullata’s Likewise, another study from the GBR herbivory on algae, thereby providing a morphology and taxonomy. Morphology reported that Astreopora species had competitive advantage for space to algae was described as thick or encrusting low susceptibility to Skeletal Eroding over coral. Thus, the SRR did not platy colonies, with inclined corallites, Band, with a prevalence of 0.1 percent. discuss this threat in terms of coral taxa, and taxonomy was described as having Skeletal Eroding Band is the most as its effects are difficult to distinguish no taxonomic issues but being similar to prevalent coral disease on the GBR between coral genera and species. Astreopora scabra. (Page and Willis, 2007). In New Therefore, an unstudied Astreopora Caledonia, Astreopora was reported to species is likely to have some The public comments and have a disease prevalence of 0.5 percent, susceptibility to the trophic effects of information we gathered did not which was the fifth highest prevalence fishing. provide information on morphology, of 12 genera reported (Tribollet et al., The SRR rated sedimentation, and confirmed that there are no known 2011). In Indonesia, Astreopora had a nutrients, and sea-level rise as ‘‘low- taxonomic problems for A. cucullata, disease prevalence of 1.5 percent, which medium’’ importance to corals overall. but that there is a high level of species was the 2nd highest reported among 35 The study cited above reports high identification uncertainty for this taxa (Haapkyla et al., 2007). sediment rejection efficiency in A. species. Veron (Veron, 2014) states that In a study of sediment rejection in 22 myriophthalma. This one study is A. cucullata is not readily distinguished coral species (including one Astreopora inadequate to rate the susceptibility as from other Astreopora but Veron species), A. myriophthalma cleared 98 low, thus we conclude that Astreopora (Lamberts, 1980; Lamberts, 1982; Veron, percent of the sediment within 48 has some susceptibility to 2000) considers it a valid species, thus hours, the seventh most efficient of the sedimentation. Although there is no we conclude it is sufficiently distinctive 22 species at clearing sediment genus-level or species-specific to be identified by experts, and that the (Stafford-Smith, 1993). Astreopora information on the susceptibilities of distribution and abundance information species trade has been reported to be Astreopora species to nutrients, the SRR described below for this species is light and sporadic (CITES, 2010). There rated it as ‘‘low-medium’’ importance to sufficiently reliable (Fenner, 2014b). is no information available on the corals. Thus, we conclude that an effects of any other threat for Astreopora unstudied Astreopora species has some Spatial Information species. susceptibility to nutrients. Sea-level rise The SRR and SIR provided the Genus Conclusion was not addressed at the genus or following information on A. cucullata’s Based on the information from the species level in the SRR or SIR. distribution, habitat, and depth range. SRR, SIR, public comments, and Increasing sea levels may increase land- Astreopora cucullata’s distribution is a based sources of pollution due to supplemental information, we can make broad distribution, from the Red Sea inundation, resulting in changes to coral the following inferences about the and central Indo-Pacific to the central community structure, thus an unstudied susceptibilities of an unstudied Pacific. The SRR and SIR described A. Astreopora species is likely to have Astreopora species to ocean warming, cucullata’s habitat as protected reef some susceptibility to sea-level rise. disease, acidification, sedimentation, environments, and the depth range as Although there is no genus-level or nutrients, trophic effects of fishing, sea- five to 15 m. The public comments level rise, predation, and collection and species-specific information on the susceptibilities of Astreopora species to provided the following information. trade. The SRR rated ocean warming One comment stated that A. cucculata and disease as ‘‘high’’ importance, and predation, there is no information suggesting they are not susceptible to was recorded from Apra Harbor, Guam, ocean acidification as ‘‘medium-high’’ but no sample or photo was provided importance, to corals. These were rated these threats. Thus, we conclude that an for confirmation. We gathered as the three most important threats to unstudied Astreopora species has some supplemental information, including reef-building corals overall. The studies susceptibility to predation. The SRR Veron (2014), which reports that A. cited above on thermal stress in rated ornamental trade (referred to in cucullata is confirmed in 31 of his 133 Astreopora report moderate levels of the proposed rule as Collection and bleaching in response to warming Trade) as ‘‘low’’ importance to corals Indo-Pacific ecoregions, and strongly events, but low mortality levels. The overall. Although there is no other predicted to be found in an additional studies cited above report variable genus-level or species-specific 15. Astreopora cucullata occurs in most levels of disease in Astreopora. Thus, information on the susceptibilities of reef environments except reef flats we conclude that Astreopora has some Astreopora species to collection and (Lamberts, 1980; Lamberts, 1982; Veron, susceptibility to ocean warming and trade, there is no information suggesting 2000). It has been reported as ‘‘found disease. Although there is no genus- they are not susceptible to these threats. only in deep waters at reef edges’’ level or species-specific information on Thus we conclude that an unstudied (Lamberts, 1980), and is likely to have the susceptibilities of Astreopora Astreopora species is likely to have a depth range of approximately 3 m to species to ocean acidification, the SRR some susceptibility to collection and at least 20 m. Fenner (personal comm.) rated it as ‘‘medium-high’’ importance trade. reports it is on outer reef slopes in to corals. Thus, we conclude that an In conclusion, an unstudied American Samoa. Thus, based on all the unstudied Astreopora species has some Astreopora species is likely to have available information, A. cucullata’s susceptibility to ocean acidification. some susceptibility to ocean warming, habitat includes most coral reef habitats, The SRR rated the trophic effects of disease, ocean acidification, trophic including at least upper reef slopes, fishing as ‘‘medium’’ importance, the effects of fishing, sedimentation, mid-slope terraces, lower reef slopes, fourth most important threat to corals nutrients, sea-level rise, predation, and lower reef crests, and lagoons in depths overall. This threat was not addressed at collection and trade. ranging from two to 20 m depth.

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Demographic Information past 50 to 100 years, but a precise Regulatory Mechanisms The SRR and SIR provided the quantification is not possible based on In the proposed rule, we did not following information on A. cucullata’s the limited species-specific information. provide any species-specific abundance. Astreopora cucullata is Other Biological Information information on the regulatory reported as rare. The SIR reported it is mechanisms or conservation efforts for common in parts of its range such as in The SRR and SIR provided the A. cucullata. Criticisms of our approach American Samoa (Fenner et al., 2008) following information on A. cucullata’s received during public comment led us and Guam (Lamberts, 1982). Astreopora life history. Reproductive characteristics to the following analysis to attempt to cucullata was found in 10 of 51 sites of A. cucullata have not been analyze regulatory mechanisms on a (Donnelly et al., 2003) and four of 39 determined. However, other species in species basis. Records confirm that A. sites (Turak and DeVantier, 2003) in the Astreopora genus (Astreopora cucullata occurs in 31 Indo-Pacific Indonesian national park surveys. gracilis, Astreopora myriophthalma, ecoregions that encompass 30 countries’ The public comments did not provide and Astreopora listeri) are EEZs. The 30 countries are Australia, any new or supplemental information hermaphroditic broadcast spawners. Brunei, China, Djibouti, Egypt, on A. cucullata’s abundance. We The public comments and information Federated States of Micronesia, Fiji, gathered supplemental information, we gathered provided no additional France (French Pacific Island including Veron (2014), which reports biological information. Territories), Indonesia, Israel, Jordan, that A. cucullata occupied 6.8 percent Susceptibility to Threats Malaysia, Marshall Islands, Myanmar, of 2,984 dive sites sampled in 30 New Zealand (Tokelau), Niue, Palau, ecoregions of the Indo-Pacific, and had To describe A. cucullata’s threat Papua New Guinea, Philippines, Samoa, a mean abundance rating of 1.25 on a 1 susceptibilities, the SRR and SIR Saudi Arabia, Solomon Islands, Sudan, to 5 rating scale at those sites in which provided genus-level information for the Thailand, Timor-Leste, Tonga, Tuvalu, it was found. Based on this semi- effects on Astreopora of ocean warming, United States (American Samoa, Guam), quantitative system, the species’ acidification, disease, predation, Vietnam, and Yemen. The regulatory abundance was characterized as sedimentation, nutrients, and collection mechanisms relevant to A. cucullata, ‘‘uncommon,’’ and overall abundance and trade. The SRR and SIR provided described first as the percentage of the was described as ‘‘rare.’’ Veron did not the following species-specific above countries that utilize them to any infer trends in abundance from these information on A. cucullata’s threats. A degree and second, as the percentages of data. As described in the Indo-Pacific single A. cucullata export was reported those countries whose regulatory Species Determinations introduction from Saudi Arabia in 1999. The SRR mechanisms may be limited in scope, above, based on results from Richards et and SIR did not provide any other are as follows: General coral protection al. (2008) and Veron (2014), the absolute species-specific information on the (23 percent with 0 percent limited in abundance of this species is likely at effects of these threats on A. cucullata. scope), coral collection (67 percent with least tens of millions of colonies. We interpreted the threat susceptibility 30 percent limited in scope), pollution Carpenter et al. (2008) extrapolated and exposure information from the SRR control (50 percent with 10 percent species abundance trend estimates from and SIR in the proposed rule for A. limited in scope), fishing regulations on total live coral cover trends and habitat cucullata’s vulnerabilities as follows: reefs (87 percent with 17 percent types. For A. cucullata, the overall High vulnerability to ocean warming, limited in scope), and managing areas decline in abundance (‘‘Percent moderate vulnerability to disease, ocean for protection and conservation (97 Population Reduction’’) was estimated acidification, trophic effects of reef percent with 10 percent limited in at 34 percent, and the decline in fishing, and nutrients, and low scope). The most common regulatory abundance before the 1998 bleaching vulnerability to sedimentation, sea level mechanisms in place for A. cucullata event (‘‘Back-cast Percent Population rise, predation, and collection and trade. are reef fishing regulations and area Reduction’’) was estimated at 13 Public comments did not provide any management for protection and percent. However, as summarized above new or supplemental information on A. conservation. Coral collection and in the Inter-basin Comparison sub- cucullata’s threats, but we gathered pollution control laws are also section, live coral cover trends are species-specific and genus-level somewhat common for the species, but highly variable both spatially and supplemental information on this 30 percent of coral collection laws are temporally, producing patterns on small species’ threat exposures, limited in scope and may not provide scales that can be easily taken out of susceptibilities, and vulnerabilities. substantial protection. General coral context, thus quantitative inferences to Astreopora cucullata has been rated as protection laws are much less common species-specific trends should be moderately or highly susceptible to regulatory mechanisms for the interpreted with caution. At the same bleaching and disease, but these ratings management of A. cucullata. time, an extensive body of literature are not based on species-specific data documents broad declines in live coral (Carpenter et al., 2008). No other Vulnerability to Extinction cover and shifts to reef communities species-specific information is available As explained above in the Risk dominated by hardier coral species or for the susceptibility of A. cucullata to Analyses section, a species’ algae over the past 50 to 100 years any other threat. Based on the available vulnerability to extinction results from (Birkeland, 2004; Fenner, 2012; Pandolfi genus-level and species information the combination of its spatial and et al., 2003; Sale and Szmant, 2012). summarized above, A. cucullata likely demographic characteristics, threat These changes have likely occurred, and has some susceptibilities to ocean susceptibilities, and consideration of the are occurring, from a combination of warming, disease, acidification, trophic baseline environment and future global and local threats. Given that A. effects of fishing, sedimentation, projections of threats. The SRR stated cucullata occurs in many areas affected nutrients, predation, sea-level rise, and that factors that increase the potential by these broad changes, and has some collection and trade. The available extinction risk for A. cucullata are its susceptibility to both global and local information does not support more rarity and that it belongs to a family that threats, we conclude that it is likely to precise ratings of susceptibilities of A. is highly susceptible to stress. It listed have declined in abundance over the cucullata to the threats. factors that reduce the potential

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extinction risk including a widespread because the increasingly severe capacity in the form of absolute distribution and the fact that it appears conditions expected in the foreseeable numbers of colonies and variation in to be less vulnerable to bleaching than future will be non-uniform and susceptibility between individual other species in its family. therefore will likely be a large number colonies. As discussed in the Corals and Subsequent to the proposed rule, we of colonies that are either not exposed Coral Reefs section above, the more received and gathered supplemental or do not negatively respond to a threat colonies a species has, the lower the species- or genus-specific information, at any given point in time. proportion of colonies that are likely to described above, that expands our Listing Determination be exposed to a particular threat at a knowledge regarding the species particular time, and all individuals that abundance, distribution, and threat In the proposed rule using the are exposed will not have the same susceptibilities. We developed our determination tool formula approach, A. response. assessment of the species’ vulnerability cucullata was proposed for listing as Notwithstanding the projections to extinction using all the available threatened because of: High through 2100 that indicate increased information. As explained in the Risk vulnerability to ocean warming (ESA severity over time of the three high Analyses section, our assessment in this Factor E); moderate vulnerability to importance threats, the combination of final rule emphasizes the ability of the disease (C) and acidification (E); these biological and environmental species’ spatial and demographic traits common generalized range wide characteristics indicates that the species to moderate or exacerbate its abundance (E); moderate overall possesses sufficient buffering capacity vulnerability to extinction, as opposed distribution (based on wide geographic to avoid being in danger of extinction to the approach we used in the distribution and shallow depth within the foreseeable future throughout proposed rule, which emphasized the distribution (E); and inadequacy of its range. It is possible that this species’ species’ susceptibility to threats. existing regulatory mechanisms (D). extinction risk may increase in the The following characteristics of A. In this final rule, we changed the future if global threats continue and cucullata, in conjunction with the listing determination for A. cucullata increase in severity and the species information described in the Corals and from threatened to not warranted. We exposure to threats increases throughout Coral Reefs section, Coral Habitat sub- made this determination based on a its range. Should the species experience more species-specific and holistic section, and Threats Evaluation section reduced abundance or range assessment of whether this species above, affect its vulnerability to constriction of a certain magnitude, the meets the definition of either a extinction currently and over the ability of these characteristics to threatened or endangered coral largely foreseeable future. Its geographic moderate exposure to threats will in response to public comments, distribution includes the Red Sea, parts diminish. However, the species is not including more appropriate of the western Indian Ocean, and most likely to become of such low abundance consideration of the buffering capacity of the ecoregions throughout the or so spatially fragmented as to be in of this species’ spatial and demographic western and central Pacific Ocean. Its danger of extinction due to depensatory traits to lessen its vulnerability to geographic distribution moderates processes, the potential effects of threats. Thus, based on the best vulnerability to extinction because some environmental stochasticity, or the areas within its range are projected to available information above on A. potential for mortality from catastrophic have less than average warming and cucullata’s spatial structure, events within the foreseeable future acidification over the foreseeable future, demography, threat susceptibilities, and throughout its range. Therefore, A. including the western Indian Ocean, the management, none of the five ESA cucullata is not warranted for listing at central Pacific, and other areas, so listing factors, alone or in combination, this time under any of the listing factors. portions of the population in these areas are causing this species to be likely to will be less exposed to severe become endangered throughout its range Genus Isopora conditions. Its depth range is from two within the foreseeable future, and thus Genus Introduction to 20 meters. This moderates is not warranted for listing at this time, vulnerability to extinction over the because: The family Acroporidae includes five foreseeable future because deeper areas (1) Astreopora cucullata’s distribution genera, Acropora, Montipora, of its range will usually have lower in the Red Sea, central Indo-Pacific, and Astreopora, Isopora, and Anacropora. irradiance than surface waters, and the central Pacific Ocean is spread over Isopora was formerly considered a sub- acidification is generally predicted to a very large area. While some areas genus of Acropora, but was recently accelerate most in waters that are deeper within its range are projected to be elevated to genus level (Wallace et al., and cooler than those in which the affected by warming and acidification, 2007). The genus contains seven species occurs. Its habitat includes at other areas are projected to have less species, all occurring in the Indo- least upper reef slopes, mid-slope than average warming and acidification, Pacific. Isopora have branching or terraces, lower reef slopes, lower reef including the central Pacific, and other encrusting colonies. The SRR and SIR crests, and lagoons. This moderates areas. This distribution and the provided no genus-level introductory vulnerability to extinction over the heterogeneous habitats it occupies information on Isopora. foreseeable future because the species is reduce exposure to any given threat Genus Susceptibility to Threats not limited to one habitat type but event or adverse condition that does not occurs in numerous types of reef occur uniformly throughout the species The SRR and SIR provided the environments that will, on local and range. As explained above in the following information on the threat regional scales, experience highly Threats Evaluation section, we have not susceptibilities of the genus Isopora. variable thermal regimes and ocean identified any threat that is expected to Isopora cuneata has intermediate chemistry at any given point in time. Its occur uniformly throughout the species bleaching susceptibility relative to other absolute abundance of at least tens of range within the foreseeable future; and acroporids but showed severe losses in millions of colonies, combined with (2) While A. cucullata’s qualitative a 2006 mass bleaching event in the spatial variability in ocean warming and abundance is characterized as rare, its Marshall Islands, with only shaded acidification across the species range, absolute abundance at least tens of bases of colonies surviving. Isopora moderates vulnerability to extinction millions of colonies, providing buffering cuneata was a common species in the

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Acropora palifera zone of the Chagos, personal comm.). There is no Sea-level rise was not addressed at the but I. cuneata was nearly completely information available on the effects of genus or species level in the SRR or SIR. eliminated in 1998 and has not yet any other threat for Isopora species. Increasing sea levels may increase land- regenerated. Competition with algae based sources of pollution due to Genus Conclusion significantly reduces growth rates of I. inundation, resulting in changes to coral cuneata. At high latitude Lord Howe Based on the information from the community structure, thus an unstudied Island, I. cuneata was found to host five SRR, SIR, public comments, and Isopora species is likely to have some types of C zooxanthellae, with an ability supplemental information, we can make susceptibility to sea-level rise. The SRR to host specialized types in turbid the following inferences about the rated predation and ornamental trade environments. The species is also susceptibilities of an unstudied Isopora (referred to in the proposed rule as capable of photo-adapting to low light species to ocean warming, disease, Collection and Trade) as ‘‘low’’ environments by increasing acidification, sedimentation, nutrients, importance to corals overall. Although zooxanthellae density altering trophic effects of fishing, sea-level rise, there is no genus-level or species- photosynthetic mechanisms (dark predation, and collection and trade. The specific information on the reaction enzymes or electron transport SRR rated ocean warming and disease as susceptibilities of Isopora species to rates). ‘‘high’’ importance, and ocean collection and trade, there is no The public comments did not provide acidification as ‘‘medium-high’’ information suggesting they are not any new or supplemental information importance, to corals. These were rated susceptible to these threats. Thus, we on the threat susceptibilities of the as the three most important threats to conclude that an unstudied Isopora genus Isopora. We gathered reef-building corals overall. The studies species has some susceptibility to supplemental information that provided described above report moderate to high collection and trade. the following material. A large study of levels of bleaching in Isopora species in In conclusion, an unstudied Isopora the bleaching responses of over 100 response to warming events. With species is likely to be highly susceptible coral species on the GBR to the 2002 regard to disease, the information above to ocean warming, and to have some bleaching event included three Isopora indicates variable levels (from low to susceptibility to disease, ocean species (Done et al., 2003b). At that high) of disease in Isopora species. acidification, trophic effects of fishing, time, Isopora species were still Thus, we conclude that Isopora is likely sedimentation, nutrients, sea-level rise, considered Acropora species, and they to be highly susceptible to ocean predation, and collection and trade. are listed in the report as Acropora warming and to have some Isopora crateriformis palifera, A. cuneata, and A. susceptibility to disease. Although there brueggemanni, but these three species is no genus-level or species-specific Introduction are now referred to as Isopora palifera, information on the susceptibilities of I. cuneata, and I. brueggemanni. For I. The SRR and SIR provided the Isopora species to ocean acidification, following information on I. palifera, approximately 42 percent of the SRR rated it as ‘‘medium-high’’ the observed colonies were bleached, crateriformis’ morphology and importance to corals. Thus, we conclude taxonomy. Morphology was described resulting in I. palifera being more that an unstudied Isopora species has affected than 43 of the 45 Acropora as solid encrusting plates sometimes some susceptibility to ocean over one meter diameter, and taxonomy species in the study, and one of the 20 acidification. most affected species in the study. For was described as having no taxonomic I. cuneata and I. brueggemanni, The SRR rated the trophic effects of issues. approximately 20 percent of the fishing as ‘‘medium’’ importance, the The public comments and observed colonies for both species were fourth most important threat to corals information we gathered did not bleached, an intermediate bleaching overall. This threat was not addressed at provide any new or supplemental level compared to the 45 Acropora the genus or species level in the SRR or information on morphology, but found species in the study (Done et al., 2003b). SIR, because it is an ecosystem-level that there is a moderate level of In response to a 2008 bleaching event in process. That is, removal of herbivorous taxonomic uncertainty for I. Papua New Guinea, two Pocilloporidae fish from coral reef systems by fishing crateriformis, and that there is a and 14 Acroporidae species (including I. alters trophic interactions by reducing moderate level of species identification brueggemanni) were monitored: five of herbivory on algae, thereby providing a uncertainty for this species. Veron the 16 species had severe or high competitive advantage for space to algae (2014) states that I. crateriformis is ‘‘relative susceptibility’’ to bleaching, over coral. Thus, the SRR did not easily confused with I. cuneata, but (including I. brueggemanni, which was discuss this threat in terms of coral taxa, Veron (2000; 2014), Wallace (1999b) and rated as high). All 29 I. brueggemanni as its effects are difficult to distinguish Wallace et al. (2012) continue to colonies were bleached severely, but between coral genera and species. consider it a valid species, and it can be none were killed (Bonin, 2012). Therefore, an unstudied Isopora species identified by experts (Fenner, 2014b). In a study of coral disease on the GBR, is likely to have some susceptibility to Thus, the distribution and abundance approximately one percent of colonies the trophic effects of fishing. information described below for this of observed Isopora were affected by The SRR rated sedimentation, species is sufficiently reliable (Fenner, Skeletal Eroding Band, the most nutrients, and sea-level rise as ‘‘low- 2014b). prevalent coral disease on the GBR medium’’ importance to corals overall. Spatial Information (Page and Willis, 2007). Isopora had a Although there is no genus-level or disease prevalence of 1% in Indonesia, species-specific information on the The SRR and SIR provided the which was tied for 5th highest among 35 susceptibilities of Isopora species to following information on I. taxa (Haapkyla et al., 2007). Isopora sedimentation or nutrients, the SRR crateriformis’ distribution, habitat, and crateriformis and I. palifera were rated them as ‘‘low-medium’’ depth range. Isopora crateriformis’ affected differently by white diseases in importance to corals. Thus, we conclude distribution is from Sumatra (Indonesia) American Samoa: an outbreak resulted that an unstudied Isopora species has to American Samoa, and there are in low prevalence in I. crateriformis, but some susceptibility to sedimentation reports from the western and central high prevalence in I. palifera (D. Fenner, and nutrients. Indian Ocean that need confirmation.

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The SRR reported that this species is Veron did not infer trends in abundance nutrients, predation, and collection and found most commonly in shallow, high- from these data. As described in the trade. The SRR and SIR did not provide wave energy environments, from low Indo-Pacific Species Determinations any other species-specific information tide to at least 12 meters deep, and has introduction above, based on results on the effects of these threats on I. been reported from mesophotic depths from Richards et al. (2008) and Veron crateriformis. We interpreted threat (<50 m depth). The SIR reported that I. (2014), the absolute abundance of this susceptibility and exposure information crateriformis is one of the most common species is likely at least millions of from the SRR and SIR in the proposed species on upper reef slopes of colonies. rule for I. crateriformis’ vulnerabilities southwest Tutuila, American Samoa. Carpenter et al. (2008) extrapolated as follows: High vulnerability to ocean Rangewide, its predominant habitat is species abundance trend estimates from warming, moderate vulnerability to reef flats and lower reef crests, and it total live coral cover trends and habitat disease, ocean acidification, trophic also occurs in adjacent habitats such us types. For I. crateriformis, the overall effects of reef fishing, and nutrients, and upper reef slopes. decline in abundance (‘‘Percent low vulnerability to sedimentation, sea Public comments did not provide any Population Reduction’’) was estimated level rise, predation, and collection and new or supplemental information on the at 38 percent, and the decline in trade. distribution and habitat of I. abundance before the 1998 bleaching Public comments did not provide any crateriformis. Isopora crateriformis is event (‘‘Back-cast Percent Population new or supplemental information on I. reported from American Samoa (Kenyon Reduction’’) was estimated at 14 crateriformis’ threat susceptibilities. We et al., 2010). Veron (2014) reports that percent. However, as summarized above gathered the following species-specific I. crateriformis is confirmed in 13 of his in the Inter-basin Comparison sub- and genus-level supplemental 133 Indo-Pacific ecoregions, and is section, live coral cover trends are information on this species’ threat strongly predicted to be found in an highly variable both spatially and susceptibilities. Isopora crateriformis is additional 17. Wallace (1999b) reports temporally, producing patterns on small not rated as moderately or highly its occurrence in three of her 29 Indo- scales that can be easily taken out of susceptible to bleaching or disease, but Pacific areas, many of which are larger context, thus quantitative inferences of this rating is not based on species- than Veron’s ecoregions. Richards et al. species-specific trends should be specific data (Carpenter et al., 2008). (2009) calculated the geographic range interpreted with caution. At the same Based on information for the genus of this species at about 11 million km2, time, an extensive body of literature Isopora, an unstudied species such as I. the 35th smallest range of the 114 documents broad declines in live coral crateriformis can be predicted to have species of Acropora and Isopora that cover and shifts to reef communities high susceptibility to ocean warming. she calculated. Worldwide, reef flats dominated by hardier coral species or Fenner (personal comm.) reports seeing have a larger area than reef slopes algae over the past 50 to 100 years a ‘‘white disease’’ or ‘‘tissue loss’’ on I. (Vecsei, 2004). Most coral abundance (Birkeland, 2004; Fenner, 2012; Pandolfi crateriformis that appeared similar to surveys are carried out only on reef et al., 2003; Sale and Szmant, 2012). white syndrome during a brief disease slopes, and thus may significantly These changes have likely occurred, and outbreak in American Samoa, but underestimate the abundance of species are occurring, from a combination of prevalence was low. Since only one such as I. crateriformis that are more global and local threats. Given that I. observation of disease on I. crateriformis common on reef flats than reef slopes. crateriformis occurs in many areas is reported, it is likely that I. crateriformis has some susceptibility to Demographic Information affected by these broad changes, and likely has some susceptibility to both disease. Based on species-specific and The SRR and SIR reported I. global and local threats, we conclude genus-level information described crateriformis’ abundance as sometimes that it is likely to have declined in above, I. crateriformis likely is highly common and occasionally locally abundance over the past 50 to 100 years, susceptible to ocean warming and likely abundant. Isopora crateriformis has but a precise quantification is not has some susceptibility to disease, been reported as common in Indonesia possible based on the limited species- ocean acidification, trophic effects of (Veron, 2000) and as one of the most specific information. fishing, sedimentation, nutrients, sea- prevalent corals in American Samoa level rise, predation, and collection and (Birkeland et al., 1987). Other Biological Information trade. The available information does Public comments did not provide The SRR and SIR provided the not support more precise ratings of the information on the abundance of I. following information on I. susceptibilities of I. crateriformis to the crateriformis. We gathered crateriformis’ life history. Isopora threats. supplemental information, which crateriformis is not prone to asexual Regulatory Mechanisms includes the following. Richards et al. reproduction via fragmentation, based (2013b) conclude from their data that on its semi-encrusting morphology. In the proposed rule, we did not this species is globally widespread, Supplemental information we gathered provide any species-specific locally restricted, and locally rare, and added that, while I. crateriformis often information on the regulatory thus in the second rarest category with has a lower plate edge on colonies on mechanisms or conservation efforts for the predicted consequence of local slopes, colonies are very hard and thus I. crateriformis. We received criticism of extinction. Veron (2014) reports that I. unlikely to fragment often (D. Fenner, that approach in public comments and crateriformis occupied 0.3 percent of personal comm.). Public comments did in response we present a species- 2,984 dive sites sampled in 30 not provide anything additional to the specific analysis of regulatory ecoregions of the Indo-Pacific, and had above-described biological information. mechanisms in this final rule. Records a mean abundance rating of 1.4 on a 1 confirm that I. crateriformis occurs in 13 to 5 rating scale at those sites in which Susceptibility to Threats Indo-Pacific ecoregions that encompass it was found. Based on this semi- To describe I. crateriformis’ threat 17 countries’ EEZs. The 17 countries are quantitative system, the species’ susceptibilities, the SRR and SIR Australia, Brunei, Fiji, France (French abundance was characterized as ‘‘rare.’’ provided genus-level information for the Pacific Island Territories), Indonesia, Overall abundance was described as effects on Isopora of ocean warming, Kiribati, Malaysia, New Zealand ‘‘occasionally common on reef flats.’’ acidification, disease, sedimentation, (Tokelau), Niue, Papua New Guinea,

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Philippines, Samoa, Solomon Islands, The following characteristics of I. number of colonies that are either not Timor-Leste, Tonga, Tuvalu, and the crateriformis, in conjunction with the exposed or do not negatively respond to United States (American Samoa). The information described in the Corals and a threat at any given point in time. regulatory mechanisms relevant to I. Coral Reefs section, Coral Habitat sub- However, its qualitative abundance is crateriformis, described first as the section, and Threats Evaluation section described as rare, which combined with percentage of the above countries that above, affect its vulnerability to its restricted depth distribution utilize them to any degree and second, extinction currently and over the indicates it is likely that a high as the percentage of those countries foreseeable future. Its geographic range proportion of individuals will be whose regulatory mechanisms may be extends from Sumatra (Indonesia) to affected by threats that are typically limited in scope, are as follows: General American Samoa, and the Philippines to more severe in shallow habitats at any coral protection (41 percent with none the GBR. On one hand, this moderates given point in time. limited in scope), coral collection (82 vulnerability to extinction because the Listing Determination percent with 35 percent limited in central Pacific portion of its range is scope), pollution control (53 percent projected to have less than average In the proposed rule using the determination tool formula, I. with 12 percent limited in scope), warming over the foreseeable future, crateriformis was proposed for listing as fishing regulations on reefs (100 percent thus population in these areas will be threatened because of: High with 24 percent limited in scope), and less exposed to severe warming vulnerability to ocean warming (ESA managing areas for protection and conditions. On the other hand, the Factor E); moderate vulnerability to conservation (100 percent with none species’ geographic distribution limited in scope). The most common disease (C) and acidification (E); exacerbates vulnerability to extinction common generalized range wide regulatory mechanisms in place for I. because much of it lies within the crateriformis are reef fishing regulations abundance (E); moderate overall western equatorial Pacific, an area distribution (based on moderate and area management for protection and projected to have the highest seawater conservation. Coral collection and geographic distribution and moderate temperatures in the foreseeable future. depth distribution (E); and inadequacy pollution control laws are also common Its depth range is from zero to 12 for the species, but 35 percent of coral of existing regulatory mechanisms (D). meters. On one hand, its depth range In this final rule, we confirmed our collection laws are limited in scope and may moderate vulnerability to listing determination for I. crateriformis may not provide substantial protection. extinction over the foreseeable future as threatened. Based on the best General coral protection laws are the because deeper areas of its range will available information provided above on least common regulatory mechanisms usually have lower irradiance than I. crateriformis’ spatial structure, for the management of I. crateriformis. surface waters, and acidification is demography, threat susceptibilities, and Vulnerability to Extinction generally predicted to accelerate most in management, it is likely to become waters that are deeper and cooler than endangered throughout its range within As explained above in the Risk those in which the species occurs. On the foreseeable future, and thus Analyses section, a species’ the other hand, its depth range may warrants listing as threatened at this vulnerability to extinction results from exacerbate vulnerability to extinction time, because: the combination of its spatial and over the foreseeable future if the species (1) Isopora crateriformis is highly demographic characteristics, threat occurs predominantly in the shallower susceptible to ocean warming (ESA susceptibilities, and consideration of the portion of its depth range, since those Factor E), and susceptible to disease (C), baseline environment and future areas will have higher irradiance and acidification (E), trophic effects of projections of threats. The SRR stated thus be more severely affected by fishing (A), and nutrients (A, E), and that factors that increase the risk of warming-induced bleaching. Its habitat predation (C). In addition, existing extinction were the high susceptibility includes at least reef flats, lower reef regulatory mechanisms to address global to threats inferred to be common to crests, and upper reef slopes. This threats that contribute to extinction risk members of the family Acroporidae. It moderates vulnerability to extinction for this species are inadequate (D); listed factors that reduce the risk of over the foreseeable future because the (2) The majority of Isopora extinction including its prevalence in species is not limited to one habitat type crateriformis’ distribution is within the areas of heavy wave action as water but occurs in numerous types of reef Coral Triangle and western equatorial motion can reduce bleaching environments that will, on local and Pacific, which is projected to have the vulnerability. regional scales, experience highly most rapid and severe impacts from Subsequent to the proposed rule, we variable thermal regimes and ocean climate change and localized human received and gathered supplemental chemistry at any given point in time. impacts for coral reefs over the 21st species- or genus-specific information, Shallow areas may experience more century, as described in the Threats described above, that expands our frequent changing environmental Evaluation. Multiple ocean warming knowledge regarding the species conditions, extremes, high irradiance, events have already occurred within the abundance, distribution, and threat and multiple simultaneous stressors, western equatorial Pacific that suggest susceptibilities. We developed our however, high energy environments future ocean warming events may be assessment of the species’ vulnerability experience high levels of mixing which more severe than average in this part of to extinction using all the available can dilute adverse environmental the world. A range constrained to this information. As explained in the Risk conditions. Its absolute abundance of at particular geographic area that is likely Analyses section, our assessment in this least millions of colonies, combined to experience severe and increasing final rule emphasizes the ability of the with spatial variability in ocean threats indicates that a high proportion species’ spatial and demographic traits warming and acidification across the of the population of this species is likely to moderate or exacerbate its species range, moderates vulnerability to be exposed to those threats over the vulnerability to extinction, as opposed to extinction because the increasingly foreseeable future; and to the approach we used in the severe conditions expected in the (3) Isopora crateriformis’ qualitative proposed rule, which emphasized the foreseeable future will be non-uniform abundance is rare overall. Considering species’ susceptibility to threats. and therefore will likely be a large that much of the range of this species

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includes areas where severe and proportion of its population from shallow, high wave-energy increasing impacts are predicted, this catastrophic events. environments. Its predominant habitat level of abundance combined with its The combination of these biological is high energy environments such as restricted depth distribution, leaves the and environmental characteristics lower reef crests and reef flats, but it is species vulnerable to becoming of such indicates that the species does not also found in upper reef slopes, lagoons, low abundance within the foreseeable exhibit the characteristics of one that is and adjacent habitats. Its depth range is future that it may be at risk from currently in danger of extinction, as low tide to 15 meters deep. depensatory processes, environmental described previously in the Risk Public comments provided the stochasticity, or catastrophic events, as Analyses section, and thus does not following information. One public explained in more detail in the Corals warrant listing as endangered at this comment stated that I. cuneata is widely and Coral Reefs and Risk Analyses time. distributed in Indonesian waters. We sections. Range-wide, a multitude of gathered supplemental information, The combination of these biological conservation efforts are already broadly including Veron (2014) which reports and environmental characteristics and employed that are likely benefiting I. that I. cuneata is confirmed in 43 of his future projections of threats indicates crateriformis. However, considering the 133 Indo-Pacific ecoregions, and is that the species is likely to be in danger global scale of the most important strongly predicted to be found in an of extinction within the foreseeable threats to the species, and the additional nine. Wallace (1999b) reports future throughout its range and warrants ineffectiveness of conservation efforts at it from 11 of her 29 Indo-Pacific areas, listing as threatened at this time due to addressing the root cause of global many of which are larger than Veron’s factors A, C, D, and E. threats (i.e., GHG emissions), we do not ecoregions. Richards et al. (2009) The available information above on I. believe that any current conservation calculated the geographic range of I. crateriformis’ spatial structure, efforts or conservation efforts planned cuneata at 27 million km2, which was demography, threat susceptibilities, and in the future will result in affecting the the 45th smallest among the 114 management also indicate that the species status to the point at which Acropora species for which ranges were species is not currently in danger of listing is not warranted. calculated. extinction and thus does not warrant listing as Endangered because: Isopora cuneata Demographic Information (1) While I. crateriformis’ distribution Introduction is mostly in the Coral Triangle and The SRR and SIR reported I. cuneata’s western equatorial Pacific, which The SRR and SIR provided the abundance as generally common, increases it extinction risk as described following information on I. cuneata’s occasionally locally abundant, and by above, its habitat includes at least reef morphology and taxonomy. Morphology far the most predominant of acroporids flats, lower reef crests, and upper reef was described as sometimes flattened on some areas of the Great Barrier Reef. slopes. This moderates vulnerability to solid encrusting plates like Isopora Public comments provided the extinction currently because the species crateriformis, but usually also forms following information. One public is not limited to one habitat type but ‘‘Mohawk’’ ridges parallel to the main comment stated that I. cuneata is very occurs in numerous types of reef wave motion or short flattened blades. abundant in all Indonesian waters. We environments that will, on local and Taxonomy was described as having no gathered supplemental information regional scales, experience highly taxonomic issues. which included the following. variable thermal regimes and ocean Public comments and information we Worldwide, reef flats have a larger area chemistry at any given point in time, as gathered provided the following than reef slopes (Vecsei, 2004). Most described in more detail in the Coral information on the morphology or coral abundance surveys are carried out Habitat and Threats Evaluation sections. taxonomy of I. cuneata. Isopora cuneata only on reef slopes, and thus may (2) While I. crateriformis’ depth range has moderate taxonomic uncertainty, significantly underestimate the is primarily restricted to shallow and moderate species identification abundance of species such as I. cuneata habitats from zero to 12 meters, it has uncertainty (Fenner, 2014b). Veron that are more common on reef flats and been reported from 50 meters in (2014) states that I. cuneata is easily crests than reef slopes. Richards et al. American Samoa. This moderates confused with I. palifera which it (2013b) consider this to be a species that vulnerability to extinction over the closely resembles, but Veron (2000; is globally widespread, locally foreseeable future because there may be 2014), Wallace (1999a) and Wallace et restricted, and locally rare, and thus in depth refugia for I. crateriformis in some al. (2012) continue to consider it a valid the second rarest category with the parts of its range from threats that are species, and it can be identified by predicted consequence of local typically more severe in shallow experts (Fenner, 2014b). Thus, we extinction. Veron (2014) reports that I. habitats. conclude that the distribution and cuneata occupied 5.1 percent of 2,984 (3) Even though this species is abundance information described below dive sites sampled in 30 ecoregions of considered rare, the absolute abundance for this species is sufficiently reliable the Indo-Pacific, and had a mean of I. crateriformis is at least millions of (Fenner, 2014b). abundance rating of 1.76 on a 1 to 5 colonies. In addition, it is ‘‘occasionally rating scale at those sites in which it common on reef flats,’’ a habitat type Spatial Information was found. Based on this semi- that has larger area than reef slopes. The SRR and SIR provided the quantitative system, the species’ There is no evidence of depensatory following information on I. cuneata’s abundance was characterized as processes such as reproductive failure distribution, habitat, and depth range. ‘‘uncommon.’’ Overall abundance was from low density of reproductive Isopora cuneata’s distribution is from described as ‘‘uncommon.’’ Veron did individuals and genetic processes such the east coast of Africa to the central not infer trends in abundance from as inbreeding affecting this species. Pacific. One expert source does not these data. As described in the Indo- Thus, its absolute abundance indicates recognize records from east Africa Pacific Species Determinations it is currently able to avoid high (Riegl, 1995), and the SRR questions introduction above, based on results mortality from environmental whether they should be checked. The from Richards et al. (2008) and Veron stochasticity, and mortality of a high SRR reported that I. cuneata’s habitat is (2014), the absolute abundance of this

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species is likely at least tens of millions effects on Isopora of ocean warming, species-specific information is available of colonies. acidification, disease, sedimentation, for the susceptibility of I. cuneata to any Carpenter et al. (2008) extrapolated nutrients, predation, and collection and other threat. Based on genus-level and species abundance trend estimates from trade. The SRR and SIR also provided species information, I. cuneata is total live coral cover trends and habitat the following species-specific predicted to likely be highly susceptible types. For I. cuneata, the overall decline information on I. cuneata’s threats. to ocean warming and to have some in abundance (‘‘Percent Population Isopora cuneata showed intermediate susceptibility to disease, acidification, Reduction’’) was estimated at 37 bleaching susceptibility relative to other trophic effects of fishing, nutrients, percent, and the decline in abundance acroporids on the Great Barrier Reef in sedimentation, sea-level rise, predation, before the 1998 bleaching event (‘‘Back- 2002, but showed severe losses in a and collection and trade. cast Percent Population Reduction’’) 2006 mass bleaching event in the Regulatory Mechanisms was estimated at 15 percent. However, Marshall Islands, with only shaded as summarized above in the Inter-basin bases of colonies surviving. Isopora In the proposed rule, we did not Comparison sub-section, live coral cover cuneata was a common species in the provide any species-specific trends are highly variable both spatially Acropora palifera zone of the Chagos, information on the regulatory and temporally, producing patterns on but I. cuneata was nearly completely mechanisms or conservation efforts for small scales that can be easily taken out eliminated in 1998 and has not yet I. cuneata. We received criticism of that of context, thus quantitative inferences regenerated. Competition with algae approach in public comments and in of species-specific trends should be significantly reduces growth rates of I. response we present a species-specific interpreted with caution. At the same cuneata. At high latitude Lord Howe analysis of regulatory mechanisms in time, an extensive body of literature Island, I. cuneata was found to host five this final rule. Records confirm that I. documents broad declines in live coral types of C zooxanthellae, with an ability cuneata occurs in 43 Indo-Pacific cover and shifts to reef communities to host specialized types in turbid ecoregions that encompass 23 countries’ dominated by hardier coral species or environments. The species is also EEZs. The 23 countries are Australia, algae over the past 50 to 100 years capable of photo-adapting to low light China, Federated States of Micronesia, (Birkeland, 2004; Fenner, 2012; Pandolfi environments by increasing Fiji, France (French Pacific Island et al., 2003; Sale and Szmant, 2012). zooxanthellae density altering Territories), Indonesia, Japan, These changes have likely occurred, and photosynthetic mechanisms (dark Madagascar, Mauritius, New Zealand are occurring, from a combination of reaction enzymes or electron transport (Tokelau), Niue, Palau, Papua New global and local threats. Given that I. rates). The SRR and SIR did not provide Guinea, Philippines, Samoa, Solomon cuneata occurs in many areas affected any other species-specific information Islands, Taiwan, Timor-Leste, Tonga, by these broad changes, and likely has on the effects of these threats on I. Tuvalu, United States (American some susceptibility to both global and cuneata. We interpreted threat Samoa, PRIAs), Vanuatu, and Vietnam. local threats, we conclude that it is susceptibility and exposure information The regulatory mechanisms relevant to likely to have declined in abundance from the SRR and SIR in the proposed I. cuneata, described first as the over the past 50 to 100 years, but a rule for I. cuneata as follows: High percentage of the above countries that precise quantification is not possible vulnerability to ocean warming, utilize them to any degree and second, due to the limited species-specific moderate vulnerability to disease, as the percentage of those countries information. acidification, trophic effects of fishing, whose regulatory mechanisms may be and nutrients, and low vulnerability to limited in scope, are as follows: General Other Biological Information sedimentation, sea-level rise, predation, coral protection (35 percent with four The SRR and SIR provided the and collection and trade. percent limited in scope), coral following information on I. cuneata’s Public comments did not provide any collection (65 percent with 30 percent life history. Isopora cuneata is a new or supplemental information on I. limited in scope), pollution control (39 simultaneous hermaphroditic brooder. cuneata’s threats susceptibilities. We percent with 13 percent limited in Larvae lack zooxanthellae, and in some gathered the following species-specific scope), fishing regulations on reefs (100 areas the species can undergo several and genus-level supplemental percent with 13 percent limited in seasonal cycles of larval production. Its information on this species’ threat scope), and managing areas for brooding life history allows Isopora susceptibilities. Isopora cuneata has protection and conservation (100 species to locally dominate recruitment been rated as moderately or highly percent with none limited in scope). at Lord Howe Island, Australia; colonies susceptible to bleaching, but this rating The most common regulatory of this genus also dominate the adult is not based on species-specific data mechanisms in place for I. cuneata are population there, suggesting brooding (Carpenter et al., 2008). Done et al. reef fishing regulations and area may drive community structure in (2003b) reported that 20 percent of I. management for protection and remote areas. Isopora cuneata is not cuneata colonies on the GBR were conservation. Coral collection laws are prone to asexual reproduction via affected by bleaching in 2002, and the also somewhat common for the species, fragmentation, based on its semi- species ranked 21st in proportion of but 30 percent of coral collection laws encrusting morphology. The species coral colonies that were bleached or are limited in scope and may not shows moderate gene flow but little partially killed out of 52 studied provide substantial protection. General potential for large-scale dispersal. Acropora and Isopora species. That is, coral protection and pollution control Public comments and information we 20 of the 52 species bleached more than laws are much less common regulatory gathered did not provide anything I. cuneata and 31 bleached less. mechanisms for the management of I. additional to the above-described Isopora cuneata has been rated as cuneata. biological information. moderately or highly susceptible to disease, but this rating is not based on Vulnerability to Extinction Susceptibility to Threats species-specific data (Carpenter et al., As explained above in the Risk To describe I. cuneata’s threat 2008). Willis et al. (2004) report Black Analyses section, a species’ susceptibilities, the SRR and SIR Band Disease on I. cuneata on No Name vulnerability to extinction results from provided genus-level information for the Reef in the Great Barrier Reef. No other the combination of its spatial and

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demographic characteristics, threat bleaching. Its habitat includes at least are projected to be affected by warming susceptibilities, and consideration of the lower reef crests, reef flats, upper reef and acidification, other areas are baseline environment and future slopes, and lagoons. This moderates projected to have less than average projections of threats. The SRR stated vulnerability to extinction over the warming and acidification, including that factors that increase potential foreseeable future because the species is the western Indian Ocean, the central extinction risk for I. cuneata are high not limited to one habitat type but Pacific, and other areas. This susceptibility to threats inferred to be occurs in numerous types of reef distribution and the heterogeneous common to members of the family environments that will, on local and habitat it occupies reduce exposure to Acroporidae. A factor that reduces regional scales, experience highly any given threat event or adverse potential extinction risk is its variable thermal regimes and ocean condition that does not occur uniformly prevalence in areas of heavy wave chemistry at any given point in time. In throughout the species range. As action, as water motion may reduce addition, high energy environments bleaching vulnerability. experience high levels of mixing which explained above in the Threats Subsequent to the proposed rule, we can dilute adverse environmental Evaluation section, we have not received and gathered supplemental conditions. Its absolute abundance of at identified any threat that is expected to species- or genus-specific information, least tens of millions of colonies, occur uniformly throughout the species described above, that expands our combined with spatial variability in range within the foreseeable future); knowledge regarding the species ocean warming and acidification across (2) Isopora cuneata’ absolute abundance, distribution, and threat the species range, moderates abundance is at least tens of millions of susceptibilities. We developed our vulnerability to extinction because the colonies, providing buffering capacity in assessment of the species’ vulnerability increasingly severe conditions expected the form of absolute numbers of to extinction using all the available in the foreseeable future will be non- colonies and variation in susceptibility information. As explained in the Risk uniform and therefore will likely be a between individual colonies. As Analyses section, our assessment in this large number of colonies that are either discussed in the Corals and Coral Reefs final rule emphasizes the ability of the not exposed or do not negatively section above, the more colonies a species’ spatial and demographic traits respond to a threat at any given point species has, the lower the proportion of to moderate or exacerbate its in time. vulnerability to extinction, as opposed colonies that are likely to be exposed to to the approach we used in the Listing Determination a particular threat at a particular time, proposed rule, which emphasized the In the proposed rule using the and all individuals that are exposed will species’ susceptibility to threats. determination tool formula approach, I. not have the same response; and The following characteristics of I. cuneata was proposed for listing as (3) It is a broadcast spawner and fast cuneata, in conjunction with the threatened because of: High grower, enhancing recovery potential information described in the Corals and vulnerability to ocean warming (ESA from mortality events as described in Coral Reefs section, Coral Habitat sub- Factor E); moderate vulnerability to the Corals and Coral Reefs section section, and Threats Evaluation section disease (C) and acidification (E); above. above, affect its vulnerability to common generalized range wide extinction currently and over the abundance (E); moderate overall Notwithstanding the projections foreseeable future. Its geographic distribution (based on wide geographic through 2100 that indicate increased distribution includes most of the coral distribution and shallow depth severity over time of the three high reef ecoregions in the Indian Ocean and distribution (E); and inadequacy of importance threats, the combination of western and central Pacific Ocean. Its existing regulatory mechanisms (D). these biological and environmental geographic distribution moderates In this final rule, we changed the characteristics indicates that the species vulnerability to extinction because some listing determination for I. cuneata from possesses sufficient buffering capacity areas within its range are projected to threatened to not warranted. We made to avoid being in danger of extinction have less than average warming and this determination based on a more within the foreseeable future throughout acidification over the foreseeable future, species-specific and holistic assessment its range. It is possible that this species’ including the western Indian Ocean, the of whether this species meets the extinction risk may increase in the central Pacific, and other areas, so definition of either a threatened or future if global threats continue and portions of the population in these areas endangered coral largely in response to worsen in severity and the species’ public comments, including more will be less exposed to severe exposure to the threats increases appropriate consideration of the conditions. Its depth range is from low throughout its range. Should the species tide to at least 15 meters. On one hand, buffering capacity of this species’ spatial experience reduced abundance or range its depth range may moderate and demographic traits to lessen its constriction of a certain magnitude, the vulnerability to extinction over the vulnerability to threats. Thus, based on foreseeable future because deeper areas the best available information above on ability of these characteristics to of its range will usually have lower I. cuneata’s spatial structure, moderate exposure to threats will irradiance than surface waters, and demography, threat susceptibilities, and diminish. However, the species is not acidification is generally predicted to management, none of the five ESA likely to become of such low abundance accelerate most in waters that are deeper listing factors, alone or in combination, or so spatially fragmented as to be in and cooler than those in which the are causing this species to be likely to danger of extinction due to depensatory species occurs. On the other hand, its become endangered throughout its range processes, the potential effects of depth range may exacerbate within the foreseeable future, and thus environmental stochasticity, or the vulnerability to extinction over the it is not warranted for listing at this potential for mortality from catastrophic foreseeable future if the species occurs time, because: events within the foreseeable future predominantly in the shallower portion (1) Isopora cuneata’s distribution throughout its range. Therefore, I. of its depth range, since those areas will across the Indian Ocean and most of the cuneata is not warranted for listing at have higher irradiance and thus be more Pacific Ocean is spread over a very large this time under any of the listing factors. severely affected by warming-induced area. While some areas within its range

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Genus Montipora genera and species ranging from none to M. tuberculosa were partly bleached, very high, and mortality from none to and in 2010 all colonies were bleached. Genus Introduction near 100 percent (Bruno et al., 2001). In It was the 10th most bleached species The SRR and SIR provided an Kenya in 1998, unprotected and out of 24 species in 1998, and was tied introduction to Indo-Pacific Montipora, protected sites were compared, and it with seven other species out of 24 for covering geological history, taxonomy, was found that all Montipora species in most bleached in 2010. After the 1998 life history, and threat susceptibilities of unprotected sites died during the mass bleaching event, 75 percent of M. the genus as a whole. Montipora bleaching event while only half of the tuberculosa colonies had partial colonies are usually laminar, encrusting, Montipora species in marine protected mortality, and after the 2010 event all massive, or branching, and usually have areas died (McClanahan et al., 2001). In colonies were dead. In 1998 it was tied small protrusions between corallites, 1998 in Kenya, Tanzania, Mozambique, for third place in mortality, and in 2010 called papillae, tuberculae, or verrucae. and Madagascar, 100 percent of M. it was in a three-way tie for most The genus Montipora is the second tuberculosa colonies were affected by mortality (Sutthacheep et al., 2013). In largest genus of reef corals, with 75 bleaching at the peak of bleaching, and Kenya in 1998, 47 percent of Montipora species currently recognized, all in the 13 percent of the colonies died by the colonies bleached, and of those, 73 Indo-Pacific. end of the bleaching event (Obura, percent died. Mortality was the fifth Genus Susceptibility to Threats 2001). In Raiatea, French Polynesia, in highest of any coral genus. The 2002, 53 percent of Montipora abundance of Montipora after 1998 in The SRR and SIR provided the tuberculosa colonies and 18 percent the western Indian Ocean decreased following information on genus-level Montipora caliculata colonies were strongly in proportion to the number of threat susceptibilities for Montipora. bleached respectively, the third and degree heating weeks in 1998 Montipora has a high susceptibility to fifth most bleached species of the 11 bleaching, just below Acropora and (McClanahan et al., 2007b). In Japan, coral species included in the study one species of Montipora was a long- Millepora. One species of Montipora has (Hughes et al., 2003). been tested for susceptibility to term winner following mass bleaching On the GBR in 2002, 18 species of events (increasing from 0.2 percent to 2 acidification, and was predicted to have Montipora ranged from zero to 77 10 to 15 percent reductions in growth to percent cover), one species was a short percent affected by bleaching (Done et term loser but a long term winner pH by 2100. Montipora species have al., 2003b). During mass bleaching in moderate susceptibility to diseases. (decreasing from 1.8 percent to zero 1998, Montipora had a higher bleaching percent, and then increasing to 3.3 Montipora has been characterized as a index in Kenya (64) than in Australia ‘‘sediment-intolerant’’ genus, but percent later), and one species was a (38), but seawater temperatures were long-term loser (decreasing from 1.6 individual species range from tolerant to higher in Kenya (McClanahan et al., intolerant. Elevated nutrients have not percent to zero percent cover and 2004). At Mauritius in a bleaching event staying there) (van Woesik et al., 2011). been found to affect Montipora in 2004, Montipora had a bleaching fecundity or fertilization. Crown-of- index of 27, the 8th highest of the 32 With regard to disease, a very low thorns seastar prey preferentially on genera recorded, which was 41 percent level of Black Band Disease was found Montipora and crown-of-thorns seastar of the index of the genus with the on Montipora on the Great Barrier Reef, outbreaks can cause substantial highest index (McClanahan et al., just 3 percent of the level on staghorn mortality. The genus Montipora is 2005a). In the western Indian Ocean in Acropora (Page and Willis, 2006). heavily used in the international 1998–2005, Montipora had a bleaching Montipora had a low susceptibility to aquarium trade. index of 7.9 for eight countries, which Skeletal Eroding Band in the GBR, with The public comments did not provide was 34th highest of the 45 genera a prevalence of 0.4 percent. Skeletal any supplemental information on genus- recorded, and 19 percent of the highest Eroding Band is the most prevalent level threat susceptibilities for Indo- value (McClanahan et al., 2007a). On disease on the GBR (Page and Willis, Pacific Montipora. We gathered Howland and Baker islands in the U.S. 2007). Montipora was had the second supplemental information, which Pacific in early 2010, Montipora had a lowest rate of disease in American provides the following genus-level low percentage of bleaching with zero Samoa of the five genera with the most information on threat susceptibilities of percent bleached on Baker and 4.8 disease in American Samoa, with 0.08 Indo-Pacific Montipora for ocean percent on Howland. Montipora was the percent prevalence. The highest rate of warming (thermal stress), coral disease, 13th most bleached genus out of 14 disease was Acropora with 0.39 percent ocean acidification, and predation. With genera reported, with 4 percent as much prevalence. About 14 percent of sites in regard to thermal stress, almost all bleaching as the most bleached genus American Samoa have growth Montipora on the reef flats of two (Vargas-Angel et al., 2011). In a mass anomalies recorded on Montipora, islands in the Thousand Islands of bleaching event in Western Australia, compared to 71 percent for white Indonesia died in the 1983 El Nino mass Acropora had the highest mortality, syndrome on Acropora, so disease is bleaching. A branching species, with Montipora having the second relatively low on Montipora in Montipora digitata, subsequently highest mortality (87 percent), while American Samoa (Fenner and Heron, recovered on one island but not the massive and encrusting corals (such as 2008). Montipora had the fourth highest other (Brown and Suharsono, 1990). In Porites and faviids) had much higher prevalence of disease of coral genera in Moorea in 1998, Montipora was the survival rates. Colonies less than 10 cm American Samoa at 0.06 percent, with third most affected genus by bleaching in size were not killed (Depczynski et the highest being Acropora at 0.85 after Montastraea and Acropora, and al., 2012). percent (Aeby et al., 2008). In Guam, second in mortality, with slightly less In Okinawa, Japan, Montipora species Montipora had the fourth highest mortality than Acropora (Gleason, experienced moderate drops in prevalence out of 12 genera, with 2 1993). In Palau in 2000, many but not populations following the 1998 and percent of colonies having disease all Montipora species had heavy 2010 mass bleaching episodes (Hongo compared to 6.7% for the highest genus bleaching. In that event, 48 percent of and Yamano, 2013). At Laem Set at (Myers and Raymundo, 2009). In New all coral colonies of all species were Samui Island in the western Gulf of Caledonia, Montipora was tied for bleached, with bleaching of different Thailand in 1998, half of all colonies of lowest disease prevalence among 12

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genera, with less than 0.1 percent SIR, because it is an ecosystem-level bases with short branches that form prevalence (Tribollet et al., 2011). In process. That is, removal of herbivorous compact clumps and are pale brown in Indonesia, Montipora had the eighth fish from coral reef systems by fishing color. Genetic evidence places M. highest prevalence of disease out of 35 alters trophic interactions by reducing angulata in a clade with some other taxa, with 0.5 percent prevalence herbivory on algae, thereby providing a Montipora species, depending on which compared to 8 percent for the highest competitive advantage for space to algae gene is used. The SRR treated M. taxon (Haapkyla et al., 2007). over coral. Thus, the SRR did not angulata as a valid species. With regards to predation, Montipora discuss this threat in terms of coral taxa, The public comments and was the third most preferred prey of as its effects are difficult to distinguish information we gathered did not crown-of-thorns starfish out of the 10 between coral genera and species. provide information on morphology, most common genera on 15 reefs in the Therefore, an unstudied Montipora and confirmed that the species has low Great Barrier Reef, with a preference species is likely to have some uncertainty in morphological taxonomy. estimate 81 percent as high as the susceptibility to the trophic effects of Clustering with other species in an highest genus (Acropora) (De’ath and fishing. initial genetics study gives moderate Moran, 1998). With regards to The SRR rated sedimentation, uncertainty. There is a moderate level of sedimentation, M. aequituberculata was nutrients, and sea-level rise as ‘‘low- species identification uncertainty for the poorest species of 22 at clearing medium’’ importance to corals overall. this species, but Veron (2014) states that sediment off itself (Stafford-Smith, Montipora has been called a ‘‘sediment- M. angulata is distinctive and Veron 1993). intolerant’’ genus but there are (2000; 2014), considers the species valid, and that it is sufficiently Genus Conclusion variations in tolerance between species. We conclude that Montipora has some distinctive to be identified by experts Based on the information from the susceptibility to sedimentation. (Fenner, 2014b). Thus, we conclude that SRR, SIR, public comments, and Elevated nutrients have had no effect on the distribution and abundance supplemental information, we can make fecundity or fertilization success in information described below for this the following inferences about the Montipora, but competition with algae species is sufficiently reliable (Fenner, susceptibilities of an unstudied reduced settlement and survival of 2014b). Montipora species to ocean warming, Montipora larvae. We conclude that Spatial Information disease, acidification, sedimentation, Montipora has some susceptibility to nutrients, trophic effects of fishing, sea- nutrients. Sea-level rise was not The SRR and SIR provided the level rise, predation, and collection and addressed at the genus or species level following information on M. angulata’s trade. The SRR rated ocean warming in the SRR or SIR. Increasing sea levels distribution, habitat and depth. and disease as ‘‘high’’ importance, and may increase land-based sources of Montipora angulata’s distribution is ocean acidification as ‘‘medium-high’’ pollution due to inundation, resulting in from the northern and eastern Indian importance, to corals. These were rated changes to coral community structure, Ocean to the central Indo-Pacific to the as the three most important threats to thus an unstudied Montipora species is central Pacific. Its habitat includes reef-building corals overall. Most likely to have some susceptibility to sea- upper reef slopes, mid-slopes, lower reef studies report that the genus Montipora level rise. The little available crests, and reef flats, and its depth shows high rates of bleaching from information on predation of Montipora distribution is one to 20 m. ocean warming, almost as much as The public comments did not provide suggest that predators prefer to eat Acropora and Millepora. However, there any new or supplemental information Montipora over most other genera. was a range of bleaching responses on M. angulata’s distribution. We Thus, it is possible to predict that an reported for the genus Montipora, and a gathered supplemental information, unstudied Montipora species is likely to study of individual species showed a including Veron (2014), which reports have some susceptibility to predation. wide range of bleaching responses that this species is confirmed in 34 of The SRR rated ornamental trade between species, with some not his 133 Indo-Pacific ecoregions, and (referred to in the proposed rule as bleaching at all. While there is strongly predicted to be found in an Collection and Trade) as ‘‘low’’ variability in the available information additional 26. on the susceptibility of Montipora importance to corals overall, and this species to ocean warming, most of the threat was addressed at both the genus Demographic Information information suggests high susceptibility. and species levels in the SRR. Because The SRR and SIR provided the Thus, we conclude that an unstudied Montipora species are some of the more following information on M. angulata’s species of Montipora likely is highly popular coral species to be collected abundance. Montipora angulata’s susceptible to ocean warming. and traded, an unstudied Montipora abundance is mostly rare. Montipora has been reported to have species is likely to have some The public comments did not provide low to moderate rates of disease, thus susceptibility to collection and trade. any new or supplemental information we conclude that Montipora is likely to In conclusion, an unstudied on M. angulata’s abundance. We have some susceptibility to disease. One Montipora species is likely to have high gathered supplemental information, species of Montipora showed a susceptibility to ocean warming, and which provided the following reduction in growth at the acidification some susceptibility to disease, ocean information. Worldwide, reef flats have level anticipated for the end of the acidification, trophic effects of fishing, a larger area than reef slopes (Vecsei, century, but gamete production was not sedimentation, nutrients, sea-level rise, 2004), and most coral abundance affected. Thus we conclude that predation, and collection and trade. surveys are carried out only on reef Montipora is likely to have some Montipora angulata slopes, and thus may significantly susceptibility to ocean acidification. underestimate the abundance of species The SRR rated the trophic effects of Introduction such as M. angulata that occur primarily fishing as ‘‘medium’’ importance, the The SRR and SIR provided the on reef flats. Veron (2014) reports that fourth most important threat to corals following information on M. angulata’s M. angulata occupied 0.34 percent of overall. This threat was not addressed at morphology and taxonomy. Morphology 2,984 dive sites sampled in 30 the genus or species level in the SRR or was described as extensive encrusting ecoregions of the Indo-Pacific, and had

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a mean abundance rating of 1.3 on a 1 and information we gathered provided mechanisms or conservation efforts for to 5 rating scale at those sites in which no additional biological information. M. angulata. Criticisms of our approach it was found. Based on this semi- received during public comment led us Susceptibility to Threats quantitative system, the species’ to the following analysis to attempt to abundance was characterized as ‘‘rare,’’ To describe M. angulata’s threat analyze regulatory mechanisms on a and overall abundance was also susceptibilities, the SRR and SIR species basis. Records confirm that M. described as ‘‘rare.’’ Veron did not infer provided genus-level information for the angulata occurs in 34 Indo-Pacific trends in abundance from these data. As effects on Montipora of ocean warming, ecoregions that encompass 17 countries’ described in the Indo-Pacific Species acidification, disease, predation, EEZs. The 17 countries are Australia Determinations introduction above, sedimentation, nutrients, and collection (including Cocos-Keeling Islands), based on results from Richards et al. and trade. The SRR and SIR also Brunei, Cambodia, China, India (2008) and Veron (2014), the absolute provided the following species-specific (Andaman and Nicobar Islands), abundance of this species is likely at information on M. angulata’s threats. Indonesia, Japan, Malaysia, Myanmar, least millions of colonies. Montipora angulata contains Clade C Papua New Guinea, Philippines, zooxanthella; this clade varies in its Carpenter et al. (Carpenter et al., Solomon Islands, Sri Lanka, Taiwan, thermal tolerance, but is generally less 2008) extrapolated species abundance Thailand, Timor-Leste, and Vietnam. resistant to bleaching than Clade D. The trend estimates from total live coral The regulatory mechanisms relevant to SRR and SIR did not provide any other cover trends and habitat types. For M. M. angulata, described first as the species-specific information on the angulata, the overall decline in percentage of the above countries that effects of these threats on M. angulata. abundance (‘‘Percent Population utilize them to any degree and second, We interpreted the threat susceptibility Reduction’’) was estimated at 39 as the percentages of those countries and exposure information from the SRR percent, and the decline in abundance whose regulatory mechanisms may be and SIR in the proposed rule for M. limited in scope, are as follows: General before the 1998 bleaching event (‘‘Back- angulata’s vulnerabilities as follows: cast Percent Population Reduction’’) coral protection (29 percent with 6 High vulnerability to ocean warming; percent limited in scope), coral was estimated at 16 percent. However, moderate vulnerability to disease, ocean as summarized above in the Inter-basin collection (41 percent with 18 percent acidification, trophic effects of reef limited in scope), pollution control (35 Comparison sub-section, live coral cover fishing, nutrients, and predation, and trends are highly variable both spatially percent with 12 percent limited in low vulnerability to sedimentation, sea scope), fishing regulations on reefs (100 and temporally, producing patterns on level rise, and collection and trade. small scales that can be easily taken out percent with 18 percent limited in Public comments did not provide any scope), and managing areas for of context, thus quantitative inferences new or supplemental information on M. protection and conservation (94 percent to species-specific trends should be angulata’s threat susceptibilities. We with none limited in scope). The most interpreted with caution. At the same gathered the following species-specific common regulatory mechanisms in time, an extensive body of literature and genus-level supplemental place for M. angulata are reef fishing documents broad declines in live coral information on this species’ threat regulations and area management for cover and shifts to reef communities susceptibilities. Montipora angulata has protection and conservation. General dominated by hardier coral species or been rated as moderately or highly coral protection, pollution control, and algae over the past 50 to 100 years susceptible to bleaching, but this rating coral collection laws are much less (Birkeland, 2004; Fenner, 2012; Pandolfi is not based on species-specific data common regulatory mechanisms for the et al., 2003; Sale and Szmant, 2012). (Carpenter et al., 2008). In one study, management of M. angulata. These changes have likely occurred, and colonies of M. angulata contained Clade are occurring, from a combination of C zooxanthellae (Good et al., 2005). Vulnerability to Extinction global and local threats. Given that M. However, other Montipora species are As explained above in the Risk angulata occurs in many areas affected known to contain Clade D Analyses section, a species’ by these broad changes, and likely has zooxanthellae, depending on colony vulnerability to extinction results from some susceptibility to both global and location or depth (LaJeunesse et al., the combination of its spatial and local threats, we conclude that it is 2004b; Stat et al., 2009). Thus, it is demographic characteristics, threat likely to have declined in abundance possible that broader sampling of M. susceptibilities, and consideration of the over the past 50 to 100 years, but a angulata colonies would show that this baseline environment and future precise quantification is not possible species also hosts Clade D zooxanthellae projections of threats. The SRR stated due to the limited species-specific in some habitats. There are no studies that factors that increase the potential information. of the effects of any other threats on M. extinction risk for this species include Other Biological Information angulata. Based on species-specific and its rare abundance combined with genus-level information described presumed generic vulnerability to a The SRR and SIR provided the above, M. angulata is likely to be highly range of threats including disease, following information on M. angulata’s susceptible to ocean warming and likely bleaching, and predation as well as life history. The sexuality and to have some susceptibility to disease, potentially increasing threats from reproductive modes have been trophic effects of fishing, sedimentation, collection and trade. It listed factors that determined for 35 other species of nutrients, sea-level rise, predation, and reduce potential extinction risk Montipora, all of which are collection and trade. The available including its relatively wide geographic hermaphroditic broadcast spawners. information does not support more distribution. Also, the larvae of all other Montipora precise ratings of the susceptibilities of Subsequent to the proposed rule, we species studied contain zooxanthellae M. angulata to the threats. received and gathered supplemental that can supplement maternal species- or genus-specific information, provisioning with energy sources Regulatory Mechanisms described above, that expands our provided by their photosynthesis. Thus, In the proposed rule, we did not knowledge regarding the species these characteristics likely occur in M. provide any species-specific abundance, distribution, and threat angulata as well. The public comments information on the regulatory susceptibilities. We developed our

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assessment of the species’ vulnerability M. angulata was proposed for listing as Notwithstanding the projections to extinction using all the available threatened because of: High through 2100 that indicate increased information. As explained in the Risk vulnerability to ocean warming (ESA severity over time of the three high Analyses section, our assessment in this Factor E); moderate vulnerability to importance threats, the combination of final rule emphasizes the ability of the disease (C) and acidification (E); these biological and environmental species’ spatial and demographic traits uncommon generalized range wide characteristics indicates that the species to moderate or exacerbate its abundance (E); wide overall distribution possesses sufficient buffering capacity vulnerability to extinction, as opposed (based on wide geographic distribution to avoid being in danger of extinction to the approach we used in the and moderate depth distribution (E); within the foreseeable future throughout proposed rule, which emphasized the and inadequacy of existing regulatory its range. It is possible that this species’ species’ susceptibility to threats. mechanisms (D). extinction risk may increase in the The following characteristics of M. In this final rule, we changed the future if global threats continue and angulata, in conjunction with the listing determination for M. angulata worsen in severity and the species’ information described in the Corals and from threatened to not warranted. We exposure to the threats increases Coral Reefs section, Coral Habitat sub- made this determination based on a throughout its range. Should the species section, and Threats Evaluation section more species-specific and holistic experience reduced abundance or range above, affect its vulnerability to assessment of whether this species constriction of a certain magnitude, the extinction currently and over the meets the definition of either a ability of these characteristics to foreseeable future. Its geographic threatened or endangered coral largely moderate exposure to threats will distribution includes many coral reef in response to public comments, diminish. However, the species is not ecoregions in the central Indo-Pacific including a more appropriate likely to become of such low abundance oceans. Its geographic distribution consideration of the buffering capacity or so spatially fragmented as to be in moderates vulnerability to extinction of this species’ spatial and demographic danger of extinction due to depensatory because some areas within its range are traits to lessen its vulnerability to processes, the potential effects of projected to have less than average threats. Thus, based on the best environmental stochasticity, or the warming and acidification over the available information above on M. potential for mortality from catastrophic foreseeable future, including the central angulata’s spatial structure, events within the foreseeable future Pacific, and other areas, so portions of demography, threat susceptibilities, throughout its range. Therefore, M. the population in these areas will be none of the five ESA listing factors, angulata is not warranted for listing at less exposed to severe conditions. Its alone or in combination, are causing this time under any of the listing factors. depth range is from one to 20 meters. this species to be likely to become This moderates vulnerability to endangered throughout its range within Montipora australiensis extinction over the foreseeable future the foreseeable future, and thus it is not Introduction because deeper areas of its range will warranted for listing at this time, usually have lower temperatures than because: The SRR and SIR provided the surface waters due to local and micro- (1) Montipora angulata’s distribution following information on M. habitat variability in environmental across the central Indo-Pacific is spread australiensis’ morphology and conditions, and acidification is over a large area. While some areas taxonomy. Morphology was described generally predicted to accelerate most in within its range are projected to be as thick plates and irregular columns waters that are deeper and cooler than affected by warming and acidification, that are pale brown, and the taxonomy those in which the species occurs. Its other areas are projected to have less was described as having no taxonomic habitat includes upper reef slopes, mid- than average warming and acidification, issues. slopes, lower reef crests, and reef flats. including the western Indian Ocean, the The public comments and This moderates vulnerability to central Pacific, and other areas. This information we gathered did not extinction over the foreseeable future distribution and the heterogeneous provide any new or supplemental because the species is not limited to one habitats it occupies reduce exposure to information on morphology, and habitat type but occurs in numerous any given threat event or adverse confirmed that there are no known types of reef environments that will, on condition that does not occur uniformly taxonomic problems for M. local and regional scales, experience throughout the species range. As australiensis. There is a moderate level highly variable thermal regimes and explained above in the Threats of species identification uncertainty for ocean chemistry at any given point in Evaluation section, we have not this species, and Veron (2014) states time. Although its qualitative identified any threat that is expected to that M. australiensis is easily confused abundance is described as rare, its occur uniformly throughout the species with several other Montipora, but Veron absolute abundance is at least millions range within the foreseeable future) and (2000; 2014) also considers the species of colonies, which combined with (2) While M. angulata’s qualitative valid, and we consider it is sufficiently spatial variability in ocean warming and abundance is characterized as rare, the distinctive to be identified by experts acidification across the species range, species consists of at least millions of (Fenner, 2014b). Thus, we conclude that moderates vulnerability to extinction colonies that are broadly distributed, the distribution and abundance because the increasingly severe providing buffering capacity in the form information described below for this conditions expected in the foreseeable of absolute numbers of colonies and species is sufficiently reliable (Fenner, future will be non-uniform and variation in susceptibility between 2014b). individual colonies. As discussed in the therefore will likely be a large number Spatial Information of colonies that are either not exposed Corals and Coral Reefs section above, or do not negatively respond to a threat the more colonies a species has, the The SRR and SIR provided the at any given point in time. lower the proportion of colonies that are following information on M. likely to be exposed to a particular australiensis’ distribution, habitat, and Listing Determination threat at a particular time, and all depth range. Montipora australiensis’ In the proposed rule using the individuals that are exposed will not distribution is broad longitudinally, determination tool formula approach, have the same response. including eastern Africa, the central

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Indo-Pacific, and the entire central Inter-basin Comparison sub-section, live Public comments did not provide any Pacific, its habitat is shallow reef coral cover trends are highly variable new or supplemental information on M. environments with high wave action, both spatially and temporally, australiensis’ threats susceptibilities. and its depth range is given as 2 to 30 producing patterns on small scales that We gathered the following species- meters, which the SRR noted seems at can be easily taken out of context. Thus, specific and genus-level information on odds with the shallow reef environment quantitative inferences to species- this species’ threat susceptibilities. habitat description. specific trends should be interpreted Montipora australiensis has been rated The public comments did not provide with caution. At the same time, an as moderately or highly susceptible to any new or supplemental information extensive body of literature documents bleaching, but this rating is not based on on M. australiensis’ distribution. We broad declines in live coral cover and species-specific data (Carpenter et al., gathered supplemental information, shifts to reef communities dominated by 2008). There are no species-specific including Veron (2014), which reports hardier coral species or algae over the studies of the effects of any threats on that this species is confirmed in 17 of past 50 to 100 years (Birkeland, 2004; M. australiensis. Based on the genus- his 133 Indo-Pacific ecoregions, and Fenner, 2012; Pandolfi et al., 2003; Sale level information described above, M. strongly predicted to be found in an and Szmant, 2012). These changes have australiensis likely is highly susceptible additional 16. Veron 2014 also provides likely occurred, and are occurring, from to ocean warming, and likely has some a more recent geographic range a combination of global and local susceptibility to disease, ocean description and map for this species threats. Given that M. australiensis acidification, trophic effects of fishing, which includes areas in the western occurs in many areas affected by these sedimentation, nutrients, predation, and Indian Ocean, and most ecoregions broad changes, and likely has some collection and trade. The available between southern Japan and the GBR, susceptibility to both global and local information does not support more and between western Australia and threats, we conclude that it is likely to precise ratings of the susceptibilities of Vanuatu. We did not gather or receive have declined in abundance over the M. australiensis to the threats. any information on habitat or depth, past 50 to 100 years, but a precise Regulatory Mechanisms thus we interpret the available quantification is not possible due to the information as follows: Its predominant limited species-specific information. In the proposed rule, we did not habitat is upper reef slopes, lower reef provide any species-specific crests, and reef flats, and it likely also Other Biological Information information on the regulatory mechanisms or conservation efforts for occurs on mid-slopes and possibly other The SRR and SIR provided the habitats at depths of two to 30 m. M. australiensis. Criticisms of our following information on M. approach received during public Demographic Information australiensis’ life history. Sexuality and comment led us to the following The SRR and SIR provided the reproductive modes have been analysis to attempt to analyze regulatory following information on M. determined for 35 other species of mechanisms on a species basis. Records australiensis’ abundance. Montipora Montipora, all of which are confirm that M. australiensis occurs in australiensis has been reported as rare. hermaphroditic broadcast spawners. 17 Indo-Pacific ecoregions that The public comments did not provide Although specific observations have not encompass 13 countries’ EEZs. The 13 any new or supplemental information been published for this species, the countries are Australia, Cambodia, on M. australiensis’ abundance. We larvae of all other Montipora species France (French Pacific Island gathered supplemental information, studied contain zooxanthellae that can Territories), Indonesia, Japan, including Veron (Veron, 2014), which supplement maternal provisioning with Madagascar, Mauritius, Papua New reports that M. australiensis occupied energy sources provided by their Guinea, Philippines, Seychelles, 0.40 percent of 2,984 dive sites sampled photosynthesis. It is likely these Solomon Islands, Thailand, and in 30 ecoregions of the Indo-Pacific, and characteristics occur in this species as Vietnam. The regulatory mechanisms had a mean abundance rating of 1.50 on well. The public comments and relevant to M. australiensis, first a 1 to 5 rating scale at those sites in information we gathered provided no described as the percentage of the above which it was found. Based on this semi- additional biological information. countries that utilize them to any degree quantitative system, the species’ Susceptibility to Threats and second, as the percentages of those abundance was characterized as ‘‘rare.’’ countries whose regulatory mechanisms Overall abundance was described as To describe M. australiensis’ threat may be limited in scope, are as follows: ‘‘usually rare.’’ Veron did not infer susceptibilities, the SRR and SIR General coral protection (31 percent trends in abundance from these data. As provided genus-level information for the with 8 percent limited in scope), coral described in the Indo-Pacific Species effects on Montipora of ocean warming, collection (46 percent with 8 percent Determinations introduction above, acidification, disease, predation, limited in scope), pollution control (38 based on results from Richards et al. sedimentation, nutrients, and collection percent with 23 percent limited in (2008) and Veron (2014), the absolute and trade. The SRR and SIR did not scope), fishing regulations on reefs (100 abundance of this species is likely at provide any species-specific percent with 8 percent limited in least millions of colonies. information on the effects of these scope), and managing areas for Carpenter et al. (2008) extrapolated threats on M. australiensis. We protection and conservation (100 species abundance trend estimates from interpreted the threat susceptibility and percent with none limited in scope). total live coral cover trends and habitat exposure information from the SRR and The most common regulatory types. For M. australiensis, the overall SIR in the proposed rule for M. mechanisms in place for M. decline in abundance (‘‘Percent australiensis’ vulnerabilities as follows: australiensis are reef fishing regulations Population Reduction’’) was estimated High vulnerability to ocean warming, and area management for protection and at 37 percent, and the decline in moderate vulnerability to disease, conservation. Coral collection and abundance before the 1998 bleaching acidification, trophic effects of reef pollution control laws are also event (‘‘Back-cast Percent Population fishing, nutrients, and predation, and somewhat common for the species, but Reduction’’) was estimated at 14. low vulnerability to sedimentation, sea 23 percent of pollution control laws are However, as summarized above in the level rise, and collection and trade. limited in scope and may not provide

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substantial protection. General coral species occurs. Its habitat includes that contribute to extinction risk for the protection laws are much less common upper reef slopes, lower reef crests, reef species are inadequate (D); regulatory mechanisms for the flats, and mid-slopes. This moderates (2) The majority of Montipora management of M. australiensis. vulnerability to extinction over the australiensis’ distribution is within the foreseeable future because the species is Vulnerability to Extinction Coral Triangle which is projected to not limited to one habitat type but have the most rapid and severe impacts As explained above in the Risk occurs in numerous types of reef from climate change and localized Analyses section, a species’ environments that will, on local and human impacts for coral reefs over the vulnerability to extinction results from regional scales, experience highly 21st century, as described in the Threats the combination of its spatial and variable thermal regimes and ocean Evaluation. Multiple ocean warming demographic characteristics, threat chemistry at any given point in time. events have already occurred within the susceptibilities, and consideration of the Additionally, habitats in high wave western equatorial Pacific that suggest baseline environment and future action have increased water mixing that future ocean warming events may be projections of threats. The SRR stated can reduce irradiance and dilute other more severe than average in this part of the factors that increase the potential adverse environmental conditions. Its the world. A range constrained to this extinction risk for M. australiensis absolute abundance of at least millions particular geographic area that is likely include its rare abundance combined of colonies, combined with spatial to experience severe and increasing with presumed generic vulnerability to variability in ocean warming and threats indicates that a high proportion a range of threats including disease, acidification across the species range, of the population of this species is likely bleaching, and predation. It listed moderates vulnerability to extinction to be exposed to those threats over the factors that reduce potential extinction because the increasingly severe foreseeable future; and risk including its relatively wide conditions expected in the foreseeable (3) Montipora australiensis’ geographic distribution. future will be non-uniform and qualitative abundance is rare. Subsequent to the proposed rule, we therefore will likely be a large number received and gathered supplemental Considering the limited range of this of colonies that are either not exposed species in an area where severe and species- or genus-specific information, or do not negatively respond to a threat described above, that expands our increasing impacts are predicted, this at any given point in time. However, its level of abundance leaves the species knowledge regarding the species qualitative abundance is described as abundance, distribution, and threat vulnerable to becoming of such low rare, which combined with its restricted abundance within the foreseeable future susceptibilities. We developed our depth distribution indicates it is likely assessment of the species’ vulnerability that it may be at risk from depensatory that a high proportion of individuals processes, environmental stochasticity, to extinction using all the available will be affected by threats that are information. As explained in the Risk or catastrophic events, as explained in typically more severe in shallow more detail in the Corals and Coral Analyses section, our assessment in this habitats at any given point in time. final rule emphasizes the ability of the Reefs and Risk Analyses sections. species’ spatial and demographic traits Listing Determination The combination of these to moderate or exacerbate its In the proposed rule using the characteristics and future projections of vulnerability to extinction, as opposed determination tool formula, M. threats indicates that the species is to the approach we used in the australiensis was proposed for listing as likely to be in danger of extinction proposed rule, which emphasized the threatened because of: High within the foreseeable future throughout species’ susceptibility to threats. vulnerability to ocean warming (ESA its range and warrants listing as The following characteristics of M. Factor E); moderate vulnerability to threatened at this time due to factors A, australiensis, in conjunction with the disease (C) and acidification (E); C, D, and E. information described in the Corals and uncommon generalized range wide The available information above on Coral Reefs section, Coral Habitat sub- abundance (E); wide overall distribution M. australiensis’ spatial structure, section, and Threats Evaluation section (based on wide geographic distribution demography, threat susceptibilities, and above, affect its vulnerability to and moderate depth distribution (E); management also indicate that the extinction currently and over the and inadequacy of existing regulatory species the species is not currently in foreseeable future. Its geographic mechanisms (D). danger of extinction and thus does not distribution is mostly limited to parts of In this final rule, we confirmed the warrant listing as Endangered because: the Coral Triangle and the western listing determination for M. (1) While M. australiensis’ range is Indian Ocean. Despite the large number australiensis as threatened. Based on the mostly constrained to the Coral Triangle of islands and environments that are best available information provided which increases it extinction risk as included in the species’ range, this above on A. lokani’s spatial structure, described above, other areas within its range exacerbates vulnerability to demography, threat susceptibilities, and range are projected to have less than extinction over the foreseeable future management indicate that it is likely to average warming and acidification, such because it is mostly limited to an area become endangered throughout its range as the western Indian Ocean. projected to have the most rapid and within the foreseeable future, and thus Additionally, its habitat includes upper severe impacts from climate change and warrants listing as threatened at this reef slopes, lower reef crests, and reef localized human impacts for coral reefs time, because: flats, and it likely also occurs on mid- over the 21st century. Its depth range of (1) Montipora australiensis is highly slopes. This moderates vulnerability to two to at least 30 meters moderates susceptible to ocean warming (ESA extinction currently because the species vulnerability to extinction over the Factor E), and susceptible to disease (C), is not limited to one habitat type but foreseeable future because deeper areas ocean acidification (E), trophic effects of occurs in numerous types of reef of its range will usually have lower fishing (A), and predation (C), and environments that will, on local and irradiance than surface waters, and nutrients (A, E). These threats are regional scales, experience highly acidification is generally predicted to expected to continue and worsen into variable thermal regimes and ocean accelerate most in waters that are deeper the future. In addition, existing chemistry at any given point in time, as and cooler than those in which the regulatory mechanisms for global threats described in more detail in the Coral

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Habitat and Threats Evaluation sections; wide but somewhat discontinuous, it is interpreted with caution. At the same and known from the Red Sea and east time, an extensive body of literature (2) While M. australiensis’ qualitative Africa, parts of the Coral Triangle, documents broad declines in live coral abundance is characterized as rare, its northwestern Australia, and the central cover and shifts to reef communities absolute abundance is at least millions Pacific. Its habitat includes at least dominated by hardier coral species or of colonies. There is no evidence that upper reef slopes, mid-slopes, lower reef algae over the past 50 to 100 years this species is of such low abundance crests, and reef flats, and its depth range (Birkeland, 2004; Fenner, 2012; Pandolfi that depensatory processes, as 0 to 20 m. et al., 2003; Sale and Szmant, 2012). environmental stochasticity, or the The public comments did not provide These changes have likely occurred, and potential for catastrophic events any new or supplemental information are occurring, from a combination of currently pose a high risk to the survival on M. calcarea’s distribution. We global and local threats. Given that M. of the species. gathered supplemental information, calcarea occurs in many areas affected The combination of these including Veron (2014), which reports by these broad changes, and likely has characteristics indicates that the species that this species is confirmed in 25 of some susceptibility to both global and does not exhibit the characteristics of his 133 Indo-Pacific ecoregions, and local threats, we conclude that it is one that is currently in danger of strongly predicted to be found in an likely to have declined in abundance extinction, as described previously in additional 24. The public comments and over the past 50 to 100 years, but a the Risk Analyses section, and thus does information we gathered provided precise quantification is not possible not warrant listing as endangered at this nothing additional on M. calcarea’s based on the limited species-specific time. habitat and depth range. information. Range-wide, a multitude of Demographic Information Other Biological Information conservation efforts are already broadly employed that are likely benefiting M. The SRR and SIR provided the The SRR and SIR provided the australiensis. However, considering the following information on M. calcarea’s following information on M. calcarea’s global scale of the most important abundance. The abundance of M. life history. The reproductive threats to the species, and the calcarea has been reported as rare, but characteristics of M. calcarea have not ineffectiveness of conservation efforts at may be locally abundant in some areas. been determined. However, sexuality The public comments did not provide addressing the root cause of global and reproductive modes have been any new or supplemental information threats (i.e., GHG emissions), we do not determined for 35 other species of on M. calcarea’s abundance, but the believe that any current conservation Montipora, all of which are supplemental information provided the hermaphroditic broadcast spawners. efforts or conservation efforts planned following. Surveys in Indonesia in the future will result in affecting the Although specific observations have not recorded the species at eight of 51 sites been published for this species, the species status to the point at which (Donnelly et al., 2003), and nine of 39 listing is not warranted. larvae of all other Montipora species sites (Turak and DeVantier, 2003). studied contain zooxanthellae that can Montipora calcarea Veron (2014) reports that M. calcarea supplement maternal provisioning with occupied 5.8 percent of 2,984 dive sites energy sources provided by their Introduction sampled in 30 ecoregions of the Indo- photosynthesis. It is likely these The SRR and SIR provided the Pacific, and had a mean abundance characteristics occur in this species as following information on M. calcarea’s rating of 1.35 on a 1 to 5 rating scale at well. The public comments and morphology and taxonomy. The those sites in which it was found. Based information we gathered provided no morphology was described as irregular on this semi-quantitative system, the additional biological information. thick plates with columnar upgrowths species’ abundance was characterized as and are pale brown or blue in color, and ‘‘rare.’’ Overall abundance was Susceptibility to Threats taxonomy was described as having no described as ‘‘usually rare.’’ As To describe M. calcarea’s threat taxonomic issues. described in the Indo-Pacific Species susceptibilities, the SRR and SIR The public comments and Determinations introduction above, provided genus-level information for the information we gathered did not based on results from Richards et al. effects on Montipora of ocean warming, provide information on morphology, (2008) and Veron (2014), the absolute acidification, disease, sedimentation, and confirmed that there are no known abundance of this species is likely at nutrients, predation, and collection and taxonomic problems for M. calcarea. least tens of millions of colonies. trade. The SRR and SIR also provided There is a moderate level of species Carpenter et al. (Carpenter et al., the following species-specific identification uncertainty for this 2008) extrapolated species abundance information on M. calcarea’s threats. species, and Veron (2014) states that M. trend estimates from total live coral Montipora calcarea was not susceptible calcarea is easily confused with several cover trends and habitat types. For M. to algal or sediment impacts in other Montipora, but Veron (2000; calcarea, the overall decline in anthropogenically impacted waters in 2014), considers the species valid, and abundance (‘‘Percent Population Egypt, but one of the studies appears to we consider it is sufficiently distinctive Reduction’’) was estimated at 34 be a study of the effects of low tide. The to be identified by experts (Fenner, percent, and the decline in abundance SRR and SIR did not provide any other 2014b). Thus, we conclude the before the 1998 bleaching event (‘‘Back- species-specific information on the distribution and abundance information cast Percent Population Reduction’’) effects of these threats on M. calcarea. described below for this species is was estimated at 13 percent. However, We interpreted the threat susceptibility sufficiently reliable (Fenner, 2014b). as summarized above in the Inter-basin and exposure information from the SRR Comparison sub-section, live coral cover and SIR in the proposed rule for M. Spatial Information trends are highly variable both spatially calcarea’s vulnerabilities as follows: The SRR and SIR provided the and temporally, producing patterns on High vulnerability to ocean warming; following information on M. calcarea’s small scales that can be easily taken out moderate vulnerability to disease, ocean distribution, habitat, and depth range. of context, thus quantitative inferences acidification, trophic effects of reef Montipora calcarea’s range is fairly to species-specific trends should be fishing, nutrients and predation, and

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low vulnerability to sedimentation, sea reef fishing regulations and area depth range is from zero to 20 meters. level rise, and collection and trade. management for protection and This moderates vulnerability to Public comments did not provide any conservation. Coral collection and extinction over the foreseeable future new or supplemental information on M. pollution control laws are also because deeper areas of its range will calcarea’s threats, but we gathered the somewhat common for M. calcarea, but usually have lower irradiance than following species-specific and genus- 25 percent of coral collection laws are surface waters, and acidification is level information on this species’ threat limited in scope and may not provide generally predicted to accelerate most in susceptibilities. Montipora calcarea has substantial protection. General coral waters that are deeper and cooler than been rated as moderately or highly protection laws are much less common those in which the species occurs. Its susceptible to bleaching but not disease, regulatory mechanisms for the habitat includes at least upper reef but this rating is not based on species- management of M. calcarea. slopes, mid-slopes, lower reef crests, specific data (Carpenter et al., 2008). and reef flats. This moderates Vulnerability to Extinction There are no species-specific studies of vulnerability to extinction over the the effects of any threats on M. calcarea. As explained above in the Risk foreseeable future because the species is Based on the genus-level and species Analyses section, a species’ not limited to one habitat type but information described above, M. vulnerability to extinction results from occurs in numerous types of reef calcarea likely is highly susceptible to the combination of its spatial and environments that will, on local and ocean warming, and also likely has demographic characteristics, threat regional scales, experience highly some susceptibility to disease, ocean susceptibilities, and consideration of the variable thermal regimes and ocean acidification, trophic effects of fishing, baseline environment and future chemistry at any given point in time. sedimentation nutrients, sea-level rise, projections of threats. The SRR stated Although its qualitative abundance is predation, and collection and trade. The that factors that increase the potential described as rare, its absolute available information does not support extinction risk for M. calcarea include abundance is at least tens of millions of more precise ratings of the its rare abundance combined with colonies, which combined with spatial susceptibilities of M. calcarea to the presumed generic vulnerability to a variability in ocean warming and threats. range of threats including disease, acidification across the species range, bleaching, and predation. It listed Regulatory Mechanisms moderates vulnerability to extinction factors that reduce potential extinction because the increasingly severe In the proposed rule, we did not risk including its relatively wide conditions expected in the foreseeable provide any species-specific geographic distribution. future will be non-uniform and information on the regulatory Subsequent to the proposed rule, we therefore will likely be a large number mechanisms or conservation efforts for received and gathered supplemental of colonies that are either not exposed M. calcarea. Criticisms of our approach species- or genus-specific information, or do not negatively respond to a threat received during public comment led us described above, that expands our at any given point in time. to the following analysis to attempt to knowledge regarding the species analyze regulatory mechanisms on a abundance, distribution, and threat Listing Determination species basis. Records confirm that M. susceptibilities. We developed our In the proposed rule using the calcarea occurs in 25 Indo-Pacific assessment of the species’ vulnerability determination tool formula approach, ecoregions that encompass 28 countries’ to extinction using all the available M. calcarea was proposed for listing as EEZs. The 28 countries are Australia, information. As explained in the Risk threatened because of: High Brunei, Djibouti, Eritrea, Federated Analyses section, our assessment in this vulnerability to ocean warming (ESA States of Micronesia, Fiji, France final rule emphasizes the ability of the Factor E); moderate vulnerability to (French Pacific Island Territories), species’ spatial and demographic traits disease (C) and acidification (E); Indonesia, Madagascar, Malaysia, to moderate or exacerbate its uncommon generalized range wide Mauritius, Myanmar, New Zealand vulnerability to extinction, as opposed abundance (E); wide overall distribution (Tokelau), Niue, Palau, Papua New to the approach we used in the (based on wide geographic distribution Guinea, Philippines, Samoa, Saudi proposed rule, which emphasized the and moderate depth distribution (E); Arabia, Seychelles, Solomon Islands, species’ susceptibility to threats. and inadequacy of existing regulatory Thailand, Timor-Leste, Tonga, Tuvalu, The following characteristics of M. mechanisms (D). United States (American Samoa), calcarea, in conjunction with the In this final rule, we changed the Vietnam, and Yemen. The regulatory information described in the Corals and listing determination for M. calcarea mechanisms relevant to M. calcarea, Coral Reefs section, Coral Habitat sub- from threatened to not warranted. We described first as the percentage of the section, and Threats Evaluation section made this determination based on a above countries that utilize them to any above, affect its vulnerability to more species-specific and holistic degree and second, as the percentages of extinction currently and over the assessment of whether this species those countries whose regulatory foreseeable future. Its geographic meets the definition of either a mechanisms may be limited in scope, distribution includes the Red Sea and threatened or endangered coral largely are as follows: General coral protection many of the coral reef ecoregions in the in response to public comments, (29 percent with 4 percent limited in Indian Ocean and western and central including more appropriate scope), coral collection (61 percent with Pacific Ocean. Its geographic consideration of the buffering capacity 25 percent limited in scope), pollution distribution moderates vulnerability to of this species’ spatial and demographic control (43 percent with 11 percent extinction because some areas within its traits to lessen its vulnerability to limited in scope), fishing regulations on range are projected to have less than threats. Thus, based on the best reefs (100 percent with 14 percent average warming and acidification over available information above on M. limited in scope), and managing areas the foreseeable future, including the calcarea’s spatial structure, for protection and conservation (93 western Indian Ocean, the central demography, threat susceptibilities, and percent with none limited in scope). Pacific, and other areas, so portions of management, none of the five ESA The most common regulatory the population in these areas will be listing factors, alone or in combination, mechanisms in place for the species are less exposed to severe conditions. Its are causing this species to be likely to

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become endangered throughout its range Montipora caliculata ecoregions of the Indo-Pacific, and had within the foreseeable future, and thus a mean abundance rating of 1.55 on a 1 Introduction is not warranted for listing at this time, to 5 rating scale at those sites in which because: The SRR and SIR provided the it was found. Based on this semi- (1) Montipora calcarea’s distribution following information on M. caliculata’s quantitative system, the species’ across the Red Sea, Indian Ocean and morphology and taxonomy. Morphology abundance was characterized as the central Pacific Ocean is spread over was described as brown or blue and ‘‘common.’’ Overall abundance was a very large area. While some areas massive, and corallites are a mixture of described as ‘‘uncommon.’’ Veron did within its range are projected to be immersed and foveolate (in a funnel not infer trends in abundance from affected by warming and acidification, shape). The taxonomy was described as these data. As described in the Indo- other areas are projected to have less having no taxonomic issues. Pacific Species Determinations than average warming and acidification, The public comments and introduction above, based on results including the western Indian Ocean, the information we gathered did not from Richards et al. (2008) and Veron central Pacific, and other areas. This provide any new or supplemental (2014), the absolute abundance of this distribution and the heterogeneous information on morphology, and species is likely at least tens of millions habitats it occupies reduce exposure to confirmed that there is little taxonomic of colonies. any given threat event or adverse uncertainty for M. caliculata. There is a Carpenter et al. (Carpenter et al., condition that does not occur uniformly moderate level of species identification 2008) extrapolated species abundance throughout the species range. As uncertainty for this species, and Veron trend estimates from total live coral explained above in the Threats (2014) states that M. caliculata is easily cover trends and habitat types. For M. Evaluation section, we have not confused with several other Montipora, caliculata, the overall decline in identified any threat that is expected to but Veron (2000; 2014) also considers abundance (‘‘Percent Population occur uniformly throughout the species the species valid, and we consider it is Reduction’’) was estimated at 36 range within the foreseeable future; and sufficiently distinctive to be identified percent, and the decline in abundance (2) While M. calcarea’s qualitative by experts (Fenner, 2014b). Thus, the before the 1998 bleaching event (‘‘Back- abundance is characterized as rare, the distribution and abundance information cast Percent Population Reduction’’) species consists of at least tens of described below for this species is was estimated at 14 percent. However, millions of colonies that are broadly sufficiently reliable (Fenner, 2014b). as summarized above in the Inter-basin distributed, providing buffering capacity Comparison sub-section, live coral cover in the form of absolute numbers of Spatial Information trends are highly variable both spatially colonies and variation in susceptibility The SRR and SIR provided the and temporally, producing patterns on between individual colonies. As following information on M. caliculata’s small scales that can be easily taken out discussed in the Corals and Coral Reefs distribution, habitat, and depth range. of context, thus quantitative inferences section above, the more colonies a Montipora caliculata is found in the to species-specific trends should be species has, the lower the proportion of central Indo-Pacific and the Pacific as interpreted with caution. At the same colonies that are likely to be exposed to far east as the Pitcairn Islands. Its time, an extensive body of literature a particular threat at a particular time, habitat includes at least upper reef documents broad declines in live coral and all individuals that are exposed will slopes, mid-slopes, lower reef crests, cover and shifts to reef communities not have the same response. and reef flats, and its depth range dominated by hardier coral species or Notwithstanding the projections extends as deep as 20 m. algae over the past 50 to 100 years through 2100 that indicate increased The public comments did not provide (Birkeland, 2004; Fenner, 2012; Pandolfi severity over time of the three high any new or supplemental information et al., 2003; Sale and Szmant, 2012). importance threats, the combination of on M. caliculata’s distribution. We These changes have likely occurred, and these biological and environmental gathered supplemental information, are occurring, from a combination of characteristics indicates that the species including Veron (2014), which reports global and local threats. Given that M. possesses sufficient buffering capacity that this species is confirmed in 53 of caliculata occurs in many areas affected to avoid being in danger of extinction his 133 Indo-Pacific ecoregions, and by these broad changes, and likely has within the foreseeable future throughout strongly predicted to occur in an some susceptibility to both global and its range. It is possible that this species’ additional 29. The public comments and local threats, we conclude that it is extinction risk may increase in the information we gathered provided likely to have declined in abundance future if global threats continue and nothing additional on M. caliculata’s over the past 50 to 100 years, but a increase in severity and the species habitat and depth range. precise quantification is not possible exposure to threats increases throughout based on the limited species-specific its range. Should the species experience Demographic Information information. reduced abundance or range The SRR and SIR provided the constriction of a certain magnitude, the following information on M. caliculata’s Other Biological Information ability of these characteristics to abundance. Montipora caliculata has The SRR and SIR provided the moderate exposure to threats will been reported as uncommon. following information on M. caliculata’s diminish. However, the species is not The public comments did not provide life history. The sexuality and likely to become of such low abundance any new or supplemental information reproductive modes have been or so spatially fragmented as to be in on M. caliculata’s abundance. We determined for 35 other species of danger of extinction due to depensatory gathered supplemental information, Montipora, all of which are processes, the potential effects of including surveys in Indonesia and hermaphroditic broadcast spawners. environmental stochasticity, or the Vietnam that recorded the species at ten Although specific observations have not potential for mortality from catastrophic of 51 sites (Donnelly et al., 2003), and been published for this species, the events within the foreseeable future five of seven sites (Latypov, 2011), larvae of all other Montipora species throughout its range. Therefore, M. respectively. Veron (2014) reports that studied contain zooxanthellae that can calcarea is not warranted for listing at M. caliculata occupied 12.1 percent of supplement maternal provisioning with this time under any of the listing factors. 2,984 dive sites sampled in 30 energy sources provided by their

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photosynthesis. It is likely these precise ratings of the susceptibilities of projections of threats. The SRR stated characteristics occur in this species as M. caliculata to the threats. that factors that increase the potential well. The public comments and extinction risk for M. caliculata include Regulatory Mechanisms information we gathered provided no its presumed generic vulnerability to a additional biological information. In the proposed rule, we did not range of threats including disease, provide any species-specific bleaching, and predation. It listed Susceptibility to Threats information on the regulatory factors that reduce potential extinction To describe M. caliculata’s threat mechanisms or conservation efforts for risk including its relatively wide susceptibilities, the SRR and SIR M caliculata. Criticisms of our approach geographic distribution. provided genus-level information for the received during public comment led us Subsequent to the proposed rule, we effects on Montipora of ocean warming, to the following analysis to attempt to received and gathered supplemental acidification, disease, predation, analyze regulatory mechanisms on a species- or genus-specific information, sedimentation, nutrients, and collection species basis. Records confirm that M described above, that expands our and trade. The SRR and SIR also caliculata occurs in 53 Indo-Pacific knowledge regarding the species provided the following species-specific ecoregions that encompass 36 countries’ abundance, distribution, and threat information on M. caliculata’s threats. EEZs. The 36 countries are Australia, susceptibilities. We developed our Montipora caliculata is known to Brunei, Cambodia, China, Djibouti, assessment of the species’ vulnerability contain mycosporine-like amino acids, Eritrea, Federated States of Micronesia, to extinction using all the available which can play a role in reducing Fiji, France (French Pacific Island information. As explained in the Risk bleaching exposure. However, M. Territories), India (Andaman and Analyses section, our assessment in this caliculata was the 7th most susceptible Nicobar Islands), Indonesia, Japan, final rule emphasizes the ability of the to bleaching of the 18 Montipora listed Kiribati, Madagascar, Malaysia, species’ spatial and demographic traits on the Great Barrier Reef, but showed Marshall Islands, Myanmar, Nauru, New to moderate or exacerbate its only moderate bleaching (∼ 20%, or less Zealand (Cook Islands, Tokelau), Niue, vulnerability to extinction, as opposed than half as susceptible as congener Palau, Papua New Guinea, Philippines, to the approach we used in the Montipora tuberculosa) in French Samoa, Saudi Arabia, Solomon Islands, proposed rule, which emphasized the Polynesia during the 2002 bleaching Taiwan, Thailand, Timor-Leste, Tonga, species’ susceptibility to threats. event. The SRR and SIR did not provide Tuvalu, United Kingdom (Pitcairn The following characteristics of M. any other species-specific information Islands), United States (CNMI, Guam, caliculata, in conjunction with the on the effects of these threats on M. American Samoa, PRIAs), Vanuatu, information described in the Corals and caliculata. We interpreted the threat Vietnam, and Yemen. The regulatory Coral Reefs section, Coral Habitat sub- susceptibility and exposure information mechanisms relevant to M. caliculata, section, and Threats Evaluation section from the SRR and SIR in the proposed described first as the percentage of the above, affect its vulnerability to rule for M. caliculata’s vulnerabilities as above countries that utilize them to any extinction currently and over the follows: High vulnerability to ocean degree and second, as the percentages of foreseeable future. Its geographic warming; moderate vulnerability to those countries whose regulatory distribution includes most of the coral disease, ocean acidification, trophic mechanisms may be limited in scope, reef ecoregions in the Indian Ocean and effects of reef fishing, nutrients and are as follows: General coral protection western and central Pacific Ocean. Its predation, and low vulnerability to (28 percent with three percent limited geographic distribution moderates sedimentation, sea level rise, and in scope), coral collection (58 percent vulnerability to extinction because some collection and trade. with 31 percent limited in scope), areas within its range are projected to Public comments did not provide any pollution control (36 percent with eight have less than average warming and new or supplemental information on M. percent limited in scope), fishing acidification over the foreseeable future, caliculata’s threats, but we gathered the regulations on reefs (97 percent with 19 including the western Indian Ocean, the following species-specific and genus- percent limited in scope), and managing central Pacific, and other areas, so level supplemental information on this areas for protection and conservation portions of the population in these areas species’ threat susceptibilities. (92 percent with six percent limited in will be less exposed to severe Montipora caliculata has been rated as scope). The most common regulatory conditions. Its depth range is down to moderately or highly susceptible to mechanisms in place for M. caliculata at least 20 meters. This moderates bleaching, but this rating is not based on are reef fishing regulations and area vulnerability to extinction over the species-specific data (Carpenter et al., management for protection and foreseeable future because deeper areas 2008). Done et al. (2003b) report 50 conservation. Coral collection laws are of its range will usually have lower percent of colonies of M. caliculata were also somewhat common for the species, irradiance than surface waters, and affected by bleaching on the GBR in but 31 percent of coral collection laws acidification is generally predicted to 2002. This was more than 11 out of 17 are limited in scope and may not accelerate most in waters that are deeper Montipora species and 67 percent as provide substantial protection. General and cooler than those in which the much as the species that bleached the coral protection and pollution control species occurs. Its habitat includes at most. No other species-specific laws are much less common regulatory least upper reef slopes, mid-slopes, information is available for the mechanisms for the management of M. lower reef crests, and reef flats. This susceptibility of M. caliculata to any caliculata. moderates vulnerability to extinction other threat. Based on genus-level and over the foreseeable future because the species information described above, M. Vulnerability to Extinction species is not limited to one habitat type caliculata may be highly susceptible to As explained above in the Risk but occurs in numerous types of reef ocean warming, and likely has some Analyses section, a species’ environments that will, on local and susceptibilities to disease, ocean vulnerability to extinction results from regional scales, experience highly acidification, trophic effects of fishing, the combination of its spatial and variable thermal regimes and ocean sedimentation, nutrients, predation, and demographic characteristics, threat chemistry at any given point in time. Its collection and trade. The available susceptibilities, and consideration of the absolute abundance of at least tens of information does not support more baseline environment and future millions of colonies, combined with

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spatial variability in ocean warming and occur uniformly throughout the species sometimes brown or purple. Montipora acidification across the species range, range within the foreseeable future; and turgescens morphology was described as moderates vulnerability to extinction (2) Montipora caliculata’s absolute colonies that are massive, flat, because the increasingly severe abundance is at least tens of millions of hemispherical or columnar and are conditions expected in the foreseeable colonies, providing buffering capacity in brown, cream, or purple in color. future will be non-uniform and the form of absolute numbers of The public comments and therefore will likely be a large number colonies and variation in susceptibility information we gathered did not of colonies that are either not exposed between individual colonies. As provide any new or supplemental or do not negatively respond to a threat discussed in the Corals and Coral Reefs information on morphology, and at any given point in time. section above, the more colonies a confirmed that M. dilatata/flabellata/ species has, the lower the proportion of turgescens has little taxonomic Listing Determination colonies that are likely to be exposed to uncertainty, but a moderate level of In the proposed rule using the a particular threat at a particular time, species identification uncertainty. One determination tool formula approach, and all individuals that are exposed will public comment stated that M. dilatata M. caliculata was proposed for listing as not have the same response. and M. flabellata were described by threatened because of: High Notwithstanding the projections Studer, 1901, instead of Dana, 1846 as vulnerability to ocean warming (ESA through 2100 that indicate increased stated in the SRR. Veron (2014) states Factor E); moderate vulnerability to severity over time of the three high that M. dilatata and M. flabellata are disease (C) and acidification (E); importance threats, the combination of apparently distinctive, and M. uncommon generalized range wide these biological and environmental turgescens is distinctive and Veron abundance (E); wide overall distribution characteristics indicates that the species (2000; 2014) considers these species (based on wide geographic distribution possesses sufficient buffering capacity valid, so we consider these and moderate depth distribution (E); to avoid being in danger of extinction morphological variations of this single and inadequacy of existing regulatory within the foreseeable future throughout species sufficiently distinctive to be mechanisms (D). its range. It is possible that this species’ identified by experts (Fenner, 2014b). In this final rule, we changed the extinction risk may increase in the Thus, we consider the distribution and listing determination for M. caliculata future if global threats continue and abundance information described below for this species is sufficiently reliable from threatened to not warranted. We increase in severity and the species (Fenner, 2014b). made this determination based on a exposure to threats increases throughout more species-specific and holistic its range. Should the species experience Spatial Information reduced abundance or range assessment of whether this species The SRR and SIR provided the meets the definition of either a constriction of a certain magnitude, the ability of these characteristics to following information on M. dilatata/ threatened or endangered coral largely flabellata/turgescens’ distribution, in response to public comments, moderate exposure to threats will diminish. However, the species is not habitat, and depth range. The including more appropriate distribution of this species is the sum of likely to become of such low abundance consideration of the buffering capacity the distributions of the three nominal or so spatially fragmented as to be in of this species’ spatial and demographic species. Montipora dilatata and M. danger of extinction due to depensatory traits to lessen its vulnerability to flabellata are in Hawaii and M. processes, the potential effects of threats. Thus, based on the best turgescens ranges from the Red Sea and environmental stochasticity, or the available information above on M. east Africa to French Polynesia, thus the potential for mortality from catastrophic caliculata’s spatial structure, whole entity ranges from the Red Sea events within the foreseeable future demography, threat susceptibilities, and and east Africa to Hawaii and French throughout its range. Therefore, M. management, none of the five ESA Polynesia. This species’ habitat includes caliculata is not warranted for listing at listing factors, alone or in combination, at least upper reef slopes, mid-slopes, are causing this species to be likely to this time under any of the listing factors. lower reef slopes, lower reef crests, reef become endangered throughout its range Montipora dilatata/flabellata/turgescens flats, and lagoons, and extends to 30 m within the foreseeable future, and thus deep. is not warranted for listing at this time, Introduction The public comments provided the because: As discussed above in the response to following supplemental information. (1) Montipora caliculata’s distribution comments, public comments did not One public comment stated that M. from the Red Sea across the Indian provide any new or supplemental turgescens that was reported by Fenner Ocean and most of the Pacific Ocean is information, nor did we find any new or (2005) to be restricted within Hawaii spread over a very large area. While supplemental information, contradicting and the Northwestern Hawaiian Islands. some areas within its range are the key study used by the SRR to lump We gathered supplemental information projected to be affected by warming and these nominal species (see SRR for which provided the following. acidification, other areas are projected further explanation) into one species as Montipora dilatata was previously only to have less than average warming and a listable entity under the ESA. The SRR known from Hawaii, but has recently acidification, including the western and SIR provided the following been reported to occur in the northern Indian Ocean, the central Pacific, and information on M. dilatata/flabellate/ and southern Line Islands of Kiribati other areas. This distribution turgescens’ morphology and taxonomy. and the Cook Islands (Veron, 2014). throughout the entire region and the Montipora dilatata morphology was Within Hawaii, M. dilatata has only heterogeneous habitats it occupies described as colonies that are encrusting been observed at Kaneohe Bay on Oahu reduce exposure to any given threat to submassive, with irregular branch- and at Laysan Island in the event or adverse condition that does not like upgrowths, and are pale to dark northwestern Hawaiian Islands. occur uniformly throughout the species brown in color. Montipora flabellata However, the Laysan location has not range. As explained above in the morphology was described as colonies been confirmed recently and may need Threats Evaluation section, we have not that are encrusting, with irregular lobes, further investigation. Montipora identified any threat that is expected to and usually blue in color, but flabellata was also previously known

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only from Hawaii (Veron, 2000), but has Veron (2014), indicating that it was 2002. Montipora flabellata increased recently been reported to occur in the highly abundant at the few sites where from 7.4 to 14.3 percent of total live northern Line Islands of Kiribati (Veron, it was observed. Based on this semi- coral cover and was the fourth most 2014). In contrast, M. turgescens is quantitative system, M. dilatata and M. abundant coral. At the Big Island site, broadly distributed throughout the Indo- turgescens’ abundances were overall live coral cover increased by Pacific from South Africa and Socotra characterized as ‘‘rare’’ and ‘‘common’’ approximately 50 percent from 1983 to Island to Hawaii and French Polynesia, respectively, and overall abundances 2002, but M. flabellata was not present and from Japan to the mid-latitudes in were also described as ‘‘rare’’ and during the study (Dollar and Grigg, Australia (Veron, 2014). Veron (Veron, ‘‘common’’ respectively. Montipora 2004). 2014)) confirms M. dilatata in four of flabellata was not encountered in their Carpenter et al. (2008) extrapolated his 133 Indo-Pacific ecoregions surveys because they did not survey in species abundance trend estimates from (northwestern and main Hawaiian Hawaii (Veron, 2014). Veron did not total live coral cover trends and habitat Islands and the northern and southern infer trends in abundance from these types. For M. turgescens, the overall Line Islands), M. flabellata from three of data. As described in the Indo-Pacific decline in abundance (‘‘Percent the same four ecoregions (all but the Species Determinations introduction Population Reduction’’) was estimated southern Line Islands), and M. above, based on results from Richards et at 20 percent, and the decline in turgescens in 71 (including both Hawaii al. (2008) and Veron (2014), the absolute abundance before the 1998 bleaching ecoregions but neither Line Islands abundance of this species is likely at event (‘‘Back-cast Percent Population ecoregions). Thus, M. dilatata/ least tens of millions of colonies. Reduction’’) was estimated at 9 percent. flabellata/turgescens is confirmed in 73 Montipora dilatata and M. turgescens Estimates for M. dilatata and M. of his 133 Indo-Pacific ecoregions, and are rare in the main Hawaiian Islands, flabellata were not available. However, strongly predicted to be found in an thus they are not recorded in the Hawaii as summarized above in the Inter-basin additional 30 (Veron, 2014). Coral Reef Assessment and Monitoring Comparison sub-section, live coral cover Montipora dilatata is reported from Program (CRAMP) data-sets. In contrast, trends are highly variable both spatially subtidal environments (Veron, 2000). In CRAMP results indicate that M. and temporally, producing patterns on the only location within the main flabellata has an overall statewide mean small scales that can be easily taken out Hawaiian Islands where M. dilatata is cover of 2.2 percent, making it the fifth of context, thus quantitative inferences known, Kaneohe Bay on Oahu, it is most abundant coral in the main to species-specific trends should be limited to shallow water protected from Hawaiian Islands (CRAMP, 2008a). interpreted with caution. At the same wave action. Montipora flabellata is Jokiel and Brown (2004) reported M. time, an extensive body of literature reported from shallow reef flabellata as the sixth most abundant documents broad declines in live coral environments, and M. turgescens is coral in the main Hawaiian Islands, cover and shifts to reef communities reported from most reef environments with 0.7 percent cover. A model dominated by hardier coral species or (Veron, 2000). Montipora dilatata and predicted that M. flabellata was sixth in algae over the past 50 to 100 years. M. flabellata are both reported from 1 to coral cover of all corals in the Main These changes have likely occurred, and 10 m depth, whereas M. turgescens has Hawaiian Islands, with about 0.3 are occurring, from a combination of been reported to 30 m depth (Carpenter percent cover (Franklin et al., 2013). global and local threats. Given that M. et al., 2008). Thus we consider the Kenyon and Brainard (2006) reported turgescens occurs in many areas affected depth range for this species to be from that M. flabellata and M. turgescens by these broad changes, and likely has one to at least 30 meters. along with M. capitata dominate many some susceptibility to both global and backreef locations on the northern three Demographic Information local threats, we conclude that it is atolls in the Northwestern Hawaiian likely to have declined in abundance The SRR and SIR provided the Islands. Hunter (2011) reported that the over the past 50 to 100 years, but a following information on M. dilatata/ number of M. dilatata colonies in precise quantification is not possible flabellata/turgescens’ abundance. Kaneohe Bay, Oahu has increased with based on the limited information. Montipora dilatata is rare, M. flabellata increasing search effort, and in 2010 a is the 5th most common coral in Hawaii, total of 43 confirmed M. dilatata Other Biological Information and M. turgescens is described as colonies were located. This is the only The SRR and SIR provided the common. location in the main Hawaiian Islands following information on M. dilatata/ Public comments provided the where M. dilatata is known to occur. flabellata/turgescens’ life history. following. One comment provided There is no overall abundance trend Montipora dilatata/flabellata/turgescens quantitative transect data from Hawaii information for M. dilatata, M. is a hermaphroditic broadcast spawner. that included coral cover measures of M. flabellata, or M. turgescens, but M. The public comments and information flabellata. At Kahului Harbor channel flabellata has been monitored on some we gathered provided no additional entrance, M. flabellata was the most time-series transects in Hawaii. Dollar biological information. abundant coral. At several other sites, and Grigg (2004) monitored coral cover M. flabellata was not recorded or was over 12 and 20 year periods at three Susceptibility to Threats recorded at low levels. Supplemental sites in Hawaii, each with multiple To describe M. dilatata/flabellata/ information provided the following. transects: a semi-enclosed embayment turgescens’ threat susceptibilities, the Veron (2014) reports that M. dilatata on Maui and two open coastal sites on SRR and SIR provided genus-level and M. turgescens occupied 0.03 and Kauai and the Big Island. At the Maui information for the effects on Montipora 16.66 percent respectively of 2,984 dive site, overall live coral cover declined by of ocean warming, disease, ocean sites sampled in 30 ecoregions of the approximately 33 percent from 1990 to acidification, sedimentation, nutrients, Indo-Pacific, and had a mean abundance 2002. Montipora flabellata cover predation, and collection and trade. The rating of 3.0 and 1.40 respectively on a increased from 6.9 to 7.1 percent of total SRR and SIR also provided the 1 to 5 rating scale at those sites in which live coral cover, and was the fifth most following species-specific information it was found. The ‘‘mean abundance abundant coral. At the Kauai site, on M. dilatata/flabellata/turgescens’ when present’’ rating of 3.0 for M. overall live coral cover increased by threats. Montipora dilatata and M. dilatata was the highest of all species in approximately 30 percent from 1983 to flabellata are highly susceptible to

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bleaching, with substantial local susceptible to these diseases when common regulatory mechanisms for the declines of M. dilatata in Ka¯ne‘ohe Bay, environmental conditions are degraded, management of M. dilatata/flabellata/ Hawai‘i, from bleaching mortality. The especially the larger colonies (Thierry turgescens. SRR and SIR did not provide any other Work, personal comm.). Vulnerability to Extinction species-specific information on the Based on genus-level and species effects of these threats on M. dilatata/ information described above, M. As explained above in the Risk flabellata/turgescens. We interpreted dilatata/flabellata/turgescens likely is Analyses section, a species’ the susceptibility and exposure highly susceptible to ocean warming, vulnerability to extinction results from information from the SRR and SIR in the and likely has some susceptibilities to the combination of its spatial and proposed rule for M. dilatata/flabellata/ disease, ocean acidification, trophic demographic characteristics, threat turgescens’ vulnerabilities as follows: effects of fishing, sedimentation, susceptibilities, and consideration of the High vulnerability to ocean warming, nutrients, predation, and collection and baseline environment and future moderate vulnerability to disease, ocean trade. projections of threats. The SRR stated that factors that increase the potential acidification, trophic effects of reef Regulatory Mechanisms fishing, nutrients, and predation, and extinction risk for M. dilatata/flabellata/ low vulnerability to sedimentation, sea In the proposed rule, we did not turgescens include its presumed generic level rise, and collection and trade. provide any species-specific vulnerability to a range of threats Public comments did not provide any information on the regulatory including ocean warming, disease, new or supplemental information on M. mechanisms or conservation efforts for predation, as well as documented dilatata/flabellata/turgescens’ threats, M. dilatata/flabellata/turgescens. declines in Hawai‘i of the M. dilatata but we gathered the following species- Criticisms of our approach received component. Factors that reduce specific and genus-level supplemental during public comment led us to the potential extinction risk are the information on this species’ threat following analysis to attempt to analyze common occurrence and relatively wide susceptibilities. Montipora dilatata, M. regulatory mechanisms on a species geographic distribution of the M. flabellata, and M. turgescens have each basis. Records confirm that M dilatata/ turgescens component. been rated as moderately or highly flabellata/turgescens occurs in 73 Indo- Subsequent to the proposed rule, we susceptible to bleaching but not to Pacific ecoregions that encompass 30 received and gathered supplemental disease, however, these ratings are not countries’ EEZs. The 30 countries are species- or genus-specific information, based on species-specific data Australia (including Norfolk Island), described above, that expands our (Carpenter et al. 2008). With regard to Brunei, Cambodia, China, Federated knowledge regarding the species thermal stress, in the Northwest States of Micronesia, Fiji, France abundance, distribution, and threat Hawaiian Islands, M. turgescens (French Pacific Island Territories), India susceptibilities. We developed our bleached much less severely than (including Andaman and Nicobar assessment of the species’ vulnerability Montipora capitata in 2002 (G. Aeby Islands), Indonesia, Japan, Kiribati, to extinction using all the available personal comm.). Kenyon and Brainard Madagascar, Malaysia, Mauritius, information. As explained in the Risk (2006) report that in 2004, M. capitata Myanmar, New Zealand (Cook Islands), Analyses section, our assessment in this and M. turgescens had high levels of Palau, Papua New Guinea, Philippines, final rule emphasizes the ability of the bleaching in the northern three atolls, Seychelles, Solomon Islands, South species’ spatial and demographic traits with up to 100 percent bleaching in Africa, Sri Lanka, Taiwan, Thailand, to moderate or exacerbate its some areas. Montipora flabellata, Timor-Leste, United States (Hawaii, vulnerability to extinction, as opposed though, had very low levels of bleaching PRIAs), Vanuatu, Vietnam, and Yemen. to the approach we used in the (1.2 to 4.7 percent). Jokiel and Brown The regulatory mechanisms relevant to proposed rule, which emphasized the (2004) reported that M. dilatata and M. M. dilatata/flabellata/turgescens, species’ susceptibility to threats. flabellata had low resistance to described first as the percentage of the The following characteristics of M. bleaching in 1996 in Hawaii. Montipora above countries that utilize them to any dilatata/flabellata/turgescens, in dilatata was the most sensitive species degree and second, as the percentages of conjunction with the information to bleaching in Kaneohe Bay in 1996. It those countries whose regulatory described in the Corals and Coral Reefs was the first to bleach and few survived mechanisms may be limited in scope, section, Coral Habitat sub-section, and the event (Jokiel and Brown, 2004). The are as follows: General coral protection Threats Evaluation section above, affect majority of the species-specific and (33 percent with 10 percent limited in its vulnerability to extinction currently genus-level information above suggests scope), coral collection (53 percent with and over the foreseeable future. Its that M. dilatata/flabellata/turgescens 23 percent limited in scope), pollution geographic distribution includes nearly likely is highly susceptible to warming- control (43 percent with 10 percent all of the coral reef ecoregions in the induced bleaching. limited in scope), fishing regulations on Indian Ocean and western and central With regard to disease, M. turgescens reefs (97 percent with 20 percent Pacific Ocean. Its geographic is specifically described with mortality limited in scope), and managing areas distribution moderates vulnerability to from a rapid tissue-loss (‘‘white’’) for protection and conservation (97 extinction because some areas within its syndrome in the Northwestern percent with none limited in scope). range are projected to have less than Hawaiian Islands, and this condition The most common regulatory average warming and acidification over affected more than 21 percent of mechanisms in place for to M. dilatata/ the foreseeable future, including the Montipora colonies in a 2003 survey flabellata/turgescens are reef fishing western Indian Ocean, the central (Aeby, 2006). In the main Hawaiian regulations and area management for Pacific, and other areas, so portions of Islands, an outbreak of filamentous protection and conservation. Coral the population in these areas will be bacterial diseases began in 2012 on collection and pollution control laws less exposed to severe conditions. Its Kauai, and continued in 2013, heavily are also somewhat common for the depth range is from low tide to at least affecting the Montipora species on these species, but 23 percent of coral 30 meters. This moderates vulnerability reefs, including Montipora capitata, M. collection laws are limited in scope and to extinction over the foreseeable future flabellata, and M. patula (Work, 2013). may not provide substantial protection. because deeper areas of its range will This species appears to be highly General coral protection laws are less usually have lower irradiance than

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surface waters, and acidification is (1) Montipora dilatata/flabellata/ Montipora lobulata generally predicted to accelerate most in turgescens’ distribution across the Introduction waters that are deeper and cooler than Indian Ocean and most of the Pacific those in which the species occurs. Its Ocean is spread over a very large area. The SRR and SIR provided the habitat includes at least upper reef While some areas within its range are following information on M. lobulata’s slopes, mid-slopes, lower reef slopes, projected to be affected by warming and morphology and taxonomy. Colonies of lower reef crests, reef flats, and lagoons. acidification, other areas are projected Montipora lobulata are mottled brown This moderates vulnerability to to have less than average warming and or white and submassive. Colony extinction over the foreseeable future acidification, including the western surfaces consist of irregular mounds. because the species is not limited to one Indian Ocean, the central Pacific, and There are no taxonomic issues for M. lobulata. habitat type but occurs in numerous other areas. This distribution and the The public comments did not provide types of reef environments that will, on heterogeneous habitats it occupies local and regional scales, experience any new or supplemental information reduce exposure to any given threat highly variable thermal regimes and on M. lobulata’s morphology and event or adverse condition that does not ocean chemistry at any given point in taxonomy. We gathered supplemental time. Its absolute abundance of tens to occur uniformly throughout the species information on this species, which hundreds of millions of colonies, range. As explained above in the indicates a very high level of species combined with spatial variability in Threats Evaluation section, we have not identification uncertainty for this ocean warming and acidification across identified any threat that is expected to species. Montipora lobulata is too the species range, moderates occur uniformly throughout the species difficult to identify on reefs, even for vulnerability to extinction because the range within the foreseeable future; and experts, for the data collected on it to be increasingly severe conditions expected (2) Montipora dilatata/flabellata/ reliable. Veron (2014) states that M. in the foreseeable future will be non- turgescens’ absolute abundance is at lobulata has a poorly known uniform and therefore will likely be a least tens of millions of colonies, distribution and his distribution map is large number of colonies that are either providing buffering capacity in the form not suitable for analysis. Although not exposed or do not negatively of absolute numbers of colonies and Veron (2000; 2014), considers the respond to a threat at any given point variation in susceptibility between species valid, we conclude it not in time. individual colonies. As discussed in the sufficiently distinctive to be reliably identified (Fenner, 2014b). Thus, we do Corals and Coral Reefs section above, Listing Determination not consider the M. lobulata distribution the more colonies a species has, the and abundance information in the SRR In the proposed rule using the lower the proportion of colonies that are or SIR to be sufficiently reliable and are determination tool formula approach, likely to be exposed to a particular M. dilatata/flabellata/turgescens was unable to provide a reliable species threat at a particular time, and all proposed for listing as threatened description for M. lobulata in this final individuals that are exposed will not because of: High vulnerability to ocean rule. have the same response. warming (ESA Factor E); moderate Listing Determination vulnerability to disease (C) and Notwithstanding the projections acidification (E); common generalized through 2100 that indicate increased In the proposed rule using the range wide abundance (E); wide overall severity over time of the three high determination tool formula approach, distribution (based on wide geographic importance threats, the combination of M. lobulata was proposed for listing as distribution and moderate depth these biological and environmental threatened because of: High distribution (E); and inadequacy of characteristics indicates that the species vulnerability to ocean warming (ESA existing regulatory mechanisms (D). possesses sufficient buffering capacity Factor E); moderate vulnerability to In this final rule, we changed the to avoid being in danger of extinction disease (C) and acidification (E); listing determination for M. dilatata/ within the foreseeable future throughout uncommon generalized range wide abundance (E); narrow overall flabellata/turgescens from threatened to its range. It is possible that this species’ distribution (based on narrow not warranted. We made this extinction risk may increase in the determination based on a more species- geographic distribution and shallow future if global threats continue and depth distribution (E); and inadequacy specific and holistic assessment of increase in severity and the species whether this species meets the of existing regulatory mechanisms (D). exposure to threats increases throughout Based on the lack of information on definition of either a threatened or its range. Should the species experience endangered coral largely in response to M. lobulata’s distribution, abundance, reduced abundance or range and threat susceptibilities due to this public comments, including more constriction of a certain magnitude, the appropriate consideration of the species’ identification uncertainty, we ability of these characteristics to believe there is not sufficient evidence buffering capacity of this species’ spatial moderate exposure to threats will and demographic traits to lessen its to support a listing determination of diminish. However, the species is not vulnerability to threats. Thus, based on threatened or endangered. Therefore, we likely to become of such low abundance the best available information above on find that listing is not warranted at this M. dilatata/flabellata/turgescens’ spatial or so spatially fragmented as to be in time under any factor. danger of extinction due to depensatory structure, demography, threat Montipora patula/verrilli susceptibilities, and management, none processes, the potential effects of of the five ESA listing factors, alone or environmental stochasticity, or the Introduction in combination, are causing this species potential for mortality from catastrophic The SRR and SIR provided the to be likely to become endangered events within the foreseeable future following information on M. patula/ throughout its range within the throughout its range. Therefore, M. verrilli’s morphology and taxonomy. foreseeable future, and thus is not dilatata/flabellata/turgescens is not Morphology was described as warranted for listing at this time, warranted for listing at this time under encrusting or tiered plates that are tan because: any of the listing factors. in color, most often with purple polyps.

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Due to taxonomic issues from recent verrilli’s distribution, habitat, and depth Dollar and Grigg (2004) show genetic and micro-morphological range. Montipora patula/verrilli has a substantial declines of M. patula on a analyses, the BRT chose to evaluate very restricted range, centered on the subset of their transects over 12 years, extinction risk of Montipora patula/ Main and Northwestern Hawaiian but other transects within sites show verrilli as a species since they are Islands. Montipora verrilli has been high variability between surveys or indistinguishable genetically and micro- reported from some other locations. similar cover between the beginning and morphologically. Montipora patula has been reported to end of the study. The public comments provided the occupy shallow reef environments and The public comments provided the following information on morphology reef flats, and is common in wave-swept following information on this species’ and taxonomy. One public comment environments but less tolerant of demography. One public comment stated that there are subtle but sediment-impacted areas. Montipora stated that data from 79 monitoring sites consistent differences between the two patula/verrilli’s habitat includes at least in Hawaii from 1999 to 2012 suggest nominal species, and despite genetic upper reef slopes, mid-slopes, lower reef that M. patula and M. verrilli are analysis showing strong similarity slopes, lower reef crests, and reef flats. experiencing different trajectories in between the two species, it cannot be The depth range is described as shallow growth and abundance. A second public conclusive until more of the genome is reef flats down to 10 meters depth, with comment stated that the SRR’s analyzed. A second public comment a report of 40 meters. characterization of M. patula’s stated that since the combining of The public comments provided the populations as declining disregards morphological species into a single following information. One public public records of numerous long-term entity was only done for two groups of comment stated that a species that is monitoring programs that have species in Hawaii and for none of the highly consistent with Veron’s demonstrated its considerable other species around the world, for description of M. verrilli has been abundance along the Hawaiian coast consistency these species should be reported from the Marianas. We and its resistance to extreme conditions. considered separately. The commenter gathered supplemental information, A third public comment provided stated that these groupings are based on which stated that M. patula was quantitative coral cover data from a a single scientific publication that considered endemic to the Hawaiian variety of transects taken in Hawaii. suggests, but does not state Islands and Johnston Atoll (Veron, Montipora patula often had the third, conclusively, that these species contain 2000), but is now known to occur fourth, or fifth highest coral cover of any the same identical genomes and that throughout the Hawaiian Islands, and species. We gathered supplemental combining them makes it so that also in the Line Islands, Marquesas, and information, including Veron (2014), differences between them in abundance Austral Islands (Veron, 2014). Veron which while he did not conduct and physiological characteristics cannot (2014) reports M. patula as absent from abundance surveys in Hawaii, describes be separated. The group as a whole, Johnston Atoll, but this is an error as it the overall abundance of M. patula as suggested the commenter, might have is well known to occur there (Maragos ‘‘uncommon.’’ Montipora patula is one one status while species within the and Jokiel, 1986); (Coles et al., 2001); of the most common reef-building corals group could have another. As discussed (Brainard et al., 2005; Veron, 2000; in Hawaii. Jokiel et al. (2004) reported above in the response to comments, Williams and Miller, 2012); (Lobel and that M. patula has an overall statewide public comments did not provide any K., 2008). Veron (2014) does not report mean cover of 2.7 percent and the new or supplemental information on M. verrilli. Like M. patula, M. verrilli Hawaii Coral Reef Assessment and contradicting the SRR to lump these is reported from the Hawaiian Islands Monitoring Program (CRAMP) indicates nominal species (see SRR for further and Johnston Atoll (Veron, 2000), but is that M. patula has an overall statewide explanation) into one species as a also reported from the Mariana Islands mean cover of 3.3 percent (CRAMP, listable entity under the ESA. and Palau (Randall, 1995; Randall, 2003; 2008b). Those mean cover percentages Supplemental information we Randall and Myers, 1983). Veron (2014) make M. patula the fourth most gathered confirms the known taxonomic reports that M. patula is confirmed in abundant coral in the main Hawaiian problems for M. patula/verrilli, and five of his 133 Indo-Pacific ecoregions Islands. Fenner (2005) considered M. reports that there is a moderate level of and strongly predicted in an additional patula as one of the five most common species identification uncertainty for two ecoregions. corals in Hawaii. Grigg (1984) found this species. Montipora patula and M. Montipora patula is commonly that M. patula was the fifth most verrilli are similar (Veron, 2000; Veron, observed deeper than 10 m throughout common coral in the main Hawaiian 2014; Wallace, 1999b), and may be the Hawaiian Islands (Samuel Kahng, Islands. A species distribution model indistinguishable (Fenner, 2005). personal comm.), but its deepest depth predicted that M. patula has the second However, the species M. patula/verrilli range is not reported. The public highest coral cover of all reef-building is distinctive and not difficult to comments and information we gathered coral species in the main Hawaiian identify by experts (Fenner, 2014b). provided nothing supplemental on M. Islands (Franklin et al., 2013). Veron (2014) states that M. patula is patula/verrilli’s habitat and depth range. Montipora verrilli has been reported to very similar to M. verrilli and Veron dominate deep, still water along with Demographic Information (2000; 2014) considers the species valid. another Montipora species at Johnston As already stated, we consider M. The SRR and SIR provided the Island (Jokiel and Tyler III, 1992) and M. patula/verrilli is sufficiently distinctive following information on M. patula/ patula is reported to be one of the two to be identified by experts (Fenner, verrilli’s abundance. Montipora patula most common corals at Johnston Island 2014b). Thus, we conclude that the and M. verrilli have been reported as (NOAA, 2006). In one study, M. patula distribution and abundance information sometimes common. Montipora patula was found at every one of the 11 described below for this species is is the most abundant of the three stations at Johnston Island that were sufficiently reliable (Fenner, 2014b). Hawaiian endemic (nominal) Montipora surveyed (Coles et al., 2001). These with overall statewide mean cover of 3.3 three studies may refer to the same Spatial Information percent, making it the fourth most species. The SRR and SIR provided the abundant coral in Hawai‘i. Montipora The species has been monitored on following information on M. patula/ verrilli is less abundant in Hawai‘i. some time-series transects in Hawaii.

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Dollar and Grigg (2004) monitored coral and information we gathered provided tolerates elevated sediment loading and cover over 12 and 20 year periods at no supplemental biological information. resuspension. three sites in Hawaii, each with We gathered the following species- Susceptibility to Threats multiple transects: a semi-enclosed specific and genus-level information on embayment on Maui and two open To describe M. patula/verrilli’s threat this species’ threat susceptibilities. coastal sites on Kauai and the Big susceptibilities, the SRR and SIR Montipora patula has been rated as Island. At the Maui site, overall live provided genus-level information for the moderately or highly susceptible to coral cover declined by approximately effects on Montipora of ocean warming, bleaching and coral disease, but M. 33 percent from 1990 to 2002; M. patula acidification, disease, sedimentation, verrilli has not been rated as moderately cover declined from 13.8 to 8.2 percent nutrients, predation, and collection and or highly susceptible to bleaching and of total live coral cover, and was the trade. The SRR and SIR also provided coral disease, however, these ratings are fourth most abundant coral at this site. the following species-specific not based on species-specific data At the Kauai site, overall live coral information on M. patula/verrilli’s (Carpenter et al., 2008). Kenyon and cover increased by approximately 30 threats. Montipora patula is among the Brainard (2006) report that M. patula percent from 1983 to 2002; M. patula most bleaching-susceptible corals in the was the most frequently bleached coral increased from 24.9 to 36.0 percent of Northwestern Hawaiian Islands and in Maro, Laysan, and Lisianski in the total live coral cover, and was the may be moderately susceptible in the Northwestern Hawaiian Islands in 2004. second most abundant coral at this site. main Hawaiian Islands. What ultimately At Pearl and Hermes reef, more than At the Big Island site, overall live coral became known as the stress-tolerant half of the M. patula colonies bleached, cover increased by approximately 50 zooxanthellae clade D was first although more than half of the colonies percent from 1983 to 2002; M. patula documented in shallow-water M. patula of several other coral species also increased from 0.7 to 3.3 percent of total in Hawai’i, though it also hosts clade C bleached. In a bleaching event in 1996, live coral cover, and was the fourth in deeper waters. Both nominal M. M. patula was found to have a moderate most abundant coral at this site (Dollar patula and M. verrilli are specifically sensitivity to bleaching (Jokiel and and Grigg, 2004). Friedlander and noted with acute disease conditions Brown, 2004). At Kailua, Oahu, M. Brown (2005) monitored coral cover for (involving tissue loss/partial mortality) patula was observed to partly bleach 12 years at 20 transects in Hanalei Bay, with high frequency of occurrence (over every year for four years in April or May Kauai. Overall live coral cover increased 20 percent of surveyed sites where the and October or September (Hoegh- taxa was observed showed disease by approximately 30 percent from 1993 Guldberg, 1995). Montipora patula signs) and high prevalence (over seven to 2004, M. patula increased from colonies host multiple zooxanthellae percent in some sites) in the approximately 50 to 60 percent of total clades, depending on location and Northwestern Hawaiian Islands (Aeby, live coral cover, and was the most depth. In Hawaii, colonies from 2006). This author points out that the abundant coral (Friedlander and Brown, different sites and depths had two high prevalence sites had suffered 2005). In its public comment letter on different clades (LaJeunesse et al., severe bleaching in the previous year. the proposed rule, the National Park 2004a), and at Johnston Atoll, colonies Montipora patula may be less sediment Service summarized data collected from from different sites and depths had four tolerant than other Montipora species 1999 to 2012 at 79 sites at different different clades, including the two (Jokiel et al., 2007), and it did disappear depths from the main Hawaiian Islands found in the Hawaii colonies (Stat et al., from survey stations in Pelekane Bay, 2009). (exact locations not identified) showing Hawai‘i between 1977 and 1996 as the In the main Hawaiian Islands, an that M. patula increased in live coral bay became more impacted by sediment. outbreak of filamentous bacterial cover by approximately 2.3 percent over The SRR and SIR did not provide any diseases began in 2012 on Kauai, and the 14 year period at all sites combined. other species-specific information on continued in 2013, heavily affecting the As described in the Indo-Pacific Species the effects of these threats on M. patula/ Montipora species on these reefs, Determinations introduction above, verrilli. We interpreted the threat including M. capitata, M. flabellata, and based on results from Richards et al. susceptibility and exposure information M. patula (Work, 2013). These (2008) and Veron (2014), the absolute from the SRR and SIR in the proposed Montipora species appear to be highly abundance of this species is likely at rule for M. patula/verrilli’s susceptible to these diseases when least millions of colonies. vulnerabilities as follows: High environmental conditions are degraded, Other Biological Information vulnerability to ocean warming, especially the larger colonies (Thierry moderate vulnerabilities to disease, Work, personal comm.). It is unknown The SRR and SIR provided the ocean acidification, trophic effects of if these Montipora species are highly following information on M. patula/ fishing, sedimentation, nutrients, and susceptible to these diseases when verrilli’s life history. Montipora patula predation, and low vulnerability to sea- environmental conditions are not as and M. verrilli are both documented as level rise, and collection and trade. degraded as they are on Kauai. With hermaphroditic broadcast spawners. Public comments provided some regards to sedimentation, the SRR Release of packaged egg and sperm supplemental information on M. patula/ referred to a study that concluded M. bundles has been observed in the verrilli’s threat susceptibilities. One patula was more sensitive to sediment months of July through September at public comment stated that in nearshore than other corals and another study that Coconut Island, Oahu, during two moon areas exposed to extremes of low concluded M. verrilli was relatively phases: new to first quarter, and full to salinity and temperature such as the resistant to sedimentation. No other third quarter. Although specific larval eastern shore of the island of Hawaii species-specific information is available descriptions have not been published where there are many streams and for the susceptibility of M. patula/ for this species, the larvae of all other groundwater discharges, M. patula is verrilli to any other threat. Montipora species studied contain one of the most common corals, Based on genus-level and species- zooxanthellae that can supplement sometimes nearly covering the entire specific information described above, M. maternal provisioning with energy reef surface. Montipora patula is one of patula/verrilli likely is highly sources provided by their the most common corals in harbors susceptible to ocean warming, likely has photosynthesis. The public comments around the state of Hawaii, where it some susceptibility to disease, ocean

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acidification, trophic effects of fishing, Subsequent to the proposed rule, we large number of colonies that are either sedimentation, nutrients, sea-level rise, received and gathered supplemental not exposed or do not negatively predation, and collection and trade. The species- or genus-specific information, respond to a threat at any given point available information does not support described above, that expands our in time. more precise ratings of the knowledge regarding the species Listing Determination susceptibilities of M. patula/verrilli to abundance, distribution, and threat the threats. susceptibilities. We developed our In the proposed rule, using the assessment of the species’ vulnerability determination tool formula approach, Regulatory Mechanisms to extinction using all the available M. patula/verrilli was proposed for In the proposed rule, we did not information. As explained in the Risk listing as threatened because of: High provide any species-specific Analyses section, our assessment in this vulnerability to ocean warming (ESA information on the regulatory final rule emphasizes the ability of the Factor E); moderate vulnerability to mechanisms or conservation efforts for species’ spatial and demographic traits disease (C) and acidification (E); M. patula/verrilli. Criticisms of our to moderate or exacerbate its common generalized range wide approach received during public vulnerability to extinction, as opposed abundance (E); narrow overall comment led us to the following to the approach we used in the distribution (based on narrow analysis to attempt to analyze regulatory proposed rule, which emphasized the geographic distribution and moderate depth distribution (E); and inadequacy mechanisms on a species basis. Records species’ susceptibility to threats. of existing regulatory mechanisms (D). confirm that M. patula/verrilli occurs in The following characteristics of M. In this final rule, we changed the eight Indo-Pacific ecoregions that patula/verrilli, in conjunction with the listing determination for M. patula/ encompass four countries’ EEZs. The information described in the Corals and verrilli from threatened to not four countries are France (French Coral Reefs section, Coral Habitat sub- warranted. We made this determination Pacific Island Territories), Kiribati, section, and Threats Evaluation section based on a more species-specific and Palau, and the United States (Guam, above, affect its vulnerability to holistic assessment of whether this CNMI, Hawaii, PRIAs). The regulatory extinction currently and over the species meets the definition of either a mechanisms relevant to M. patula/ foreseeable future. Its geographic threatened or endangered coral largely verrilli, described first as the percentage distribution includes coral reef in response to public comments, of the above countries that utilize them ecoregions spanning an arc across the including more appropriate to any degree and second, as the Pacific Ocean from the Mariana to consideration of the buffering capacity percentages of those countries whose Hawaiian to Austral Islands. Its of this species’ spatial and demographic regulatory mechanisms may be limited geographic distribution moderates traits to lessen its vulnerability to in scope, are as follows: General coral vulnerability to extinction because some threats. Thus, based on the best protection (75 percent with none areas within its range are projected to available information above on M. limited in scope), coral collection (100 have less than average warming and patula/verrilli’s spatial structure, percent with 25 percent limited in acidification over the foreseeable future, demography, threat susceptibilities, and scope), pollution control (75 percent including the central Pacific, so portions management, none of the five ESA with 25 percent limited in scope), of the population in these areas will be listing factors, alone or in combination, fishing regulations on reefs (100 percent less exposed to severe conditions. Its are causing this species to be likely to with 25 percent limited in scope), and depth range is from low tide to more become endangered throughout its range managing areas for protection and than 10 meters, possibly as deep as 40 within the foreseeable future, and thus conservation (100 percent with none meters. This moderates vulnerability to it is not warranted for listing at this limited in scope). All five regulatory extinction over the foreseeable future time, because: mechanisms are very common for because deeper areas of its range will (1) Montipora patula/verrilli’s managing M. patula/verrilli, with only usually have lower irradiance than distribution range is widespread, coral collection, pollution control, and surface waters, and acidification is although disjointed and not continuous, reef fishing laws somewhat limited in generally predicted to accelerate most in from Palau to Hawaii to French scope. waters that are deeper and cooler than Polynesia. While some areas within its Vulnerability to Extinction those in which the species occurs. Its range are projected to be affected by habitat includes at least upper reef warming and acidification, other areas As explained above in the Risk slopes, mid-slopes, lower reef slopes, are projected to have less than average Analyses section, a species’ lower reef crests, and reef flats. This warming and acidification, including vulnerability to extinction results from moderates vulnerability to extinction the central Pacific. This distribution and the combination of its spatial and over the foreseeable future because the the heterogeneous habitats it occupies demographic characteristics, threat species is not limited to one habitat type reduce exposure to any given threat susceptibilities, and consideration of the but occurs in numerous types of reef event or adverse condition that does not baseline environment and future environments that will, on local and occur uniformly throughout the species projections of threats. The SRR stated regional scales, experience highly range. As explained above in the that factors that increase the potential variable thermal regimes and ocean Threats Evaluation section, we have not extinction risk for M. patula/verrilli chemistry at any given point in time. Its identified any threat that is expected to include its combined very narrow common and stable or increasing occur uniformly throughout the species geographic distribution, restriction to abundance in parts of its range, range within the foreseeable future; shallow habitats, and its generic high combined with spatial variability in (2) Montipora patula/verrilli is one of susceptibility to a range of threats ocean warming and acidification across the most abundant species in Hawaii, a (bleaching, predation) and documented the species range, moderates major part of its range, and time-series species-specific impacts from disease. vulnerability to extinction because the studies of various sites around Hawaii No species characteristics were noted in increasingly severe conditions expected since the 1980s seem to show stability the SRR that reduced expectations of in the foreseeable future will be non- in overall abundance trends in M. extinction risk. uniform and therefore will likely be a patula. The species’ abundance

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provides buffering capacity in the form Alveopora consists of 14 species, all the following inferences about the of absolute numbers of colonies and occurring in the Indo-Pacific (Veron, susceptibilities of an unstudied variation in susceptibility between 2000). Colonies are usually massive, Alveopora species to ocean warming, individual colonies. As discussed in the branching, plating, or a combination. disease, acidification, trophic effects of Corals and Coral Reefs section above, The SRR and SIR provided no genus- fishing, sedimentation, nutrients, sea- the more colonies a species has, the level introductory information on level rise, predation, and collection and lower the proportion of colonies that are Alveopora. trade. The SRR rated ocean warming and disease as ‘‘high’’ importance, and likely to be exposed to a particular Genus Susceptibility to Threats threat at a particular time, and all ocean acidification as ‘‘medium-high’’ individuals that are exposed will not The SRR and SIR provided the importance, to corals. These were rated have the same response; following information on the threat as the three most important threats to (3) The depth range for M. patula/ susceptibilities of the genus Alveopora. reef-building corals overall. The studies verrilli likely extends to 40 m depth, The genus Alveopora is listed as having reporting bleaching in the genus suggesting the possibility of depth the highest bleaching response from the Alveopora reported a wide range of refuges from ocean warming and other 17 included genera in the Indian Ocean. results, from high levels of bleaching to threats, and indicating a higher absolute Alveopora had high bleaching in Guam low levels of bleaching. There are a few area of potential occupancy within the in 1994 and South Africa in 2000, but reports of disease in Alveopora in the species range; had little bleaching or mortality in Palau Global Disease database, and Goniopora (4) Many of the areas where M. in the 2001 event. Low-to-moderate and Alveopora had low combined patula/verrilli is found in the Pacific are bleaching of Alveopora allingi was disease prevalence in Indonesia. Thus, remote and mostly uninhabited, observed in East Africa during the we conclude that Alveopora is likely to reducing the likelihood of exposure to 1997–1998 event. A few disease reports have some susceptibility to ocean local sources of impacts that result from for the genus Alveopora can be found in warming and disease. Although there is human activities; and the Global Disease Database. no other genus-level or species-specific (5) All five major categories of The public comments did not provide information on the susceptibilities of protective regulatory mechanisms supplemental information on the threat Alveopora species to ocean addressing local sources of threats are susceptibilities of the genus Alveopora. acidification, the SRR rated it as implemented by 75 to 100 percent of the We gathered supplemental information ‘‘medium-high’’ importance to corals. countries within M. patula/verrilli’s that provided the following. In Palau in Thus, we conclude that an unstudied range, with only three categories 2000, Alveopora species had ‘‘relatively Alveopora species is likely to have some somewhat limited in scope. little bleaching and mortality.’’ Forty susceptibility to ocean acidification. Notwithstanding the projections eight percent of all colonies of all The SRR rated the trophic effects of through 2100 that indicate increased species were bleached, and bleaching of fishing as ‘‘medium’’ importance, the severity over time of the three high different genera and species ranged from fourth most important threat to corals importance threats, the combination of none to very high, but no quantitative overall. This threat was not addressed at these biological and environmental results were reported for any Alveopora the genus or species level in the SRR or characteristics indicates that the species species (Bruno et al., 2001). In Kenya in SIR, because it is an ecosystem-level possesses sufficient buffering capacity a bleaching event in 1998, all Alveopora process. That is, removal of herbivorous to avoid being in danger of extinction colonies in the study sites were killed fish from coral reef systems by fishing within the foreseeable future throughout by mass bleaching (McClanahan et al., alters trophic interactions by reducing its range. It is possible that this species’ 2001). In Mauritius in a bleaching event herbivory on algae, thereby providing a extinction risk may increase in the in 2004, Alveopora colonies had a competitive advantage for space to algae future if global threats continue and bleaching index of 62, the second over coral. Thus, the SRR did not worsen in severity and the species’ highest of the 32 genera recorded discuss this threat in terms of coral taxa, exposure to the threats increases (McClanahan et al., 2005a). In the as its effects are difficult to distinguish throughout its range. Should the species western Indian Ocean, relative between coral genera and species. experience reduced abundance or range extinction risk scores for coral genera Therefore, an unstudied Alveopora constriction of a certain magnitude, the were calculated based on observed species is likely to have some ability of these characteristics to genus-level bleaching between 1998 and susceptibility to the trophic effects of moderate exposure to threats will 2005. The index of extinction risk was fishing. The SRR rated sedimentation, diminish. However, the species is not proportional to the degree of bleaching, nutrients, and sea-level rise as ‘‘low- likely to become of such low abundance and inversely proportional to the medium’’ importance to corals overall. or so spatially fragmented as to be in abundance and number of reefs on Although there is no other genus-level danger of extinction due to depensatory which a taxon was found on. The index or species-specific information on the processes, the potential effects of of extinction risk for Alveopora was the susceptibilities of Alveopora species to environmental stochasticity, or the ninth highest out of 47 genera, with a score of 0.41 based on a scale of 0 to 1 sedimentation and nutrients, the SRR potential for mortality from catastrophic rated them as ‘‘low-medium’’ events within the foreseeable future with 1 being the score of the highest scoring genus (McClanahan et al., importance to corals. Thus we conclude throughout its range. Therefore, M. that an unstudied Alveopora species is patula/verrilli is not warranted for 2007a). In Indonesia, colonies of Goniopora and Alveopora had a likely to have some susceptibility to listing at this time under any of the sedimentation and nutrients. Sea-level listing factors. combined disease prevalence of about 0.3 percent, which was considered low rise was not addressed at the genus or Genus Alveopora (Haapkyla et al., 2007). species level in the SRR or SIR. Increasing sea levels may increase land- Genus Introduction Genus Conclusion based sources of pollution due to The family Poritidae consists of six Based on the information from the inundation, resulting in changes to coral genera: Porites, Goniopora, Alveopora, SRR, SIR, public comments, and community structure, thus an unstudied Stylaraea, Poritipora, and Calathistes. supplemental information, we can make Alveopora species is likely to have some

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susceptibility to sea-level rise. The SRR public comment pointed out that in the et al., 2003; Sale and Szmant, 2012). rated predation and ornamental trade Marianas, this species is restricted to These changes have likely occurred, and (referred to in the proposed rule as depths greater than 60 meters. The four are occurring, from a combination of Collection and Trade) as ‘‘low’’ type specimens of A. allingi were global and local threats. Given that A. importance to corals overall. Although dredged from Pago Pago harbor, all from allingi occurs in many areas affected by there is no other genus-level or species- a depth of 100 feet or more (Hoffmeister, these broad changes, and likely has specific information on the 1925). We also gathered supplemental some susceptibility to both global and susceptibilities of Alveopora species to information, including Veron (2014), local threats, we conclude that it is collection and trade, there is no which reports that A. allingi is likely to have declined in abundance information suggesting they are not confirmed in 53 of his 133 Indo-Pacific over the past 50 to 100 years, but a susceptible to these threats. Thus we ecoregions, and strongly predicted to be precise quantification is not possible conclude that an unstudied Alveopora found in an additional 27. Thus, based based on the limited species-specific species is likely to have some on all the available information, A. information. allingi’s habitat includes lagoons, upper susceptibility to collection and trade. Other Biological Information In conclusion, an unstudied reef slopes, mid-slope terraces, lower Alveopora species is likely to have some reef slopes, and mesophotic areas in The SRR and SIR provided the susceptibility to ocean warming, depths ranging from five to greater than following information on A. allingi’s life disease, acidification, trophic effects of 60 m. history. On high latitude reefs (28 to 29 degrees South) in the Houtman fishing, sedimentation, nutrients, sea- Demographic Information level rise, predation, and collection and Abrolhos Islands, western Australia, trade. The SRR and SIR reported A. allingi’s two colonies of A. allingi were sampled abundance as usually uncommon. before the main mass spawning nights Alveopora allingi Public comments did not provide in late March 1987. There was no supplemental information on the Introduction indication of developed gametes, abundance of A. allingi. We gathered suggesting that this species does not The SRR and SIR provided the supplemental information, including participate in the mass spawning. Public following information on A. allingi’s Veron (2014), which reports that A. comments and information we gathered morphology and taxonomy. Its allingi occupied 1.2 percent of 2,984 did not provide anything additional to morphology was described as colonies dive sites sampled in 30 ecoregions of the above-described biological being encrusting or having short the Indo-Pacific, and had a mean information. irregular lobes with rounded surfaces or abundance rating of 1.27 on a 1 to 5 being columnar. Its taxonomy was rating scale at those sites in which it Susceptibility to Threats described as having no taxonomic was found. Based on this semi- To describe A. allingi’s threat issues, but being similar to Alveopora quantitative system, the species’ susceptibilities, The SRR and SIR catalai and abundance was characterized as provided genus-level information for the ‘‘uncommon,’’ and overall abundance effects on Alveopora of ocean warming, Alveopora marionensis. was described as ‘‘usually uncommon.’’ acidification, disease, sedimentation, Public comments and information we Veron did not infer trends in abundance nutrients, predation, and collection and gathered did not provide supplemental from these data. As described in the trade. The SRR and SIR also provided information on morphology, and Indo-Pacific Species Determinations the following species-specific confirmed that there are no known introduction above, based on results information on A. allingi’s threats. Low- taxonomic problems for A. allingi, and from Richards et al. (2008) and Veron to-moderate bleaching of Alveopora a low level of species identification (2014), the absolute abundance of this allingi was observed in East Africa uncertainty. Veron (2014) states that A. species is likely at least tens of millions during the 1997–1998 event. The SRR allingi is distinctive and Veron (2000; of colonies. and SIR did not provide any other 2014) considers the species valid, thus Carpenter et al. (2008) extrapolated species-specific information on the we consider it can be identified by species abundance trend estimates from effects of these threats on A. allingi. We experts and conclude that the total live coral cover trends and habitat interpreted threat susceptibility and distribution and abundance information types. For A. allingi, the overall decline exposure information from the SRR and described below for this species is in abundance (‘‘Percent Population SIR in the proposed rule for A. allingi’s sufficiently reliable (Fenner, 2014b). Reduction’’) was estimated at 35 vulnerabilities as follows: High percent, and the decline in abundance vulnerability to ocean warming, Spatial Information before the 1998 bleaching event (‘‘Back- moderate vulnerability to disease, ocean The SRR and SIR provided the cast Percent Population Reduction’’) acidification, trophic effects of reef following information on A. allingi’s was estimated at 14 percent. However, fishing, and nutrients, and low distribution, habitat, and depth range. as summarized above in the Inter-basin vulnerability to sedimentation, sea level Alveopora allingi has a very broad Comparison sub-section, live coral cover rise, predation, and collection and trade. distribution from the Red Sea and trends are highly variable both spatially Public comments did not provide Indian Ocean to most of the Pacific and temporally, producing patterns on supplemental information on A. allingi’s Ocean. The SRR reported that A. small scales that can be easily taken out threat susceptibilities. We gathered the allingi’s habitat is protected reef of context, thus quantitative inferences following species-specific and genus- environments and its depth range is five to species-specific trends should be level supplemental information on this to 10 m deep. Protected reef interpreted with caution. At the same species’ threat susceptibilities. environments includes a large diversity time, an extensive body of literature Alveopora allingi has been rated as of habitats, including lagoons, back-reef documents broad declines in live coral moderately or highly susceptible to pools, leeward reefs, and others. cover and shifts to reef communities bleaching but not to disease, but this Public comments provided dominated by hardier coral species or rating is not based on species-specific supplemental information on the algae over the past 50 to 100 years data (2008). Based on the genus-level distribution and habitat of A. allingi. A (Birkeland, 2004; Fenner, 2012; Pandolfi and species information described

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above, A. allingi is likely to have some Vulnerability to Extinction foreseeable future, but the species also susceptibility to warming-induced As explained above in the Risk occurs in shallow depths less affected bleaching, disease, acidification, trophic Analyses section, a species’ by acidification. Its habitat includes effects of fishing, sedimentation, vulnerability to extinction results from lagoons, upper reef slopes, mid-slope nutrients, seal-level rise, predation, and the combination of its spatial and terraces, lower reef slopes, and collection and trade. The available demographic characteristics, threat mesophotic areas, moderating information does not support more susceptibilities, and consideration of the vulnerability to extinction over the precise ratings of the susceptibility of A. baseline environment and future foreseeable future because the species is allingi to the threats. projections of threats. The SRR states not limited to one habitat type but occurs in numerous types of reef Regulatory Mechanisms that the high bleaching rate is the primary known threat of extinction for environments that will, on local and In the proposed rule, we did not A. allingi. It listed factors that reduce regional scales, experience highly variable thermal regimes and ocean provide any species-specific potential extinction risk including that chemistry at any given point in time. Its information on the regulatory A. allingi occupies a variety of habitat absolute abundance of at least tens of mechanisms or conservation efforts for types and is broadly distributed both millions of colonies, combined with A. allingi. Criticisms of our approach latitudinally and longitudinally in the spatial variability in ocean warming and received during public comment led us Indo-Pacific. to attempt the following analysis of Subsequent to the proposed rule, we acidification across the species range, regulatory mechanisms on a species received and gathered supplemental moderates vulnerability to extinction because the increasingly severe basis. Records confirm that A. allingi species- or genus-specific information, conditions expected in the foreseeable occurs in 53 Indo-Pacific ecoregions that described above, that expands our future will be non-uniform and encompass 40 countries’ EEZs. The 40 knowledge regarding the species therefore will likely be a large number countries are Australia, Cambodia, abundance, distribution, and threat of colonies that are either not exposed China, Djibouti, Egypt, Eritrea, susceptibilities. We developed our or do not negatively respond to a threat Federated States of Micronesia, Fiji, assessment of the species’ vulnerability at any given point in time. France (French Pacific Island to extinction using all the available Territories), Indonesia, Israel, Japan, information. As explained in the Risk Listing Determination Jordan, Madagascar, Malaysia, Maldives, Analyses section, our assessment in this In the proposed rule, using the Marshall Islands, Mauritius, final rule emphasizes the ability of the determination tool formula approach, A. Mozambique, Myanmar, New Zealand species’ spatial and demographic traits allingi was proposed for listing as (Tokelau), Niue, Palau, Papua New to moderate or exacerbate its threatened because of: High Guinea, Philippines, Samoa, Saudi vulnerability to extinction, as opposed vulnerability to ocean warming (ESA Arabia, Seychelles, South Africa, Sri to the approach we used in the Factor E); moderate vulnerability to Lanka, Sudan, Taiwan, Tanzania, proposed rule, which emphasized the disease (C) and acidification (E); Timor-Leste, Tonga, Tuvalu, United species’ susceptibility to threats. uncommon generalized range wide Kingdom (British Indian Ocean The following characteristics of A. abundance (E); moderate overall Territory), United States (CNMI, Guam, allingi, in conjunction with the distribution (based on wide geographic American Samoa, PRIAs), Vietnam, and information described in the Corals and distribution and shallow depth Yemen. The regulatory mechanisms Coral Reefs section, Coral Habitat sub- distribution (E); and inadequacy of relevant to A. allingi, described first as section, and Threats Evaluation section existing regulatory mechanisms (D). the percentage of the above countries above, affect its vulnerability to In this final rule, we changed the that utilize them to any degree and extinction currently and over the listing determination for A. allingi from second, as the percentage of those foreseeable future. Its geographic threatened to not warranted. We made countries whose regulatory mechanisms distribution includes many of the coral this determination based on a more may be limited in scope are as follows: reef ecoregions in the Indian Ocean and species-specific and holistic assessment General coral protection (28 percent western and central Pacific Ocean. Its of whether this species meets the with five percent limited in scope), geographic distribution moderates definition of either a threatened or coral collection (60 percent with 25 vulnerability to extinction because some endangered coral largely in response to percent limited in scope), pollution areas within its range are projected to public comments, including more control (45 percent with eight percent have less than average warming and appropriate consideration of the limited in scope), fishing regulations on acidification over the foreseeable future, buffering capacity of this species’ spatial reefs (88 percent with 20 percent including the western Indian Ocean and and demographic traits to lessen its limited in scope), and managing areas the central Pacific, so portions of the vulnerability to threats. Thus, based on for protection and conservation (95 population in these areas will be less the best available information above on percent with 10 percent limited in exposed to severe conditions. Its depth A. allingi’s spatial structure, scope). The most common regulatory range is from five to 60 meters. Its depth demography, threat susceptibilities, and mechanisms in place for A. allingi are range moderates vulnerability to management, none of the five ESA reef fishing regulations and area extinction over the foreseeable future listing factors, alone or in combination, management for protection and because of lower irradiance in the are causing this species to be likely to conservation. Coral collection and deeper portion of its range, sharply become endangered throughout its range pollution control laws are also reducing warming-induced bleaching. within the foreseeable future, and thus somewhat common for the species, but In addition, other threats usually occur it is not warranted for listing at this 25 percent of coral collection laws are at lower levels at mesophotic depths, time, because: limited in scope and may not provide such as sedimentation resulting from (1) Alveopora allingi’s distribution substantial protection. General coral land-based sources of pollution. across the Red Sea, Indian Ocean and protection laws are much less common However, A. allingi colonies in most of the Pacific Ocean is spread over regulatory mechanisms for the mesophotic habitat may be affected by a vast area. While some areas within its management of A. allingi. increasing acidification over the range are projected to be affected by

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warming and acidification, other areas Alveopora fenestrata quantitative system, the species’ are projected to have less than average abundance was characterized as Introduction warming and acidification, including ‘‘uncommon,’’ and overall abundance the western Indian Ocean and the The SRR and SIR provided the was also described as ‘‘uncommon.’’ central Pacific. This distribution and the following information on A. fenestrata’s Veron did not infer trends in abundance heterogeneous habitats it occupies morphology and taxonomy. Morphology from these data. As described in the reduce exposure to any given threat was described as generally Indo-Pacific Species Determinations event or adverse condition that does not hemispherical with the surface divided introduction above, based on results into lobes, and the taxonomy was occur uniformly throughout the species from Richards et al. (2008) and Veron described as having no taxonomic range. As explained above in the (2014), the absolute abundance of this issues, but it is similar to Alveopora species is likely at least tens of millions Threats Evaluation section, we have not marionensis and Alveopora verrilliana. of colonies. identified any threat that is expected to Public comments and information we Carpenter et al. (2008) extrapolated occur uniformly throughout the species gathered did not provide any new or species abundance trend estimates from range within the foreseeable future; supplemental information on total live coral cover trends and habitat (2) Alveopora allingi’s depth range morphology and confirmed that there types. For A. fenestrata, the overall down to 60 m and below includes are no known taxonomic problems for decline in abundance (‘‘Percent depths that provide a refuge from ocean A. fenestrata, but that there is a Population Reduction’’) was estimated warming, and increase the absolute area moderate to high level of species at 36 percent, and the decline in of potential occupancy throughout the identification uncertainty for this abundance before the 1998 bleaching range of the species; and species. Veron (2014) states that A. event (‘‘Back-cast Percent Population fenestrata is easily confused with other Reduction’’) was estimated at 14 (3) Alveopora allingi’s total Alveopora with similar growth form, but percent. However, as summarized above population size is at least tens of Veron (2000; 2014) considers the in the Inter-basin Comparison sub- millions of colonies, providing buffering species valid, and we consider it can be section, live coral cover trends are capacity in the form of absolute identified by experts, thus we conclude highly variable both spatially and numbers of colonies and variation in that the distribution and abundance temporally, producing patterns on small susceptibility between individual information described below for this scales that can be easily taken out of colonies. As discussed in the Corals and species is sufficiently reliable (Fenner, context, thus quantitative inferences to Coral Reefs section above, the more 2014b). species-specific trends should be colonies a species has, the lower the interpreted with caution. At the same Spatial Information proportion of colonies that are likely to time, an extensive body of literature be exposed to a particular threat at a The SRR and SIR provided the documents broad declines in live coral particular time, and all individuals that following information on A. fenestrata’s cover and shifts to reef communities are exposed will not have the same distribution, habitat, and depth range. dominated by hardier coral species or response. Alveopora fenestrata has a relatively algae over the past 50 to 100 years broad distribution from the Red Sea and (Birkeland, 2004; Fenner, 2012; Pandolfi Notwithstanding the projections Indian Ocean to the central Pacific. Its et al., 2003; Sale and Szmant, 2012). through 2100 that indicate increased habitat includes most coral reef These changes have likely occurred, and severity over time of the three high environments, such as upper reef are occurring, from a combination of importance threats, the combination of slopes, mid-slopes, lower reef slopes, global and local threats. Given that A. these biological and environmental lower reef crests, reef flats, and lagoons, fenestrata occurs in many areas affected characteristics indicates that the species and its depth range is from three to 30 by these broad changes, and likely has possesses sufficient buffering capacity m. some susceptibility to both local and to avoid being in danger of extinction Public comments provided the global threats, we conclude that it is within the foreseeable future throughout following information. Alveopora likely to have declined in abundance its range. It is possible that this species’ fenestrata occurs in Guam, but is not over the past 50 to 100 years, but a extinction risk may increase in the confirmed in the Northern Marianas. We precise quantification is not possible future if global threats continue and gathered supplemental information, based on the limited species-specific worsen in severity and the species’ including Veron (2014) which reports information. that A. fenestrata is confirmed in 39 of exposure to the threats increases Other Biological Information throughout its range. Should the species his 133 Indo-Pacific ecoregions, and experience reduced abundance or range strongly predicted to be found in an The SRR and SIR did not provide constriction of a certain magnitude, the additional 19. supplemental species-specific biological information for A. fenestrata. Public ability of these characteristics to Demographic Information comments provided no new or moderate exposure to threats will The SRR and SIR reported that A. supplemental biological information. diminish. However, the species is not fenestrata’s abundance is uncommon. likely to become of such low abundance Public comments provided the Susceptibility to Threats or so spatially fragmented as to be in following information. Alveopora To describe A. fenestrata’s threat danger of extinction due to depensatory fenestrata is rare on Guam. We gathered susceptibilities, the SRR and SIR processes, the potential effects of supplemental information including provided genus-level information for the environmental stochasticity, or the Veron (2014) which reports that A. effects on Alveopora of ocean warming, potential for mortality from catastrophic fenestrata occupied 1.98 percent of acidification, disease, sedimentation, events within the foreseeable future 2,984 dive sites sampled in 30 nutrients, predation, and collection and throughout its range. Therefore, A. ecoregions of the Indo-Pacific, and had trade. The SRR and SIR did not provide allingi is not warranted for listing at this a mean abundance rating of 1.29 on a 1 any other species-specific information time under any of the listing factors. to 5 rating scale at those sites in which on the effects of these threats on A. it was found. Based on this semi- fenestrata. We interpreted threat

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susceptibility and exposure information are as follows: General coral protection geographic distribution moderates from the SRR and SIR in the proposed (33 percent with 11 percent limited in vulnerability to extinction because some rule for A. fenestrata’s vulnerabilities as scope), coral collection (56 percent with areas within its range are projected to follows: High vulnerability to ocean 22 percent limited in scope), pollution have less than average warming and warming, moderate vulnerability to control (48 percent with 11 percent acidification over the foreseeable future, disease, ocean acidification, trophic limited in scope), fishing regulations on including the western Indian Ocean, so effects of fishing, and nutrients, and low reefs (85 percent with 22 percent portions of the population in these areas vulnerability to sedimentation, sea level limited in scope), and managing areas will be less exposed to severe rise, predation, and collection and trade. for protection and conservation (100 conditions. Its depth range is from three Public comments did not provide percent with 11 percent limited in to 30 meters. This moderates supplemental information on A. scope). The most common regulatory vulnerability to extinction over the fenestrata’s threat susceptibilities. We mechanisms in place for A. fenestrata foreseeable future because deeper areas gathered the following species-specific are reef fishing regulations and area of its range will usually have lower and genus-level supplemental management for protection and irradiance than surface waters, and information on this species’ conservation. Coral collection and acidification is generally predicted to susceptibilities. Alveopora fenestrata pollution control laws are also accelerate most in waters that are deeper has been rated as moderately or highly somewhat common for the species, but and cooler than those in which the susceptible to bleaching but not to 40 percent of coral collection laws are species occurs. Its habitat includes disease, but this rating is not based on limited in scope and may not provide upper reef slopes, mid-slopes, lower reef species-specific data (Carpenter et al., substantial protection. General coral slopes, lower reef crests, reef flats, and 2008). Darling et al. (2012) performed a protection laws are much less lagoons, moderating vulnerability to biological trait-based analysis to prominent regulatory mechanisms for extinction over the foreseeable future categorize the relative tolerance of coral the management of A. fenestrata. because the species is not limited to one species to environmental stress and A. habitat type but occurs in numerous Vulnerability to Extinction fenestrata was classified as a ‘‘stress- types of reef environments that will, on tolerant’’ species. There is no other As explained above in the Risk local and regional scales, experience species-specific information for the Analyses section, a species’ highly variable thermal regimes and susceptibility of A. fenestrata to any vulnerability to extinction results from ocean chemistry at any given point in threat. Based on the genus-level and the combination of its spatial and time. Its absolute abundance of at least species information described above, A. demographic characteristics, threat tens of millions of colonies, combined fenestrata is likely to have some susceptibilities, and consideration of the with spatial variability in ocean susceptibility to warming-induced baseline environment and future warming and acidification across the bleaching disease, acidification, trophic projections of threats. The SRR stated species range, moderates vulnerability effects of fishing, sedimentation, that a high bleaching rate is the primary to extinction because the increasingly nutrients, seal-level rise, predation, and known threat of extinction for A. severe conditions expected in the collection and trade. The available fenestrata. It listed factors that reduce foreseeable future will be non-uniform information does not support more potential extinction risk including and therefore will likely be a large precise ratings of the susceptibility of A. occupying a range of depths and being number of colonies that are either not fenestrata to the threats. broadly distributed both latitudinally exposed or do not negatively respond to and longitudinally in the Indo-Pacific. a threat at any given point in time. Regulatory Mechanisms Subsequent to the proposed rule, we In the proposed rule, we did not received and gathered supplemental Listing Determination provide any species-specific species- or genus-specific information, In the proposed rule, using the information on the regulatory described above, that expands our determination tool formula approach, A. mechanisms or conservation efforts for knowledge regarding the species fenestrata was proposed for listing as A. fenestrata. Criticisms of our approach abundance, distribution, and threat threatened because of: High received during public comment led us susceptibilities. We developed our vulnerability to ocean warming (ESA to attempt the following analysis of assessment of the species’ vulnerability Factor E); moderate vulnerability to regulatory mechanisms on a species to extinction using all the available disease (C) and acidification (E); basis. Records confirm that A. fenestrata information. As explained in the Risk uncommon generalized range wide occurs in 39 Indo-Pacific ecoregions that Analyses section, our assessment in this abundance (E); wide overall distribution encompass 27 countries’ EEZs. The 27 final rule emphasizes the ability of the (based on wide geographic distribution countries are Australia, Brunei, China, species’ spatial and demographic traits and moderate depth distribution (E); Egypt, Federated States of Micronesia, to moderate or exacerbate its and inadequacy of existing regulatory France (French Pacific Island vulnerability to extinction, as opposed mechanisms (D). Territories), Indonesia, Israel, Jordan, to the approach we used in the In this final rule, we changed the Kenya, Madagascar, Malaysia, Marshall proposed rule, which emphasized the listing determination for A. fenestrata Islands, Mauritius, Papua New Guinea, species’ susceptibility to threats. from threatened to not warranted. We Philippines, Saudi Arabia, Seychelles, The following characteristics of A. made this determination based on a Solomon Islands, Sri Lanka, Sudan, fenestrata, in conjunction with the more species-specific and holistic Taiwan, Tanzania, Timor-Leste, United information described in the Corals and assessment of whether this species States (CNMI, Guam, PRIAs), Vanuatu, Coral Reefs section, Coral Habitat sub- meets the definition of either a and Vietnam. The regulatory section, and Threats Evaluation section threatened or endangered coral largely mechanisms relevant to A. fenestrata, above, affect its vulnerability to in response to public comments, first described as the percentage of the extinction currently and over the including more appropriate above countries that utilize them to any foreseeable future. Its geographic consideration of the buffering capacity degree, and second as the percentage of distribution includes many of the coral of this species’ spatial and demographic those countries whose regulatory reef ecoregions in the Indian Ocean and traits to lessen its vulnerability to mechanisms may be limited in scope, western and central Pacific Ocean. Its threats. Thus, based on the best

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available information above on A. likely to become of such low abundance ecoregions, and strongly predicted to be fenestrata’ spatial structure, or so spatially fragmented as to be in found in an additional 30. One of the 30 demography, threat susceptibilities, and danger of extinction due to depensatory strongly predicted ecoregions is the management, none of the five ESA processes, the potential effects of Main Hawaiian Islands (Veron, 2014), listing factors, alone or in combination, environmental stochasticity, or the and may be based on reports that are causing this species to be likely to potential for mortality from catastrophic Hawaii is a similar type ecoregion. become endangered throughout its range events within the foreseeable future However, there are no reliable reports of within the foreseeable future, and thus throughout its range. Therefore, A. the species being found in the Main it is not warranted for listing at this fenestrata is not warranted for listing at Hawaiian Islands, in spite of many time, because: this time under any of the listing factors. divers in the water observing coral (1) Alveopora fenestrata’s distribution species (Douglas Fenner, personal across approximately three quarters of Alveopora verrilliana com.). Veron (2014)’s map indicates that the Indo-Pacific region is spread over a Introduction the report(s) of this species from the Red vast area. While some areas within its Sea have also not been verified. range are projected to be affected by The SRR and SIR provided the warming and acidification, other areas following information on A. verrilliana’s Demographic Information are projected to have less than average morphology and taxonomy. Morphology The SRR and SIR reported A. warming and acidification, including was described as short irregularly verrilliana’s abundance as the western Indian Ocean and the dividing knob-like branches and the ‘‘uncommon.’’ Public comments central Pacific. This distribution and the taxonomy was described as having no provided the following supplemental heterogeneous habitats it occupies taxonomic issues. Alveopora verrilliana information on A. verrilliana’s reduce exposure to any given threat is similar to Alveopora fenestrata. abundance. One public comment stated event or adverse condition that does not Public comments and information we that A. verrilliana is uncommon in the occur uniformly throughout the species gathered did not provide any new or Marianas with only 10 to12 colonies range. As explained above in the supplemental information on recorded so far. We gathered the Threats Evaluation section, we have not morphology, and confirmed that there following supplemental information on identified any threat that is expected to are no known taxonomic problems for the abundance of A. verrilliana. Veron occur uniformly throughout the species A. verrilliana, but that there is a high (2014) reports that A. verrilliana range within the foreseeable future; level of species identification occupied 0.27 percent of 2,984 dive (2) Alveopora fenestrata’s depth range uncertainty for this species. Veron sites sampled in 30 ecoregions of the down to 30 m and below includes (2014) states that A. verrilliana is easily Indo-Pacific, and had a mean abundance depths that provide a refuge from ocean confused with other Alveopora with a rating of 1.13 on a 1 to 5 rating scale at warming, and increase the absolute area similar growth form and it is impossible those sites in which it was found. Based of potential occupancy throughout the to confirm many citations of this on this semi-quantitative system, the range of the species; and species. However, Veron (2000; 2014) species’ abundance was characterized as (3) Alveopora fenestrata’s total considers the species valid, and we ‘‘rare,’’ and overall abundance was population size is at least tens of consider it can be identified by experts, described as ‘‘uncommon.’’ Veron did millions of colonies, providing buffering thus we conclude that the distribution not infer trends in abundance from capacity in the form of absolute and abundance information described these data. As described in the Indo- numbers of colonies and variation in below for this species is sufficiently Pacific Species Determinations susceptibility between individual reliable (Fenner, 2014b). introduction above, based on results colonies. As discussed in the Corals and Spatial Information from Richards et al. (2008) and Veron Coral Reefs section above, the more (2014), the absolute abundance of this colonies a species has, the lower the The SRR and SIR provided the species is likely at least millions of proportion of colonies that are likely to following information on A. verrilliana’s colonies. be exposed to a particular threat at a distribution, habitat, and depth range. Carpenter et al. (2008) extrapolated particular time, and all individuals that Alveopora verrilliana’s distribution is species abundance trend estimates from are exposed will not have the same from the Red Sea to the central Indo- total live coral cover trends and habitat response. Pacific to most of the Pacific. Its habitat types. For A. verrilliana, the overall Notwithstanding the projections includes most coral reef environments, decline in abundance (‘‘Percent through 2100 that indicate increased such as upper reef slopes, mid-slopes, Population Reduction’’) was estimated severity over time of the three high lower reef slopes, lower reef crests, reef at 34 percent, and the decline in importance threats, the combination of flats, and lagoons, and its depth range abundance before the 1998 bleaching these biological and environmental is three to at least 40 meters depth, and event (‘‘Back-cast Percent Population characteristics indicates that the species possibly down to 80 meters (it is not Reduction’’) was estimated at 14 possesses sufficient buffering capacity certain that the identity of the coral at percent. However, as summarized above to avoid being in danger of extinction 80 meters has been verified). in the Inter-basin Comparison sub- within the foreseeable future throughout Public comments provided the section, live coral cover trends are its range. It is possible that this species’ following supplemental information on highly variable both spatially and extinction risk may increase in the A. verrilliana’s distribution, habitat and temporally, producing patterns on small future if global threats continue and depth range. One public comment stated scales that can be easily taken out of worsen in severity and the species’ that A. verrilliana has been found in the context, thus quantitative inferences to exposure to the threats increases Marianas on shallow fringing reef species-specific trends should be throughout its range. Should the species platforms at a depth between 1.5 and 2 interpreted with caution. At the same experience reduced abundance or range meters deep, and a terrace at 17 meters time, an extensive body of literature constriction of a certain magnitude, the deep. We gathered supplemental documents broad declines in live coral ability of these characteristics to information, including Veron (2014), cover and shifts to reef communities moderate exposure to threats will which reports that A. verrilliana is dominated by hardier coral species or diminish. However, the species is not confirmed in 28 of his 133 Indo-Pacific algae over the past 50 to 100 years

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(Birkeland, 2004; Fenner, 2012; Pandolfi trophic effects of fishing, sedimentation, that the high bleaching rate is the et al., 2003; Sale and Szmant, 2012). nutrients, seal-level rise, predation, and primary known threat of extinction for These changes have likely occurred, and collection and trade. The available A. verrilliana. It listed factors that are occurring, from a combination of information does not support more reduce potential extinction risk global and local threats. Given that A. precise ratings of the susceptibility of A. including that A. verrilliana occupies a verrilliana occurs in many areas affected verrilliana to the threats. variety of habitat types and is broadly by these broad changes, and likely has distributed both latitudinally and Regulatory Mechanisms some susceptibility to both global and longitudinally in the Indo-Pacific. local threats, we conclude that it is In the proposed rule, we did not Subsequent to the proposed rule, we likely to have declined in abundance provide any species-specific received and gathered supplemental over the past 50 to 100 years, but a information on the regulatory species- or genus-specific information, precise quantification is not possible mechanisms or conservation efforts for described above, that expands our based on the limited species-specific A. verrilliana. Criticisms of our knowledge regarding the species information. approach received during public abundance, distribution, and threat comment led us to attempt the following susceptibilities. We developed our Other Biological Information analysis of regulatory mechanisms on a assessment of the species’ vulnerability The SRR and SIR provided the species basis. Records confirm that A. to extinction using all the available following information on A. verrilliana’s verrilliana occurs in 28 Indo-Pacific information. As explained in the Risk life history. Alveopora verrilliana is a ecoregions that encompass 23 countries’ Analyses section, our assessment in this hermaphroditic broadcast spawner. On EEZs. The 23 countries are Australia, final rule emphasizes the ability of the temperate latitude reefs (28 to 29 Brunei, Cambodia, China, Federated species’ spatial and demographic traits degrees S) in the Houtman Abrolhos States of Micronesia, France (French to moderate or exacerbate its Islands, western Australia, seven of 12 Pacific Island Territories), Indonesia, vulnerability to extinction, as opposed colonies sampled had ripe gametes, and Japan, Malaysia, New Zealand to the approach we used in the spawning was inferred during the time (Tokelau), Niue, Palau, Papua New proposed rule, which emphasized the of mass spawning for this region. Public Guinea, Philippines, Samoa, Solomon species’ susceptibility to threats. comments and information we gathered Islands, Taiwan, Thailand, Tonga, The following characteristics of A. did not provide anything additional to Tuvalu, United States (CNMI, Guam, verrilliana, in conjunction with the the above-described biological American Samoa), Vanuatu, and information described in the Corals and information. Vietnam. The regulatory mechanisms Coral Reefs section, Coral Habitat sub- relevant to A. verrilliana, described first section, and Threats Evaluation section Susceptibility to Threats as the percentage of the above countries above, affect its vulnerability to To describe A. verrilliana’s threat that utilize them to any degree, and extinction currently and over the susceptibilities, The SRR and SIR second as the percentages of those foreseeable future. Its geographic provided genus-level information for the countries whose regulatory mechanisms distribution includes many of the coral effects on Alveopora of ocean warming, may be limited in scope, are as follows: reef ecoregions in the western and acidification, disease, sedimentation, General coral protection (30 percent central Pacific Ocean. Its geographic nutrients, predation, and collection and with 4 percent limited in scope), coral distribution moderates vulnerability to trade. The SRR and SIR did not provide collection (61 percent with 35 percent extinction because some areas within its any other species-specific information limited in scope), pollution control (39 range are projected to have less than on the effects of these threats on A. percent with 13 percent limited in average warming and acidification over verrilliana. We interpreted threat scope), fishing regulations on reefs (100 the foreseeable future, including the susceptibility and exposure information percent with 17 percent limited in central Pacific, so portions of the from the SRR and SIR in the proposed scope), and managing areas for population in these areas will be less rule for A. verrilliana’s vulnerabilities as protection and conservation (100 exposed to severe conditions. Its depth follows: High vulnerability to ocean percent with none limited in scope). range is from three to 40 meters, which warming, moderate vulnerability to The most common regulatory moderates vulnerability to extinction disease, ocean acidification, trophic mechanisms in place for A. verrilliana over the foreseeable future because of effects of reef fishing, and nutrients, and are reef fishing regulations and area lower irradiance in the deeper portion low vulnerability to sedimentation, sea management for protection and of its range, sharply reducing warming- level rise, predation, and collection and conservation. Coral collection laws are induced bleaching. In addition, other trade. also somewhat common for the species, threats usually occur at lower levels at Public comments did not provide any but 35 percent of coral collection laws mesophotic depths, such as new or supplemental information on A. are limited in scope and may not sedimentation resulting from land-based verrilliana’s threats. We gathered the provide substantial protection. General sources of pollution. However, A. following species-specific and genus- coral protection and pollution control verrilliana colonies in mesophotic level supplemental information on this laws are much less common regulatory habitat may be affected by increasing species’ threat susceptibilities. mechanisms for the management of A. acidification over the foreseeable future, Alveopora verrilliana has been rated as verrilliana. but the species also occurs in shallow moderately or highly susceptible to depths less affected by acidification. Its bleaching but not to disease, but this Vulnerability to Extinction habitat includes most coral reef rating is not based on species-specific As explained above in the Risk environments, such as upper reef data (2008). There is no species-specific Analyses section, a species’ slopes, mid-slopes, lower reef slopes, information for the exposure or vulnerability to extinction results from lower reef crests, reef flats, and lagoons. susceptibility of A. verrilliana to any the combination of its spatial and This moderates vulnerability to threat. Based on the genus-level and demographic characteristics, threat extinction over the foreseeable future species information described above, A. susceptibilities, and consideration of the because the species is not limited to one verrilliana likely has some susceptibility baseline environment and future habitat type but occurs in numerous to ocean warming, disease, acidification, projections of threats. The SRR states types of reef environments that will, on

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local and regional scales, experience range. As explained above in the The larvae of all Porites species studied highly variable thermal regimes and Threats Evaluation section, we have not contain zooxanthellae that can ocean chemistry at any given point in identified any threat that is expected to supplement maternal provisioning with time. Its total abundance is unknown, occur uniformly throughout the species energy sources provided by their and it is uncommon or rare. Its absolute range within the foreseeable future; photosynthesis. The SRR and SIR abundance of at least millions of (2) Alveopora verrilliana’s depth provided no genus-level introductory colonies, combined with spatial distribution down to 40 meters includes information on Porites. variability in ocean warming and depths that provide a refuge from ocean Genus Susceptibility to Threats acidification across the species range, warming, and increase the absolute area moderates vulnerability to extinction of potential occupancy throughout the The SRR and SIR provided the because the increasingly severe range of the species; and following information on the threat conditions expected in the foreseeable (3) Alveopora verrilliana’s total susceptibilities of the genus Porites. On future will be non-uniform and population size is at least millions of the GBR and in the western Indian therefore will likely be a large number colonies, providing buffering capacity in Ocean, massive Porites generally have of colonies that are either not exposed the form of absolute numbers of moderate susceptibility to bleaching, or do not negatively respond to a threat colonies and variation in susceptibility while branching Porites generally have at any given point in time. between individual colonies. As higher susceptibility to bleaching, comparable to Pocillopora and Listing Determination discussed in the Corals and Coral Reefs section above, the more colonies a Acropora. For example, Porites In the proposed rule, using the species has, the lower the proportion of horizontalata was a bleaching ‘‘loser’’ in determination tool formula approach, A. colonies that are likely to be exposed to Okinawa, disappearing after the 1998 verrilliana was proposed for listing as a particular threat at a particular time, event. Recent work comparing P. lobata threatened because of: High and all individuals that are exposed will from extreme lagoonal environments vulnerability to ocean warming (ESA not have the same response. with individuals from more benign Factor E); moderate vulnerability to Notwithstanding the projections forereef habitats in American Samoa disease (C) and acidification (E); through 2100 that indicate increased indicates that thermal history of these uncommon generalized range wide severity over time of the three high corals plays a large part in their reaction abundance (E); wide overall distribution importance threats, the combination of to thermal stress. (based on wide geographic distribution these biological and environmental The SRR reported that a study that and wide depth distribution (E); and characteristics indicates that the species looked at 328 colonies of massive inadequacy of existing regulatory possesses sufficient buffering capacity Porites from 69 reefs of the GBR found mechanisms (D). to avoid being in danger of extinction a decline in calcification of 14.2 percent In this final rule, we changed the within the foreseeable future throughout since 1990, predominantly because listing determination for A. verrilliana its range. It is possible that this species’ extension declined by 13.3 percent. This from threatened to not warranted. We extinction risk may increase in the is similar to the estimates of a global made this determination based on a future if global threats continue and decline in aragonite saturation state of 16 percent since the beginning of global more species-specific and holistic worsen in severity and the species’ assessment of whether this species industrialization. The study agreed with exposure to the threats increases meets the definition of either a earlier, more limited work on Porites on throughout its range. Should the species threatened or endangered coral largely the GBR and in laboratory and experience reduced abundance or range in response to public comments, mesocosm experiments that showed constriction of a certain magnitude, the including more appropriate declines in calcification with reduced ability of these characteristics to consideration of the buffering capacity aragonite saturation state in P. moderate exposure to threats will of this species’ spatial and demographic cylindrical, P. compressa, and P. lutea diminish. However, the species is not traits to lessen its vulnerability to adults, and P. astreoides juveniles. likely to become of such low abundance threats. Thus, based on the best Acidification has not been found to or so spatially fragmented as to be in available information above on A. interfere with settlement of larvae in P. danger of extinction due to depensatory verrilliana’s spatial structure, astreoides in the Caribbean. demography, threat susceptibilities, and processes, the potential effects of The SRR reported several studies management, none of the five ESA environmental stochasticity, or the showing subacute (lesions resulting in listing factors, alone or in combination, potential for mortality from catastrophic slow progressive tissue loss) tissue loss, are causing this species to be likely to events within the foreseeable future black band disease, and endolithic become endangered throughout its range throughout its range. Therefore, A. hypermycosis in Porites. The SIR within the foreseeable future, and thus verrilliana is not warranted for listing at reported that the genus Porites had the it is not warranted for listing at this this time under any of the listing factors. highest prevalence of disease time, because: Genus Porites throughout Guam; however, it may have (1) Alveopora verrilliana’s also been a function of the fact that distribution across more than half of the Genus Introduction Porites corals are also the most common. Indo-Pacific region is spread over a vast Porites colonies are flat (laminar or Likewise, in a study from Hawaii, with area. While some areas within its range encrusting), massive, or branching. 12 diseases recorded among three coral are projected to be affected by warming Massive colonies are spherical or genera, Porites was shown to have the and acidification, other areas are hemispherical when small, and helmet highest prevalence of disease. Porites projected to have less than average or dome-shaped when large, and may be was also shown to have severe damage warming and acidification, including over five meters across (Veron, 2000). as a result of high disease prevalence of the central Pacific. This distribution and Porites is the third largest genus of reef black-band disease in Southeastern the heterogeneous habitats it occupies building scleractinia, and Veron (2000) India. reduce exposure to any given threat recognizes 52 species. This description The SRR reported that Porites is event or adverse condition that does not of the Porites genus focuses on the Indo- susceptible to crown-of-thorns seastar occur uniformly throughout the species Pacific, where most of the species occur. (Acanthaster planci) and corallivorous

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snail predation, including predation of genera, and had 32 percent as much highest prevalence, with 6.7 percent of Coralliphilia violacea on both massive bleaching as the most bleached genus colonies having disease (Myers and and branching forms. Massive Porites (Vargas-Angel et al., 2011). Porites in Raymundo, 2009). Porites was tied for are susceptible, but not a preferred prey, Okinawa, Japan, experienced no the second highest disease prevalence of of the predatory asteroid Culcita decrease in populations following the 12 genera in New Caledonia, with 0.7 novaeguineae, and the butterflyfish 1998 and 2010 mass bleaching episodes. percent of colonies showing disease Chaetodon unimaculatus. Porites is Okinawa has turbid waters from runoff (Tribollet et al., 2011). Porites massive intermediate for its sediment tolerance increased by human activities (Hongo was tied for third highest disease in the western Indian Ocean. In and Yamano, 2013). prevalence of 35 taxa in Indonesia, with contrast, Porites is often found in In areas of Papua New Guinea, where 1.5 percent prevalence. Porites relatively turbid waters in Asia and the volcanic carbon dioxide bubbling branching had the 14th highest disease eastern Pacific and were considered produced pH equal to that predicted for prevalence of 35 taxa in Indonesia, with sediment tolerant. About 25,000–50,000 2100, massive Porites dominated the 0.25 percent of colonies showing pieces of Porites spp. per year are community, indicating they are more disease. Other Porites had no disease in traded. resistant to low pH than other corals Indonesia (Haapkyla et al., 2007). The public comments did not provide (Fabricius et al., 2011). Massive Porites Predation was studied by De’ath and any new or supplemental information growth rates in bays in Palau, with pH Moran (1998), who reported that Porites on the threat susceptibilities of the approaching that predicted for 2100 and was the least preferred prey of crown- genus Porites. We gathered aragonite saturation equal to that of-thorns starfish out of the 10 most supplemental information that provided predicted for 2100, was similar to common genera on 15 reefs in the GBR. the following. Thermal stress was colonies in water with current mean pH Porites species are relatively less studied by Gleason (1993), who reported and aragonite saturation (Shamberger et susceptible to the effects of land-based that Porites was little affected by al., in press). sources of pollution than many other bleaching in Moorea, French Polynesia. Raymundo et al. (2005) reported that reef-building corals. Porites species are Bruno et al. (2001) reported that in Porites had the highest levels of disease heavily collected and widely traded Palau in 2000, four different species of in the Philippines, where only rarely internationally. There is no information Porites ranged from low-moderate levels did other genera show disease. on the effects of fishing, sea-level rise, of bleaching to very high-moderate, and Individual species of Porites differed or any other threat to Porites species. ranged from low-moderate mortality to greatly in the prevalence of disease, Genus Conclusions high mortality. Done et al. (2003b) with zero prevalence in about half of the reported bleaching levels in seven species, and a wide range of prevalence Based on the information from the species of Porites and one in the others. Further, there was no SRR, SIR, public comments, and morphological group (massive) of consistent difference between massive supplemental information, we can make Porites. Individual species ranged from and branching species: branching the following inferences about the eight to 33 percent affected by species displayed the entire range of susceptibilities of an unstudied Porites bleaching. The two least affected species prevalence; massive Porites having species to ocean warming, disease, (P. cylindrica and P. annae) were relatively high prevalence, though not acidification, sedimentation, nutrients, branching and the most affected was as high as three branching species; and trophic effects of fishing, sea-level rise, massive (P. vaughani), though it had a one massive Porites (P. evermanni) predation, and collection and trade. The low mortality. Generally, massive having zero prevalence (Raymundo et SRR rated ocean warming and disease as Porites were affected more than average. al., 2005). Porites had the lowest ‘‘high’’ importance, and ocean The species with the greatest mortality prevalence of disease (0.025 percent) of acidification as ‘‘medium-high’’ was a species with columns and plates the only five genera with diseases importance, to corals. These were rated (P. rus) though another species (P. recorded in American Samoa. Porites as the three most important threats to lichen) with columns and plates had a tissue loss was found at 15 percent of reef-building corals overall. Most mortality rate nearly as low as the sites compared to 71 percent of sites for studies reported moderate to high levels lowest mortality species, and another Acropora white syndrome, the most of bleaching in Porites, but one study species with columns (P. heronensis) common disease(Fenner and Heron, reported low levels and some individual had high bleaching (Done et al., 2003b). 2008). In another study in American species had low levels. In three studies, Pandolfi et al. (2011) reported that Samoa, Porites had the third highest branching species showed higher levels massive species of Porites bleached level of prevalence of any genus, with of bleaching than massive species, and about average for genera in Kenya and a prevalence of 0.11 percent (Aeby et one study showed the reverse. Australia in 1998. A study that al., 2008). Growth anomalies are Generally, Porites as a whole has monitored the impacts of the 1998 and occasional on massive Porites in moderate to high susceptibility to ocean 2010 bleaching events on coral in Japan backreef pools on Ofu, American Samoa warming. However, different species of (van Woesik et al., 2011) reported that but less common on reef slopes in Porites have a wide range of one species of branching Porites was American Samoa. Growth anomalies are susceptibilities to ocean warming, thus neither a winner or a loser (increasing abundant on one color morph of Porites we conclude that an unstudied Porites from 1.4 percent cover to four percent cylindrica in one small area of one back species has some susceptibility to ocean and then decreasing to 0.9 percent), and reef pool in Tutuila, American Samoa, warming. Most studies found high six species of branching Porites were but not on another color morph. A white levels of disease in Porites, but one long-term losers (decreasing to 0 percent disease that is rare on Tutuila, killed all study found low levels. We conclude cover and staying there). Vargas-Angel Porites rus colonies (about 50) in front that an unstudied Porites species has et al. (2011) reported that Porites had a of Vaoto Lodge, Ofu, American Samoa. some susceptibility to disease. Several fairly low percentage of bleaching on What appears to possibly be the same studies reported that calcification Howland and Baker islands in the U.S. disease is killing all yellow massive declined with decreasing pH in short Pacific, with 16.1 percent on Baker and Porites in the Hurricane House back reef term experiments, but massive Porites 24.6 percent on Howland. Porites was pool on Ofu, American Samoa (Fenner, are common and have normal growth the ninth most-bleached genus out of 14 2013b). In Guam, Porites had by far the rates in natural areas of low pH. We

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conclude that Porites has some horizontalata’s morphology and upper reef slopes, mid-slope terraces, susceptibility to ocean acidification. taxonomy. Morphology was described lower reef crests, and lagoons in depth The SRR rated the trophic effects of as composites of encrusting plates and ranging from five to 30 m depth. fishing as ‘‘medium’’ importance, the contorted fused branches. With respect Demographic Information fourth most important threat to corals to taxonomy, Porites is known to be overall. This threat was not addressed at morphologically plastic and multiple The SRR and SIR provided the the genus or species level in the SRR or sympatric species frequently exhibit following information on P. SIR, because it is an ecosystem-level intergradation of skeletal characteristics. horizontalata’s abundance. Porites process. That is, removal of herbivorous The results of a study of genetics of horizontalata has been reported as fish from coral reef systems by fishing other Porites species found that genetics sometimes common. Public comments alters trophic interactions by reducing did not correspond well with Porites did not provide any new or herbivory on algae, thereby providing a species based on morphology. The supplemental information on P. competitive advantage for space to algae laminar parts of colonies of P. horizontalata’s abundance. We gathered over coral. Thus, the SRR did not horizontalata resemble Porites supplemental information including discuss this threat in terms of coral taxa, vaughani, the branching parts may have Veron (2014) and Richards et al. (2008). as its effects are difficult to distinguish corallites arranged in a star-like pattern Veron (2014) reports that P. between coral genera and species. like Porites rus, and the corallite horizontalata occupied 4.2 percent of Therefore, an unstudied Porites species features are most similar to Porites 2,984 dive sites sampled in 30 is likely to have some susceptibility to eridani. ecoregions of the Indo-Pacific, and had the trophic effects of fishing. Public comments and information we a mean abundance rating of 1.62 on a 1 The SRR rated sedimentation, gathered did not provide any new or to 5 rating scale at those sites in which nutrients, and sea-level rise as ‘‘low- supplemental information on it was found. Based on this semi- medium’’ importance to corals overall. morphology, and confirmed that there quantitative system, the species’ Porites is reported to have intermediate are no known taxonomic problems for P. abundance was characterized as to high sediment tolerance. Thus we horizontalata, and that there is a ‘‘uncommon,’’ and overall abundance conclude that an unstudied Porites has moderate level of species identification was described as ‘‘sometimes common some susceptibility to sedimentation. uncertainty for this species. Veron in isolated habitats.’’ Veron did not infer Although there is no genus-level or (2000; 2014) states that P. horizontalata trends in abundance from these data. As species-specific information on the is easily confused with P. rus, but the described in the Indo-Pacific Species susceptibilities of Porites species to species can be identified by experts Determinations introduction above, nutrients, the SRR rated it as ‘‘low- (Fenner, 2014b), thus we conclude that based on results from Richards et al. medium’’ importance to corals.. Thus, the distribution and abundance (2008) and Veron (2014), the absolute we conclude that an unstudied Porites information described below for this abundance of this species is likely at species has some susceptibility to species is sufficiently reliable (Fenner, least tens of millions of colonies. Carpenter et al. (2008) extrapolated nutrients. Sea-level rise was not 2014b). species abundance trend estimates from addressed at the genus or species level Spatial Information total live coral cover trends and habitat in the SRR or SIR. Increasing sea levels The SRR and SIR provided the types. For P. horizontalata, the overall may increase land-based sources of following information on P. decline in abundance (‘‘Percent pollution due to inundation, resulting in horizontalata’s distribution, habitat, and Population Reduction’’) was estimated changes to coral community structure, depth range. Porites horizontalata’s at 37 percent, and the decline in thus an unstudied Porites species is distribution is from the central Indian abundance before the 1998 bleaching likely to have some susceptibility to sea- Ocean to the central Indo-Pacific and event (‘‘Back-cast Percent Population level rise. The SRR rated predation and central Pacific. The SRR reported that P. Reduction’’) was estimated at 15 ornamental trade (referred to in the horizontalata’s habitat is shallow reef percent. However, as summarized above proposed rule as Collection and Trade) environments, and the depth range is in the Inter-basin Comparison sub- as ‘‘low’’ importance to corals overall. from five to 20 m, though it is also section, live coral cover trends are The only study of predation reporting known to range into deep water. Porites highly variable both spatially and on Porites indicated it was a not a horizontalata is uncommon in Guam temporally, producing patterns on small preferred prey item of crown-of-thorns and found in deeper quiet waters. scales that can be easily taken out of starfish. Thus, we conclude that Porites Public comments did not provide any context, thus quantitative inferences to has a low susceptibility to predation. new or supplemental information on P. species-specific trends should be Porites species are heavily collected and horizontalata’s distribution. We interpreted with caution. At the same widely traded internationally. Thus we gathered supplemental information time, an extensive body of literature conclude that Porites has some including Veron (2014), which reports documents broad declines in live coral susceptibility to collection and trade. that P. horizontalata is confirmed in 28 cover and shifts to reef communities In conclusion, an unstudied Porites of his 133 Indo-Pacific ecoregions, and dominated by hardier coral species or species is likely to have some strongly predicted to be found in an algae over the past 50 to 100 years susceptibility to ocean warming, additional 13. Supplemental (Birkeland, 2004; Fenner, 2012; Pandolfi disease, ocean acidification, trophic information on the depth range of P. et al., 2003; Sale and Szmant, 2012). effects of fishing, sedimentation, horizontalata in American Samoa These changes have likely occurred, and nutrients, sea-level rise, and collection indicates it is from about 10 m to at least are occurring, from a combination of and trade, and low susceptibility to 30 m deep, and it has been observed at global and local threats. Given that P. predation. 20 to 30 m of depth in New Caledonia, horizontalata occurs in many areas Porites horizontalata where it appears much as it does in affected by these broad changes, and American Samoa in similar locations (D. that it likely has some susceptibility to Introduction Fenner, personal comm.). Thus, based both global and local threats, we The SRR and SIR provided the on all the available information, P. conclude that it is likely to have following information on P. horizontalata’s habitat includes at least declined in abundance over the past 50

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to 100 years, but a precise quantification (Goreau et al., 1972) as well as information on regulatory mechanisms is not possible based on the limited observations on Guam suggest that or conservation efforts for P. species-specific information. Porites species in the subgenus horizontalata. Criticisms of our Synaraea are among the least-preferred approach received during public Other Biological Information prey of the crown-of-thorns starfish. The comment led us to the following The SRR and SIR provided the comment stated that other studies analysis to attempt to analyze regulatory following information on P. (Colgan, 1987; Pratchett, 2007) suggest mechanisms on a species basis. Records horizontalata’s life history. Porites that Porites species in general are among confirm that P. horizontalata occurs in horizontalata is a gonochoric broadcast the least preferred prey of crown-of- 28 Indo-Pacific ecoregions that spawner. Although specific observations thorns. The comment further stated that encompass 25 countries’ EEZs. The 25 have not been published for this workers on Guam have never seen countries are Brunei, China, Federated species, the larvae of all other Porites crown-of-thorns predation on P. States of Micronesia, Fiji, France species studied contain zooxanthellae horizontalata and suspect that this (French Pacific Island Territories), that can supplement maternal species is among the least preferred prey Indonesia, Japan, Malaysia, Marshall provisioning with energy sources of crown-of-thorns. The comment Islands, Myanmar, New Zealand provided by their photosynthesis. The suggests changing the predation (Tokelau), Niue, Palau, Papua New public comments did not provide new susceptibility to low (3) or moderate to Guinea, Philippines, Samoa, Solomon or supplemental information, and we low (2.5) in the determination tool. A Islands, Taiwan, Thailand, Timor-Leste, did not find new or supplemental third comment suggested P. Tonga, Tuvalu, United States (CNMI, information on the above-described horizontalata be considered a Guam, American Samoa, PRIAs), biological information. ‘‘Synaraea’’ species instead of a Vanuatu, and Vietnam. The regulatory Susceptibility to Threats branching Porites species. The common mechanisms relevant to P. Synaraea species Porites rus has horizontalata, described first as the To describe P. horizontalata’s threat bleaching levels that are lower than both susceptibilities, the SRR and SIR percentage of the above countries that Porites branching and Porites massive utilize them to any degree and second, provided genus-level information for the corals. Porites horizontalata is within effects on Porites of ocean warming, as the percentages of those countries the Synaraea sub-genus and has not whose regulatory mechanisms may be acidification, disease, predation, been observed to bleach in Guam to sedimentation, nutrients, and collection limited in scope, are as follows: General date. coral protection (28 percent with 4 and trade. The SRR and SIR also We gathered the following provided the following species-specific percent limited in scope), coral supplemental species-specific collection (64 percent with 40 percent information on P. horizontalata’s information on susceptibility to threats threats. Porites horizontalata was a limited in scope), pollution control (36 for P. horizontalata. This species has percent with 12 percent limited in bleaching ‘‘loser’’ in Okinawa, been rated as moderately or highly disappearing after the 1998 event. The scope), fishing regulations on reefs (96 susceptible to bleaching and disease, percent with 16 percent limited in SRR and SIR did not provide any other but this rating is not based on species- species-specific information on the scope), and managing areas for specific data (Carpenter et al., 2008). protection and conservation (96 percent effects of these threats on P. Porites horizontalata was found to be a horizontalata. We interpreted threat with 4 percent limited in scope). The long term loser in Japan following most common regulatory mechanisms in susceptibility and exposure information bleaching events (decreasing from 1.2 place for P. horizontalata are reef from the SRR and SIR in the proposed percent cover to zero and staying there) fishing regulations and area rule for P. horizontalata’s vulnerabilities (van Woesik et al., 2011). Porites management for protection and as follows: High vulnerability to ocean horizontalata had the ninth highest conservation. Coral collection laws are warming; moderate vulnerability to disease prevalence of 21 species of also somewhat utilized for the species, disease, ocean acidification, trophic Porites in the Philippines. Porites but 40 percent of coral collection laws effects of reef fishing, and nutrients, and horizontalata had a prevalence of 4, are limited in scope and may not low vulnerability to sedimentation, sea which was 20 percent of the prevalence provide substantial protection. General level rise, predation, and collection and of the species with the highest coral protection and pollution control trade. prevalence (Raymundo et al., 2005). Several public comments provided There is no species-specific information laws are less prominent regulatory supplemental information on P. for the susceptibility of P. horizontalata mechanisms for the management of P. horizontalata’s threat susceptibilities. to any other threat. Based on horizontalata. One public comment stated that the information provided in the Porites Vulnerability to Extinction Loya (2001) study of the effects of genus description and the species- bleaching in Okinawa, which reported specific information above, P. As explained above in the Risk P. horizontalata as a loser, did not horizontalata likely has some Analyses section, a species’ actually directly observe bleaching but susceptibility to ocean warming, vulnerability to extinction results from rather looked at before and after disease, acidification, trophic effects of the combination of its spatial and abundances and deduced that species fishing, sedimentation, nutrients, sea- demographic characteristics, threat had or had not suffered from bleaching. level rise, and collection and trade, and susceptibilities, and consideration of the It also stated that the sampling effort low susceptibility to predation. The baseline environment and future was small and the changes in low available information does not support projections of threats. The SRR stated abundances may not even have been more precise ratings of the that factors that increase the potential statistically significant. The comment susceptibilities of P. horizontalata to the extinction risk for P. horizontalata suggests reducing the ocean warming threats. include the fairly low tolerance to component for this species in the thermal stress and susceptibility to determination tool to moderate to low Regulatory Mechanisms acidification based on genus-level (2.5) or to low (3). Another public In the proposed rule, we did not information. It listed factors that reduce comment stated that a published study provide any species-specific potential extinction risk including the

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species’ broad distribution and the low number of colonies that are either not Coral Reefs section above, the more predation susceptibility of the genus. exposed or do not negatively respond to colonies a species has, the lower the Subsequent to the proposed rule, we a threat at any given point in time. proportion of colonies that are likely to received and gathered supplemental be exposed to a particular threat at a Listing Determination species- or genus-specific information, particular time, and all individuals that described above, that expands our In the proposed rule using the are exposed will not have the same knowledge regarding the species determination tool formula approach, P. response. abundance, distribution, and threat horizontalata was proposed for listing Notwithstanding the projections susceptibilities. We developed our as threatened because of: High through 2100 that indicate increased assessment of the species’ vulnerability vulnerability to ocean warming (ESA severity over time of the three high to extinction using all the available Factor E); moderate vulnerability to importance threats, the combination of information. As explained in the Risk disease (C) and acidification (E); these biological and environmental Analyses section, our assessment in this common generalized range wide characteristics indicates that the species final rule emphasizes the ability of the abundance (E); wide overall distribution possesses sufficient buffering capacity species’ spatial and demographic traits (based on wide geographic distribution to avoid being in danger of extinction to moderate or exacerbate its and moderate depth distribution (E); within the foreseeable future throughout vulnerability to extinction, as opposed and inadequacy of existing regulatory its range. It is possible that this species’ to the approach we used in the mechanisms (D). extinction risk may increase in the proposed rule, which emphasized the In this final rule, we changed the future as global threats continue and species’ susceptibility to threats. listing determination for P. increase in severity and the species The following characteristics of P. horizontalata from threatened to not exposure to threats increases throughout horizontalata, in conjunction with the warranted. We made this determination its range. Should the species experience information described in the Corals and based on a more species-specific and reduced abundance or range Coral Reefs section, Coral Habitat sub- holistic assessment of whether this constriction of a certain magnitude, the section, and Threats Evaluation section species meets the definition of either a ability of these characteristics to above, affect its vulnerability to threatened or endangered coral largely moderate exposure to threats will extinction currently and over the in response to public comments, diminish. However, the species is not foreseeable future. Its geographic including more appropriate likely to become of such low abundance distribution includes many of the coral consideration of the buffering capacity or so spatially fragmented as to be in of this species’ spatial and demographic reef ecoregions in the central Indo- danger of extinction due to depensatory traits to lessen its vulnerability to Pacific, and western and central Pacific processes, the potential effects of threats. Thus, based on the best Ocean. Its geographic distribution environmental stochasticity, or the available information above on P. moderates vulnerability to extinction potential for mortality from catastrophic horizontalata’s spatial structure, because some areas within its range are events within the foreseeable future demography, threat susceptibilities, and projected to have less than average throughout its range. Therefore, P. management, none of the five ESA warming and acidification over the horizontalata is not warranted for listing listing factors, alone or in combination, foreseeable future including the central at this time under any of the listing are causing this species to be likely to Pacific, and other areas, so portions of factors. the population in these areas will be become endangered throughout its range less exposed to severe conditions. Its within the foreseeable future, and thus Porites napopora depth range is from five to 30 meters, is not warranted for listing at this time, Introduction and has been found deeper. This because: moderates vulnerability to extinction (1) Porites horizontalata’s distribution The SRR and SIR provided the over the foreseeable future because across the central Indo-Pacific and following information on P. napopora’s deeper areas of its range will usually central Pacific Ocean is spread over a morphology and taxonomy. Morphology have lower irradiance than surface vast area. While some areas within its was described as broad basal plates with waters, and acidification is generally range are projected to be affected by irregular clumps of tapered irregularly predicted to accelerate most in waters warming and acidification, other areas fused branches. Porites is known to be that are deeper and cooler than those in are projected to have less than average morphologically plastic and multiple which the species occurs. Its habitat warming and acidification, including sympatric species frequently exhibit includes at least upper reef slopes, mid- the western Indian Ocean, the central intergradation of skeletal characteristics. slope terraces, lower reef crests, and Pacific, and other areas. This The results of a study of the genetics did lagoons. This moderates vulnerability to distribution and the heterogeneous not correspond well with the Porites extinction over the foreseeable future habitats it occupies reduce exposure to species based on morphology. Porites because the species is not limited to one any given threat event or adverse napopora is similar to P. nigrescens and habitat type but occurs in numerous condition that does not occur uniformly P. negrosensis. types of reef environments that will, on throughout the species range. As Public comments and information we local and regional scales, experience explained above in the Threats gathered did not provide any new or highly variable thermal regimes and Evaluation section, we have not supplemental information on ocean chemistry at any given point in identified any threat that is expected to morphology, but did confirm that there time. Its absolute abundance of at least occur uniformly throughout the species is moderate taxonomic uncertainty for tens of millions of colonies, combined range within the foreseeable future; and P. napopora and a moderate level of with spatial variability in ocean (2) Porites horizontalata’s absolute species identification uncertainty. warming and acidification across the abundance is at least tens of millions of Veron (Veron, 2014) states that P. species range, moderates vulnerability colonies, which provides buffering napopora is distinctive, and P. to extinction because the increasingly capacity in the form of absolute napopora can be identified by experts severe conditions expected in the numbers of colonies and variation in (Fenner, 2014b), thus we conclude that foreseeable future will be non-uniform susceptibility between individual the distribution and abundance and therefore will likely be a large colonies. As discussed in the Corals and information described below for this

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species is sufficiently reliable (Fenner, highly variable both spatially and susceptibilities. Porites napopora has 2014b). temporally, producing patterns on small been rated as moderately or highly scales that can be easily taken out of susceptible to disease but not to Spatial Information context, thus quantitative inferences to bleaching, but this rating is not based on The SRR and SIR provided the species-specific trends should be species-specific data (2008). With regard following information on P. napopora’s interpreted with caution. At the same to disease, P. napopora had the 13th distribution, habitat, and depth range. time, an extensive body of literature highest disease prevalence of 21 species The SRR and SIR described P. documents broad declines in live coral of Porites in the Philippines. Porites napopora’s distribution as the Coral cover and shifts to reef communities napopora had a prevalence of 0.2, Triangle plus Micronesia and the dominated by hardier coral species or which was one percent of the Marianas Islands. Its habitat includes at algae over the past 50 to 100 years prevalence of the species with the least upper reef slopes, mid-slopes, (Birkeland, 2004; Fenner, 2012; Pandolfi highest prevalence (Raymundo et al., lower reef crests, reef flats, and lagoons, et al., 2003; Sale and Szmant, 2012). 2005). There is no species-specific and the depth range as three to 15 These changes have likely occurred, and information for the susceptibility of P. meters. are occurring, from a combination of napopora to any other threat. Based on Public comments did not provide any global and local threats. Given that P. information provided in the Porites new or supplemental information on P. napopora occurs in many areas affected genus description above, P. napopora is napopora’s distribution. We gathered by these broad changes, and likely has predicted to have some susceptibility to supplemental information including some susceptibility to both global and ocean warming, disease, acidification, Veron (Veron, 2014) which provides an local threats, we conclude that it is and likely has some susceptibility to updated, much more detailed range map likely to have declined in abundance trophic effects of fishing, sedimentation, for this species than the maps used in over the past 50 to 100 years, but a nutrients, sea-level rise, and collection the SRR. Veron reports that this species precise quantification is not possible and trade. Genus-level information is confirmed in 13 of his 133 Indo- based on the limited species specific indicates this species has low Pacific ecoregions, and is strongly information. susceptibility to predation. predicted to be found in an additional 13. Other Biological Information Regulatory Mechanisms The SRR and SIR provided the In the proposed rule, we did not Demographic Information following information on P. napopora’s provide any species-specific The SRR and SIR provided the life history. Although specific information on the regulatory following information on P. napopora’s observations have not been published mechanisms or conservation efforts for abundance. Porites napopora has been for this species, the larvae of all other P. napopora. Criticisms of our approach reported as sometimes common. Porites species studied contain received during public comment led us Public comments did not provide any zooxanthellae that can supplement to the following analysis to attempt to new or supplemental information on P. maternal provisioning with energy analyze regulatory mechanisms on a napopora’s abundance. We gathered sources provided by their species basis. Records confirm that P. supplemental information including photosynthesis. The public comments napopora occurs in 13 Indo-Pacific Veron (Veron, 2014), which reports that did not provide new or supplemental ecoregions that encompass 10 countries’ P. napopora occupied 2.6 percent of information, and we did not find new or EEZs. The 10 countries are Brunei, 2,984 dive sites sampled in 30 supplemental information on the above- China, Federated States of Micronesia, ecoregions of the Indo-Pacific, and had described biological information. Indonesia, Japan, Malaysia, Philippines, a mean abundance rating of 1.79 on a 1 Taiwan, Timor-Leste, and Vietnam. The to 5 rating scale at those sites in which Susceptibility to Threats regulatory mechanisms relevant to P. it was found. Based on this semi- To describe P. napopora’s threat napopora, described first as the quantitative system, the species’ susceptibilities, the SRR and SIR percentage of the above countries that abundance was characterized as provided genus-level information for the utilize them to any degree, and second ‘‘uncommon,’’ and overall abundance effects on Acropora of ocean warming, as the percentages of those countries was described as ‘‘sometimes common acidification, disease, predation, whose regulatory mechanisms may be in isolated habitats.’’ Veron did not infer sedimentation, nutrients, and collection limited in scope, are as follows: General trends in abundance from these data. As and trade. The SRR and SIR did not coral protection (30 percent with none described in the Indo-Pacific Species provide any other species-specific limited in scope), coral collection (60 Determinations introduction above, information on the effects of these percent with 30 percent limited in based on results from Richards et al. threats on P. napopora. We interpreted scope), pollution control (30 percent (2008) and Veron (2014), the absolute threat susceptibility and exposure with 10 percent limited in scope), abundance of this species is likely at information from the SRR and SIR in the fishing regulations on reefs (100 percent least millions of colonies. proposed rule for P. napopora’s with 30 percent limited in scope), and Carpenter et al. (2008) extrapolated vulnerabilities as follows: High managing areas for protection and species abundance trend estimates from vulnerability to ocean warming; conservation (100 percent with none total live coral cover trends and habitat moderate vulnerability to disease, ocean limited in scope). The most common types. For P. napopora, the overall acidification, trophic effects of fishing, regulatory mechanisms in place for P. decline in abundance (‘‘Percent and nutrients, and low vulnerability to napopora are reef fishing regulations Population Reduction’’) was estimated sedimentation, sea level rise, predation, and area management for protection and at 33 percent, and the decline in and collection and trade. conservation. Coral collection laws are abundance before the 1998 bleaching Public comments did not provide any also somewhat utilized for the species, event (‘‘Back-cast Percent Population new or supplemental information on P. but 30 percent of coral collection laws Reduction’’) was estimated at 15 percent napopora’s threat susceptibilities. We are limited in scope and may not in the study. However, as summarized gathered the following species-specific provide substantial protection. General above in the Inter-basin Comparison and genus-level supplemental coral protection and pollution control sub-section, live coral cover trends are information on this species’ threat laws are less prominent regulatory

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mechanisms for the management of P. generally predicted to accelerate most in severe impacts from climate change and napopora. waters that are deeper and cooler than localized human impacts for coral reefs those in which the species occurs. On over the 21st century, as described in Vulnerability to Extinction the other hand, its depth range may the Threats Evaluation. Multiple ocean As explained above in the Risk exacerbate vulnerability to extinction warming events have already occurred Analyses section, a species’ over the foreseeable future if the species within the western equatorial Pacific vulnerability to extinction results from occurs predominantly in the shallower that suggest future ocean warming the combination of its spatial and portion of its depth range, since those events may be more severe than average demographic characteristics, threat areas will have higher irradiance and in this part of the world. In addition, the susceptibilities, and consideration of the thus be more severely affected by species has a depth distribution of three baseline environment and future warming-induced bleaching. Its habitat to 15 m. Such a geographic and depth projections of threats. The SRR stated includes at least upper reef slopes, mid- distribution is likely to experience that factors that increase the potential slopes, lower reef crests, reef flats, and severe and increasing threats, indicating extinction risk for P. napopora include lagoons. This moderates vulnerability to that a high proportion of the population the species’ distribution that is extinction over the foreseeable future of this species is likely to be exposed to restricted to the western Pacific and the because the species is not limited to one those threats over the foreseeable future. fairly low tolerance to thermal stress habitat type but occurs in numerous The combination of these and susceptibility to acidification based types of reef environments that will, on characteristics and future projections of on genus-level information. It listed local and regional scales, experience threats indicates that the species is factors that reduce potential extinction highly variable thermal regimes and likely to be in danger of extinction risk including its high tolerance of ocean chemistry at any given point in within the foreseeable future throughout sediment stress and turbid water, and time. There is not enough information its range and warrants listing as low predation susceptibility of the about its abundance to determine if it threatened at this time due to factors A, genus. moderates or exacerbates extinction: It C, D, and E. Subsequent to the proposed rule, we is uncommon overall but common in The available information above on P. received and gathered supplemental parts of its range, and has at least napopora’s spatial structure, species- or genus-specific information, millions of colonies, but the great demography, threat susceptibilities, and described above, that expands our majority of the population is within an management also indicate that the knowledge regarding the species area expected to be severely impacted species is not currently in danger of abundance, distribution, and threat by threats over the foreseeable future. extinction and thus does not warrant susceptibilities. We developed our listing as Endangered because: assessment of the species’ vulnerability Listing Determination (1) While P. napopora’s distribution is to extinction using all the available In the proposed rule using the restricted mostly to the Coral Triangle, information. As explained in the Risk determination tool formula approach, P. which increases it extinction risk as Analyses section, our assessment in this napopora was proposed for listing as described above, its habitat includes final rule emphasizes the ability of the threatened because of: High shallow reef environments, which species’ spatial and demographic traits vulnerability to ocean warming (ESA describes a variety of reef zones and to moderate or exacerbate its Factor E); moderate vulnerability to habitat types in the coral reef ecosystem. vulnerability to extinction, as opposed disease (C) and acidification (E); This moderates vulnerability to to the approach we used in the common generalized range wide extinction currently because the species proposed rule, which emphasized the abundance (E); narrow overall is not limited to one habitat type but species’ susceptibility to threats. distribution (based on moderate occurs in numerous types of reef The following characteristics of P. geographic distribution and shallow environments that will, on local and napopora, in conjunction with the depth distribution (E); and inadequacy regional scales, experience highly information described in the Corals and of existing regulatory mechanisms (D). variable thermal regimes and ocean Coral Reefs section, Coral Habitat sub- In this final rule, we did not change chemistry at any given point in time, as section, and Threats Evaluation section the listing determination for P. described in more detail in the Coral above, affect its vulnerability to napopora. Based on the best available Habitat and Threats Evaluation sections. extinction currently and over the information provided above on P. There is no evidence to suggest that the foreseeable future. Its geographic napopora’s spatial structure, species is so spatially fragmented that distribution is limited to parts of the demography, threat susceptibilities, and depensatory processes, environmental Coral Triangle and the western management indicate that it is likely to stochasticity, or the potential for equatorial Pacific Ocean. Despite the become endangered throughout its range catastrophic events currently pose a large number of islands and within the foreseeable future, and thus high risk to the survival of the species; environments that are included in the warrants listing as threatened at this and species’ range, this range exacerbates time, because: (2) Porites napopora’s its absolute vulnerability to extinction over the (1) Porites napopora is susceptible to abundance is likely at least millions of foreseeable future because it is mostly warming induced bleaching (ESA Factor colonies and is described as ‘‘sometimes limited to an area projected to have the E), disease (C), trophic effects of fishing common in isolated habitats’’ providing most rapid and severe impacts from (A), and nutrients (A, E). These threats areas of localized abundance which climate change and localized human are expected to continue and worsen allows for variation in the responses of impacts for coral reefs over the 21st into the future. In addition, existing individuals to threats to play a role in century. Its depth range is down to 15 regulatory mechanisms to address global moderating vulnerability to extinction meters. On one hand, its depth range threats that contribute to extinction risk for the species to some degree, as may moderate vulnerability to for this species are inadequate (D); and described in more detail in the Corals extinction over the foreseeable future (2) Porites napopora’s distribution is and Coral Reefs section. There is no because deeper areas of its range will constrained mostly to the Coral Triangle evidence of depensatory processes such usually have lower irradiance than and western equatorial Pacific, which is as reproductive failure from low density surface waters, and acidification is projected to have the most rapid and of reproductive individuals and genetic

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processes such as inbreeding affecting distribution, habitat, and depth range. context, thus quantitative inferences to this species. Thus, its absolute The SRR and SIR described P. species-specific trends should be abundance indicates it is currently able nigrescens’ distribution as occurring interpreted with caution. At the same to avoid high mortality from from the Red Sea and east Africa to the time, an extensive body of literature environmental stochasticity, and central Pacific. Its habitat includes coral documents broad declines in live coral mortality of a high proportion of its reef environments protected from wave cover and shifts to reef communities population from catastrophic events. action, including at least upper reef dominated by hardier coral species or The combination of these slopes, mid-slopes, lower reef slopes, algae over the past 50 to 100 years characteristics indicates that the species and lagoons, and its depth range as 0 to (Birkeland, 2004; Fenner, 2012; Pandolfi does not exhibit the characteristics of 20 meters. et al., 2003; Sale and Szmant, 2012). one that is currently in danger of The public comments provided These changes have likely occurred, and extinction, as described previously in information that P. nigrescens is widely are occurring, from a combination of the Risk Analyses section, and thus does distributed in all Indonesian waters. We global and local threats. Given that P. not warrant listing as endangered at this gathered supplemental information, nigrescens occurs in many areas affected time. including Veron (2014), which reports by these broad changes, and that it is Range-wide, a multitude of that this species is confirmed in 56 of likely has some susceptibility to both conservation efforts are already broadly his 133 Indo-Pacific ecoregions, and global and local threats, we conclude employed that are likely benefiting P. strongly predicted to be found in an that it is likely to have declined in napopora. However, considering the additional 18. abundance over the past 50 to 100 years, global scale of the most important Demographic Information but a precise quantification is not threats to the species, and the possible based on the limited species ineffectiveness of conservation efforts at The SRR and SIR provided the specific information. following information on P. nigrescens’ addressing the root cause of global Other Biological Information threats (i.e., GHG emissions), we do not abundance. Porites nigrescens has been believe that any current conservation reported as sometimes common. Where The public comments and found, it can be a part of a locally efforts or conservation efforts planned information we gathered did not abundant branching poritid assemblage. in the future will result in affecting the provide any new or supplemental The public comments and biological information on P. nigrescens. species status to the point at which information we gathered provided listing is not warranted. supplemental information on P. Susceptibility to Threats Porites nigrescens nigrescens’ abundance. One public To describe P. nigrescens’ threat comment stated that P. nigrescens is susceptibilities, the SRR and SIR Introduction very abundant in all Indonesian waters. provided genus-level information for the The SRR and SIR provided the We gathered supplemental information, effects on Porites of ocean warming, following information on P. nigrescens’ including Veron (2014), which reports acidification, disease, predation, morphology and taxonomy. The that P. nigrescens occupied 29.05 sedimentation, nutrients, and collection morphology was described as percent of 2,984 dive sites sampled in and trade. The SRR and SIR did not branching, sometimes with an 30 ecoregions of the Indo-Pacific, and provide any other species-specific encrusting base, and concave calices had a mean abundance rating of 2.01 on information on the effects of these give the surface a pitted appearance. a 1 to 5 rating scale at those sites in threats on P. nigrescens. We interpreted Porites is known to be morphologically which it was found. Based on this semi- the threat susceptibility and exposure plastic and multiple sympatric species quantitative system, the species’ information from the SRR and SIR in the frequently exhibit intergradation of abundance was characterized as ‘‘very proposed rule for P. nigrescens’ skeletal characteristics. The results of a common.’’ Overall abundance was vulnerabilities as follows: High genetics study did not correspond well described as ‘‘sometimes common.’’ vulnerability to ocean warming, with the Porites species based on Veron did not infer trends in abundance moderate vulnerability to disease, ocean morphology. Porites nigrescens is from these data. As described in the acidification, trophic effects of fishing, similar in appearance to Porites Indo-Pacific Species Determinations and nutrients, and low vulnerability to cylindrica. introduction above, based on results sedimentation, sea-level rise, predation, The public comments and from Richards et al. (2008) and Veron and collection and trade. information we gathered did not (2014), the absolute abundance of this Public comments did not provide any provide any new or supplemental species is likely at least tens of millions new or supplemental information on P. information on morphology, and of colonies. nigrescens’ threat susceptibilities. We confirmed that there is moderate Carpenter et al. (2008) extrapolated gathered the following species-specific taxonomic uncertainty for P. nigrescens species abundance trend estimates from and genus-level supplemental and that there is a moderate level of total live coral cover trends and habitat information on this species’ threat species identification uncertainty for types. For P. nigrescens, the overall susceptibilities. Porites nigrescens has this species. Veron (2014) states that P. decline in abundance (‘‘Percent not been rated as moderately or highly nigrescens is easily distinguished from Population Reduction’’) was estimated susceptible to bleaching, but this rating other branching Porites, thus we at 35 percent, and the decline in is not based on species-specific data conclude it can be identified by experts, abundance before the 1998 bleaching (2008). Porites nigrescens appears to and that the distribution and abundance event (‘‘Back-cast Percent Population have high susceptibility to thermal information described below for this Reduction’’) was estimated at 14 percent stress and warming-induced bleaching. species is sufficiently reliable (Fenner, in the study. However, as summarized Porites nigrescens had high bleaching 2014b). above in the Inter-basin Comparison rates in East Africa in 1998 (Obura, sub-section, live coral cover trends are 2001) and Palau in 2000 (Bruno et al., Spatial Information highly variable both spatially and 2001). In East Africa, 99 percent of P. The SRR and SIR provided the temporally, producing patterns on small nigrescens colonies were affected by following information on P. nigrescens’ scales that can be easily taken out of bleaching at the peak of bleaching in

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1998 in Kenya, Tanzania, Mozambique, Marshall Islands, Mauritius, information. As explained in the Risk and Madagascar. This was the third- Mozambique, Myanmar, New Zealand Analyses section, our assessment in this most affected species out of 14 species, (Tokelau), Niue, Palau, Papua New final rule emphasizes the ability of the and was affected 99 percent as much as Guinea, Philippines, Samoa, Saudi species’ spatial and demographic traits the most affected species. At the end of Arabia, Seychelles, Solomon Islands, to moderate or exacerbate its bleaching, 87 percent of colonies were Somalia, South Africa, Sri Lanka, vulnerability to extinction, as opposed dead, which was the fifth-highest Taiwan, Tanzania, Thailand, Timor- to the approach we used in the mortality species, and 94 percent of the Leste, Tonga, Tuvalu, United Kingdom proposed rule, which emphasized the mortality level of the highest mortality (British Indian Ocean Territory), United species’ susceptibility to threats. species (Obura, 2001). In Palau in 2000, States (American Samoa, PRIAs), The following characteristics of P. P. nigrescens had very high to moderate Vanuatu, Vietnam, and Yemen. The nigrescens, in conjunction with the bleaching, and very high mortality. Of regulatory mechanisms available to P. information described in the Corals and all P. nigrescens colonies at the study nigrescens, described first as a Coral Reefs section, Coral Habitat sub- site, 48 percent bleached, and bleaching percentage of the above countries that section, and Threats Evaluation section of different genera and species ranged utilize them to any degree and second, above, affect its vulnerability to from none to very high, with mortality as the percentages of those countries extinction currently and over the from zero to near 100 percent (Bruno et whose regulatory mechanisms may be foreseeable future. Its geographic al., 2001). Loya et al. (Loya et al., 2001) limited in scope, are as follows: General distribution includes most of the coral reported that P. nigrescens was a ‘‘loser’’ coral protection (28 percent with 7 reef ecoregions in the Indian Ocean and in a 1998 bleaching event in Japan percent limited in scope), coral western and central Pacific Ocean. Its where it went down to zero abundance collection (56 percent with 28 percent geographic distribution moderates and cover (Loya et al., 2001). limited in scope), pollution control (35 vulnerability to extinction because some Porites nigrescens has been rated as percent with 7 percent limited in areas within its range are projected to moderately or highly susceptible to scope), fishing regulations on reefs (95 have less than average warming and disease, but these ratings are not based percent with 23 percent limited in acidification over the foreseeable future, on species-specific data (Carpenter et scope), and managing areas for including the western Indian Ocean, the al., 2008). Raymundo et al. (2005) protection and conservation (93 percent central Pacific, and other areas, so reported P. nigrescens had the seventh- with 5 percent limited in scope). The portions of the population in these areas highest disease prevalence of 21 species most common regulatory mechanisms in will be less exposed to severe of Porites in the Philippines. Porites place for P. nigrescens are reef fishing conditions. Its depth range is down to nigrescens had a moderate level of regulations and area management for at least 20 meters. This moderates disease prevalence relevant to the other protection and conservation. Coral vulnerability to extinction over the coral species in the study. No other collection laws are somewhat utilized foreseeable future because deeper areas species-specific information is available but some are limited in scope and may of its range will usually have lower for the susceptibility of P. nigrescens to not provide substantial protection for P. irradiance than surface waters, and any other threat. nigrescens. General coral protection and acidification is generally predicted to Based on species-specific and genus- pollution control laws are much less accelerate most in waters that are deeper level information above, P. nigrescens is prominent regulatory mechanisms for and cooler than those in which the likely highly susceptible to ocean the management of P. nigrescens. species occurs. Its habitat includes at warming and also likely has some least upper reef slopes, mid-slopes, susceptibilities to disease, ocean Vulnerability to Extinction lower reef slopes, and lagoons protected acidification, trophic effects of fishing, As explained above in the Risk from wave action. This moderates sedimentation, nutrients, sea-level rise, Analyses section, a species’ vulnerability to extinction over the predation, and collection and trade. The vulnerability to extinction results from foreseeable future because the species is available information does not support the combination of its spatial and not limited to one habitat type but more precise ratings of the demographic characteristics, threat occurs in numerous types of reef susceptibilities of P. nigrescens to the susceptibilities, and consideration of the environments that will, on local and threats. baseline environment and future regional scales, experience highly projections of threats. The SRR stated Regulatory Mechanisms variable thermal regimes and ocean that factors that increase the potential chemistry at any given point in time. Its In the proposed rule, we did not extinction risk for P. nigrescens include abundance of at least tens of millions of provide any species-specific the fairly low tolerance to thermal stress colonies, combined with spatial information on the regulatory and susceptibility to acidification variability in ocean warming and mechanisms or conservation efforts for impacts in the genus. It listed factors acidification across the species range, P. nigrescens. Public comments were that reduce potential extinction risk moderates vulnerability to extinction critical of that approach, and we including the species’ broad because the increasingly severe therefore attempt to analyze regulatory distribution, the high tolerance of conditions expected in the foreseeable mechanisms and conservation efforts on sediment stress and turbid water, and future will be non-uniform and a species basis, where possible, in this low disease and predation susceptibility therefore will likely be a large number final rule. Records confirm that P. of the genus. of colonies that are either not exposed nigrescens occurs in 56 Indo-Pacific Subsequent to the proposed rule, we or do not negatively respond to a threat ecoregions that encompass 43 countries’ received and gathered supplemental at any given point in time. EEZs. The 43 countries are Australia, species- or genus-specific information, Brunei, Cambodia, China, Djibouti, described above, that expands our Listing Determination Eritrea, Federated States of Micronesia, knowledge regarding the species In the proposed rule using the Fiji, France (French Pacific Island abundance, distribution, and threat determination tool formula approach, P. Territories), India (Andaman and susceptibilities. We developed our nigrescens was proposed for listing as Nicobar Islands), Indonesia, Japan, assessment of the species’ vulnerability threatened because of: High Kenya, Kiribati, Madagascar, Malaysia, to extinction using all the available vulnerability to ocean warming (ESA

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Factor E); moderate vulnerability to these biological and environmental al., 2007a). Done et al. (2003b) reported disease (C) and acidification (E); characteristics indicates that the species that overall bleaching rates for two common generalized range wide possesses sufficient buffering capacity species of Pachyseris were 15 percent abundance (E); wide overall distribution to avoid being in danger of extinction and 38 percent on the GBR in 2002, (based on wide geographic distribution within the foreseeable future throughout which were the seventh and third and moderate depth distribution (E); its range. It is possible that this species’ highest levels of bleaching out of 16 and inadequacy of existing regulatory extinction risk may increase in the species of Agariciids. There is no mechanisms (D). future if global threats continue and information available on the effects of In this final rule, we changed the increase in severity and the species any other threat for Pachyseris. listing determination for P. nigrescens exposure to threats increases throughout Genus Conclusion from threatened to not warranted. We its range. Should the species experience made this determination based on a reduced abundance or range Based on the information from the more species-specific and holistic constriction of a certain magnitude, the SRR, SIR, public comments, and assessment of whether this species ability of these characteristics to supplemental information, we can make meets the definition of either a moderate exposure to threats will the following inferences about the threatened or endangered coral largely diminish. However, the species is not susceptibilities of an unstudied in response to public comments, likely to become of such low abundance Pachyseris species to ocean warming, including more appropriate or so spatially fragmented as to be in disease, acidification, sedimentation, consideration of the buffering capacity danger of extinction due to depensatory nutrients, trophic effects of fishing, sea- of this species’ spatial and demographic processes, the potential effects of level rise, predation, and collection and traits to lessen its vulnerability to environmental stochasticity, or the trade. The SRR rated ocean warming threats. Thus, based on the best potential for mortality from catastrophic and disease as ‘‘high’’ importance, and available information above on P. events within the foreseeable future ocean acidification as ‘‘medium-high’’ nigrescens’ spatial structure, throughout its range. Therefore, P. importance, to corals. These were rated demography, threat susceptibilities, and nigrescens is not warranted for listing at as the three most important threats to management, none of the five ESA this time under any of the listing factors. reef-building corals overall. Pachyseris listing factors, alone or in combination, has a variable level of susceptibility to are causing this species to be likely to Genus Pachyseris bleaching, with most reports of bleaching being moderate to high. Thus, become endangered throughout its range Genus Introduction within the foreseeable future, and thus we conclude that an unstudied is not warranted for listing at this time, The family Agaricidae includes six Pachyseris species is likely to have high because: genera, Agaricia (Caribbean only), susceptibility to ocean warming. (1) Porites nigrescens’ distribution Leptoseris, Pavona, Pachyseris, Although there is no other genus-level from the Red Sea and east Africa across Gardineroseris, and Coeloseris. or species-specific information on the most of the Pacific Ocean is spread over Pachyseris contains four species, all in susceptibilities of Pachyseris species to a very large area. While some areas the Indo-Pacific. Pachyseris species are disease and ocean acidification, the SRR within its range are projected to be foliose, and one species can produce rated them as ‘‘high’’ and ‘‘medium- affected by warming and acidification, short columns or branches. The SRR high’’ importance to corals, respectively. other areas are projected to have less and SIR provided no genus-level Thus, we conclude that an unstudied than average warming and acidification, introductory information on Pachyseris. Pachyseris species is likely to have including the western Indian Ocean, the Genus Susceptibility to Threats some susceptibility to disease and ocean central Pacific, and other areas. This acidification. distribution and the heterogeneous The SRR and SIR provided the The SRR rated the trophic effects of habitats it occupies reduce exposure to following information on the threat fishing as ‘‘medium’’ importance, the any given threat event or adverse susceptibilities of the genus Pachyseris. fourth most important threat to corals condition that does not occur uniformly A series of studies reported that overall. This threat was not addressed at throughout the species range. As Pachyseris experiences variable but high the genus or species level in the SRR or explained above in the Threats levels of bleaching, though in some SIR, because it is an ecosystem-level Evaluation section, we have not places it may be bleaching tolerant. process. That is, removal of herbivorous identified any threat that is expected to Pachyseris’ high bleaching rate and fish from coral reef systems by fishing occur uniformly throughout the species relative rarity may give it a relatively alters trophic interactions by reducing range within the foreseeable future; and high extirpation risk in the western herbivory on algae, thereby providing a (2) Porites nigrescens’ absolute Indian Ocean. Trade in this genus is competitive advantage for space to algae abundance is at least tens of millions of relatively high. over coral. Thus, the SRR did not colonies, providing buffering capacity in The public comments did not provide discuss this threat in terms of coral taxa, the form of absolute numbers of any new or supplemental information as its effects are difficult to distinguish colonies and variation in susceptibility on the threat susceptibilities of the between coral genera and species. between individual colonies. As genus Pachyseris. We gathered Therefore, an unstudied Pachyseris discussed in the Corals and Coral Reefs supplemental information that provided species is likely to have some section above, the more colonies a the following details. Pachyseris had a susceptibility to the trophic effects of species has, the lower the proportion of bleaching index of 8.3 for eight fishing. colonies that are likely to be exposed to countries in the western Indian Ocean The SRR rated sedimentation, a particular threat at a particular time, in 1998–2005, which was 33rd highest nutrients, and sea-level rise as ‘‘low- and all individuals that are exposed will of the 45 genera recorded, and 20 medium’’ importance to corals overall. not have the same response. percent of the highest value. As a genus, Although there is no genus-level or Notwithstanding the projections its moderate bleaching rate combined species-specific information on the through 2100 that indicate increased with relative rarity may give it a susceptibilities of Pachyseris species to severity over time of the three high relatively high extirpation risk in the sedimentation and nutrients, the SRR importance threats, the combination of western Indian Ocean (McClanahan et rated them as ‘‘low-medium’’

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importance to corals.. Thus, we distribution, habitat, and depth range. small scales that can be easily taken out conclude that an unstudied Pachyseris The SRR and SIR described P. rugosa’s of context, thus quantitative inferences species is likely to have some distribution as from the Red Sea and to species-specific trends should be susceptibility to sedimentation and east Africa to the central Pacific. interpreted with caution. At the same nutrients. Sea-level rise was not Regarding habitat, the SRR and SIR time, an extensive body of literature addressed at the genus or species level stated that P. rugosa may develop into documents broad declines in live coral in the SRR or SIR. Increasing sea levels large mound-shaped colonies in shallow cover and shifts to reef communities may increase land-based sources of water but smaller colonies occur in a dominated by hardier coral species or pollution due to inundation, resulting in wide range of habitats including those algae over the past 50 to 100 years changes to coral community structure, exposed to strong wave action. It is (Birkeland, 2004; Fenner, 2012; Pandolfi thus an unstudied Pachyseris species is associated with fine-grained sediments et al., 2003; Sale and Szmant, 2012). likely to have some susceptibility to sea- on the Great Barrier Reef, and could be These changes have likely occurred, and level rise. Although there is no genus- an indicator of quiet water or a are occurring, from a combination of level or species-specific information on moderate energy environment. Thus, its global and local threats. Given that P. the susceptibilities of Pachyseris species habitat includes at least upper reef rugosa occurs in many areas affected by to predation, there is no information slopes, mid-slopes, and lagoons. Its these broad changes, and likely has suggesting they are not susceptible to depth range is from five to 20 meters, some susceptibility to both global and this threat. Thus, we conclude that an and it may be excluded from shallow local threats, we conclude that it is unstudied Pachyseris species has some environments by excess light. likely to have declined in abundance susceptibility to predation. The SRR Public comments did not provide any over the past 50 to 100 years, but a rated predation and ornamental trade new or supplemental information on P. precise quantification is not possible (referred to in the proposed rule as rugosa’s distribution. We gathered based on the limited species-specific Collection and Trade) as ‘‘low’’ supplemental information, including information. Veron (2014), which reports that this importance to corals overall. Because Other Biological Information the available general information species is confirmed in 57 of his 133 suggests that collection and trade of Indo-Pacific ecoregions, and strongly The SRR and SIR provided the Pachyseris species is relatively high, we predicted to be found in an additional following information on P. rugosa’s life conclude an unstudied Pachyseris 17. history. Pachyseris rugosa is a gonochoric broadcast spawner. This species is likely to have some Demographic Information species contains clade C zooxanthellae, susceptibility to collection and trade. The SRR and SIR reported P. rugosa’s In conclusion, an unstudied with a predominance of clade C3h in abundance as common. areas of greater temperature or turbidity. Pachyseris species is likely to have high Public comments did not provide any Public comments and information we susceptibility to ocean warming, and new or supplemental information on P. gathered added no new or supplemental some susceptibility to disease, ocean rugosa’s abundance. We gathered information to the above-described acidification, trophic effects of fishing, supplemental information, including biological information. sedimentation, nutrients, predation, sea- Veron (2014), which reports that P. level rise, and collection and trade. rugosa occupied 23.5 percent of 2,984 Susceptibility to Threats Pachyseris rugosa dive sites sampled in 30 ecoregions of To describe P. rugosa’s threat the Indo-Pacific, and had a mean susceptibilities, the SRR and SIR Introduction abundance rating of 1.45 on a 1 to 5 provided genus-level information for the In The SRR and SIR provided the rating scale at those sites in which it effects on Pachyseris of ocean warming, following information on P. rugosa’s was found. Based on this semi- acidification, disease, sedimentation, morphology and taxonomy. Morphology quantitative system, the species’ nutrients, predation, and collection and was described as colonies that are abundance was characterized as trade. The SRR and SIR also provided upright, irregular, fused, bifacial plates, ‘‘common,’’ and overall abundance was the following species-specific and taxonomy was described as having also described as ‘‘common.’’ Veron did information on P. rugosa’s threats. no taxonomic issues, but being similar not infer trends in abundance from Pachyseris rugosa is vulnerable to a to Pachyseris gemmae and Pachyseris these data. As described in the Indo- ciliate disease skeletal eroding band. involuta. Pacific Species Determinations Although overall disease presence was Public comments and information we introduction above, based on results low during a survey in Indonesia, the gathered did not provide any new or from Richards et al. (2008) and Veron black-band progressed across P. rugosa supplemental information on (2014), the absolute abundance of this at an average rate of 0.63cm/d. Mass morphology, and confirmed that there species is likely at least tens of millions mortality of this species on the GBR has are no known taxonomic problems for P. of colonies. been attributed to crown of thorns rugosa, and a low level of species Carpenter et al. (2008) extrapolated starfish, although predation was not identification uncertainty. Veron (2014) species abundance trend estimates from observed directly. Pachyseris rugosa has states that P. rugosa is very distinctive total live coral cover trends and habitat suffered high partial mortality as a and Veron (2000; 2014) considers the types. For P. rugosa, the overall decline result of dredging, but its branching species valid, and we consider it can be in abundance (‘‘Percent Population structure should make it an efficient identified by experts, thus we conclude Reduction’’) was estimated at 36 sediment-rejecter. The species that the distribution and abundance percent, and the decline in abundance disappeared in Jakarta Bay between information described below for this before the 1998 bleaching event (‘‘Back- 1920 and 2005, which was attributed to species is sufficiently reliable (Fenner, cast Percent Population Reduction’’) decreased water quality from coastal 2014b). was estimated at 14 percent. However, development. Pachyseris rugosa as summarized above in the Inter-basin experiences substantial export, Spatial Information Comparison sub-section, live coral cover averaging 1195 specimens annually The SRR and SIR provided the trends are highly variable both spatially from 1991 to 2008, decreasing in 1997– following information on P. rugosa’s and temporally, producing patterns on 2003, but returning to 2085 per year in

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2004–2008. The SRR and SIR did not reports of the effects of any other threats Vulnerability to Extinction provide any other species-specific on P. rugosa. Based on genus-level and As explained above in the Risk information on the effects of these species-specific information describe Analyses section, a species’ threats on P. rugosa. We interpreted above, P. rugosa is likely to have high vulnerability to extinction results from threat susceptibility and exposure susceptibility to ocean warming and the combination of its spatial and information from the SRR and SIR in the some susceptibility to disease, ocean demographic characteristics, threat proposed rule for P. rugosa’s acidification, trophic effects of fishing, susceptibilities, and consideration of the vulnerabilities as follows: High nutrients, sedimentation, sea level rise, baseline environment and future vulnerability to ocean warming, predation, and collection and trade. The projections of threats. The SRR stated moderate vulnerability to disease, ocean available information does not support that factors that increase the potential acidification, and trophic effects of more precise ratings of the susceptibility extinction risk for P. rugosa are that it fishing, and low vulnerability to of P. rugosa to the threats. has had high (but variable) observed sedimentation, sea level rise, predation, Regulatory Mechanisms bleaching in response to warming and collection and trade. events, has been observed to be Public comments did not provide any In the proposed rule, we did not susceptible to multiple types of disease, new or supplemental information on P. provide any species-specific and has been inferred to be susceptible rugosa’s susceptibility to threats. We information on the regulatory to poor water quality. Substantial gathered the following supplemental mechanism or conservation efforts for P. collection from the aquarium trade species-specific and genus-level rugosa. Criticisms of our approach could lead to local extirpation in some information on this species’ threat received during public comment led us areas. It listed factors that reduce susceptibilities. Pachyseris rugosa has to attempt the following analysis of potential extinction risk including that been rated as moderately or highly regulatory mechanisms on a species P. rugosa has a widespread distribution susceptible to bleaching but not disease, basis. Records confirm that P. rugosa from the central Pacific to Africa, and it but this rating is not based on species- occurs in 57 Indo-Pacific ecoregions that can have a high local abundance. specific data (Carpenter et al., 2008). encompass 36 countries’ EEZs. The 36 Subsequent to the proposed rule, we With regard to thermal stress, 15 percent countries are Australia, Brunei, China, received and gathered supplemental of P. rugosa colonies were affected by Egypt, Federated States of Micronesia, species- or genus-specific information, bleaching on the GBR in 2002. The Fiji, France (French Pacific Island described above, that expands our median bleaching level among Territories), India (including Andaman knowledge regarding the species Agariciidae colonies was 10 percent, and Nicobar Islands), Indonesia, Israel, abundance, distribution, and threat and the maximum was 58 percent. The Japan, Jordan, Madagascar, Malaysia, susceptibilities. We developed our only other Pachyseris reported, P. Maldives, Mauritius, Myanmar, New assessment of the species’ vulnerability speciosa, bleached at a rate of 38 Zealand (Tokelau), Niue, Palau, Papua to extinction using all the available percent (Done et al., 2003b). All New Guinea, Philippines, Samoa, Saudi information. As explained in the Risk colonies of P. rugosa were partly Arabia, Solomon Islands, Sri Lanka, Analyses section, our assessment in this bleached at Laem Set at Samui Island in Sudan, Taiwan, Thailand, Timor-Leste, final rule emphasizes the ability of the the western Gulf of Thailand in 1998, Tonga, Tuvalu, United Kingdom (British species’ spatial and demographic traits and all were completely bleached in Indian Ocean Territory), United States to moderate or exacerbate its 2010. However, after both bleaching (American Samoa, PRIAs), Vanuatu, and vulnerability to extinction, as opposed events, all colonies recovered and were Vietnam. The regulatory mechanisms to the approach we used in the healthy (Sutthacheep et al., 2013). In relevant to P. rugosa, described first as proposed rule, which emphasized the Palau in 2000, P. rugosa had variable the percentage of the above countries species’ susceptibility to threats. but generally high bleaching levels and that utilize them to any degree, and The following characteristics of P. high mortality: 48 percent of all colonies second as the percentage of those rugosa, in conjunction with the of all species were bleached, and countries whose regulatory mechanisms information described in the Corals and bleaching of different genera and may be limited in scope, are as follows: Coral Reefs section, Coral Habitat sub- species ranged from none to very high, General coral protection (28 percent section, and Threats Evaluation section and mortality from zero to near 100 with 6 percent limited in scope), coral above, affect its vulnerability to percent (Bruno et al., 2001). Based on collection (61 percent with 31 percent extinction currently and over the species specific and genus information limited in scope), pollution control (44 foreseeable future. Its geographic presented above, P. rugosa is predicted percent with 8 percent limited in distribution includes most of the coral to have a moderate to high level of scope), fishing regulations on reefs (92 reef ecoregions in the Indian Ocean and susceptibility to bleaching. With regard percent with 19 percent limited in western and central Pacific Ocean, and to disease, Page and Willis (2007) scope), managing areas for protection some in the Red Sea. Its geographic reported that skeletal eroding band has and conservation (97 percent with 8 distribution moderates vulnerability to been found in P. rugosa on the GBR, percent limited in scope). The most extinction because some areas within its where it is the most prevalent disease common regulatory mechanisms in range are projected to have less than on corals. However, the prevalence on place for P. rugosa are reef fishing average warming and acidification over P. rugosa was too low to record in regulations and area management for the foreseeable future, including the transects. Darling et al. (2012) protection and conservation. Coral western Indian Ocean, the central performed a biological trait-based collection and pollution control laws Pacific, and other areas, so portions of analysis to categorize the relative are also somewhat common for the the population in these areas will be tolerance of coral species to species, but 31 percent of coral less exposed to severe conditions. Its environmental stress. Pachyseris rugosa collection laws are limited in scope and depth range is from five to at least 20 was classified as a ‘‘generalist’’ species, may not provide substantial protection. meters. This moderates vulnerability to defined as species that can do well in General coral protection laws are much extinction over the foreseeable future habitats where competition is limited by less common regulatory mechanisms for because deeper areas of its range will low levels of stress. There are no other the management of P. rugosa. usually have lower irradiance than

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surface waters, and acidification is some areas within its range are (Veron, 2000) recognizes 14 species in generally predicted to accelerate most in projected to be affected by warming and the genus Pavona. Colonies of Pavona waters that are deeper and cooler than acidification, other areas are projected species have plates, branches, or are those in which the species occurs. Its to have less than average warming and massive. The SRR and SIR provided no habitat includes at least upper reef acidification, including the western genus-level introductory information on slopes, mid-slopes, and lagoons. This Indian Ocean, the central Pacific, and Pavona. moderates vulnerability to extinction other areas. This distribution and the Genus Susceptibility to Threats over the foreseeable future because the heterogeneous habitats it occupies species is not limited to one habitat type reduce exposure to any given threat The SRR and SIR provided the but occurs in numerous types of reef event or adverse condition that does not following information on the threat environments that will, on local and occur uniformly throughout the species susceptibilities of the genus Pavona. regional scales, experience highly range. As explained above in the One study reports Pavona had mixed variable thermal regimes and ocean Threats Evaluation section, we have not bleaching susceptibility on the GBR. chemistry at any given point in time. Its identified any threat that is expected to Other studies reported that both massive abundance of at least tens of millions of occur uniformly throughout the species and encrusting Pavona have been highly colonies, combined with spatial range within the foreseeable future; and susceptible to bleaching in the eastern variability in ocean warming and (2) Pachyseris rugosa is described as Pacific. Calcification in one Pavona acidification across the species range, common throughout its vast geographic species slowed in reduced aragonite moderates vulnerability to extinction range and its total population size is at saturation state. Two massive Pavona in because the increasingly severe least tens of millions of colonies, the eastern Pacific showed little conditions expected in the foreseeable providing buffering capacity in the form calcification reduction over 30 years in future will be non-uniform and of absolute numbers of colonies and response to acidification. The presence therefore, there will likely be a large variation in susceptibility between of several species of Pavona in low number of colonies that are either not individual colonies. As discussed in the aragonite saturation states in the Eastern exposed or do not negatively respond to Corals and Coral Reefs section above, Pacific suggests some tolerance to a threat at any given point in time. the more colonies a species has, the acidification. There are a medium number of acute white diseases found in Listing Determination lower the proportion of colonies that are likely to be exposed to a particular Pavona by surveys in the Pacific. In the proposed rule using the threat at a particular time, and all Members of the genus Pavona are determination tool formula approach, P. individuals that are exposed will not susceptible to predation by crown-of- rugosa was proposed for listing as have the same response. thorns seastar (Acanthaster planci), but threatened because of: High Notwithstanding the projections susceptibility is variable among species vulnerability to ocean warming (ESA through 2100 that indicate increased in the eastern Pacific. The genus Pavona Factor E); moderate vulnerability to severity over time of the three high is generally regarded as moderately disease (C) and acidification (E); importance threats, the combination of tolerant to sediment stress. More than common generalized range wide these biological and environmental 1,000 pieces of Pavona are traded per abundance (E); wide overall distribution characteristics indicates that the species year. The public comments did not provide (based on wide geographic distribution possesses sufficient buffering capacity any new or supplemental information and moderate depth distribution (E); to avoid being in danger of extinction on the threat susceptibilities of the and inadequacy of existing regulatory within the foreseeable future throughout genus Pavona. We gathered mechanisms (D). its range. It is possible that this species’ In this final rule, we changed the supplemental information that provided extinction risk may increase in the listing determination for P. rugosa from the following. With regard to thermal future if global threats continue and threatened to not warranted. We made stress, Brown and Suharsono (1990) increase in severity and the species this determination based on a more reported that less than half of the exposure to threats increases throughout species-specific and holistic assessment Pavona on the reef flats of two islands of whether this species meets the its range. Should the species experience in the Thousand Islands of Indonesia definition of either a threatened or reduced abundance or range died in the 1983 El Nino mass endangered coral largely in response to constriction of a certain magnitude, the bleaching. In the mass bleaching event public comments, including more ability of these characteristics to in 1998 in the Ryukyu Islands of Japan, appropriate consideration of the moderate exposure to threats will Pavona was highly susceptible to buffering capacity of this species’ spatial diminish. However, the species is not bleaching, and mortality was 100 and demographic traits to lessen its likely to become of such low abundance percent, higher than any other of the six vulnerability to threats. Thus, based on or so spatially fragmented as to be in genera included in the study (Kayanne the best available information above on danger of extinction due to depensatory et al., 2002). In contrast, during the P. rugosa’s spatial structure, processes, the potential effects of same 1998 bleaching event in Kenya, demography, threat susceptibilities, and environmental stochasticity, or the mortality of Pavona colonies was zero, management, none of the five ESA potential for mortality from catastrophic and Pavona was one of five genera out listing factors, alone or in combination, events within the foreseeable future of the 18 genera in the study that had are causing this species to likely become throughout its range. Therefore, P. no mortality (McClanahan et al., 2004). endangered throughout its range within rugosa is not warranted for listing at this Pavona’s bleaching index was the the foreseeable future, and thus it is not time under any of the listing factors. second lowest of the 18 genera warranted for listing at this time, Genus Pavona (McClanahan et al., 2004). In a because: bleaching event on Palau in 2000, three (1) Pachyseris rugosa’s distribution Genus Introduction species of Pavona had high levels of from the Red Sea across the Indian The family Agaricidae includes six bleaching and high mortality. Forty- Ocean and most of the Pacific Ocean genera, Agaricia (Caribbean only), eight percent of all colonies of all includes tens of thousands of islands Leptoseris, Pavona, Pachyseris, species were bleached, and both and reefs spread over a vast area. While Gardineroseris, and Coeloseris. Veron bleaching and mortality of different

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genera and species ranged from zero to as its effects are difficult to distinguish that Pacific P. diffluens is likely to be a near 100 percent (Bruno et al., 2001). In between coral genera and species. similar but different species from a bleaching event on the GBR in 2002, Therefore, an unstudied Pavona species western Indian Ocean P. diffluens.’’ We between seven percent and 57 percent is likely to be susceptible to the trophic treat P. diffluens as the colonies in the of six species of Pavona were affected effects of fishing. Red Sea and Indian Ocean only, as this (Done et al., 2003b). In a bleaching event The SRR rated sedimentation, is the best currently available scientific on Mauritius in 2004, Pavona had the nutrients, and sea-level rise as ‘‘low- information. Veron (2000; 2014) fourth lowest bleaching of the 32 genera medium’’ importance to corals overall. considers the species valid, and we recorded (McClanahan et al., 2005a). In The SRR reported that one study consider it is sufficiently distinctive to a bleaching event on Howland and showed Pavona decussata had an be identified by experts, thus we Baker Islands in 2010, between 32 and intermediate level of susceptibility to conclude that the distribution and 37 percent of Pavona colonies bleached sedimentation. Thus, we conclude that abundance information described below (Vargas-Angel et al., 2011). During the an unstudied Pavona species is likely to for this species is sufficiently reliable same 2010 bleaching event in Thailand, have some susceptibility to (Fenner, 2014b). between 47 and 67 percent of Pavona sedimentation. Although there is no Spatial Information colonies bleached (Sutthacheep et al., genus-level or species-specific 2013). information on the susceptibilities of The SRR and SIR provided the In a broad study of 45 genera in the Pavona species to nutrients, the SRR following information on P. diffluens’ western Indian Ocean in 1998 to 2005, rated it as ‘‘low-medium’’ importance to distribution, habitat, and depth range. Pavona ranked 31st in bleaching corals.. Thus, we conclude that an Pavona diffluens occurs from the Red susceptibility (McClanahan et al., unstudied Pavona species is likely to Sea to the Arabian Gulf, and records 2007a). Pavona had a low prevalence of have some susceptibility to nutrients. show this species from the Marianas disease in Guam, with 0.5% of colonies Sea-level rise was not addressed at the Islands and American Samoa, but the with disease, tied for sixth highest genus or species level in the SRR or SIR. records from the Marianas Islands were prevalence out of 12 genera, with the Increasing sea levels may increase land- unlikely. Its habitat includes at least highest genus having 6.7 percent (Myers based sources of pollution due to upper reef slopes, mid-slopes, lower reef and Raymundo, 2009). There is no other inundation, resulting in changes to coral crests, reef flats, and lagoons, in depths supplemental information on the community structure, thus an unstudied ranging from five to at least 20 m. The public comments and susceptibilities or vulnerabilities of Pavona species is likely to have some information we gathered provided Pavona to other threats. susceptibility to sea-level rise. The SRR supplemental information on the reported that Pavona was susceptible to Genus Conclusion distribution of P. diffluens. One public starfish predation (but the level varied Based on the information from the comment stated that the occurrence of by species) and that the genus is traded SRR, SIR, public comments, and P. diffluens in the Marianas indicates in a moderate amount. Thus, we supplemental information, we can make that this species has a broader range conclude that an unstudied Pavona the following inferences about the than has been recognized by the species has some susceptibility to susceptibilities of an unstudied Pavona authors. We gathered supplemental species to ocean warming, disease, predation and to collection and trade. In conclusion, an unstudied Pavona information, including additional ocean acidification, sedimentation, species is likely to have some reports of P. diffluens from American nutrients, trophic effects of fishing, sea- susceptibility to ocean warming, Samoa (Fenner, 2014b; Kenyon et al., level rise, predation, and collection and disease, acidification, trophic effects of 2010), but the taxonomic question for trade. The SRR rated ocean warming fishing, nutrients, sedimentation, them remains. Veron (2014) reports that and disease as ‘‘high’’ importance, and this species is confirmed in five of his ocean acidification as ‘‘medium-high’’ nutrients, sea-level rise, predation, and collection and trade. 133 Indo-Pacific ecoregions, and importance, to corals. These were rated strongly predicted to be found in an as the three most important threats to Pavona diffluens additional three, all of which are in the reef-building corals overall. There was a Introduction western Indian Ocean. The public wide range of reported susceptibility of comments and information we gathered Pavona colonies to ocean warming and The SRR and SIR provided the provided nothing new or supplemental acidification. One study reported a following information on P. diffluens’ on P. diffluens’ habitat and depth range. moderate disease prevalence in Pavona morphology and taxonomy. Morphology and another reported a low prevalence. was described as submassive, and the Demographic Information Thus, we conclude that an unstudied taxonomy was described as having no The SRR and SIR provided the Pavona species is likely to have some taxonomic issues, but it is similar to following information on P. diffluens’ susceptibility to ocean warming, Pavona gigantea and Pavona abundance. Pavona diffluens has been disease, and acidification. explanulata. reported as uncommon. The SRR rated the trophic effects of The public comments and The public comments did not provide fishing as ‘‘medium’’ importance, the information we gathered did not any new or supplemental information fourth most important threat to corals provide any new or supplemental on P. diffluens’ abundance, but we overall. This threat was not addressed at information on morphology. There is gathered supplemental information that the genus or species level in the SRR or high taxonomic uncertainty about provided the following: Veron (Fenner, SIR, because it is an ecosystem-level colonies that appear similar to P. 2014b; Veron, 2014) reported that P. process. That is, removal of herbivorous diffluens in the Pacific, but low diffluens occupied 0.47% of 2,984 dive fish from coral reef systems by fishing taxonomic uncertainty about P. sites sampled in 30 ecoregions of the alters trophic interactions by reducing diffluens in the Red Sea and Indian Indo-Pacific, and had a mean abundance herbivory on algae, thereby providing a Ocean. Both colonies in the Red Sea/ rating of 1.43 on a 1 to 5 rating scale at competitive advantage for space to algae Indian Ocean, and in the Pacific, are those sites in which it was found. Based over coral. Thus, the SRR did not easily distinguished from other Pavona. on this semi-quantitative system, the discuss this threat in terms of coral taxa, Veron (2014) states that, ‘‘We believe species’ abundance is characterized as

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‘‘rare,’’ and overall abundance is of fishing, low vulnerabilities to collection and general coral protection described as ‘‘uncommon.’’ Veron did sedimentation, sea-level rise, predation, laws are less common regulatory not infer trends in abundance from and collection and trade, and unknown mechanisms for the management of P. these data. As described in the Indo- vulnerability to nutrients. diffluens. Pacific Species Determinations Public comments did not provide any Vulnerability to Extinction introduction above, based on results new or supplemental information on P. from Richards et al. (2008) and Veron diffluens’ threat susceptibilities. We As explained above in the Risk (2014), the absolute abundance of this gathered the following species-specific Analyses section, a species’ species is likely at least millions of and genus-level supplemental vulnerability to extinction results from colonies. information on this species’ threat the combination of its spatial and Carpenter et al. (2008) extrapolated susceptibilities. P. diffluens has not demographic characteristics, threat species abundance trend estimates from been rated as moderately or highly susceptibilities, and consideration of the total live coral cover trends and habitat susceptible to bleaching or disease, but baseline environment and future types. For P. diffluens, the overall this rating is not based on species- projections of threats. The SRR stated decline in abundance (‘‘Percent specific data (Carpenter et al., 2008). that P. diffluens’ fairly moderate-to-low Population Reduction’’) was estimated There is no species-specific information tolerance to thermal stress and the at 36 percent, and the decline in for the exposure or susceptibility of P. species’ narrow distribution range abundance before the 1998 bleaching diffluens to any threat. Based on genus- increase the potential extinction risk. It event (‘‘Back-cast Percent Population level and species information described listed factors that reduce potential Reduction’’) was estimated at 20 above, P. diffluens likely has some extinction risk for P. diffluens including percent. However, as summarized above susceptibilities to ocean warming, its moderate tolerance of sediment stress in the Inter-basin Comparison sub- disease, acidification, trophic effects of and its low susceptibility of the genus section, live coral cover trends are fishing, sedimentation, nutrients, sea- to disease and predation. highly variable both spatially and level rise, predation, and collection and Subsequent to the proposed rule, we temporally, producing patterns on small trade. The available information does received and gathered supplemental scales that can be easily taken out of not support more precise ratings of the species- or genus-specific information, context. Thus, these changes have likely susceptibilities of P. diffluens to the described above, that expands our occurred, and are occurring, from a threats. knowledge regarding the species combination of global and local threats. abundance, distribution, and threat Regulatory Mechanisms Given that P. diffluens occurs in many susceptibilities. We developed our areas affected by these broad changes, In the proposed rule we did not assessment of the species’ vulnerability and likely has some susceptibility to provide any species-specific to extinction using all the available both global and local threats, we information on the regulatory information. As explained in the Risk conclude that it is likely to have mechanisms or conservation efforts for Analyses section, our assessment in this declined in abundance over the past 50 P. diffluens. Criticisms of our approach final rule emphasizes the ability of the to 100 years, but a precise quantification received during public comment led us species’ spatial and demographic traits is not possible based on the limited to the following analysis to attempt to to moderate or exacerbate its species-specific information. analyze regulatory mechanisms on a vulnerability to extinction, as opposed species basis. Records confirm that to the approach we used in the Other Biological Information Pavona diffluens occurs in five Indo- proposed rule, which emphasized the The SRR and SIR provided the Pacific ecoregions that encompass 14 species’ susceptibility to threats. following information on P. diffluens’ countries’ EEZs. The 14 countries are The following characteristics of P. life history. The reproductive Djibouti, Egypt, Eritrea, France (French diffluens, in conjunction with the characteristics of P. diffluens have not Pacific Island Territories), Iran, Israel, information described in the Corals and been determined, but six other species Jordan, Madagascar, Oman, Pakistan, Coral Reefs section, Coral Habitat sub- in the genus are known to be gonochoric Saudi Arabia, Sudan, United Arab section, and Threats Evaluation section broadcast spawners. The public Emirates, and Yemen. The regulatory above, affect its vulnerability to comments did not provide new or mechanisms relevant to P. diffluens, extinction currently and over the supplemental information, and we did described first as the percentage of the foreseeable future. Its geographic not find new or supplemental above countries that utilize them to any distribution is limited only to parts of information on the above-described degree, and second, as the percentages the western Indian Ocean along coastal biological information. of those countries whose regulatory East Africa, the Red Sea, and the Gulf mechanisms may be limited in scope, of Oman. This range exacerbates Susceptibility to Threats are as follows: General coral protection vulnerability to extinction over the To describe P. diffluens’ threat (21 percent with 7 percent limited in foreseeable future because of its size and susceptibilities, the SRR and SIR scope), coral collection (43 percent with localized human impacts for coral reefs provided genus-level information for the 7 percent limited in scope), pollution over the 21st century. In addition, parts effects on Pavona of ocean warming, control (64 percent with 7 percent of the Red Sea are projected to disease, acidification, sedimentation, limited in scope), fishing regulations on experience severe impacts from climate predation, and collection and trade. The reefs (71 percent with 21 percent change more rapidly than other parts of SRR and SIR did not provide any other limited in scope), and managing areas the Indo-Pacific region. Its depth range species-specific information on the for protection and conservation (79 of five to 25 meters moderates effects of these threats on P. diffluens. percent with 21 percent limited in vulnerability to extinction over the We interpreted the threat susceptibility scope). The most common regulatory foreseeable future because deeper areas and exposure information from the SRR mechanisms in place for P. diffluens are of its range will usually have lower and SIR in the proposed rule as follows: reef fishing regulations and area irradiance than surface waters, and High vulnerability to ocean warming, management for protection and acidification is generally predicted to moderate vulnerabilities to disease, conservation. Pollution control laws are accelerate most in waters that are deeper ocean acidification, and trophic effects also common for the species. Coral and cooler than those in which the

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species occurs. Its habitat includes at particular geographic area this size, depensatory processes such as least upper reef slopes, mid-slopes, predicted to experience increasing reproductive failure from low density of lower reef crests, reef flats, and lagoons. threat impacts, indicates that a high reproductive individuals and genetic This moderates vulnerability to proportion of the population of this processes such as inbreeding affecting extinction over the foreseeable future species is likely to be exposed to threats this species. Thus, its abundance because the species is not limited to one that occur throughout this range over indicates it is currently able to avoid habitat type but occurs in numerous the foreseeable future; and high mortality from environmental types of reef environments that will, on (3) Pavona diffluens’ qualitative stochasticity, and mortality of a high local and regional scales, experience abundance is rare, which means it does proportion of its population from highly variable thermal regimes and not possess as much buffering capacity catastrophic events. ocean chemistry at any given point in in the form of variability in response The combination of these time. Its abundance of at least millions between individuals or absolute characteristics indicates that the species of colonies, combined with spatial abundance that would be afforded to a does not exhibit the characteristics of variability in ocean warming and more abundant or common species. one that is currently in danger of acidification across the species range, Combined with the limited range of this extinction, as described previously in moderates vulnerability to extinction species, this level of abundance leaves the Risk Analyses section, and thus does because the increasingly severe the species vulnerable to becoming of not warrant listing as endangered at this conditions expected in the foreseeable such low abundance within the time. future will be non-uniform and foreseeable future that it may be at risk Range-wide, a multitude of therefore will likely be a large number from depensatory processes, conservation efforts are already broadly of colonies that are either not exposed environmental stochasticity, or employed that are likely benefiting P. or do not negatively respond to a threat catastrophic events, as explained in diffluens. However, considering the at any given point in time. However, its more detail in the Corals and Coral global scale of the most important qualitative abundance is described as Reefs and Risk Analyses sections. threats to the species, and the rare, which can exacerbate its The combination of these ineffectiveness of conservation efforts at vulnerability given its restricted range. characteristics and projections of future addressing the root cause of global threats indicates that the species is Listing Determination threats (i.e., GHG emissions), we do not likely to be in danger of extinction believe that any current conservation In the proposed rule using the within the foreseeable future throughout efforts or conservation efforts planned determination tool formula approach, P. its range and warrants listing as in the future will result in affecting the diffluens was proposed for listing as threatened at this time due to factors A, species status to the point at which threatened because of: Moderate C, D, and E. listing is not warranted. vulnerability to ocean warming (ESA The available information above on P. Factor E), disease (C) and acidification diffluens’ spatial structure, demography, Genus Pectinia threat susceptibilities, and management (E); uncommon generalized range wide Genus Introduction abundance (E); narrow overall also indicate that the species is not distribution (based on narrow currently in danger of extinction and The family Pectiniidae includes five geographic distribution and moderate thus does not warrant listing as genera, Pectinia, Echinomorpha, depth distribution (E); and inadequacy Endangered because: Echinophyllia, Oxypora and Mycedium. of existing regulatory mechanisms (D). (1) While P. diffluens’ distribution is Veron (2000) recognizes nine species of In this final rule, the listing constrained only to parts the western Pectinia. Colonies are laminar to determination for P. diffluens remained Indian Ocean along coastal East Africa, branching, and may have high walls threatened. Based on the best available the Red Sea, and the Gulf of Oman, the separating wide valleys. The SRR and information provided above on P. species’ range still includes SIR provided no genus-level diffluens’ spatial structure, demography, heterogeneous habitat across its range, introductory information on Pectinia. threat susceptibilities, and management, including at least upper reef slopes, Genus Susceptibility to Threats it is likely to become endangered mid-slopes, lower reef crests, reef flats, throughout its range within the and lagoons. Thus, the species is not The SRR and SIR provided the foreseeable future, and thus warrants limited to one habitat type but occurs in following information on the threat listing as threatened at this time, numerous types of reef environments susceptibilities of the genus Pectinia. A because: that will, on local and regional scales, case study from the Waikiki Aquarium (1) Pavona diffluens is susceptible to experience highly variable thermal reported tolerance of Pectinia alcicornis ocean warming (E), disease (C), ocean regimes and ocean chemistry at any to low pH. With regards to disease, the acidification (E), trophic effects of given point in time, as described in SRR referred to a study that reported fishing (A), nutrients (A, E), and more detail in the Coral Habitat and crustacean parasites in Pectinia lactuca predation (C). In addition, the species Threats Evaluation sections. There is no in American Samoa. However, has inadequate regulatory mechanisms evidence to suggest that the species is so taxonomists have not recorded any for global threats (D); spatially fragmented or geographically Pectinia species there so far (D. Fenner, (2) Pavona diffluens’ distribution is constrained that depensatory processes, personal comm.). Another study mostly constrained to a small part of the environmental stochasticity, or the referred to in the SRR reported Pectinia Indian Ocean where projections of local potential for catastrophic events was not infected by ciliate skeletal threats (e.g., land-based sources of currently pose a high risk to the survival eroding band on the GBR. The SRR pollution) and general effects of climate of the species; and referred to two studies that reported that change are both frequent and severe (2) While P. diffluens’ qualitative Pectinia is tolerant of sediment, one over the foreseeable future. The Red Sea abundance is rare, its absolute study that indicated it was tolerant of in particular is projected to experience abundance is at least millions of high nutrients, and one study that frequent warming events sooner than colonies, which allows for some reported it decreased along a gradient of most other parts of the Indo-Pacific variation in the responses of individuals reduced water quality. The SRR region. A range constrained to a to threats. There is no evidence of reported that Pectinidae species are

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highly susceptible to crown-of-thorns The SRR rated the trophic effects of Public comments and information we seastar. The SRR reported that the genus fishing as ‘‘medium’’ importance, the gathered did not provide any new or Pectinia is heavily exported—several fourth most important threat to corals supplemental information on thousand specimens are exported overall. This threat was not addressed at morphology, and confirmed that there annually. the genus or species level in the SRR or are no known taxonomic problems for P. The public comments did not provide SIR, because it is an ecosystem-level alcicornis, but a moderate level of any new or supplemental information process. That is, removal of herbivorous species identification uncertainty exists. on the threat susceptibilities of the fish from coral reef systems by fishing Veron (2014) states that P. alcicornis is genus Pectinia. We gathered alters trophic interactions by reducing sometimes confused with other Pectinia supplemental information that provided herbivory on algae, thereby providing a species and Veron (2000; 2014) the following. With regard to thermal competitive advantage for space to algae considers the species valid, thus we stress, during a bleaching event on the over coral. Thus, the SRR did not conclude it can be identified by experts, GBR in 2002, between five and 11 discuss this threat in terms of coral taxa, and that the distribution and abundance percent of three species of Pectinia were as its effects are difficult to distinguish information described below for this affected (Done et al., 2003a). In Palau in between coral genera and species. species is sufficiently reliable (Fenner, 2000, Pectinia lactuca and Pectinia Therefore, an unstudied Pectinia species 2014b). peonia both had high levels of bleaching is likely to have some susceptibility to Spatial Information and high mortality. Forty-eight percent the trophic effects of fishing. of all colonies of all species were The SRR and SIR provided the The SRR rated sedimentation, bleached, and both bleaching and following information on P. alcicornis’ nutrients, and sea-level rise as ‘‘low- mortality of different genera and species distribution, habitat, and depth range. medium’’ importance to corals overall. ranged from zero to near 100 percent The SRR and SIR described P. (Bruno et al., 2001). Ruiz-Moreno et al. Studies of the effects of sediment and alcicornis’ distribution as broadly (2012) reported that the family nutrients on Pectinia were inconsistent, distributed from the northern Indian Pectinidae had the highest disease thus we conclude that an unstudied Ocean to Fiji. It inhabits turbid water prevalence of any family of corals in the Pectinia species is likely to have some and other low-light environments in Pacific, and third highest of all coral susceptibility to sediment and nutrients. most coral reef habitats, including at families they studied in the Caribbean Sea-level rise was not addressed at the least upper reef slopes, mid-slopes, and Indo-Pacific. However, the family genus or species level in the SRR or SIR. lagoons, and caves, at depths of five to Pectinidae has five genera, and the Increasing sea levels may increase land- 25 m. study did not report on the genus based sources of pollution due to Public comments did not provide any Pectinia. There is no other supplemental inundation, resulting in changes to coral new or supplemental information on P. information on the susceptibilities of community structure, thus an unstudied alcicornis’ distribution. We gathered Pectina to threats. Pectinia species is likely to have some supplemental information including, susceptibility to sea-level rise. The SRR Veron (2014), which reports that this Genus Conclusion reported that Pectinidae species are species is confirmed in 39 of his 133 Based on the information from the highly susceptible to crown-of-thorns Indo-Pacific ecoregions, and strongly SRR, SIR, public comments, and seastar, thus we conclude that an predicted to be found in an additional supplemental information, we can make unstudied Pectinia species is likely to 16. the following inferences about the have some susceptibility to collection susceptibilities of an unstudied Pectinia and trade. The SRR rated ornamental Demographic Information species to ocean warming, disease, trade (referred to in the proposed rule as The SRR and SIR reported P. ocean acidification, sedimentation, Collection and Trade) as ‘‘low’’ alcicornis’ abundance as usually nutrients, trophic effects of fishing, sea- importance to corals overall. The SRR uncommon. level rise, predation, and collection and reported that Pectinia is heavily traded, Public comments did not provide any trade. The SRR rated ocean warming thus we conclude that an unstudied new or supplemental information on P. and disease as ‘‘high’’ importance, and Pectinia species is likely to have some alcicornis’ abundance. We gathered ocean acidification as ‘‘medium-high’’ susceptibility to collection and trade. supplemental information including importance, to corals. These were rated In conclusion, an unstudied Pectinia Veron (2014), which reports that P. as the three most important threats to species is likely to have some alcicornis occupied 16.6 percent of reef-building corals overall. Pectinia susceptibility to ocean warming, 2,984 dive sites sampled in 30 shows a variable level of warming- disease, ocean acidification, trophic ecoregions of the Indo-Pacific, and had induced bleaching, thus we conclude effects of fishing, sedimentation, a mean abundance rating of 1.6 on a 1 that an unstudied Pectinia is likely to nutrients, sea-level rise, predation, and to 5 rating scale at those sites in which have some susceptibility to ocean collection and trade. it was found. Based on this semi- warming. Although there is no other quantitative system, the species’ genus-level or species-specific Pectinia alcicornis abundance was characterized as information on the susceptibility of Introduction ‘‘common,’’ and overall abundance was Pectinia species to disease, the SRR described as ‘‘usually uncommon.’’ rated it as ‘‘high’’ importance to corals, The SRR and SIR provided the Veron did not infer trends in abundance thus we conclude that an unstudied following information on P. alcicornis’ from these data. As described in the Pectinia is likely to have some morphology and taxonomy. Morphology Indo-Pacific Species Determinations susceptibility to disease. One study was described as irregular clusters with introduction above, based on results reported one species of Pectinia had thin, flat, grooved plates and tall, from Richards et al. (2008) and Veron some resistant to acidification, thus upward-projecting spires that can (2014), the absolute abundance of this with only one study, we conclude that dominate its structure. The taxonomy species is likely at least tens of millions an unstudied Pectinia is likely to have was described as having no taxonomic of colonies. some susceptibility to ocean issues but being similar in appearance Carpenter et al. (2008) extrapolated acidification. to Pectinia paeonia. species abundance trend estimates from

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total live coral cover trends and habitat quality gradient on the Great Barrier Sri Lanka, Taiwan, Thailand, Timor- types. For P. alcicornis, the overall Reef. Pectinia alcicornis exports were Leste, Vanuatu, and Vietnam. The decline in abundance (‘‘Percent reported at the species level only for regulatory mechanisms relevant to P. Population Reduction’’) was estimated 2000–2003, with a total of 133 alcicornis, described first as the at 38 percent, and the decline in specimens reported. The SRR and SIR percentage of the above countries that abundance before the 1998 bleaching did not provide any other species- utilize them to any degree, and second event (‘‘Back-cast Percent Population specific information on the effects of as the percentage of those countries Reduction’’) was estimated at 15 these threats on P. alcicornis. We whose regulatory mechanisms may be percent. However, as summarized above interpreted threat susceptibility and limited in scope, are as follows: General in the Inter-basin Comparison sub- exposure information from the SRR and coral protection (33 percent with 10 section, live coral cover trends are SIR in the proposed rule for P. percent limited in scope), coral highly variable both spatially and alcicornis’ vulnerabilities as follows: collection (52 percent with 29 percent temporally, producing patterns on small High vulnerability to ocean warming, limited in scope), pollution control (38 scales that can be easily taken out of moderate vulnerability to disease, ocean percent with 14 percent limited in context. Thus, quantitative inferences to acidification, trophic effects of fishing, scope), fishing regulations on reefs (100 species-specific trends should be and predation, and low vulnerability to percent with 14 percent limited in interpreted with caution. At the same sedimentation, nutrients, sea level rise, scope), and managing areas for time, an extensive body of literature and collection and trade. protection and conservation (95 percent documents broad declines in live coral Public comments did not provide any with none limited in scope). The most cover and shifts to reef communities new or supplemental information on P. common regulatory mechanisms in dominated by hardier coral species or alcicornis’ threats susceptibilities. We place for P. alcicornis are reef fishing algae over the past 50 to 100 years gathered supplemental species-specific regulations and area management for (Birkeland, 2004; Fenner, 2012; Pandolfi and genus-level information on this protection and conservation. Coral et al., 2003; Sale and Szmant, 2012). species’ threat susceptibilities. Pectinia collection laws are also somewhat These changes have likely occurred, and alcicornis has been rated as moderately utilized for the species, but 29 percent are occurring, from a combination of or highly susceptible to bleaching but of coral collection laws are limited in global and local threats. Given that P. not to disease, however this rating is not scope and may not provide substantial alcicornis occurs in many areas affected based on species-specific data protection. General coral protection and by these broad changes, and likely has (Carpenter et al. 2008). With regard to pollution control laws are less common some susceptibility to both global and thermal stress, eight percent of P. regulatory mechanisms for the local threats, we conclude that it is alcicornis was affected by bleaching on management of P. alcicornis. likely to have declined in abundance the GBR in 2002. The other two Pectinia Vulnerability to Extinction over the past 50 to 100 years, but a species included in the study were precise quantification is not possible affected by bleaching at rates of three As explained above in the Risk based on the limited species-specific percent and 12 percent, and the range Analyses section, a species’ information. for all members of family Pectiniidae vulnerability to extinction results from was zero to 17 percent (Done et al., the combination of its spatial and Other Biological Information 2003a). There is no other supplemental demographic characteristics, threat The SRR and SIR reported that P. information on the effects of threats on susceptibilities, and consideration of the alcicornis is a hermaphroditic broadcast this species. Based on genus-level and baseline environment and future spawner. The public comments and species-specific information described projections of threats. The SRR stated information we gathered provided no above, P. alcicornis likely has some that high bleaching rate is the primary new or supplemental biological susceptibility to ocean warming, threat of extinction for Pectinia, information. disease, acidification, trophic effects of although P. alcicornis may be relatively resistant in some areas. Factors that Susceptibility to Threats fishing, sedimentation, nutrients, sea- level rise, predation, and collection and increase potential extinction risk for P. To describe P. alcicornis’ threat trade. The available information does alcicornis include susceptibility to susceptibilities, the SRR and SIR not support more precise ratings of this bleaching, predation, and harvesting. It provided genus-level information for the species’ threat susceptibilities. listed factors that reduce potential effects on Pectinia of ocean warming, extinction risk including that P. acidification, disease, predation, Regulatory Mechanisms alcicornis occupies a variety of habitat sedimentation, nutrients, and collection In the proposed rule, we did not types and is broadly distributed both and trade. The SRR and SIR also provide any species-specific latitudinally and longitudinally in the provided the following species-specific information on the regulatory Indo-Pacific. information on P. alcicornis’ threats. mechanisms or conservation efforts for Subsequent to the proposed rule, we Pectinia alcicornis showed very little P. alcicornis. Public comments were received and gathered supplemental mortality on the GBR in the 2001–2002 critical of that approach and we species- or genus-specific information, mass bleaching event. Pectinia therefore attempt to analyze regulatory described above, that expands our alcicornis harbors Clade C mechanisms on a species basis in this knowledge regarding the species zooxanthellae in Okinawa and the final rule. Records confirm that Pectinia abundance, distribution, and threat South China Sea, but contained Clade D alcicornis occurs in 39 Indo-Pacific susceptibilities. We developed our zooxanthellae in Palau after the 2001 ecoregions that encompass 21 countries’ assessment of the species’ vulnerability mass bleaching event. It is one of many EEZs. The 21 countries are Australia, to extinction using all the available species that has been raised in the Brunei, China, Federated States of information. As explained in the Risk Waikiki Aquarium, which is Micronesia, Fiji, France (French Pacific Analyses section, our assessment in this characterized by high-nutrient, low-pH Island Territories), India (Andaman and final rule emphasizes the ability of the waters. Although it is generally a Nicobar Islands), Indonesia, Japan, species’ spatial and demographic traits sediment-tolerant genus, P. alcicornis Malaysia, Myanmar, Palau, Papua New to moderate or exacerbate its decreased along a deteriorating water Guinea, Philippines, Solomon Islands, vulnerability to extinction, as opposed

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to the approach we used in the (based on wide geographic distribution Notwithstanding the projections proposed rule, which emphasized the and moderate depth distribution (E); through 2100 that indicate increased species’ susceptibility to threats. and inadequacy of existing regulatory severity over time of the three high The following characteristics of P. mechanisms (D). importance threats, the combination of alcicornis, in conjunction with the In this final rule, we changed the these biological and environmental information described in the Corals and listing determination for P. alcicornis characteristics indicates that the species Coral Reefs section, Coral Habitat sub- from threatened to not warranted. We possesses sufficient buffering capacity section, and Threats Evaluation section made this determination based on a to avoid being in danger of extinction above, affect its vulnerability to more species-specific and holistic within the foreseeable future throughout extinction currently and over the assessment of whether this species its range. It is possible that this species’ foreseeable future. Its geographic meets the definition of either a extinction risk may increase in the distribution is from the northern Indian threatened or endangered coral largely future if global threats continue and Ocean to Fiji. Its geographic distribution in response to public comments, worsen in severity and the species’ moderates vulnerability to extinction including more appropriate exposure to the threats increases because some areas within its range are consideration of the buffering capacity throughout its range. Should the species projected to have less than average of this species’ spatial and demographic experience reduced abundance or range warming and acidification over the traits to lessen its vulnerability to constriction of a certain magnitude, the foreseeable future, including the central threats. Thus, based on the best ability of these characteristics to Pacific, and other areas, so portions of available information above on P. moderate exposure to threats will the population in these areas will be alcicornis’ spatial structure, diminish. However, the species is not less exposed to severe conditions. Its demography, threat susceptibilities, and likely to become of such low abundance depth range is five to 25 m. This management, none of the five ESA or so spatially fragmented as to be in moderates vulnerability to extinction listing factors, alone or in combination, danger of extinction due to depensatory over the foreseeable future because are causing this species to likely become processes, the potential effects of deeper areas of its range will usually endangered throughout its range within environmental stochasticity, or the have lower irradiance than surface the foreseeable future, and thus it is not potential for mortality from catastrophic waters, and acidification is generally warranted for listing at this time, events within the foreseeable future predicted to accelerate most in waters because: throughout its range. Therefore, P. that are deeper and cooler than those in (1) Pectinia alcicornis’ distribution alcicornis is not warranted for listing at which the species occurs. Its inhabits from the northern Indian Ocean through this time under any of the listing factors. turbid water and other low-light the western Pacific Ocean to Fiji environments in most coral reef Genus Acanthastrea includes tens of thousands of islands habitats, including at least upper reef and reefs spread over a vast area. While Genus Introduction slopes, mid-slopes, lagoons, and caves. some areas within its range are This moderates vulnerability to The family Mussidae has 13 genera, projected to be affected by warming and extinction over the foreseeable future eight of which are restricted to the Indo- acidification, other areas are projected because the species is not limited to one Pacific, including Acanthastrea. The to have less than average warming and habitat type but occurs in numerous genus Acanthastrea contains 12 known acidification, including the central types of reef environments that will, on species. Most Acanthastrea are local and regional scales, experience Pacific and other areas. This encrusting, but one is massive. The SRR highly variable thermal regimes and distribution and the heterogeneous and SIR provided no genus-level ocean chemistry at any given point in habitats it occupies reduce exposure to introductory information on time. Turbidity in particular can any given threat event or adverse Acanthastrea. condition that does not occur uniformly moderate exposure to high irradiance by Genus Susceptibility to Threats blocking light and resulting heat from throughout the species range. As the water column. Its absolute explained above in the Threats The SRR and SIR provided the abundance of at least tens of millions of Evaluation section, we have not following information on the threat colonies, combined with spatial identified any threat that is expected to susceptibilities of the genus variability in ocean warming and occur uniformly throughout the species Acanthastrea. The genus Acanthastrea acidification across the species range, range within the foreseeable future; has been reported to be highly moderates vulnerability to extinction (2) Pectinia alcicornis’ total susceptibility to bleaching in Australia because the increasingly severe population size is at least tens of and in the western Indian Ocean. The conditions expected in the foreseeable millions of colonies, providing buffering genus sustained moderate bleaching in future will be non-uniform and capacity in the form of absolute Palau in 1994 and several Acanthastrea therefore will likely be a large number numbers of colonies and variation in species were relatively unaffected of colonies that are either not exposed susceptibility between individual during the 2002 event on the GBR (Done or do not negatively respond to a threat colonies. As discussed in the Corals and et al., 2003b). Although no exports of at any given point in time. Coral Reefs section above, the more Acanthastrea were reported from 2000– colonies a species has, the lower the 2009, 1,000 Acanthastrea pieces were Listing Determination proportion of colonies that are likely to exported from Indonesia in 2010. In the proposed rule using the be exposed to a particular threat at a The public comments did not provide determination tool formula approach, P. particular time, and all individuals that any new or supplemental information alcicornis was proposed for listing as are exposed will not have the same on the threat susceptibilities of the threatened because of: High response; and genus Acanthastrea. We gathered vulnerability to ocean warming (ESA (3) Pectinia alcicornis extends down supplemental information which Factor E); moderate vulnerability to to 25 meters depth, providing some provided the following details. All disease (C) and acidification (E); buffering capacity against threat- Acanthastrea in protected areas in uncommon generalized range wide induced mortality events that may be Kenya were killed by mass bleaching in abundance (E); wide overall distribution more severe in shallow habitats; 1998 (McClanahan et al., 2001). Out of

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four Acanthastrea species on the GBR, competitive advantage for space to algae taxonomic issues but being similar in three species were not affected by the over coral. Thus, the SRR did not appearance to Acanthastrea echinata. 2002 GBR bleaching event, while 22 discuss this threat in terms of coral taxa, Public comments and information we percent of one species was affected as its effects are difficult to distinguish gathered did not provide any new or (Done et al., 2003b). At Mauritius in a between coral genera and species. supplemental information on bleaching event in 2004, Acanthastrea Therefore, an unstudied Acanthastrea morphology, and confirmed that there had a bleaching index of nine, the 22nd species is likely to have some are no known taxonomic problems for highest of the 32 genera recorded, which susceptibility to the trophic effects of A. brevis, but a moderate to high level was 14 percent of the index of the genus fishing. of species identification uncertainty. with the highest index (McClanahan et The SRR rated sedimentation, Veron (2014) states that it is ‘‘readily al., 2005a). In the western Indian Ocean nutrients, and sea-level rise as ‘‘low- confused with Acanthastrea echinata,’’ in 1998–2005, Acanthastrea had a medium’’ importance to corals overall. but Veron (2000; 2014) considers the bleaching index of 14.4 for eight One study found an Acanthastrea species valid, thus we conclude it can countries, which was 24th highest of the species to have moderate sediment- be identified by experts and that the 45 genera recorded, and 35 percent of clearing ability. Thus we conclude that distribution and abundance information the highest value (McClanahan et al., an unstudied Acanthastrea species is described below for this species is 2007a). likely to have some susceptibility to sufficiently reliable (Fenner, 2014b). With regard to land-based sources of sedimentation. Although there is no Spatial Information pollution, Stafford-Smith (1993) genus-level or species-specific reported that 14 of 20 Acanthastrea information on the susceptibilities of The SRR and SIR provided the echinata samples cleared over 98 Acanthastrea species to nutrients, the following information on A. brevis’ percent of sediment within 48 hours, SRR rated it as ‘‘low-medium’’ distribution, habitat, and depth range. the 12th best score. This score was 70 importance to corals. Thus, we conclude Acanthastrea brevis is distributed from percent of the highest scoring species. that an unstudied Acanthastrea species the Red Sea and western Indian Ocean There is no other supplemental has some susceptibility to nutrients. to American Samoa in the central information on the effects of threats on Sea-level rise was not addressed at the Pacific. Its habitat includes all coral reef the genus Acanthastrea. genus or species level in the SRR or SIR. habitats, in a depth range of one to 20 Increasing sea levels may increase land- m. Genus Conclusion Public comments provided the based sources of pollution due to Based on the information from the following information on distribution inundation, resulting in changes to coral SRR, SIR, public comments, and for A. brevis. One public comment community structure, thus an unstudied supplemental information, we can make stated that A. brevis likely occurs in the Acanthastrea species is likely to have the following inferences about the Marianas and will be included in an some susceptibility to sea-level rise. The susceptibilities of an unstudied upcoming book. We gathered SRR rated predation and ornamental Acanthastrea species to ocean warming, supplemental information, including trade (referred to in the proposed rule as disease, ocean acidification, Veron (2014), which reports that this Collection and Trade) as ‘‘low’’ sedimentation, nutrients, trophic effects species is confirmed in 29 of his 133 importance to corals overall. Although of fishing, sea-level rise, predation, and Indo-Pacific ecoregions, and strongly there is no genus-level or species- collection and trade. The SRR rated predicted to be found in an additional specific information on the ocean warming and disease as ‘‘high’’ 17. Acanthastrea brevis is found in the susceptibilities of Acanthastrea species importance, and ocean acidification as Northern Marianas and American to predation, there is no information ‘‘medium-high’’ importance, to corals. Samoa as well (D. Fenner, personal suggesting they are not susceptible to These were rated as the three most comm.) and the Marianas are one of the this threat. Thus, we conclude that an important threats to reef-building corals predicted areas for A. brevis in the unstudied Acanthastrea species has overall. The above information on Veron (2014) information. Public some susceptibility to predation. Acanthastrea shows a wide range of comments and information we gathered Because the available information susceptibility to ocean warming, thus did not provide any more information suggests that Acanthastrea species are we conclude that an unstudied on the habitat and depth range of this lightly collected and traded, an Acanthastrea species is likely to have species. some susceptibility to ocean warming. unstudied Acanthastrea species is likely Although there is no genus-level or to have low susceptibility to collection Demographic Information species-specific information on the and trade. The SRR and SIR reported A. brevis’ susceptibilities of Acanthastrea species In conclusion, an unstudied abundance as uncommon but to disease and ocean acidification, the Acanthastrea species is likely to have conspicuous. SRR rated it as ‘‘medium-high’’ some susceptibility to ocean warming, Public comments did not provide any importance to corals. Thus, we conclude disease, acidification, sedimentation, new or supplemental information on A. that an unstudied Acanthastrea species nutrients, trophic effects of fishing, sea- brevis’ abundance. We gathered is likely to have some susceptibility to level rise, and predation, and is likely supplemental information, including disease and ocean acidification. to have low susceptibility to collection Veron (2014), which reports that A. The SRR rated the trophic effects of and trade. brevis occupied 6.5 percent of 2,984 fishing as ‘‘medium’’ importance, the Acanthastrea brevis dive sites sampled in 30 ecoregions of fourth most important threat to corals the Indo-Pacific, and had a mean overall. This threat was not addressed at Introduction abundance rating of 1.49 on a 1 to 5 the genus or species level in the SRR or The SRR and SIR provided the rating scale at those sites in which it SIR, because it is an ecosystem-level following information on A. brevis’ was found. Based on this semi- process. That is, removal of herbivorous morphology and taxonomy. Morphology quantitative system, the species’ fish from coral reef systems by fishing was described as mostly submassive, abundance was characterized as alters trophic interactions by reducing attached and colonial, and the ‘‘uncommon,’’ and overall abundance herbivory on algae, thereby providing a taxonomy was described as having no was also described as ‘‘uncommon.’’

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Veron did not infer trends in abundance did not provide any other species- limited in scope), pollution control (55 from these data. As described in the specific information on the effects of percent with 10 percent limited in Indo-Pacific Species Determinations these threats on A. brevis. We scope), fishing regulations on reefs (90 introduction above, based on results interpreted threat susceptibility and percent with 19 percent limited in from Richards et al. (2008) and Veron exposure information from the SRR and scope), and managing areas for (2014), the absolute abundance of this SIR in the proposed rule for A. brevis’ protection and conservation (97 percent species is likely at least tens of millions vulnerabilities as follows: High with 10 percent limited in scope). The of colonies. vulnerability to ocean warming, most common regulatory mechanisms in Carpenter et al. (2008) extrapolated moderate vulnerability to disease, ocean place for A. brevis are reef fishing species abundance trend estimates from acidification, and trophic effects of regulations and area management for total live coral cover trends and habitat fishing, and low vulnerability to protection and conservation. Coral types. For A. brevis, the overall decline sedimentation, sea level rise, and collection and pollution control laws in abundance (‘‘Percent Population collection and trade, and unknown are somewhat common for the species, Reduction’’) was estimated at 36 vulnerability to nutrients. but 26 percent of coral collection laws percent, and the decline in abundance Public comments did not provide any are limited in scope and may not before the 1998 bleaching event (‘‘Back- new or supplemental information on A. provide substantial protection. General cast Percent Population Reduction’’) brevis’ threats susceptibilities. We coral protection laws are much less was estimated at 14 percent. However, gathered supplemental species-specific common regulatory mechanisms for the as summarized above in the Inter-basin and genus-level information on this management of A. brevis. Comparison sub-section, live coral cover species’ threat susceptibilities. trends are highly variable both spatially Acanthastrea brevis was not rated as Vulnerability to Extinction and temporally, producing patterns on moderately or highly susceptible to As explained above in the Risk small scales that can be easily taken out bleaching or coral disease by Carpenter Analyses section, a species’ of context. Thus, quantitative inferences et al. (2008), but they did not use vulnerability to extinction results from to species-specific trends should be species-specific data for their ratings. the combination of its spatial and interpreted with caution. At the same Based on genus-level and species demographic characteristics, threat time, an extensive body of literature information described above, A. brevis susceptibilities, and consideration of the documents broad declines in live coral likely has some susceptibility to ocean baseline environment and future cover and shifts to reef communities warming, disease, ocean acidification, projections of threats. The SRR stated dominated by hardier coral species or trophic effects of fishing, nutrients, that high susceptibility to bleaching is algae over the past 50 to 100 years sedimentation, sea-level rise, and the primary factor that increases (Birkeland, 2004; Fenner, 2012; Pandolfi predation, and low susceptibility to potential extinction risk for A. brevis. It et al., 2003; Sale and Szmant, 2012). collection and trade. listed factors that reduce potential These changes have likely occurred, and extinction risk for A. brevis including Regulatory Mechanisms are occurring, from a combination of the fact that it occupies a variety of global and local threats. Given that A. In the proposed rule, we did not habitat types and is broadly distributed, brevis occurs in many areas affected by provide any species-specific both latitudinally and longitudinally, in these broad changes, and likely has information on the regulatory the Indo-Pacific. some susceptibility to both local and mechanisms or conservation efforts for Subsequent to the proposed rule, we global threats, we conclude it is likely A. brevis. Criticisms of our approach received and gathered supplemental to have declined in abundance over the received during public comment led us species- or genus-specific information, past 50 to 100 years, but a precise to attempt the following analysis of described above, that expands our quantification is not possible based on regulatory mechanisms on a species knowledge regarding the species the limited species-specific information. basis. Records confirm that abundance, distribution, and threat Acanthastrea brevis occurs in 29 Indo- susceptibilities. We developed our Other Biological Information Pacific ecoregions that encompass 31 assessment of the species’ vulnerability The SRR and SIR provided the countries’ EEZs. The 31 countries are to extinction using all the available following information on A. brevis’ life Australia, Djibouti, Egypt, Eritrea, information. As explained in the Risk history. Although specific larval Federated States of Micronesia, Fiji, Analyses section, our assessment in this descriptions have not been published France (French Pacific Island final rule emphasizes the ability of the for this species, the larvae of three other Territories), Indonesia, Israel, Jordan, species’ spatial and demographic traits Acanthastrea species studied do not Kiribati, Madagascar, Malaysia, to moderate or exacerbate its contain zooxanthellae that can Mauritius, New Zealand (Tokelau), vulnerability to extinction, as opposed supplement maternal provisioning with Niue, Palau, Papua New Guinea, to the approach we used in the energy sources provided by their Philippines, Samoa, Saudi Arabia, proposed rule, which emphasized the photosynthesis. The public comments Seychelles, Solomon Islands, Sri Lanka, species’ susceptibility to threats. did not provide new or supplemental Sudan, Tonga, Tuvalu, United Kingdom The following characteristics of A. information, and we did not find new or (British Indian Ocean Territory), United brevis, in conjunction with the supplemental information on the above- States (American Samoa), Vietnam, and information described in the Corals and described biological information. Yemen. The regulatory mechanisms Coral Reefs section, Coral Habitat sub- relevant to A. brevis, described first as section, and Threats Evaluation section Susceptibility to Threats the percentage of the above countries above, affect its vulnerability to To describe A. brevis’ threat that utilize them to any degree, and extinction currently and over the susceptibilities, the SRR and SIR second as the percentage of those foreseeable future. Its geographic provided genus-level information for the countries whose regulatory mechanisms distribution is from the Red Sea and effects on Acanthastrea of ocean may be limited in scope, are as follows: western Indian Ocean to American warming, acidification, disease, General coral protection (29 percent Samoa in the central Pacific. Its sedimentation, nutrients, predation, and with 6 percent limited in scope), coral geographic distribution moderates collection and trade. The SRR and SIR collection (65 percent with 26 percent vulnerability to extinction because some

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areas within its range are projected to none of the five ESA listing factors, brevis is not warranted for listing at this have less than average warming and alone or in combination, are causing time under any of the listing factors. acidification over the foreseeable future, this species to likely become Acanthastrea hemprichii including the western Indian Ocean, the endangered throughout its range within central Pacific, and other areas, so the foreseeable future, and thus it is not Introduction portions of the population in these areas warranted for listing at this time, The SRR and SIR provided the will be less exposed to severe because: following information on A. conditions. Its depth range is from one (1) Acanthastrea brevis’ distribution hemprichii’s morphology and to 20 meters. This moderates from the western Indian Ocean to the taxonomy. Morphology was described vulnerability to extinction over the central Pacific across is spread over a as encrusting to massive and frequently foreseeable future because deeper areas vast area, approximately half of the over one meter across, and the of its range will usually have lower Indo-Pacific region. While some areas taxonomy was described as having no irradiance than surface waters, and within its range are projected to be taxonomic issues but being similar in acidification is generally predicted to affected by warming and acidification, appearance to Acanthastrea echinata, accelerate most in waters that are deeper other areas are projected to have less Acanthastrea bowerbanki, and and cooler than those in which the than average warming and acidification, species occurs. Its habitat includes all including the western Indian Ocean, the Acanthastrea hillae. coral reef habitats. This moderates central Pacific, and other areas. This Public comments and information we vulnerability to extinction over the distribution and the heterogeneous gathered did not provide any new or foreseeable future because the species is habitats it occupies reduce exposure to supplemental information on not limited to one habitat type but any given threat event or adverse morphology, and confirmed that there occurs in numerous types of reef condition that does not occur uniformly are no known taxonomic problems for environments that will, on local and throughout the species range. As A. hemprichii and a low to moderate regional scales, experience highly explained above in the Threats level of species identification variable thermal regimes and ocean Evaluation section, we have not uncertainty. Veron (2014) states that A. chemistry at any given point in time. Its identified any threat that is expected to hemprichii is usually distinctive and abundance of at least tens of millions of occur uniformly throughout the species Veron (2000; 2014) considers the colonies, combined with spatial range within the foreseeable future; and species valid, thus we conclude it can variability in ocean warming and (2) Acanthastrea brevis’s absolute be identified by experts and that the acidification across the species range, abundance is at least tens of millions of distribution and abundance information moderates vulnerability to extinction colonies, providing buffering capacity in described below for this species is because the increasingly severe the form of absolute numbers of sufficiently reliable (Fenner, 2014b). conditions expected in the foreseeable colonies and variation in susceptibility Spatial Information future will be non-uniform and between individual colonies. As therefore will likely be a large number discussed in the Corals and Coral Reefs The SRR and SIR provided the of colonies that are either not exposed section above, the more colonies a following information on A. or do not negatively respond to a threat species has, the lower the proportion of hemprichii’s distribution, habitat, and at any given point in time. colonies that are likely to be exposed to depth range. Acanthastrea hemprichii’s a particular threat at a particular time, distribution extends from the Red Sea Listing Determination and all individuals that are exposed will and east Africa to the central Indo- In the proposed rule using the not have the same response. Pacific and central Pacific, it occupies determination tool formula approach, A. Notwithstanding the projections most reef habitats, and its depth range brevis was proposed for listing as through 2100 that indicate increased is from two to 20 m depth. threatened because of: High severity over time of the three high Public comments did not provide any vulnerability to ocean warming (ESA importance threats, the combination of new or supplemental information on A. Factor E); moderate vulnerability to these biological and environmental hemprichii’s distribution. We gathered disease (C) and acidification (E); characteristics indicates that the species supplemental information, including uncommon generalized range wide possesses sufficient buffering capacity Veron (2014), which reports that this abundance (E); wide overall distribution to avoid being in danger of extinction species is confirmed in 47 of his 133 (based on wide geographic distribution within the foreseeable future throughout Indo-Pacific ecoregions, and strongly and moderate depth distribution (E); its range. It is possible that this species’ predicted to be found in an additional and inadequacy of existing regulatory extinction risk may increase in the 23. mechanisms (D). future if global threats continue and Demographic Information In this final rule, we changed the worsen in severity and the species’ listing determination for A. brevis from exposure to the threats increases The SRR and SIR reported A. threatened to not warranted. We made throughout its range. Should the species hemprichii’s abundance as uncommon. this determination based on a more experience reduced abundance or range Public comments did not provide any species-specific and holistic assessment constriction of a certain magnitude, the new or supplemental information on A. of whether this species meets the ability of these characteristics to hemprichii’s abundance. We gathered definition of either a threatened or moderate exposure to threats will supplemental information, including endangered coral largely in response to diminish. However, the species is not Veron (2014), which reports that A. public comments, including more likely to become of such low abundance hemprichii occupied 11.4 percent of appropriate consideration of the or so spatially fragmented as to be in 2,984 dive sites sampled in 30 buffering capacity of this species’ spatial danger of extinction due to depensatory ecoregions of the Indo-Pacific, and had and demographic traits to lessen its processes, the potential effects of a mean abundance rating of 1.47 on a 1 vulnerability to threats. Thus, based on environmental stochasticity, or the to 5 rating scale at those sites in which the best available information above on potential for mortality from catastrophic it was found. Based on this semi- A. brevis’ spatial structure, demography, events within the foreseeable future quantitative system, the species’ threat susceptibilities, and management, throughout its range. Therefore, A. abundance was characterized as

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‘‘common,’’ and overall abundance was effects on Acanthastrea of ocean Japan, Jordan, Kenya, Madagascar, described as ‘‘uncommon.’’ Veron did warming, disease, acidification, Malaysia, Marshall Islands, Myanmar, not infer trends in abundance from sedimentation, nutrients, predation, and Papua New Guinea, Philippines, Saudi these data. As described in the Indo- collection and trade. The SRR and SIR Arabia, Seychelles, Solomon Islands, Pacific Species Determinations also provided the following species- Somalia, Sudan, Taiwan, Tanzania, introduction above, based on results specific information on A. hemprichii’s Thailand, Vietnam, and Yemen. The from Richards et al. (2008) and Veron threats. Acanthastrea hemprichii was regulatory mechanisms relevant to A. (2014), the absolute abundance of this relatively unaffected during the 2002 hemprichii, first described as the species is likely at least tens of millions bleaching event on the Great Barrier percentage of the above countries that of colonies. Reef. The SRR and SIR did not provide utilize them to any degree, and second Carpenter et al. (2008) extrapolated any other species-specific information as the percentage of those countries species abundance trend estimates from on the effects of these threats on A. whose regulatory mechanisms may be total live coral cover trends and habitat hemprichii. We interpreted threat limited in scope, are as follows: General types. For Acanthastrea hemprichii, the susceptibility and exposure information coral protection (20 percent with three overall decline in abundance (‘‘Percent from the SRR and SIR in the proposed percent limited in scope), coral Population Reduction’’) was estimated rule for A. hemprichii’s vulnerabilities collection (47 percent with 20 percent at 35 percent, and the decline in as follows: High vulnerability to ocean limited in scope), pollution control (43 abundance before the 1998 bleaching warming, moderate vulnerability to percent with 10 percent limited in event (‘‘Back-cast Percent Population disease, ocean acidification, trophic scope), fishing regulations on reefs (87 Reduction’’) was estimated at 14 effects of fishing, and predation, low percent with 17 percent limited in percent. However, as summarized above vulnerability to sedimentation, sea level scope), and managing areas for in the Inter-basin Comparison sub- rise, and collection and trade, and protection and conservation (90 percent section, live coral cover trends are unknown susceptibility for nutrients. with 10 percent limited in scope). The highly variable both spatially and Public comments did not provide any most common regulatory mechanisms in temporally, producing patterns on small new or supplemental information on A. place for A. hemprichii are reef fishing scales that can be easily taken out of hemprichii’s threats. We gathered regulations and area management for context. Thus, quantitative inferences to supplemental species-specific and protection and conservation. Coral species-specific trends should be genus-level information on this species’ collection and pollution control laws interpreted with caution. At the same threat susceptibilities. Acanthastrea are somewhat common for the species, time, an extensive body of literature hemprichii was not rated as moderately but 20 percent of coral collection laws documents broad declines in live coral or highly susceptible to bleaching or are limited in scope and may not cover and shifts to reef communities disease by Carpenter et al. (2008), but provide substantial protection. General dominated by hardier coral species or they did not have species-specific data. coral protection laws are much less algae over the past 50 to 100 years Done et al. (2003b) reported no common regulatory mechanisms for the (Birkeland, 2004; Fenner, 2012; Pandolfi bleaching in A. hemprichii on the GBR management of A. hemprichii. et al., 2003; Sale and Szmant, 2012). in 2002. Eight of 14 species of Mussidae Vulnerability to Extinction These changes have likely occurred, and bleached with six to 26% of colonies are occurring, from a combination of bleached, and for species in other As explained above in the Risk global and local threats. Given that A. families, as much as 80% of colonies Analyses section, a species’ hemprichii occurs in many areas bleached. Based on genus-level and vulnerability to extinction results from affected by these broad changes, and species-specific information described the combination of its spatial and likely has some susceptibility to local above, A. hemprichii likely has some demographic characteristics, threat and global threats, we conclude it has susceptibility to ocean warming, susceptibilities, and consideration of the likely declined in abundance over the disease, acidification, trophic effects of baseline environment and future past 50 to 100 years, but a precise fishing, nutrients, sedimentation, sea projections of threats. The SRR stated quantification is not possible based on level rise, predation, and collection and that high susceptibility to bleaching is the limited species specific information. trade. The available information does the primary factor that increases not support more precise ratings of the potential extinction risk for A. Other Biological Information susceptibility of A. hemprichii to the hemprichii. It listed factors that reduce The SRR and SIR provided the threats. potential extinction risk for A. following information on A. hemprichii are includes the fact that it Regulatory Mechanisms hemprichii’s life history. Although occupies a variety of habitat types and specific larval descriptions have not In the proposed rule, we did not is broadly distributed, both latitudinally been published for this species, the provide any species-specific and longitudinally, in the Indo-Pacific. larvae of three other Acanthastrea information on the regulatory Subsequent to the proposed rule, we species studied do not contain mechanisms or conservation efforts for received and gathered supplemental zooxanthellae that can supplement A. hemprichii. Criticisms of our species- or genus-specific information, maternal provisioning with energy approach received during public described above, that expands our sources provided by their comment led us to attempt the following knowledge regarding the species photosynthesis. The public comments analysis of regulatory mechanisms on a abundance, distribution, and threat did not provide new or supplemental species basis. Records confirm that susceptibilities. We developed our information, and we did not find new or Acanthastrea hemprichii occurs in 47 assessment of the species’ vulnerability supplemental information on the above- Indo-Pacific ecoregions that encompass to extinction using all the available described biological information. 30 countries’ EEZs. The 30 countries are information. As explained in the Risk Australia, China, Djibouti, Egypt, Analyses section, our assessment in this Susceptibility to Threats Eritrea, Federated States of Micronesia, final rule emphasizes the ability of the To describe A. hemprichii’s threat Fiji, France (French Pacific Island species’ spatial and demographic traits susceptibilities, the SRR and SIR Territories), India (Andaman and to moderate or exacerbate its provided genus-level information for the Nicobar Islands), Indonesia, Israel, vulnerability to extinction, as opposed

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to the approach we used in the and inadequacy of existing regulatory to avoid being in danger of extinction proposed rule, which emphasized the mechanisms (D). within the foreseeable future throughout species’ susceptibility to threats. In this final rule, we changed the its range. It is possible that this species’ The following characteristics of A. listing determination for A. hemprichii extinction risk may increase in the hemprichii, in conjunction with the from threatened to not warranted. We future if global threats continue and information described in the Corals and made this determination based on a increase in severity and the species Coral Reefs section, Coral Habitat sub- more species-specific and holistic exposure to threats increases throughout section, and Threats Evaluation section assessment of whether this species its range. Should the species experience above, affect its vulnerability to meets the definition of either a reduced abundance or range extinction currently and over the threatened or endangered coral largely constriction of a certain magnitude, the foreseeable future. Its geographic in response to public comments, ability of these characteristics to distribution includes most of the coral including more appropriate moderate exposure to threats will reef ecoregions in the Red sea and consideration of the buffering capacity diminish. However, the species is not western Indian Ocean and many in the of this species’ spatial and demographic likely to become of such low abundance central Indo-Pacific and western and traits to lessen its vulnerability to or so spatially fragmented as to be in central Pacific Ocean. Its geographic threats. Thus, based on the best danger of extinction due to depensatory distribution moderates vulnerability to available information above on A. processes, the potential effects of extinction because some areas within its hemprichii’s spatial structure, environmental stochasticity, or the range are projected to have less than demography, threat susceptibilities, and potential for mortality from catastrophic average warming and acidification over management, none of the five ESA events within the foreseeable future the foreseeable future, including the listing factors, alone or in combination, throughout its range. Therefore, A. western Indian Ocean, the central are causing this species to be likely to hemprichii is not warranted for listing at Pacific, and other areas, so portions of become endangered throughout its range this time under any of the listing factors. within the foreseeable future, and thus the population in these areas will be is not warranted for listing at this time, Acanthastrea ishigakiensis less exposed to severe conditions. Its because: Introduction depth range is from two to 20 meters. (1) Acanthastrea hemprichii’s This moderates vulnerability to distribution includes the Red Sea and The SRR and SIR provided the extinction over the foreseeable future east coast of Africa, plus many of the following information on A. because deeper areas of its range will coral reef ecoregions in the central Indo- ishigakiensis’ morphology and usually have lower irradiance than Pacific and central Pacific Ocean taxonomy. Morphology was described surface waters, and acidification is includes and is spread over a vast area. as massive and usually hemispherical generally predicted to accelerate most in While some areas within its range are and often more than 0.5 meters across, waters that are deeper and cooler than projected to be affected by warming and and taxonomy was described as having those in which the species occurs. Its acidification, other areas are projected no taxonomic issues but being similar in habitat includes most reef habitats. This to have less than average warming and appearance to Acanthastrea hillae and moderates vulnerability to extinction acidification, including the western Symphyllia erythraea. over the foreseeable future because the Indian Ocean, the central Pacific, and Public comments and information we species is not limited to one habitat type other areas. This distribution and the gathered did not provide any new or but occurs in numerous types of reef heterogeneous habitats it occupies supplemental information on environments that will, on local and reduce exposure to any given threat morphology, and confirmed that there regional scales, experience highly event or adverse condition that does not are no known taxonomic problems for variable thermal regimes and ocean occur uniformly throughout the species A. ishigakiensis, but that there is a chemistry at any given point in time. Its range. As explained above in the moderate level of species identification abundance of at least tens of millions of Threats Evaluation section, we have not uncertainty for this species. Veron colonies, combined with spatial identified any threat that is expected to (2014) states that A. ishigakiensis is variability in ocean warming and occur uniformly throughout the species readily confused with A. hillae, but acidification across the species range, range within the foreseeable future; and Veron (2000; 2014) also considers the moderates vulnerability to extinction (2) Acanthastrea hemprichii’s species valid, thus we conclude it can because the increasingly severe absolute abundance is at least tens of be identified by experts and that the conditions expected in the foreseeable millions of colonies, providing buffering distribution and abundance information future will be non-uniform and capacity in the form of absolute described below for this species is therefore will likely be a large number numbers of colonies and variation in sufficiently reliable (Fenner, 2014b). of colonies that are either not exposed susceptibility between individual or do not negatively respond to a threat colonies. As discussed in the Corals and Spatial Information at any given point in time. Coral Reefs section above, the more The SRR and SIR provided the Listing Determination colonies a species has, the lower the following information on Acanthastrea proportion of colonies that are likely to ishigakiensis’ distribution, habitat, and In the proposed rule using the be exposed to a particular threat at a depth range. Acanthastrea ishigakiensis’ determination tool formula approach, A. particular time, and all individuals that distribution extends from the Red Sea hemprichii was proposed for listing as are exposed will not have the same and east coast of Africa to the central threatened because of: High response. Pacific, but excludes Australia. Its vulnerability to ocean warming (ESA Notwithstanding the projections habitat includes upper reef slopes, Factor E); moderate vulnerability to through 2100 that indicate increased lagoons and other areas protected from disease (C) and acidification (E); severity over time of the three high wave action, in depths from one to 15 uncommon generalized range wide importance threats, the combination of m depth. abundance (E); wide overall distribution these biological and environmental Public comments provided the (based on wide geographic distribution characteristics indicates that the species following information on A. and moderate depth distribution (E); possesses sufficient buffering capacity ishigakiensis’ distribution. One public

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comment stated that R.H. Randall likely declined in abundance over the information on the regulatory recalls seeing this species in Guam at 60 past 50 to 100 years, but a precise mechanisms or conservation efforts for m deep. We gathered supplemental quantification is not possible based on A. ishigakiensis. Criticisms of our information, including Veron (2014), the lack of species specific information. approach received during public which reports that this species is comment led us to attempt the following Other Biological Information confirmed in 25 of his 133 Indo-Pacific analysis of regulatory mechanisms on a ecoregions, and strongly predicted to be The SRR and SIR provided the species basis. Records confirm A. found in an additional 19. following information on A. ishigakiensis occurs in 24 Indo-Pacific ishigakiensis’ life history. Although ecoregions that encompass 25 countries’ Demographic Information specific larval descriptions have not EEZs. The 25 countries are Egypt, The SRR and SIR reported A. been published for this species, the Federated States of Micronesia, Fiji, ishigakiensis’ abundance as uncommon larvae of three other Acanthastrea France (French Pacific Island but conspicuous. species studied do not contain Territories), Indonesia, Israel, Japan, Public comments did not provide any zooxanthellae that can supplement Jordan, Kenya, Madagascar, Malaysia, new or supplemental information on A. maternal provisioning with energy Mauritius, Mozambique, Papua New ishigakiensis’ abundance. We gathered sources provided by their Guinea, Philippines, Saudi Arabia, supplemental information, including photosynthesis. The public comments Seychelles, Solomon Islands, Sudan, Veron (2014), which reports that A. did not provide new or supplemental Tanzania, United States (CNMI, Guam), ishigakiensis occupied 2.9 percent of information, and we did not find new or Vanuatu, Vietnam, and Yemen. 2,984 dive sites sampled in 30 supplemental information on the above- Regulatory mechanisms relevant to A. ecoregions of the Indo-Pacific, and had described biological information. ishigakiensis, described first as the a mean abundance rating of 1.3 on a 1 Susceptibility to Threats percentage of the above countries that to 5 rating scale at those sites in which utilize them to any degree, and second it was found. Based on this semi- To describe A. ishigakiensis’ threat as the percentage of those countries quantitative system, the species’ susceptibilities, the SRR and SIR whose regulatory mechanisms may be abundance was characterized as provided genus-level information for the limited in scope, are as follows: General ‘‘uncommon,’’ and overall abundance effects on Acanthastrea of ocean coral protection (21 percent with eight was described as ‘‘uncommon but warming, disease, acidification, percent limited in scope), coral conspicuous.’’ Veron did not infer sedimentation, nutrients, predation, and collection (63 percent with 25 percent trends in abundance from these data. As collection and trade. The SRR and SIR limited in scope), pollution control (50 described in the Indo-Pacific Species did not provide any other species- percent with 13 percent limited in Determinations introduction above, specific information on the effects of scope), fishing regulations on reefs (88 based on results from Richards et al. these threats on A. ishigakiensis. We percent with 21 percent limited in (2008) and Veron (2014), the absolute interpreted threat susceptibility and scope), and managing areas for abundance of this species is likely at exposure information from the SRR and protection and conservation (100 least tens of millions of colonies. SIR in the proposed rule for A. percent with eight percent limited in Carpenter et al. (2008) extrapolated ishigakiensis’ vulnerabilities as follows: scope). The most common regulatory species abundance trend estimates from High vulnerability to ocean warming, mechanisms in place for A. total live coral cover trends and habitat moderate vulnerability to disease, ocean ishigakiensis are reef fishing regulations types. For A. ishigakiensis, the overall acidification, trophic effects of fishing, and area management for protection and decline in abundance (‘‘Percent and predation, low vulnerability to conservation. Coral collection and Population Reduction’’) was estimated sedimentation, sea level rise, and pollution control laws are somewhat at 34 percent, and the decline in collection and trade, and unknown common the species, but 25 percent of abundance before the 1998 bleaching susceptibility to nutrients. coral collection laws are limited in event (‘‘Back-cast Percent Population Public comments did not provide any scope and may not provide substantial Reduction’’) was estimated at 14 new or supplemental information on A. protection. General coral protection percent. However, as summarized above ishigakinesis’ threats susceptibilities. laws are much less common regulatory in the Inter-basin Comparison sub- We gathered supplemental species- mechanisms for the management of A. section, live coral cover trends are specific and genus-level information on ishigakiensis. highly variable both spatially and this species’ threat susceptibilities. temporally, producing patterns on small Acanthastrea ishigakiensis was not Vulnerability to Extinction scales that can be easily taken out of rated as moderately or highly As explained above in the Risk context. Thus, quantitative inferences to susceptible to bleaching or disease by Analyses section, a species’ species-specific trends should be Carpenter et al. (2008), but they did not vulnerability to extinction results from interpreted with caution. At the same have species-specific data. No species- the combination of its spatial and time, an extensive body of literature specific information is available for the demographic characteristics, threat documents broad declines in live coral susceptibility of A. ishigakiensis to any susceptibilities, and consideration of the cover and shifts to reef communities threat. Based on genus-level information baseline environment and future dominated by hardier coral species or described above, A. ishigakiensis likely projections of threats. The SRR stated algae over the past 50 to 100 years has some susceptibility to ocean that high susceptibility to bleaching is (Birkeland, 2004; Fenner, 2012; Pandolfi warming, disease, ocean acidification, the primary factor that increases et al., 2003; Sale and Szmant, 2012). trophic effects of fishing, nutrients, potential extinction risk for A. These changes have likely occurred, and sedimentation, sea level rise, predation, ishigakiensis. It listed factors that are occurring, from a combination of and low susceptibility to collection and reduce potential extinction risk global and local threats. Given that A. trade. including the fact that A. ishigakiensis ishigakiensis occurs in many areas is broadly distributed, both latitudinally affected by these broad changes, and Regulatory Mechanisms and longitudinally, in the Indo-Pacific. likely has some susceptibility to local In the proposed rule, we did not Subsequent to the proposed rule, we and global threats, we conclude it has provide any species-specific received and gathered supplemental

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species- or genus-specific information, absolute abundance of at least tens of identified any threat that is expected to described above, that expands our millions of colonies, combined with occur uniformly throughout the species knowledge regarding the species spatial variability in ocean warming and range within the foreseeable future; and abundance, distribution, and threat acidification across the species range, (2) Acanthastrea ishigakiensis’ susceptibilities. We developed our moderates vulnerability to extinction absolute abundance is at least tens of assessment of the species’ vulnerability because the increasingly severe millions of colonies, providing buffering to extinction using all the available conditions expected in the foreseeable capacity in the form of absolute information. As explained in the Risk future will be non-uniform and numbers of colonies and variation in Analyses section, our assessment in this therefore will likely be a large number susceptibility between individual final rule emphasizes the ability of the of colonies that are either not exposed colonies. As discussed in the Corals and species’ spatial and demographic traits or do not negatively respond to a threat Coral Reefs section above, the more to moderate or exacerbate its at any given point in time. colonies a species has, the lower the vulnerability to extinction, as opposed Listing Determination proportion of colonies that are likely to to the approach we used in the be exposed to a particular threat at a proposed rule, which emphasized the In the proposed rule using the particular time, and all individuals that species’ susceptibility to threats. determination tool formula approach, A. are exposed will not have the same ishigakiensis was proposed for listing as The following characteristics of A. response. threatened because of: High Notwithstanding the projections ishigakiensis, in conjunction with the vulnerability to ocean warming (ESA information described in the Corals and through 2100 that indicate increased Factor E); moderate vulnerability to severity over time of the three high Coral Reefs section, Coral Habitat sub- disease (C) and acidification (E); section, and Threats Evaluation section importance threats, the combination of uncommon generalized range wide these biological and environmental above, affect its vulnerability to abundance (E); moderate overall extinction currently and over the characteristics indicates that the species distribution (based on wide geographic possesses sufficient buffering capacity foreseeable future. Its geographic distribution and shallow depth distribution includes most of the coral to avoid being in danger of extinction distribution (E); and inadequacy of within the foreseeable future throughout reef ecoregions in the Red Sea and existing regulatory mechanisms (D). western Indian Ocean and many in the its range. It is possible that this species’ In this final rule, we changed the extinction risk may increase in the western and central Pacific Ocean. Its listing determination for A. geographic distribution moderates future if global threats continue and ishigakiensis from threatened to not increase in severity and the species vulnerability to extinction because some warranted. We made this determination areas within its range are projected to exposure to threats increases throughout based on a more species-specific and its range. Should the species experience have less than average warming and holistic assessment of whether this reduced abundance or range acidification over the foreseeable future, species meets the definition of either a constriction of a certain magnitude, the including the western Indian Ocean, the threatened or endangered coral largely ability of these characteristics to central Pacific, and other areas, so in response to public comments, moderate exposure to threats will portions of the population in these areas including more appropriate diminish. However, the species is not will be less exposed to severe consideration of the buffering capacity likely to become of such low abundance conditions. Its depth range is from one of this species’ spatial and demographic or so spatially fragmented as to be in to 15 meters, and there is one anecdotal traits to lessen its vulnerability to danger of extinction due to depensatory record from Guam of this species threats. Thus, based on the best processes, the potential effects of observed at 60 meters depth. On one available information above on A. hand, its depth range may moderate ishigakiensis’ spatial structure, environmental stochasticity, or the vulnerability to extinction over the demography, threat susceptibilities, and potential for mortality from catastrophic foreseeable future because deeper areas management, none of the five ESA events within the foreseeable future of its range will usually have lower listing factors, alone or in combination, throughout its range. Therefore, A. irradiance than surface waters, and are causing this species to be likely to ishigakiensis is not warranted for listing acidification is generally predicted to become endangered throughout its range at this time under any of the listing accelerate most in waters that are deeper within the foreseeable future, and thus factors. and cooler than those in which the is not warranted for listing at this time, Acanthastrea regularis species occurs. On the other hand, its because: depth range may exacerbate (1) Acanthastrea ishigakiensis’ Introduction vulnerability to extinction over the distribution includes the Red Sea and The SRR and SIR provided the foreseeable future if the species occurs most of the western Indian Ocean along following information on A. regularis’ predominantly in the shallower portion with many of the coral reef ecoregions morphology and taxonomy. Morphology of its depth range, since those areas will in the western and central Pacific. was described as massive and with have higher irradiance and thus be more While some areas within its range are corallites united by fused compound severely affected by warming-induced projected to be affected by warming and walls, and taxonomy was described as bleaching. Its habitat includes upper acidification, other areas are projected having no taxonomic issues but being reef slopes, lagoons, and other areas to have less than average warming and similar in appearance to Montastraea protected from wave action. This acidification, including the western and Favia underwater. moderates vulnerability to extinction Indian Ocean, the central Pacific, and Public comments and information we over the foreseeable future because the other areas. This distribution and the gathered did not provide any new or species is not limited to one habitat type heterogeneous habitats it occupies supplemental information on but occurs in numerous types of reef reduce exposure to any given threat morphology, and confirmed that there environments that will, on local and event or adverse condition that does not are no known taxonomic problems for regional scales, experience highly occur uniformly throughout the species A. regularis, and a moderate level of variable thermal regimes and ocean range. As explained above in the species identification uncertainty for chemistry at any given point in time. Its Threats Evaluation section, we have not this species. Veron (2014) states that A.

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regularis is readily confused with Favia in the Inter-basin Comparison sub- gathered supplemental species-specific species but Veron (2000; 2014) section, live coral cover trends are and genus-level information on this considers the species valid, thus we highly variable both spatially and species’ threat susceptibilities. conclude it can be identified by experts temporally, producing patterns on small Acanthastrea regularis was not rated as and that the distribution and abundance scales that can be easily taken out of moderately or highly susceptible to information described below for this context. Thus, quantitative inferences to bleaching or disease by Carpenter et al. species is sufficiently reliable (Fenner, species-specific trends should be (2008), but they did not have species- 2014b). interpreted with caution. At the same specific data. Based on genus-level time, an extensive body of literature information presented above, A. Spatial Information documents broad declines in live coral regularis likely has some susceptibility The SRR and SIR provided the cover and shifts to reef communities to ocean warming, disease, ocean following information on A. regularis’ dominated by hardier coral species or acidification, trophic effects of fishing, distribution, habitat, and depth range. algae over the past 50 to 100 years nutrients, sedimentation, sea-level rise, Acanthastrea regularis’ distribution is (Birkeland, 2004; Fenner, 2012; Pandolfi and predation, and low susceptibility to restricted, and includes the Coral et al., 2003; Sale and Szmant, 2012). collection and trade. Triangle and some islands in the west These changes have likely occurred, and Regulatory Mechanisms and central Pacific. Its habitat includes are occurring, from a combination of most reef habitats, including upper reef global and local threats. Given that A. In the proposed rule, we did not slopes, mid-slopes, lower reef crests, regularis occurs in many areas affected provide any species-specific reef flats, and lagoons in depths from by these broad changes, and likely has information on the regulatory two to 20 m. some susceptibility to local and global mechanisms or conservation efforts for Public comments provided the threats, we conclude it has likely A. regularis. Criticisms of our approach following information on distribution of declined in abundance over the past 50 received during public comment led us A. regularis. One public comment stated to 100 years, but a precise quantification to attempt the following analysis of that A. regularis is likely in the is not possible based on the limited regulatory mechanisms on a species Marianas. We gathered supplemental species-specific information. basis. Records confirm that A. regularis information, including Veron (2014), occurs in 17 Indo-Pacific ecoregions that which reports that this species is Other Biological Information encompass eight countries’ EEZs. The confirmed in 17 of his 133 Indo-Pacific The SRR and SIR provided the eight countries are Australia, Federated ecoregions, and strongly predicted to be following information on A. regularis’ States of Micronesia, Fiji, Indonesia, found in an additional 16. life history. Although specific larval Malaysia, Papua New Guinea, descriptions have not been published Philippines, and Vietnam. The Demographic Information for this species, the larvae of three other regulatory mechanisms relevant to A. The SRR and SIR reported A. Acanthastrea species studied do not regularis, described first as the regularis’ abundance as uncommon. contain zooxanthellae that can percentage of the above countries that Public comments did not provide any supplement maternal provisioning with utilize them to any degree, and second new or supplemental information on A. energy sources provided by their as the percentage of those countries regularis’ abundance. We gathered photosynthesis. whose regulatory mechanisms may be supplemental information, including The public comments did not provide limited in scope, are as follows: General Veron (2014), which reports that A. new or supplemental information, and coral protection (25 percent with none regularis occupied 5.1 percent of 2,984 we did not find new or supplemental limited in scope), coral collection (63 dive sites sampled in 30 ecoregions of information on the above-described percent with 25 percent limited in the Indo-Pacific, and had a mean biological information. scope), pollution control (63 percent abundance rating of 1.21 on a 1 to 5 with 25 percent limited in scope), rating scale at those sites in which it Susceptibility to Threats fishing regulations on reefs (100 percent was found. Based on this semi- To describe A. regularis’ threat with 13 percent limited in scope), and quantitative system, the species’ susceptibilities, the SRR and SIR managing areas for protection and abundance was characterized as provided genus-level information for the conservation (100 percent with none ‘‘uncommon,’’ and overall abundance effects on Acanthastrea of ocean limited in scope). The most common was also described as ‘‘uncommon.’’ warming, acidification, disease, regulatory mechanisms in place for A. Veron did not infer trends in abundance sedimentation, nutrients, predation, and regularis are reef fishing regulations and from these data. As described in the collection and trade. The SRR and SIR area management for protection and Indo-Pacific Species Determinations did not provide any other species- conservation. Coral collection and introduction above, based on results specific information on the effects of pollution control laws are also from Richards et al. (2008) and Veron these threats on A. regularis. We somewhat common for the species, but (2014), the absolute abundance of this interpreted threat susceptibility and 25 percent of those laws are limited in species is likely at least millions of exposure information from the SRR and scope and may not provide substantial colonies. SIR in the proposed rule for A. regularis’ protection. General coral protection Carpenter et al. (2008) extrapolated vulnerabilities as follows: High laws are much less common regulatory species abundance trend estimates from vulnerability to ocean warming, mechanisms for the management of A. total live coral cover trends and habitat moderate vulnerability to disease, ocean regularis. types. For A. regularis, the overall acidification, and trophic effects of decline in abundance (‘‘Percent fishing, and predation, low vulnerability Vulnerability to Extinction Population Reduction’’) was estimated to sedimentation, sea level rise, and As explained above in the Risk at 36 percent, and the decline in collection and trade, and unknown Analyses section, a species’ abundance before the 1998 bleaching vulnerability to nutrients. vulnerability to extinction results from event (‘‘Back-cast Percent Population Public comments did not provide any the combination of its spatial and Reduction’’) was estimated at 14 new or supplemental information on A. demographic characteristics, threat percent. However, as summarized above regularis’ threat susceptibilities. We susceptibilities, and consideration of the

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baseline environment and future extinction over the foreseeable future the nine most important threats. This projections of threats. The SRR stated because the species is not limited to one distribution and the heterogeneous that high susceptibility to bleaching is habitat type but occurs in numerous habitats it occupies reduce exposure to the primary factor that increases types of reef environments that will, on any given threat event or adverse potential extinction risk for A. regularis. local and regional scales, experience condition that does not occur uniformly This species occupies a variety of highly variable thermal regimes and throughout the species range. As habitat types and extends down to 20 ocean chemistry at any given point in explained above in the Threats meters depth which are factors listed in time. Its absolute abundance of at least Evaluation section, we have not the SRR that reduce potential extinction millions of colonies, combined with identified any threat that is expected to risk. spatial variability in ocean warming and occur uniformly throughout the species Subsequent to the proposed rule, we acidification across the species range, range within the foreseeable future; and received and gathered supplemental moderates vulnerability to extinction species- or genus-specific information, because the increasingly severe (2) Acanthastrea regularis’ absolute described above, that expands our conditions expected in the foreseeable abundance is at least millions of knowledge regarding the species future will be non-uniform and colonies, providing buffering capacity in abundance, distribution, and threat therefore will likely be a large number the form of absolute numbers of susceptibilities. We developed our of colonies that are either not exposed colonies and variation in susceptibility assessment of the species’ vulnerability or do not negatively respond to a threat between individual colonies. As to extinction using all the available at any given point in time. discussed in the Corals and Coral Reefs information. As explained in the Risk section above, the more colonies a Listing Determination Analyses section, our assessment in this species has, the lower the proportion of final rule emphasizes the ability of the In the proposed rule using the colonies that are likely to be exposed to species’ spatial and demographic traits determination tool formula approach, A. a particular threat at a particular time, to moderate or exacerbate its regularis was proposed for listing as and all individuals that are exposed will vulnerability to extinction, as opposed threatened because of: High not have the same response. to the approach we used in the vulnerability to ocean warming (ESA proposed rule, which emphasized the Factor E); moderate vulnerability to Notwithstanding the projections species’ susceptibility to threats. disease (C) and acidification (E); through 2100 that indicate increased The following characteristics of A. uncommon generalized range wide severity over time of the three high regularis, in conjunction with the abundance (E); moderate overall importance threats, the combination of information described in the Corals and distribution (based on moderate these biological and environmental Coral Reefs section, Coral Habitat sub- geographic distribution and moderate characteristics indicates that the species section, and Threats Evaluation section depth distribution (E); and inadequacy possesses sufficient buffering capacity above, affect its vulnerability to of existing regulatory mechanisms (D). to avoid being in danger of extinction extinction currently and over the In this final rule, we changed the within the foreseeable future throughout foreseeable future. Acanthastrea listing determination for A. regularis its range. It is possible that this species’ regularis is not highly susceptible to any from threatened to not warranted. We extinction risk may increase in the of the nine most important threats, made this determination based on a future if global threats continue and although it has some susceptibility to more species-specific and holistic increase in severity and the species each. Its geographic distribution is assessment of whether this species exposure to threats increases throughout mostly constrained to parts of the Coral meets the definition of either a its range. Should the species experience Triangle and western equatorial Pacific threatened or endangered coral largely reduced abundance or range Ocean—areas which are projected to in response to public comments, constriction of a certain magnitude, the including more appropriate have the most rapid and severe impacts ability of these characteristics to consideration of the buffering capacity from climate change and localized moderate exposure to threats will human impacts for coral reefs over the of this species’ spatial and demographic diminish. However, the species is not 21st century. For a species that is highly traits to lessen its vulnerability to likely to become of such low abundance susceptible to climate change related threats. Thus, based on the best or so spatially fragmented as to be in threats, this range would exacerbate available information above on A. vulnerability to extinction but A. regularis’ spatial structure, demography, danger of extinction due to depensatory regularis is not highly susceptible threat susceptibilities, and management, processes, the potential effects of susceptibility. Vulnerability to none of the five ESA listing factors, environmental stochasticity, or the extinction may be exacerbated by the alone or in combination, are causing potential for mortality from catastrophic severe nature of local threats predicted this species to be likely to become events within the foreseeable future within its range, however, A. regularis endangered throughout its range within throughout its range. Therefore, A. is not highly susceptible to any local the foreseeable future, and thus is not regularis is not warranted for listing at sources of impact either. Its depth range warranted for listing at this time, this time under any of the listing factors. because: is from two to 20 meters. This Genus Barabattoia moderates vulnerability to extinction (1) While A. regularis’ distribution is over the foreseeable future because mostly constrained to parts of the Coral Genus Introduction deeper areas of its range will usually Triangle and western equatorial Pacific have lower irradiance than surface Ocean, its distribution is spread over a The family Favidae includes 24 waters, and acidification is generally large area across the Coral Triangle, the genera, more than any other family, predicted to accelerate most in waters Marianas archipelago, Palau, including Barabattoia. Barabattoia that are deeper and cooler than those in Micronesia, and Fiji. While some areas contains two species, B. laddi and B. which the species occurs. Its habitat within its range are projected to be amicorum. Colonies are massive or includes upper reef slopes, mid-slopes, affected by warming and acidification, encrusting. The SRR and SIR provided lower reef crests, reef flats, and lagoons. A. regularis is not highly susceptible to no genus-level introductory information This moderates vulnerability to ocean warming, acidification, or any of on Barabattoia.

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Genus Susceptibility to Threats SIR, because it is an ecosystem-level species identification uncertainty for The SRR and SIR provided the process. That is, removal of herbivorous this species, since it is so rare that following information on the threat fish from coral reef systems by fishing surveyors get little experience with it. susceptibilities of the genus Barabattoia. alters trophic interactions by reducing Veron (2014) states that B. laddi is Barabattoia amicorum has low-to- herbivory on algae, thereby providing a distinctive and Veron (2000; 2014) moderate bleaching susceptibility with competitive advantage for space to algae considers the species valid, thus we an unknown degree of resultant over coral. Thus, the SRR did not conclude it is sufficiently distinctive to be identified by experts, and that the mortality (Bruno et al., 2001). discuss this threat in terms of coral taxa, The public comments did not provide as its effects are difficult to distinguish distribution and abundance information any new or supplemental information between coral genera and species. described below for this species is sufficiently reliable (Fenner, 2014b). on the threat susceptibilities of the Therefore, an unstudied Barabattoia genus Barabattoia. We gathered species is likely to have some Spatial Information susceptibility to the trophic effects of supplemental information that provided The SRR and SIR provided the the following. With regard to thermal fishing. The SRR rated sedimentation, following information on B. laddi’s stress, B. amicorum experienced low to distribution, habitat, and depth range. moderate bleaching in Palau in 2000, nutrients, and sea-level rise as ‘‘low- medium’’ importance to corals overall. Barabattoia laddi’s range is somewhat but mortality was not reported (Bruno et restricted, centered on the Coral al., 2001). Forty-eight percent of all Although there is no genus-level or species-specific information on the Triangle and extending to the central colonies of all species were bleached, Pacific including perhaps French and bleaching of different genera and susceptibilities of Barabattoia species to sedimentation and nutrients, there is no Polynesia. The SRR and SIR described species ranged from none to very high, B. laddi’s habitat as recorded only from and mortality of different genera and information suggesting they are not susceptible to these threats. Thus we shallow lagoons, and the depth range as species ranged from none to near 100 0 to 10 m. The public comments percent (Bruno et al., 2001). There is no conclude that an unstudied Barabattoia species is likely to have some provided the following details. One information on the susceptibilities of public comment stated that B. laddi Barabattoia to any other threats. susceptibility to sedimentation and nutrients. Sea-level rise was not tentatively occurs in Apra Harbor, Genus Conclusion addressed at the genus or species level Guam. We gathered supplemental in the SRR or SIR. Increasing sea levels information, including Veron (2014), Based on the information from the which reports that this species is SRR, SIR, public comments, and may increase land-based sources of pollution due to inundation, resulting in confirmed in 22 of his 133 Indo-Pacific supplemental information, we can make ecoregions, and strongly predicted to be the following inferences about the changes to coral community structure, thus an unstudied Barabattoia species is found in an additional 15. Surveys in susceptibilities of an unstudied Indonesia record the species at multiple likely to have some susceptibility to sea- Barabattoia species to ocean warming, sites with depths greater than 10 m level rise. The SRR rated predation and disease, acidification, sedimentation, (Bigot and Amir, 2009; Donnelly et al., ornamental trade (referred to in the nutrients, trophic effects of fishing, sea- 2003; Turak and DeVantier, 2003) and proposed rule as Collection and Trade) level rise, predation, and collection and surveys in the Maldives record the as ‘‘low’’ importance to corals overall. trade. The SRR rated ocean warming species at multiple sites with depths up Because there is no information on the and disease as ‘‘high’’ importance, and to 20 m (Bigot and Amir, 2009; Donnelly effects of predation and ornamental ocean acidification as ‘‘medium-high’’ et al., 2003; Turak and DeVantier, 2003). trade on Barabattoia, we conclude that importance, to corals. These were rated These surveys were done in different Barabattoia has some susceptibility to as the three most important threats to habitats, including reef slopes and predation and ornamental trade. reef-building corals overall. The one lagoons. Thus, based on all the available In conclusion, an unstudied available study on the effects of ocean information, B. laddi’s habitat includes Barabattoia species is likely to have warming on Barabattoia found that B. at least upper reef slopes, mid-slope some susceptibility to ocean warming, amicorum in Palau experienced low to terraces, and lagoons in depths ranging disease, acidification, disease, moderate bleaching (Bruno et al., 2001). from zero to 20 m. Even though there is only one study sedimentation, nutrients, trophic effects available, since there are only two of fishing, sea-level rise, predation, and Demographic Information species within the genus Barabattoia, it collection and trade. The SRR and SIR reported B. laddi’s is reasonable to make inferences about Barabattoia laddi abundance as rare. The public the susceptibility of B. laddi to ocean comments did not provide any new or warming. Although there is no other Introduction supplemental information on B. laddi’s genus-level or species-specific The SRR and SIR provided the abundance, but we gathered information on the susceptibilities of following information on B. laddi’s supplemental information, including Barabattoia species to ocean warming, morphology and taxonomy: the Veron (2014), which reports that B. disease, and acidification, the SRR rated morphology was described as clusters of laddi occupied 5.2 percent of 2,984 dive them as ‘‘high’’ or ‘‘medium-high’’ tubular corallites, and the taxonomy sites sampled in 30 ecoregions of the importance to corals. Thus, we conclude was described as having no taxonomic Indo-Pacific, and had a mean abundance that an unstudied Barabattoia species is issues but being similar in appearance rating of 1.33 on a 1 to 5 rating scale at likely to have some susceptibility to to B. amicorum and Montastraea sp. those sites in which it was found. Based ocean warming, disease, and The public comments and on this semi-quantitative system, the acidification. information we gathered did not species’ abundance was characterized as The SRR rated the trophic effects of provide any new or supplemental ‘‘uncommon,’’ and overall abundance fishing as ‘‘medium’’ importance, the information on morphology, and was described as ‘‘rare.’’ Veron did not fourth most important threat to corals confirmed that there are no known infer trends in abundance from these overall. This threat was not addressed at taxonomic problems for B. laddi, and data. As described in the Indo-Pacific the genus or species level in the SRR or that there is a low to moderate level of Species Determinations introduction

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above, based on results from Richards et specific information on the effects of protection and conservation (100 al. (2008) and Veron (2014), the absolute these threats on B. laddi. We interpreted percent with 13 percent limited in abundance of this species is likely at the threat susceptibility and exposure scope). The most common regulatory least tens of millions of colonies. information from the SRR and SIR in the mechanisms in place for B. laddi are Carpenter et al. (2008) extrapolated proposed rule for B. laddi’s reef fishing regulations and area species abundance trend estimates from vulnerabilities as follows: Moderate management for protection and total live coral cover trends and habitat vulnerability to ocean warming, disease, conservation. Coral collection and types. For B. laddi, the overall decline acidification, trophic effects of fishing, pollution control laws are also in abundance (‘‘Percent Population and nutrients, low vulnerability to somewhat common for the species, but Reduction’’) was estimated at 35 sedimentation, sea level rise, and 33 percent of coral collection laws are percent, and the decline in abundance collection and trade, and unknown limited in scope and may not provide before the 1998 bleaching event (‘‘Back- vulnerability to predation. substantial protection. General coral cast Percent Population Reduction’’) Public comments did not provide any protection laws are much less common was estimated at 14 percent. However, new or supplemental information on B. regulatory mechanisms for the as summarized above in the Inter-basin laddi’s threats. We gathered the management of B. laddi. Comparison sub-section, live coral cover following species-specific supplemental trends are highly variable both spatially information on this species’ threat Vulnerability to Extinction and temporally, producing patterns on susceptibilities. Barabattoia laddi has As explained above in the Risk small scales that can be easily taken out not been rated as moderately or highly Analyses section, a species’ of context. Thus, quantitative inferences susceptible to bleaching or disease, but vulnerability to extinction results from to species-specific trends should be this rating is not based on species- the combination of its spatial and interpreted with caution. At the same specific data (2008). No other species- demographic characteristics, threat time, an extensive body of literature specific information is available for the susceptibilities, and consideration of the documents broad declines in live coral susceptibility of B. laddi to any other baseline environment and future cover and shifts to reef communities threat. Based on the available genus- projections of threats. The SRR stated dominated by hardier coral species or level information described above, B. that factors that increase the potential algae over the past 50 to 100 years laddi likely has some susceptibility to extinction risk are the species’ limited (Birkeland, 2004; Fenner, 2012; Pandolfi ocean warming, disease, acidification, western Pacific distribution, its et al., 2003; Sale and Szmant, 2012). trophic effects of fishing, sedimentation, occurrence in shallow lagoons and its These changes have likely occurred, and nutrients, predation, sea-level rise, and rare abundance. are occurring, from a combination of collection and trade. The available Subsequent to the proposed rule, we global and local threats. Given that B. information does not support more received and gathered supplemental laddi occurs in many areas affected by precise ratings of the susceptibility of B. species- or genus-specific information, these broad changes, and likely has laddi to the threats. described above, that expands our some susceptibility to local and global knowledge regarding the species Regulatory Mechanisms threats, we conclude that it is likely to abundance, distribution, and threat have declined in abundance over the In the proposed rule, we did not susceptibilities. We developed our past 50 to 100 years, but a precise provide any species-specific assessment of the species’ vulnerability quantification is not possible based on information on the regulatory to extinction using all the available the limited species specific information. mechanisms or conservation efforts for information. As explained in the Risk B. laddi. Criticisms of our approach Analyses section, our assessment in this Other Biological Information received during public comment led us final rule emphasizes the ability of the The SRR and SIR provided the to attempt the following analysis of species’ spatial and demographic traits following information on B. laddi’s life regulatory mechanisms on a species to moderate or exacerbate its history. The reproductive characteristics basis. Records confirm B. laddi occurs vulnerability to extinction, as opposed of B. laddi have not been determined. in 22 Indo-Pacific ecoregions that to the approach we used in the There is only one other species in the encompass 15 countries’ EEZs. The 15 proposed rule, which emphasized the genus, B. amoricum, which is a countries are Australia, Brunei, China, species’ susceptibility to threats. hermaphroditic broadcast spawner that France (French Pacific Island The following characteristics of B. participated in multispecies spawning Territories), Indonesia, Malaysia, laddi, in conjunction with the events at Magnetic Island and Orpheus Marshall Islands, Palau, Papua New information described in the Corals and Island on the Great Barrier Reef. The Guinea, Philippines, Solomon Islands, Coral Reefs section, Coral Habitat sub- larvae of B. amoricum do not contain Taiwan, United Kingdom (Pitcairn section, and Threats Evaluation section zooxanthellae that might supplement Islands), United States (PRIAs), and above, affect its vulnerability to maternal provisioning with energy from Vietnam. The regulatory mechanisms extinction currently and over the photosynthesis. The public comments relevant to B. laddi, described first as foreseeable future. Barabattoia laddi has and information we gathered provided the percentage of the above countries not been rated highly susceptible to no new or supplemental biological that utilize them to any degree and ocean warming or disease, the two most information. second, as the percentages of those important threats to corals in this final countries whose regulatory mechanisms rule, nor is it highly susceptible to the Susceptibility to Threats may be limited in scope, are as follows: other threats identified in this rule. Its To describe B. laddi’s threat General coral protection (33 percent geographic distribution includes coral susceptibilities, the SRR and SIR with none limited in scope), coral reef ecoregions in the western and provided genus-level information for the collection (67 percent with 33 percent central Pacific Ocean from Malaysia to effects on Barabattoia of ocean limited in scope), pollution control (47 the Pitcairn Islands. Its geographic warming, disease, acidification, percent with 20 percent limited in distribution in combination with its low sedimentation, nutrients, predation, and scope), fishing regulations on reefs (93 to moderate susceptibility to threats, collection and trade. The SRR and SIR percent with 27 percent limited in moderates vulnerability to extinction did not provide any other species- scope), and managing areas for because it is spread across a large area.

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While its range includes the Coral (1) Barabattoia laddi’s distribution throughout its range. Therefore, B. laddi Triangle, it also includes some areas includes many of the coral reef is not warranted for listing at this time projected to have less than average ecoregions in the western and central under any of the listing factors. warming and acidification over the Pacific, from Malaysia as far east as the Genus Caulastrea foreseeable future, including the central Pitcairn Islands, and is spread over a Pacific so portions of the population in very large area. While some areas within Genus Introduction these areas will be less exposed to its range are projected to be affected by The family Favidae includes 24 severe conditions, plus those that are warming and acidification, other areas genera, more than any other family, exposed may not show negative are projected to have less than average including Caulastrea. The genus responses because of low or moderate warming and acidification, including Caulastrea contains five species, susceptibility. Its depth range is from the central Pacific, and other areas. This including C. echinulata. Colonies are zero to 20 meters. This would distribution and the heterogeneous branching, and branches may be short or exacerbate vulnerability to extinction habitats it occupies reduce exposure to close together. The SRR and SIR over the foreseeable future for a species any given threat event or adverse provided no genus-level introductory with high susceptibility to the nine most condition that does not occur uniformly information on Caulastrea. important threats, but B. laddi is not throughout the species range. As highly susceptible. Its habitat includes explained above in the Threats Genus Susceptibility to Threats at least upper reef slopes, mid-slope Evaluation section, we have not The SRR and SIR provided the terraces, and lagoons. Its absolute identified any threat that is expected to following information on the threat abundance of at least tens of millions of occur uniformly throughout the species susceptibilities of the genus Caulastrea. colonies, combined with low to range within the foreseeable future; Caulastrea furcata was not observed to moderate susceptibility and spatial (2) Barabattoia laddi’s absolute bleach in 1998 in Palau. variability in ocean warming and abundance is at least tens of millions of The public comments did not provide acidification across the species range, colonies, providing buffering capacity in any new or supplemental information moderates vulnerability to extinction the form of absolute numbers of on the threat susceptibilities of the because the increasingly severe colonies and variation in susceptibility conditions expected in the foreseeable between individual colonies. As genus Caulastrea. We gathered future will be non-uniform and discussed in the Corals and Coral Reefs supplemental information which therefore will likely be a large number section above, the more colonies a provided the following details. In a of colonies that are either not exposed species has, the lower the proportion of study of warming-induced bleaching of or do not negatively respond to a threat colonies that are likely to be exposed to over 100 coral species on the GBR in at any given point in time. a particular threat at a particular time, 2002, approximately 10 percent of C. and all individuals that are exposed will furcata colonies were affected by Listing Determination not have the same response; and bleaching, making it one of the least In the proposed rule using the (3) The best available information affected species in the study (Done et determination tool formula approach, B. suggests that Barabattoia laddi is not al., 2003b). There is no information on laddi was proposed for listing as highly susceptible to any of the nine the susceptibilities or vulnerabilities of threatened because of: Moderate threats identified in this rule, so even if Caulastrea to any other threats. vulnerability to ocean warming (ESA a proportion of its population overlaps Genus Conclusion Factor E), disease (C) and acidification in time and space with a threat event, (E); uncommon generalized range wide many colonies may not exhibit a Based on the information from the abundance (E); narrow overall negative response. SRR, SIR, public comments, and distribution (based on moderate Notwithstanding the projections supplemental information, we can make geographic distribution and shallow through 2100 that indicate increased the following inferences about the depth distribution (E); and inadequacy severity over time of the three high susceptibilities of an unstudied of existing regulatory mechanisms (D). importance threats, the combination of Caulastrea species to ocean warming, In this final rule, we changed the these biological and environmental disease, acidification, sedimentation, listing determination for B. laddi from characteristics indicates that the species nutrients, trophic effects of fishing, sea- threatened to not warranted. We made possesses sufficient buffering capacity level rise, predation, and collection and this determination based on a more to avoid being in danger of extinction trade. The SRR rated ocean warming species-specific and holistic assessment within the foreseeable future throughout and disease as ‘‘high’’ importance, and of whether this species meets the its range. It is possible that this species’ ocean acidification as ‘‘medium-high’’ definition of either a threatened or extinction risk may increase in the importance, to corals. These were rated endangered coral largely in response to future if global threats continue and as the three most important threats to public comments, including more increase in severity and the species reef-building corals overall. Caulastrea appropriate consideration of the exposure to threats increases throughout has shown low levels or no thermal- buffering capacity of this species’ spatial its range. Should the species experience induced bleaching in two studies, one and demographic traits to lessen its reduced abundance or range reported in the SRR, and one reported vulnerability to threats. Thus, based on constriction of a certain magnitude, the above (Done et al., 2003b). Thus, we the best available information above on ability of these characteristics to conclude that an unstudied Caulastrea B. laddi’s spatial structure, demography, moderate exposure to threats will is likely to have low susceptibility to threat susceptibilities, and management, diminish. However, the species is not ocean warming. Although there is no none of the five ESA listing factors, likely to become of such low abundance other genus-level or species-specific alone or in combination, are causing or so spatially fragmented as to be in information on the susceptibilities of this species to be likely to become danger of extinction due to depensatory Caulastrea species to disease and ocean endangered throughout its range within processes, the potential effects of acidification, the SRR rated them as the foreseeable future, and thus is not environmental stochasticity, or the ‘‘high’’ and ‘‘medium-high’’ importance warranted for listing at this time, potential for mortality from catastrophic to corals, respectively. Thus, we because: events within the foreseeable future conclude that an unstudied Caulastrea

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species is likely to have some similar in appearance to Caulastrea total live coral cover trends and habitat susceptibility to disease and ocean furcata. types. For C. echinulata, the overall acidification. The public comments and decline in abundance (‘‘Percent The SRR rated the trophic effects of information we gathered did not Population Reduction’’) was estimated fishing as ‘‘medium’’ importance, the provide any new or supplemental at 36 percent, and the decline in fourth most important threat to corals information on morphology, and abundance before the 1998 bleaching overall. This threat was not addressed at indicated that there is moderate event (‘‘Back-cast Percent Population the genus or species level in the SRR or taxonomic uncertainty for C. echinulata Reduction’’) was estimated at 14 SIR, because it is an ecosystem-level and a moderate level of species percent. However, as summarized above process. That is, removal of herbivorous identification uncertainty for this in the Inter-basin Comparison sub- fish from coral reef systems by fishing species. Veron (2014) states that C. section, live coral cover trends are alters trophic interactions by reducing echinulata is commonly confused with highly variable both spatially and herbivory on algae, thereby providing a C. furcata, but the species can be temporally, producing patterns on small competitive advantage for space to algae identified by experts (Fenner, 2014b), scales that can be easily taken out of over coral. Thus, the SRR did not thus we conclude that the distribution context. Thus, quantitative inferences to discuss this threat in terms of coral taxa, and abundance information described species-specific trends should be as its effects are difficult to distinguish below for this species is sufficiently interpreted with caution. At the same between coral genera and species. reliable (Fenner, 2014b). time, an extensive body of literature Therefore, an unstudied Caulastrea Spatial Information documents broad declines in live coral species is likely to have some cover and shifts to reef communities susceptibility to the trophic effects of The SRR and SIR provided the dominated by hardier coral species or fishing. following information on C. echinulata’s algae over the past 50 to 100 years The SRR rated sedimentation and distribution, habitat, and depth range. (Birkeland, 2004; Fenner, 2012; Pandolfi nutrients as ‘‘low-medium’’ importance The distribution includes the Coral et al., 2003; Sale and Szmant, 2012). to corals overall. Although there is no Triangle and GBR and a few nearby These changes have likely occurred, and genus-level or species-specific areas. Its primary habitat is horizontal are occurring, from a combination of information on the susceptibilities of substrates protected from wave action global and local threats. Given that C. Caulastrea species to sedimentation and and with turbid water, which can occur echinulata occurs in many areas nutrients, there is no information in a variety of reef habitats, including at affected by these broad changes, and suggesting they are not susceptible to least upper reef slopes, mid-slopes, and likely has some susceptibility to local these threats. Thus, we conclude that an lagoons. Its depth range is one to 20 and global threats, we conclude that it unstudied Caulastrea species is likely to meters. is likely to have declined in abundance have some susceptibility to The public comments did not provide over the past 50 to 100 years, but a sedimentation and nutrients. Sea-level any new or supplemental information precise quantification is not possible rise was not addressed at the genus or on C. echinulata’s distribution. We due to the limited species-specific species level in the SRR or SIR. gathered supplemental information, information. including Veron (2014), which reports Increasing sea levels may increase land- Other Biological Information based sources of pollution due to that this species is confirmed in 15 of The public comments and inundation, resulting in changes to coral his 133 Indo-Pacific ecoregions, and information we gathered did not community structure, thus an unstudied strongly predicted to be found in an provide any other biological information Caulastrea species is likely to have additional 12. on this species. some susceptibility to sea-level rise. The Demographic Information SRR rated predation and ornamental The SRR and SIR reported C. Susceptibility to Threats trade (referred to in the proposed rule as echinulata’s abundance as uncommon. The SRR and SIR provided the Collection and Trade) as ‘‘low’’ The public comments did not provide following species-specific information importance to corals overall. There is no any new or supplemental information on C. echinulata’s threats. Trade in C. information on the effects of predation on C. echinulata’s abundance. We echinulata is heavy. From 1999 to 2009, and collection and trade on Caulastrea, gathered supplemental information, gross exports averaged 8,713 specimens thus we conclude that Caulastrea likely including Veron (2014), which reports annually, with the vast majority has some susceptibility to predation and that C. echinulata occupied 0.34 percent originating in Indonesia. Take quotas collection and trade. of 2,984 dive sites sampled in 30 over that same period increased from In conclusion, an unstudied ecoregions of the Indo-Pacific, and had 9,000 in 1999 to 10,670 in 2010. Some Caulastrea species is likely to have low a mean abundance rating of 1.3 on a 1 general (i.e., family-level and coral- susceptibility to ocean warming, and to 5 rating scale at those sites in which level) information was also provided for some susceptibility to disease, ocean it was found. Based on this semi- the effects of ocean warming, acidification, sedimentation, nutrients, quantitative system, the species’ acidification, disease, predation, trophic effects of fishing, sea-level rise, abundance was characterized as ‘‘rare,’’ sedimentation, nutrients, and collection predation, and collection and trade. and overall abundance was described as and trade. The SRR and SIR did not Caulastrea echinulata ‘‘uncommon.’’ Veron did not infer provide any other species-specific trends in abundance from these data. As information on the effects of these Introduction described in the Indo-Pacific Species threats on C. echinulata. We interpreted The SRR and SIR provided the Determinations introduction above, threat susceptibility and exposure following information on C. echinulata’s based on results from Richards et al. information from the SRR and SIR in the morphology and taxonomy. Morphology (2008) and Veron (2014), the absolute proposed rule for C. echinulata’s was described as elongated, closely abundance of this species is likely at vulnerabilities as follows: Moderate compacted corallites on the ends of least millions of colonies. vulnerability to ocean warming, disease, branches, and taxonomy was described Carpenter et al. (2008) extrapolated acidification, trophic effects of fishing, as having no taxonomic issues but being species abundance trend estimates from and nutrients, low vulnerability to sea

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level rise and collection and trade, and substantial protection. General coral threats predicted within its range, unknown vulnerability to sedimentation protection laws are much less common however, C. echinulata is not highly and predation. regulatory mechanisms for the susceptible to any local sources of Public comments did not provide any management of C. echinulata. impact either. Its depth range is from new or supplemental information on C. one to 20 meters. This moderates Vulnerability to Extinction echinulata’s threat susceptibilities. We vulnerability to extinction over the gathered the following species-specific As explained above in the Risk foreseeable future because deeper areas and genus-level supplemental Analyses section, a species’ of its range will usually have lower information on this species’ threat vulnerability to extinction results from irradiance, and acidification is generally susceptibilities. Caulastrea echinulata the combination of its spatial and predicted to accelerate most in waters has not been rated as moderately or demographic characteristics, threat that are deeper and cooler than those in highly susceptible to bleaching or susceptibilities, and consideration of the which the species occurs. Its habitat disease, but this rating is not based on baseline environment and future includes horizontal substrates protected species-specific data (Carpenter et al., projections of threats. The SRR stated from wave action and with turbid water, 2008). Based on genus information that factors that increase the potential which can occur on at least upper reef described above, C. echinulata is likely extinction risk for C. echinulata are its slopes, mid-slopes, and lagoons. This to have low susceptibility to ocean uncommon abundance and that it is moderates vulnerability to extinction warming, and likely has some heavily traded. It listed factors that over the foreseeable future because the susceptibility to disease, ocean reduce potential extinction risk species is not limited to one habitat type acidification, trophic effects of fishing, including that the species distribution is but occurs in numerous types of reef sedimentation, nutrients, sea-level rise, broad latitudinally, and that its environments that will, on local and predation, and collection and trade. The preferred habitat type (turbid regional scales, experience highly available information does not support conditions) may provide some refuge variable thermal regimes and ocean more precise ratings of the from global threats such as bleaching (to chemistry at any given point in time. In susceptibilities of C. echinulata to the which it may have relatively low addition, turbidity can mitigate against threats. susceptibility). the effects of high irradiance by Subsequent to the proposed rule, we Regulatory Mechanisms blocking it from the water column in received and gathered supplemental turbid environments. Its absolute In the proposed rule, we did not species- or genus-specific information, abundance of at least millions of provide any species-specific described above, that expands our colonies, combined with its low information on the regulatory knowledge regarding the species susceptibility to ocean warming, mechanisms or conservation efforts for abundance, distribution, and threat moderates vulnerability to extinction C. echinulata. Criticisms of our susceptibilities. We developed our because the increasingly severe approach received during public assessment of the species’ vulnerability conditions expected in the foreseeable comment led us to attempt the following to extinction using all the available future will be non-uniform and analysis of regulatory mechanisms on a information. As explained in the Risk therefore will likely be a large number species basis. Records confirm C. Analyses section, our assessment in this of colonies that are either not exposed echinulata occurs in 15 Indo-Pacific final rule emphasizes the ability of the or do not negatively respond to a threat ecoregions that encompass 12 countries’ species’ spatial and demographic traits at any given point in time. Further, its EEZs. The 12 countries are Australia, to moderate or exacerbate its absolute abundance of at least tens of Brunei, China, Fiji, Indonesia, Japan, vulnerability to extinction, as opposed millions of colonies also provides Malaysia, Palau, Papua New Guinea, to the approach we used in the buffering capacity against collection Philippines, Solomon Islands, and proposed rule, which emphasized the pressures for the purposes of Taiwan. The regulatory mechanisms species’ susceptibility to threats. international trade. relevant to C. echinulata, described first The following characteristics of C. as the percentage of the above countries echinulata, in conjunction with the Listing Determination that utilize them to any degree and information described in the Corals and In the proposed rule using the second, as the percentages of those Coral Reefs section, Coral Habitat sub- determination tool formula, C. countries whose regulatory mechanisms section, and Threats Evaluation section echinulata was proposed for listing as may be limited in scope, are as follows: above, affect its vulnerability to threatened because of: Moderate General coral protection (25 percent extinction currently and over the vulnerability to ocean warming (ESA with none limited in scope), coral foreseeable future. Caulastrea Factor E), disease (C) and acidification collection (67 percent with 42 percent echinulata has low susceptibility to (E); uncommon generalized range wide limited in scope), pollution control (42 ocean warming-induced bleaching, abundance (E); narrow overall percent with 8 percent limited in based on species-specific and genus- distribution (based on narrow scope), fishing regulations on reefs (100 level information. Its geographic geographic distribution and moderate percent with 25 percent limited in distribution is mostly constrained to depth distribution (E); and inadequacy scope), and managing areas for parts of the Coral Triangle and western of existing regulatory mechanisms (D). protection and conservation (100 equatorial Pacific Ocean—areas which In this final rule, we changed the percent with none limited in scope). are projected to have the most rapid and listing determination for C. echinulata The most common regulatory severe impacts from climate change and from threatened to not warranted. We mechanisms in place for C. echinulata localized human impacts for coral reefs made this determination based on a are reef fishing regulations and area over the 21st century. For a species that more species-specific and holistic management for protection and is highly susceptible to climate change assessment of whether this species conservation. Coral collection and related threats, this range would meets the definition of either a pollution control laws are also exacerbate vulnerability to extinction threatened or endangered coral largely somewhat utilized for the species, but but C. echinulata has low susceptibility. in response to public comments, 42 percent of coral collection laws are Vulnerability to extinction may be including more appropriate limited in scope and may not provide exacerbated by the severe nature of local consideration of the buffering capacity

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of this species’ spatial and demographic worsen in severity and the species’ the effects of ocean acidification on E. traits to lessen its vulnerability to exposure to the threats increases paradivisa, which is discussed in the threats. Thus, based on the best throughout its range. Should the species description of that species below. We available information above on C. experience reduced abundance or range gathered supplemental information echinulata’s spatial structure, constriction of a certain magnitude, the which provided the following. The 1998 demography, threat susceptibilities, and ability of these characteristics to Palau bleaching event affected at least management, none of the five ESA moderate exposure to threats will three Euphyllia species (E. divisa, E. listing factors, alone or in combination, diminish. However, the species is not glabrescens, and E. paraancora), and all are causing this species to be likely to likely to become of such low abundance three species reported high levels of become endangered throughout its range or so spatially fragmented as to be in bleaching (Bruno et al., 2001). Euphyllia within the foreseeable future, and thus danger of extinction due to depensatory was the largest live trade genus from it is not warranted for listing at this processes, the potential effects of 1985 to 1997 (Green and Shirley, 1999) time, because: environmental stochasticity, or the and in 1999 (Bruckner, 2001). There is (1) Caulastrea echinulata’s low potential for mortality from catastrophic no other supplemental information on sensitivity to bleaching and depth range events within the foreseeable future the effects of threats on the genus down to 20 m, along with its preference throughout its range. Therefore, C. Euphyllia. for turbid water habitat, all combine to echinulata is not warranted for listing at Genus Conclusion provide refuge from thermal stress and this time under any of the listing factors. may decrease synergistic impacts from Based on the information from the other threats; Genus Euphyllia SRR, SIR, public comments, and (2) While Caulastrea echinulata’s Genus Introduction supplemental information, we can make distribution is mostly constrained to the following inferences about the parts of the Coral Triangle and western The family Euphyllidae contains five susceptibilities of an unstudied equatorial Pacific Ocean, its distribution genera, all in the Indo-Pacific, including Euphyllia species to ocean warming, is spread over a large area across the Euphyllia. The genus Euphyllia contains disease, ocean acidification, Coral Triangle, southern Japan and Fiji. eight species. The SRR and SIR sedimentation, nutrients, trophic effects While some areas within its range are provided no genus-level introductory of fishing, sea-level rise, predation, and projected to be affected by warming and information on Euphyllia. collection and trade. The SRR rated acidification, other areas are projected Genus Susceptibility to Threats ocean warming and disease as ‘‘high’’ to have less than average warming and importance, and ocean acidification as acidification. This distribution and the The SRR and SIR provided the ‘‘medium-high’’ importance, to corals. heterogeneous habitats it occupies following information on the threat These were rated as the three most reduce exposure to any given threat susceptibilities of the genus Euphyllia. important threats to reef-building corals event or adverse condition that does not Euphyllia species experienced high overall. The one available study occur uniformly throughout the species bleaching, but mortality is unknown, reporting the effects of ocean warming range. As explained above in the following the 1997/1998 mass bleaching on Euphyllia reported high levels of Threats Evaluation section, we have not event in Palau. In Indonesia, the family bleaching. We conclude that an identified any threat that is expected to Euphyllidae had no prevalence of coral unstudied Euphyllia species is likely to occur uniformly throughout the species disease. When raised in acidified have high susceptibility to ocean range within the foreseeable future; and conditions, Euphyllia paradivisa warming. Family Euphyllidae was (3) Caulastrea echinulata’s absolute showed little change in skeletal found to be disease-free in Indonesia. abundance is at least tens of millions of morphology, while Galaxea and However, this single study provides colonies, providing buffering capacity in Stylophora showed substantial skeletal inadequate information to conclude low the form of absolute numbers of change and Pocillopora died. The SRR susceptibility to disease, thus we colonies and variation in susceptibility reported that abundance of Euphyllia conclude that an unstudied Euphyllia between individual colonies. Its recruits was enhanced in areas where species is likely to have some absolute abundance also provides fish were excluded, indicating it may be susceptibility to disease. The one buffering capacity against collection more tolerant of the shaded conditions available study on a Euphyllia species pressures for purposes of international created by increased algal biomass in in acidified water did not show effects trade. As discussed in the Corals and overfished areas. Euphyllia divisa was on skeletal growth. This is the Tibbits Coral Reefs section above, the more fairly sensitive to exposure to cyanide; (2009) study on E. paradivisa that a colonies a species has, the lower the concentrations at or below those used in public comment stated is flawed. As proportion of colonies that are likely to cyanide fishing caused a progressive described below in the E. paradivisa be exposed to a particular threat at a tissue detachment, microbial infection, species description below, we reviewed particular time, and all individuals that and death. Large patches of Euphyllia the study and we concur that the are exposed will not have the same species can form in turbid areas in methods were flawed, thus the study response. Indonesia, suggesting a toleration of does not provide an adequate basis to Notwithstanding the projections high sediment loads. Euphyllia cristata conclude low susceptibility. Therefore, through 2100 that indicate increased is heavily used in the aquarium trade we conclude that an unstudied severity over time of the three high with species-specific exports or quotas Euphyllia species is likely to have some importance threats, the combination of from Indonesia, Fiji, Malaysia, and susceptibility to ocean acidification. these biological and environmental Tonga. Actual reported annual exports The SRR rated the trophic effects of characteristics indicates that the species from Indonesia alone averaged over fishing as ‘‘medium’’ importance, the possesses sufficient buffering capacity 36,000 pieces from 2000 to 2008. fourth most important threat to corals to avoid being in danger of extinction The public comments did not provide overall. This threat was not addressed at within the foreseeable future throughout any new or supplemental information the genus or species level in the SRR or its range. It is possible that this species’ on the threat susceptibilities of the SIR, because it is an ecosystem-level extinction risk may increase in the genus Euphyllia, except for a public process. That is, removal of herbivorous future if global threats continue and comment on a study cited in the SRR on fish from coral reef systems by fishing

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alters trophic interactions by reducing are no known taxonomic problems for E. was estimated at 14 percent. However, herbivory on algae, thereby providing a cristata, and a moderate level of species as summarized above in the Inter-basin competitive advantage for space to algae identification uncertainty. Veron (2014) Comparison sub-section, live coral cover over coral. Thus, the SRR did not states that E. cristata is sometimes trends are highly variable both spatially discuss this threat in terms of coral taxa, confused with Euphyllia glabrescens. and temporally, producing patterns on as its effects are difficult to distinguish However, it can be identified by experts small scales that can be easily taken out between coral genera and species. (Fenner, 2014b), thus we conclude that of context. Thus, quantitative inferences Therefore, an unstudied Euphyllia the distribution and abundance to species-specific trends should be species is likely to have some information described below for this interpreted with caution. At the same susceptibility to the trophic effects of species is sufficiently reliable (Fenner, time, an extensive body of literature fishing. 2014b). documents broad declines in live coral cover and shifts to reef communities The SRR rated sedimentation and Spatial Information nutrients as ‘‘low-medium’’ importance dominated by hardier coral species or to corals overall. One study reported The SRR and SIR provided the algae over the past 50 to 100 years Euphyllia tolerates turbid waters, following information on E. cristata’s (Birkeland, 2004; Fenner, 2012; Pandolfi suggesting tolerance of sedimentation, distribution, habitat, and depth range. et al., 2003; Sale and Szmant, 2012). and one study suggested that Euphyllia Euphyllia cristata’s distribution is the These changes have likely occurred, and may be tolerant of increased algae due central Indo-Pacific and the central are occurring, from a combination of to nutrients. However, these single Pacific. Its habitat includes most coral global and local threats. Given that E. studies provide inadequate information reef environments, and its depth range cristata occurs in many areas affected by to conclude low susceptibilities, thus is one to 35 meters. these broad changes, and likely has we conclude that an unstudied Public comments did not provide any some susceptibility to both global and Euphyllia species is likely to have some new or supplemental information on E. local threats, we conclude that it is susceptibility to sedimentation and cristata’s distribution. We gathered likely to have declined in abundance nutrients. Sea-level rise was not supplemental information, including over the past 50 to 100 years, but a addressed at the genus or species level Veron (2014), which reports that this precise quantification is not possible in the SRR or SIR. Increasing sea levels species is confirmed in 37 of his 133 based on limited species specific may increase land-based sources of Indo-Pacific ecoregions, and strongly information. predicted to be found in an additional pollution due to inundation, resulting in Other Biological Information changes to coral community structure, 12. Public comments and information thus an unstudied Euphyllia species is we gathered did not provide any more The public comments and likely to have some susceptibility to sea- information on E. cristata’s habitat and information we gathered did not level rise. Although there is no genus- depth range. provide any other biological information on this species. level or species-specific information on Demographic Information the susceptibility of Euphyllia species to The SRR and SIR reported E. cristata’s Susceptibility to Threats predation, there is no information abundance as uncommon. The SRR and SIR provided the suggesting they are not susceptible to Public comments did not provide any following species-specific information these threats. Thus, we conclude that an new or supplemental information on E. on E. cristata’s threats. Euphyllia unstudied Euphyllia species is likely to cristata’s abundance. We gathered cristata is heavily used in the aquarium have some susceptibility to predation. supplemental information, including trade with species-specific exports or Some Euphyllia species are heavily Veron (2014), which reports that E. quotas from Indonesia, Fiji, Malaysia, exploited in the ornamental trade, thus cristata occupied 12.1 percent of 2,984 and Tonga. Actual reported annual we conclude that an unstudied dive sites sampled in 30 ecoregions of exports from Indonesia alone averaged Euphyllia species is likely to have high the Indo-Pacific, and had a mean over 36,000 pieces from 2000 to 2008. susceptibility to collection and trade. abundance rating of 1.33 on a 1 to 5 Genus-level information is provided for In conclusion, an unstudied Euphyllia rating scale at those sites in which it the effects on Euphyllia of ocean species is likely to have high was found. Based on this semi- warming, disease, ocean acidification, susceptibility to ocean warming and quantitative system, the species’ land-based sources of pollution collection and trade, and some abundance was characterized as (sedimentation, nutrients, toxins, and susceptibility to disease, ocean ‘‘common,’’ and overall abundance was salinity), predation, and collection/ acidification, trophic effects of fishing, described as ‘‘uncommon but trade. The SRR and SIR did not provide sedimentation, nutrients, sea-level rise, conspicuous.’’ Veron did not infer any other species-specific information and predation. trends in abundance from these data. As on the effects of these threats on E. Euphyllia cristata described in the Indo-Pacific Species cristata. We interpreted threat Determinations introduction above, susceptibility and exposure information Introduction based on results from Richards et al. from the SRR and SIR in the proposed The SRR and SIR provided the (2008) and Veron (2014), the absolute rule for E. cristata’s vulnerabilities as following information on E. cristata’s abundance of this species is likely at follows: High vulnerability to ocean morphology and taxonomy. Morphology least tens of millions of colonies. warming; moderate vulnerability to was described as branching separate Carpenter et al. (2008) extrapolated disease, ocean acidification, trophic corallites without a shared wall but species abundance trend estimates from effects of fishing, and nutrients, and low close together, and solitary polyps are total live coral cover trends and habitat vulnerability to sedimentation, sea level common, and taxonomy was described types. For E. cristata, the overall decline rise, predation, and collection and trade. as having no taxonomic issues. in abundance (‘‘Percent Population Public comments did not provide any Public comments and information we Reduction’’) was estimated at 36 new or supplemental information on E. gathered did not provide any new or percent, and the decline in abundance cristata’s threat susceptibilities. We supplemental information on before the 1998 bleaching event (‘‘Back- gathered supplemental species-specific morphology, and confirmed that there cast Percent Population Reduction’’) and genus-level information on this

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species’ threat susceptibilities. Vulnerability to Extinction those in which the species occurs. Its Euphyllia cristata was not rated as As explained above in the Risk habitat includes most coral reef moderately or highly susceptible to Analyses section, a species’ environments. This moderates bleaching or coral disease by Carpenter vulnerability to extinction results from vulnerability to extinction over the et al. (2008), but they did not have the combination of its spatial and foreseeable future because the species is species-specific data. There are no demographic characteristics, threat not limited to one habitat type but studies of the effects of any threat on susceptibilities, and consideration of the occurs in numerous types of reef this species. Based on genus-level baseline environment and future environments that will, on local and information presented above, E. cristata projections of threats. The SRR stated regional scales, experience highly is likely to have high susceptibility to that factors that increase potential variable thermal regimes and ocean ocean warming and collection and extinction risk for E. cristata include its chemistry at any given point in time. Its trade, and some susceptibility to heavy involvement in international absolute abundance of at least tens of millions of colonies, combined with disease, ocean acidification, trophic trade combined with its rare existence spatial variability in ocean warming and effects of fishing, nutrients, but conspicuous colonies, suggesting it acidification across the species range, sedimentation, sea-level rise, and is vulnerable to overexploitation. moderates vulnerability to extinction predation. Euphyllia cristata appears to be because the increasingly severe susceptible to bleaching. The SRR noted conditions expected in the foreseeable Regulatory Mechanisms that its geographic distribution is future will be non-uniform and moderate, although wider than its In the proposed rule, we did not therefore will likely be a large number congeners under consideration in this provide any species-specific of colonies that are either not exposed review. information on the regulatory or do not negatively respond to a threat Subsequent to the proposed rule, we mechanisms or conservation efforts for at any given point in time. Further, its received and gathered supplemental E. cristata. Criticisms of our approach absolute abundance of at least tens of species- or genus-specific information, received during public comment led us millions of colonies also provides described above, that expands our to attempt the following analysis of buffering capacity against collection knowledge regarding the species regulatory mechanisms on a species pressures for the purposes of abundance, distribution, and threat basis. Records confirm E. cristata occurs international trade. susceptibilities. We developed our in 37 Indo-Pacific ecoregions that assessment of the species’ vulnerability Listing Determination encompass 21 countries’ EEZs. The 21 to extinction using all the available countries are Australia, Brunei, China, In the proposed rule using the information. As explained in the Risk determination tool formula approach, E. Federated States of Micronesia, Fiji, Analyses section, our assessment in this France (French Pacific Island cristata was proposed for listing as final rule emphasizes the ability of the threatened because of: High Territories), Indonesia, Japan, Malaysia, species’ spatial and demographic traits Maldives, Myanmar, Palau, Papua New vulnerability to ocean warming (ESA to moderate or exacerbate its Factor E); moderate vulnerability to Guinea, Philippines, Solomon Islands, vulnerability to extinction, as opposed Taiwan, Thailand, Timor-Leste, United disease (C) and acidification (E); to the approach we used in the uncommon generalized range wide States (CNMI, Guam), Vanuatu, and proposed rule, which emphasized the abundance (E); moderate overall Vietnam. The regulatory mechanisms species’ susceptibility to threats. distribution (based on moderate relevant to E. cristata, described first as The following characteristics of E. geographic distribution and moderate the percentage of the above countries cristata, in conjunction with the depth distribution (E); and inadequacy that utilize them to any degree, and information described in the Corals and of existing regulatory mechanisms (D). second as the percentage of those Coral Reefs section, Coral Habitat sub- In this final rule, we changed the countries whose regulatory mechanisms section, and Threats Evaluation section listing determination for E. cristata from may be limited in scope, are as follows: above, affect its vulnerability to threatened to not warranted. We made General coral protection (38 percent extinction currently and over the this determination based on a more with five percent limited in scope), foreseeable future. Its geographic species-specific and holistic assessment coral collection (62 percent with 29 distribution includes many of the coral of whether this species meets the percent limited in scope), pollution reef ecoregions from the northern Indian definition of either a threatened or control (43 percent with 14 percent Ocean through the western and central endangered coral largely in response to limited in scope), fishing regulations on Pacific Ocean. Its geographic public comments, including more reefs (100 percent with 14 percent distribution moderates vulnerability to appropriate consideration of the limited in scope), and managing areas extinction because some areas within its buffering capacity of this species’ spatial for protection and conservation (95 range are projected to have less than and demographic traits to lessen its percent with none limited in scope). average warming and acidification over vulnerability to threats. Thus, based on The most common regulatory the foreseeable future, including the the best available information above on mechanisms in place for E. cristata are western Indian Ocean, the central E. cristata’s spatial structure, reef fishing regulations and area Pacific, and other areas, so portions of demography, threat susceptibilities, and management for protection and the population in these areas will be management, none of the five ESA conservation. Coral collection and less exposed to severe conditions. Its listing factors, alone or in combination, pollution control laws are also depth range is from one to 35 meters. are causing this species to be likely to somewhat utilized for the species, but This moderates vulnerability to become endangered throughout its range 29 percent of coral collection laws are extinction over the foreseeable future within the foreseeable future, and thus limited in scope and may not provide because deeper areas of its range will is not warranted for listing at this time, substantial protection. General coral usually have lower irradiance than because: protection laws are much less common surface waters, and acidification is (1) Euphyllia cristata’s distribution in regulatory mechanisms for the generally predicted to accelerate most in the northern Indian Ocean, central Indo- management of E. cristata. waters that are deeper and cooler than Pacific, and central Pacific is spread

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over a vast area. While some areas cristata is not warranted for listing at Public comments did not provide any within its range are projected to be this time under any of the listing factors. new or supplemental information on E. affected by warming and acidification, paraancora’s abundance. We gathered Euphyllia paraancora other areas are projected to have less supplemental information that provides than average warming and acidification, Introduction the following. Euphyllia paraancora has including the central Pacific, and other The SRR and SIR provided the been reported from large monospecific areas. This distribution and the following information on E. stands at 60 to 70 m depth in Saipan heterogeneous habitats it occupies paraancora’s morphology and (Rooney et al., 2012). Veron (2014) reduce exposure to any given threat taxonomy. Morphology was described reports that E. paraancora occupied 1.9 event or adverse condition that does not as branching separate corallites without percent of 2,984 dive sites sampled in occur uniformly throughout the species a shared wall, and tentacles have 30 ecoregions of the Indo-Pacific, and range. As explained above in the anchor-shaped ends. Taxonomy was had a mean abundance rating of 1.46 on Threats Evaluation section, we have not described as having no taxonomic issues a 1 to 5 rating scale at those sites in identified any threat that is expected to but tentacles are similar to Euphyllia which it was found. Based on this semi- occur uniformly throughout the species ancora, and the skeleton is the same as quantitative system, the species’ range within the foreseeable future; Euphyllia glabrescens, Euphyllia abundance was characterized as (2) Euphyllia cristata’s absolute paraglabrescens, and Euphyllia ‘‘uncommon,’’ and overall abundance abundance is at least tens of millions of paradivisa. was also described as ‘‘uncommon.’’ colonies, providing buffering capacity in Public comments and information we Veron did not infer trends in abundance the form of absolute numbers of gathered did not provide any new or from these data. As described in the colonies and variation in susceptibility supplemental information on Indo-Pacific Species Determinations between individual colonies. Its morphology, and confirmed that there introduction above, based on results absolute abundance also provides are no known taxonomic problems for E. from Richards et al. (2008) and Veron buffering capacity against collection paraancora, but there is a low level of (2014), the absolute abundance of this pressures for purposes of international species identification uncertainty for species is likely at least millions of trade. As discussed in the Corals and this species. The species can be easily colonies. Coral Reefs section above, the more identified by experts, thus we conclude Carpenter et al. (2008) extrapolated colonies a species has, the lower the that the distribution and abundance species abundance trend estimates from proportion of colonies that are likely to information described below for this total live coral cover trends and habitat be exposed to a particular threat at a species is sufficiently reliable (Fenner, types. For E. paraancora, the overall particular time, and all individuals that 2014b). decline in abundance (‘‘Percent are exposed will not have the same Population Reduction’’) was estimated response; and Spatial Information at 36 percent, and the decline in (3) Euphyllia cristata occurs from one The SRR and SIR provided the abundance before the 1998 bleaching to 35 meters of depth which provides following information on E. event (‘‘Back-cast Percent Population vertical moderation of exposure to paraancora’s distribution, habitat, and Reduction’’) was estimated at 14 threats and increases the absolute area depth range. Euphyllia paraancora is percent. However, as summarized above of potential occupancy within the found in the Coral Triangle, Taiwan, the in the Inter-basin Comparison sub- species range, therefore buffering Mariana Islands, New Caledonia and section, live coral cover trends are against extinction risk. Vanuatu. The SIR reports that colonies highly variable both spatially and Notwithstanding the projections found in Guam were in turbid temporally, producing patterns on small through 2100 that indicate increased environments. Its habitat includes reef scales that can be easily taken out of severity over time of the three high environments protected from wave context. Thus, quantitative inferences to importance threats, the combination of action, including at least upper reef species-specific trends should be these biological and environmental slopes, mid-slopes, lower reef slopes, interpreted with caution. At the same characteristics indicates that the species and lagoons, from three to 30 m deep. time, an extensive body of literature possesses sufficient buffering capacity One public comment confirmed the documents broad declines in live coral to avoid being in danger of extinction presence of E. paraancora in Guam. We cover and shifts to reef communities within the foreseeable future throughout gathered supplemental information, dominated by hardier coral species or its range. It is possible that this species’ including Veron (2014), which reports algae over the past 50 to 100 years extinction risk may increase in the that this species is confirmed in 19 of (Birkeland, 2004; Fenner, 2012; Pandolfi future if global threats continue and his 133 Indo-Pacific ecoregions, and et al., 2003; Sale and Szmant, 2012). increase in severity and the species strongly predicted to be found in an These changes have likely occurred, and exposure to threats increases throughout additional 15. Euphyllia paraancora has are occurring, from a combination of its range. Should the species experience been reported in water as deep as 70 m global and local threats. Given that E. reduced abundance or range (Carpenter et al., 2008; Rooney et al., paraancora occurs in many areas constriction of a certain magnitude, the 2012). Based on all the available affected by these broad changes, and ability of these characteristics to information, its habitat includes least likely has some susceptibility to both moderate exposure to threats will upper reef slopes, mid-slopes, lower reef global and local threats, we conclude diminish. However, the species is not slopes, lagoons, and mesophotic areas, that it is likely to have declined in likely to become of such low abundance from three to 70 m deep. abundance over the past 50 to 100 years, or so spatially fragmented as to be in but a precise quantification is not danger of extinction due to depensatory Demographic Information possible based on limited species processes, the potential effects of The SRR and SIR reported E. specific information. environmental stochasticity, or the paraancora’s abundance as uncommon. Other Biological Information potential for mortality from catastrophic However, it has reportedly been found events within the foreseeable future in large monospecific stands at six to 8 The public comments and throughout its range. Therefore, E. m depth in Taiwan. information we gathered did not

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provide any other biological information some susceptibility to disease, ocean rare existence but conspicuous colonies, on this species. acidification, trophic effects of fishing, suggesting it is vulnerable to nutrients, sedimentation, sea-level rise, overexploitation. The species appears Susceptibility to Threats and predation. bleaching-susceptible. Its geographic To describe E. paraancora’s threat distribution is also somewhat restricted, Regulatory Mechanisms susceptibilities, the SRR and SIR centered in the threat-prone Coral provided the following species-specific In the proposed rule, we did not Triangle Region. information on E. paraancora’s threats. provide any species-specific Subsequent to the proposed rule, we Euphyllia paraancora and its congeners information on the regulatory received and gathered supplemental experienced high bleaching but mechanisms or conservation efforts for species- or genus-specific information, mortality is unknown following the E. paraancora. We received criticism of described above, that expands our 1997/1998 mass bleaching event in that approach in public comments and knowledge regarding the species Palau (Bruno et al., 2001). Euphyllia in response we present a species- abundance, distribution, and threat paraancora in Taiwan contained both specific analysis of regulatory susceptibilities. We developed our Clades C and D zooxanthellae, with mechanisms in this final rule. Records assessment of the species’ vulnerability Clade D primarily in stressful confirm that Euphyllia paraancora to extinction using all the available environments like shallow waters and occurs in 19 Indo-Pacific ecoregions that information. As explained in the Risk reef edges. Euphyllia paraancora is encompass 16 countries’ EEZs. The 16 Analyses section, our assessment in this specifically listed in the CITES countries Australia, Brunei, China, final rule emphasizes the ability of the databases with a 2008 annual export Federated States of Micronesia, France species’ spatial and demographic traits quota of ∼ 5000 (up from 1000 in 2004) (French Pacific Island Territories), to moderate or exacerbate its ‘‘maricultured’’ pieces from Indonesia Indonesia, Japan, Malaysia, Palau, vulnerability to extinction, as opposed although the meaning of ‘‘maricultured’’ Papua New Guinea, Philippines, to the approach we used in the is unclear. Genus-level information is Solomon Islands, Taiwan, Timor-Leste, proposed rule, which emphasized the provided for the effects on Euphyllia of United States (CNMI, Guam), and species’ susceptibility to threats. ocean warming, ocean acidification, Vietnam. The regulatory mechanisms The following characteristics of E. disease, land-based sources of pollution relevant to E. paraancora, described paraancora, in conjunction with the (sedimentation, nutrients, toxins, and first as the percentage of the above information described in the Corals and salinity), predation, and collection/ countries that utilize them to any Coral Reefs section, Coral Habitat sub- trade. The SRR and SIR did not provide degree, and second as the percentage of section, and Threats Evaluation section any other species-specific information those countries whose regulatory above, affect its vulnerability to on the effects of these threats on E. mechanisms may be limited in scope, extinction currently and over the paraancora. We interpreted threat are as follows: General coral protection foreseeable future. Its geographic susceptibility and exposure information (38 percent with none limited in scope), distribution occurs in the Coral from the SRR and SIR in the proposed coral collection (63 percent with 25 Triangle, the western equatorial Pacific rule for E. paraancora’s vulnerabilities percent limited in scope), pollution Ocean, the Mariana Islands, and New as follows: High vulnerability to ocean control (44 percent with 19 percent Caledonia. Despite the large number of warming; moderate vulnerability to limited in scope), fishing regulations on islands and environments that are disease, ocean acidification, trophic reefs (100 percent with 19 percent included in the species’ range, this effects of fishing, and nutrients, and low limited in scope), and managing areas range exacerbates vulnerability to vulnerability to sedimentation, sea level for protection and conservation (100 extinction over the foreseeable future rise, and collection and trade. percent with none limited in scope). because it is mostly limited to an area Public comments did not provide any The most common regulatory projected to have the most rapid and new or supplemental information on E. mechanisms in place for E. paraancora severe impacts from climate change and paraancora’s threats susceptibilities. We are reef fishing regulations and area localized human impacts for coral reefs gathered supplemental species-specific management for protection and over the 21st century. Its depth range and genus-level information on this conservation. Coral collection and goes down to 70 meters which stretches species’ threat susceptibilities. pollution control laws are also into the mesophotic zone. This Euphyllia paraancora was not rated as somewhat utilized for the species, but moderates vulnerability to extinction moderately or highly susceptible to 25 percent of coral collection laws are over the foreseeable future because bleaching or disease by Carpenter et al. limited in scope and may not provide deeper areas of its range will usually (2008), but they did not have species- substantial protection. General coral have lower irradiance than surface specific data. In Palau in 2000, E. protection laws are much less common waters, and acidification is generally paraancora had high levels of regulatory mechanisms for the predicted to accelerate most in waters bleaching, but an unknown level of management of E. paraancora. that are deeper and cooler than those in mortality. In that event, 48 percent of all which the species occurs. Its habitat coral colonies of all species were Vulnerability to Extinction includes at least upper reef slopes, mid- bleached, with bleaching of different As explained above in the Risk slopes, lower reef slopes, lagoons, and genera and species ranging from none to Analyses section, a species’ mesophotic areas. This moderates very high, and mortality from none to vulnerability to extinction results from vulnerability to extinction over the near 100 percent (Bruno et al., 2001). the combination of its spatial and foreseeable future because the species is There are no other studies of the effects demographic characteristics, threat not limited to one habitat type but of any threat on this species. Combined susceptibilities, and consideration of the occurs in numerous types of reef with genus-level information presented baseline environment and future environments that will, on local and above, E. paraancora is likely to have projections of threats. The SRR stated regional scales, experience highly high susceptibility to ocean warming that factors that increase potential variable thermal regimes and ocean and collection and trade. Further based extinction risk for E. paraancora chemistry at any given point in time. Its on genus level information, E. include its heavy involvement in absolute abundance of at least millions paraancora can be predicted to have international trade combined with its of colonies, combined with spatial

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variability in ocean warming and occur uniformly throughout the species paraglabrescens, and Euphyllia acidification across the species range, range. As explained above in the paraancora. moderates vulnerability to extinction Threats Evaluation section, we have not The public comments and because the increasingly severe identified any threat that is expected to information we gathered did not conditions expected in the foreseeable occur uniformly throughout the species provide any new or supplemental future will be non-uniform and range within the foreseeable future; and information on morphology, and therefore will likely be a large number (2) Euphyllia paraancora’s absolute confirmed that there are no known of colonies that are either not exposed abundance is at least millions of taxonomic problems for E. paradivisa, or do not negatively respond to a threat colonies, providing buffering capacity in and a low level of species identification at any given point in time. Further, its the form of absolute numbers of uncertainty for this species. Veron absolute abundance of at least tens of colonies and variation in susceptibility (2014) states that E. paradivisa is very distinctive. The species can be easily millions of colonies also provides between individual colonies. Its identified by experts, thus we conclude buffering capacity against collection absolute abundance also provides that the distribution and abundance pressures for the purposes of buffering capacity against collection information described below for this international trade. pressures for purposes of international species is sufficiently reliable (Fenner, trade. As discussed in the Corals and Listing Determination 2014b). In the proposed rule using the Coral Reefs section above, the more determination tool formula approach, E. colonies a species has, the lower the Spatial Information paraancora was proposed for listing as proportion of colonies that are likely to The SRR and SIR provided the threatened because of: High be exposed to a particular threat at a following information on E. paradivisa’s vulnerability to ocean warming (ESA particular time, and all individuals that distribution, habitat, and depth range. Factor E); moderate vulnerability to are exposed will not have the same Euphyllia paradivisa’s distribution is disease (C) and acidification (E); response. restricted to the Coral Triangle, and its uncommon generalized range wide Notwithstanding the projections habitat is shallow or mid-slope reef abundance (E); wide overall distribution through 2100 that indicate increased environments protected from wave (based on moderate geographic severity over time of the three high action, from five to 20 meters depth. distribution and wide depth distribution importance threats, the combination of The public comments did not provide (E); and inadequacy of existing these biological and environmental any new or supplemental information regulatory mechanisms (D). characteristics indicates that the species on E. paradivisa’s distribution. We In this final rule, we changed the possesses sufficient buffering capacity gathered supplemental information, listing determination for E. paraancora to avoid being in danger of extinction including Veron (2014) which reports from threatened to not warranted. We within the foreseeable future throughout that E. paradivisa is confirmed in eight made this determination based on a its range. It is possible that this species’ of his 133 Indo-Pacific ecoregions, and more species-specific and holistic extinction risk may increase in the strongly predicted to be found in an assessment of whether this species future as global threats continue and additional eight. Fenner (2013a) meets the definition of either a increase in severity and the species reported E. paradivisa (supported by threatened or endangered coral largely exposure to threats increases throughout photographs), from American Samoa at in response to public comments, its range. Should the species experience about 25 m deep protected from wave including more appropriate reduced abundance or range action. Veron (2014) reports it from consideration of the buffering capacity constriction of a certain magnitude, the American Samoa based on that record. of this species’ spatial and demographic ability of these characteristics to Thus, based on all the available traits to lessen its vulnerability to moderate exposure to threats will information, E. paradivisa’s habitat threats. Thus, based on the best diminish. However, the species is not includes environments protected from available information above on E. likely to become of such low abundance wave action on at least upper reef paraancora’s spatial structure, or so spatially fragmented as to be in slopes, mid-slope terraces, and lagoons demography, threat susceptibilities, and danger of extinction due to depensatory in depths ranging from two to 25 m management, none of the five ESA processes, the potential effects of depth. listing factors, alone or in combination, environmental stochasticity, or the Demographic Information are causing this species to be likely to potential for mortality from catastrophic become endangered throughout its range events within the foreseeable future The SRR and SIR reported that E. within the foreseeable future, and thus throughout its range. Therefore, E. paradivisa’s abundance is uncommon. is not warranted for listing at this time, paraancora is not warranted for listing The public comments did not provide because: at this time under any of the listing any new or supplemental information (1) Euphyllia paraancora’s depth factors. on E. paradivisa’s abundance. We distribution of three to 70 m is gathered supplemental information, exceptionally broad and deep for most Euphyllia paradivisa including Veron (2014) which reported reef-building coral species. The ability Introduction that E. paradivisa occupied 0.2 percent to occupy a broad range of depths likely of 2,984 dive sites sampled in 30 provides refugia from threats that may The SRR and SIR provided the ecoregions of the Indo-Pacific, and had be more severe in shallow environments following information on E. paradivisa’s a mean abundance rating of 1.5 on a 1 because irradiance is usually lower at morphology and taxonomy. Morphology to 5 rating scale at those sites in which depths at the deeper end of this species’ was described as branching separate it was found. Based on this semi- range. It also increases the absolute area corallites without a shared wall and quantitative system, the species’ of potential occupancy throughout the branching tentacles. The taxonomy was abundance was characterized as ‘‘rare,’’ species range. This distribution and the described as having no taxonomic issues and overall abundance was described as heterogeneous habitats it occupies but having tentacles similar to Euphyllia ‘‘uncommon.’’ Veron did not infer reduce exposure to any given threat divisa and skeleton that is the same as trends in abundance from these data. As event or adverse condition that does not Euphyllia glabrescens, Euphyllia described in the Indo-Pacific Species

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Determinations introduction above, meaning of ‘‘maricultured’’ is unclear. more precise ratings of the based on results from Richards et al. The SRR and SIR did not provide any susceptibilities of E. paradivisa to the (2008) and Veron (2014), the absolute other species-specific information on threats. abundance of this species is likely at the effects of these threats on E. Regulatory Mechanisms least tens of millions of colonies. paradivisa. We interpreted the threat Carpenter et al. (2008) extrapolated susceptibility and exposure information In the proposed rule, we did not species abundance trend estimates from from the SRR and SIR in the proposed provide any species-specific total live coral cover trends and habitat rule for E. paradivisa’s vulnerabilities to information on the regulatory types. For E. paradivisa, the overall threats as follows: High vulnerability to mechanism or conservation efforts for E. decline in abundance (‘‘Percent ocean warming, moderate vulnerability paradivisa. Criticisms of our approach Population Reduction’’) was estimated to disease, ocean acidification, trophic received during public comment led us at 38 percent, and the decline in effects of fishing, and nutrients, low to attempt the following analysis of abundance before the 1998 bleaching vulnerability to sedimentation, sea level regulatory mechanisms on a species event (‘‘Back-cast Percent Population rise, and collection and trade, and basis. Records confirm that Euphyllia Reduction’’) was estimated at 15 unknown vulnerability to predation. paradivisa occurs in eight Indo-Pacific percent. However, as summarized above The public comments provided the ecoregions that encompass 15 countries’ in the Inter-basin Comparison sub- following supplemental information on EEZs. The 15 countries are Brunei, Fiji, section, live coral cover trends are E. paradivisa’s threat susceptibilities. A France (French Pacific Island highly variable both spatially and public comment stated that the SRR Territories), Indonesia, Malaysia, New temporally, producing patterns on small appeared to rely solely upon collection Zealand (Tokelau), Niue, Papua New scales that can be easily taken out of and trade to rate the extinction risk of Guinea, Philippines, Samoa, Timor- context. Thus, quantitative inferences to this species, subsequently leading to the Leste, Tonga, Tuvalu, United States species-specific trends should be proposed Endangered listing. However, (American Samoa), and Vietnam. The interpreted with caution. At the same the SRR (and the Determination Tool in regulatory mechanisms relevant to E. time, an extensive body of literature the proposed rule) both considered the paradivisa, described first as the documents broad declines in live coral susceptibilities and vulnerabilities of percentage of the above countries that cover and shifts to reef communities this species to multiple threats to help utilize them to any degree and second, dominated by hardier coral species or determine its extinction risk and as the percentages of those countries algae over the past 50 to 100 years proposed listing status. Likewise, as whose regulatory mechanisms may be (Birkeland, 2004; Fenner, 2012; Pandolfi explained in the Determination limited in scope, are as follows: General et al., 2003; Sale and Szmant, 2012). Framework section above, this final rule coral protection (33 percent with none These changes have likely occurred, and considers the susceptibilities, limited in scope), coral collection (80 are occurring, from a combination of exposures, and vulnerabilities of each percent with 40 percent limited in global and local threats. Given that E. species to the nine major threats to scope), pollution control (53 percent paradivisa occurs in many areas determine its extinction risk and listing with 20 percent limited in scope), affected by these broad changes, and status, including for E. paradivisa. fishing regulations on reefs (100 percent likely has some susceptibility to both The public comment also stated that with 20 percent limited in scope), global and local threats, we conclude an unpublished study cited by the SRR managing areas for protection and that it is likely to have declined in on the effects of ocean acidification on conservation (100 percent with none abundance over the past 50 to 100 years, E. paradivisa (Tibbits, 2009) is flawed. limited in scope). The most common but a precise quantification is not The study reported that the skeletal regulatory mechanisms in place for E. possible due to the limited species- morphology of E. paradivisa specimens paradivisa are reef fishing regulations specific information. kept in acidified conditions over a three and area management for protection and month period ‘‘did not change conservation. Coral collection and Other Biological Information noticeably.’’ We reviewed the study, pollution control laws are also common The public comments and and we concur with the public for the species, but 40 percent of coral information we gathered did not comment, in that the methods used in collection laws are limited in scope and provide any other biological information the study to lower pH were flawed, thus may not provide substantial protection. on this species. the results should not be considered General coral protection laws are much reliable information on the potential less common regulatory mechanisms for Susceptibility to Threats effects of ocean acidification on E. the management of E. paradivisa. To describe E. paradivisa’s threat paradivisa. susceptibilities, the SRR and SIR We gathered the following species- Vulnerability to Extinction provided genus-level information for the specific supplemental information on As explained above in the Risk effects on Euphyllia of ocean warming, this species’ threat susceptibilities. Analyses section, a species’ disease, acidification, sedimentation, Euphyllia paradivisa was not rated as vulnerability to extinction results from predation, and collection and trade. The moderately or highly susceptible to the combination of its spatial and SRR and SIR also provided the bleaching and disease, but these ratings demographic characteristics, threat following species-specific information are not based on species-specific data susceptibilities, and consideration of the on E. paradivisa’s threats. When raised (Carpenter et al., 2008). Based on the baseline environment and future in acidified conditions, E. paradivisa genus and species-specific information projections of threats. The SRR stated showed little change in skeletal described above, E. paradivisa is likely that factors that increase the potential morphology, while Galaxea and to have high susceptibility to ocean extinction risk for E. paradivisa include Stylophora showed substantial skeletal warming and collection and trade, some its heavy involvement in international change and Pocillopora died. Euphyllia susceptibility to disease, acidification, trade combined with its rare existence paradivisa is specifically listed in the trophic effects of fishing, nutrients, and but conspicuous colonies, suggesting it CITES databases with annual export predation, and low susceptibility to is vulnerable to overexploitation. The quotas of up to 2380 ‘‘maricultured’’ sedimentation and sea-level rise. The species appears bleaching-susceptible. pieces from Indonesia, although the available information does not support Its geographic distribution is also

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somewhat restricted, centered in the future will be non-uniform and geographic area that is likely to threat-prone Coral Triangle Region. No therefore will likely be a large number experience severe and increasing threats known factors were noted by the BRT to of colonies that are either not exposed indicates that a high proportion of the reduce the extinction risk of this or do not negatively respond to a threat population of this species is likely to be species. at any given point in time. However, its exposed to those threats over the Subsequent to the proposed rule, we qualitative abundance is described as foreseeable future; and received and gathered supplemental rare, which can exacerbate its (3) Euphyllia paradivisa’s semi- species- or genus-specific information, vulnerability given its restricted range. quantitative abundance is rare. described above, that expands our Considering the limited range of this knowledge regarding the species Listing Determination species in an area where severe and abundance, distribution, and threat In the proposed rule using the increasing impacts are predicted, this susceptibilities. We developed our determination tool formula, E. level of abundance leaves the species assessment of the species’ vulnerability paradivisa was proposed for listing as vulnerable to becoming of such low to extinction using all the available endangered because of: High abundance within the foreseeable future information. As explained in the Risk vulnerability to ocean warming (ESA that it may be at risk from depensatory Analyses section, our assessment in this Factor E); moderate vulnerability to processes, environmental stochasticity, final rule emphasizes the ability of the disease (C) and acidification (E); or catastrophic events, as explained in species’ spatial and demographic traits uncommon generalized range wide more detail in the Corals and Coral to moderate or exacerbate its abundance (E); narrow overall Reefs and Risk Analyses sections. vulnerability to extinction, as opposed distribution (based on narrow The combination of these to the approach we used in the geographic distribution and moderate characteristics and projections of future proposed rule, which emphasized the depth distribution (E); and inadequacy threats indicates that the species is species’ susceptibility to threats. of existing regulatory mechanisms (D). likely to be in danger of extinction The following characteristics of E. In this final rule, we changed our within the foreseeable future throughout paradivisa, in conjunction with the listing determination of E. paradivisa its range and warrants listing as information described in the Corals and from endangered to threatened. We threatened at this time due to factors A, Coral Reefs section, Coral Habitat sub- made this determination based on a C, D, and E. section, and Threats Evaluation section more species-specific and holistic The available information above on E. above, affect its vulnerability to assessment of whether this species paradivisa’s spatial structure, extinction currently and over the meets the definition of either a demography, threat susceptibilities, and foreseeable future. Its geographic threatened or endangered coral largely management also indicate that the distribution is mostly limited to parts of in response to public comments, species is not currently in danger of the Coral Triangle. Despite the large including more appropriate extinction and thus does not warrant number of islands and environments consideration of the buffering capacity listing as Endangered because: that are included in the species’ range, of this species’ spatial and demographic (1) While E. paradivisa’ range is this range exacerbates vulnerability to traits to lessen its vulnerability to mostly within the Coral Triangle, which extinction over the foreseeable future threats. Thus, based on the best increases it extinction risk as described because it is mostly limited to an area available information provided above on above, its habitat includes environments projected to have the most rapid and E. paradivisa’s spatial structure, protected from wave action on at least severe impacts from climate change and demography, threat susceptibilities, and upper reef slopes, mid-slope terraces, localized human impacts for coral reefs management indicate that it is likely to and lagoons. This moderates over the 21st century. Its depth range of become endangered throughout its range vulnerability to extinction currently two to 25 meters moderates within the foreseeable future, and thus because the species is not limited to one vulnerability to extinction over the warrants listing as threatened at this habitat type but occurs in numerous foreseeable future because deeper areas time, because: types of reef environments that will, on of its range will usually have lower (1) Euphyllia paradivisa is susceptible local and regional scales, experience irradiance than surface waters, and to warming-induced bleaching (ESA highly variable thermal regimes and acidification is generally predicted to Factor E), disease (C), ocean ocean chemistry at any given point in accelerate most in waters that are deeper acidification (E), trophic effects of time, as described in more detail in the and cooler than those in which the fishing (A), nutrients (A, E), predation Coral Habitat and Threats Evaluation species occurs. Its habitat includes (C), and collection and trade (B). These sections. There is no evidence to suggest environments protected from wave threats are expected to continue and that the species is so spatially action on at least upper reef slopes, mid- worsen into the future. In addition, the fragmented that depensatory processes, slope terraces, and lagoons. This species has inadequate existing environmental stochasticity, or the moderates vulnerability to extinction regulatory mechanisms for global threats potential for catastrophic events over the foreseeable future because the (D). currently pose a high risk to the survival species is not limited to one habitat type (2) Euphyllia paradivisa’s distribution of the species; and but occurs in numerous types of reef is limited mostly to the Coral Triangle, (2) While Euphyllia paradivisa’s environments that will, on local and which is projected to have the most qualitative abundance is rare, its regional scales, experience highly rapid and severe impacts from climate absolute abundance is millions of variable thermal regimes and ocean change and localized human impacts for colonies, which allows for some chemistry at any given point in time. Its coral reefs over the 21st century, as variation in the responses of individuals abundance of at least tens of millions of described in the Threats Evaluation. to threats. There is no evidence of colonies, combined with spatial Multiple ocean warming events have depensatory processes such as variability in ocean warming and already occurred within the Coral reproductive failure from low density of acidification across the species range, Triangle that suggest future ocean reproductive individuals and genetic moderates vulnerability to extinction warming events may be more severe processes such as inbreeding affecting because the increasingly severe than average in this part of the world. this species. Thus, its absolute conditions expected in the foreseeable A range constrained to this particular abundance indicates it is currently able

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to avoid high mortality from depth range. Physogyra lichtensteini is event (‘‘Back-cast Percent Population environmental stochasticity, and distributed from the Red Sea and the Reduction’’) was estimated at 15 mortality of a high proportion of its Indian Ocean to the western and central percent. However, as summarized above population from catastrophic events. Pacific Ocean. The SRR described P. in the Inter-basin Comparison sub- The combination of these characteristics lichtensteini’s habitat as turbid reef section, live coral cover trends are indicates that the species does not environments, crevices and overhangs, highly variable both spatially and exhibit the characteristics of one that is especially in turbid water with tidal temporally, producing patterns on small currently in danger of extinction, as currents, and shallow but shaded waters scales that can be easily taken out of described previously in the Risk such as caves on the GBR, with a depth context. Thus, quantitative inferences to Analyses section, and thus does not range of one to 20 meters. The SIR species-specific trends should be warrant listing as endangered at this added that the species is also known to interpreted with caution. At the same time. occur in clear water. time, an extensive body of literature Range-wide, a multitude of The public comments did not provide documents broad declines in live coral conservation efforts are already broadly any new or supplemental information cover and shifts to reef communities employed that are likely benefiting E. on P. lichtensteini’s distribution. We dominated by hardier coral species or paradivisa. However, considering the gathered supplemental information, algae over the past 50 to 100 years global scale of the most important including Veron (2014), which reports (Birkeland, 2004; Fenner, 2012; Pandolfi threats to the species, and the that P. lichtensteini is confirmed in 54 et al., 2003; Sale and Szmant, 2012). ineffectiveness of conservation efforts at of his 133 Indo-Pacific ecoregions, and These changes have likely occurred, and addressing the root cause of global strongly predicted to be found in an are occurring, from a combination of threats (i.e., greenhouse gas emissions), additional 18. In addition to shaded global and local threats. Given that P. we do not believe that any current habitats, including turbid and clear lichtensteini occurs in many areas conservation efforts or conservation water, P. lichtensteini also occurs in full affected by these broad changes, and efforts planned in the future will result sun (D. Fenner, personal comm.), thus likely has some susceptibility to global in affecting the species status to the the species occurs in variety of habitats. and local threats, we conclude that it is point at which listing is not warranted. Thus, based on all the available likely to have declined in abundance information, P. lichtensteini’s occurs in over the past 50 to 100 years, but a Genus Physogyra both turbid and clear upper reef slopes, precise quantification is not possible Genus Introduction mid-slopes, lower reef crests, reef flats, due to the limited species-specific lagoons, and caves in depth ranging The family Euphyllidae consists of information. from one to 20 m depth. five genera: Euphyllia, Catalaphyllia, Other Biological Information Nemenzophyllia, Plerogyra, and Demographic Information The SRR and SIR provided the Physogyra. The genus Physogyra is The SRR and SIR reported P. following information on P. monospecific, meaning it only includes lichtensteini’s abundance as common in lichtensteini’s life history. Physogyra P. lichtensteini (Veron, 2000), so there is turbid water and crevices and lichtensteini is a gonochoric broadcast no need to provide genus-level overhangs, especially in turbid water spawner. Larvae do not contain information. with tidal currents. zooxanthellae. The public comments Physogyra lichtensteini The public comments did not provide provided no additional biological any new or supplemental information information. We gathered supplemental Introduction on P. lichtensteini’s abundance. We information, including the following: The SRR and SIR provided the gathered supplemental information, Darling et al. (2012) found that P. following information on P. including Veron (2014), which reports lichtensteini has a ‘‘stress-tolerant’’ life lichtensteini’s morphology and that P. lichtensteini occupied 30.9 history strategy, defined as slow growth taxonomy. Morphology was described percent of 2,984 dive sites sampled in and large colonies which can survive as massive or thick, platy and 30 ecoregions of the Indo-Pacific, and through stress and disturbances. had a mean abundance rating of 1.31 on meandroid forms with short, widely Susceptibility to Threats separated valleys, and taxonomy was a 1 to 5 rating scale at those sites in described as having no taxonomic which it was found. Based on this semi- The SRR and SIR provided the issues, but being similar to Plerogyra quantitative system, the species’ following species-specific information sinuosa. abundance was characterized as on P. lichtensteini’s threats. Physogyra The public comments did not provide ‘‘common,’’ and overall abundance was lichtensteini has been identified as any new or supplemental information described as ‘‘common in protected vulnerable to extinction due to its high on morphology or taxonomy. We habitats.’’ Veron did not infer trends in bleaching rate, low diversity of its gathered supplemental information, abundance from these data. As genus, and narrow habitat range. The including Veron (2014), which states described in the Indo-Pacific Species species bleached at 31°C in Palau in that P. lichtensteini is one of the world’s Determinations introduction above, 1998. Physogyra lichtensteini contains most distinctive species. In addition, based on results from Richards et al. Clade C zooxanthellae in the South Veron (2000; 2014) considers the (2008) and Veron (2014), the absolute China Sea. Physogyra lichtensteini is species valid, thus we conclude it can abundance of this species is likely at preyed upon on by butterflyfish in be identified by experts and that the least tens of millions of colonies. Indonesia. Since P. lichtensteini prefers distribution and abundance information Carpenter et al. (2008) extrapolated turbid waters the risk of sediment described below for this species is species abundance trend estimates from impacts are low. The genus Physogyra is sufficiently reliable (Fenner, 2014b). total live coral cover trends and habitat heavily traded, primarily exported from types. For P. lichtensteini, the overall Indonesia. Between 1999 and 2010, the Spatial Information decline in abundance (‘‘Percent trade quota for Indonesia has been The SRR and SIR provided the Population Reduction’’) was estimated approximately 10,000 specimens following information on P. at 37 percent, and the decline in annually. The SRR and SIR also lichtensteini’s distribution, habitat, and abundance before the 1998 bleaching provided genus-level and coral-level

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information for the effects on Physogyra susceptibilities of P. lichtensteini to the extinction risk for P. lichtensteini are its of thermal stress, acidification, disease, threats. high bleaching rate and that it’s heavily collected. It listed factors that reduce predation, sedimentation, nutrients, and Regulatory Mechanisms collection and trade. The SRR and SIR potential extinction risk including that did not provide any other species- In the proposed rule, we did not P. lichtensteini has a wide latitudinal specific information on the effects of provide any species-specific distribution, is common, and tolerates these threats on P. lichtensteini. We information on the regulatory difficult (turbid) environments. interpreted the threat susceptibility and mechanisms or conservation efforts for Subsequent to the proposed rule, we exposure information from the SRR and P. lichtensteini. Criticisms of our received and gathered supplemental approach received during public SIR in the proposed rule for P. species- or genus-specific information, comment led us to attempt the following lichtensteini’s vulnerabilities as follows: described above, that expands our analysis of regulatory mechanisms on a High vulnerability to ocean warming; knowledge regarding the species species basis. Records confirm P. moderate vulnerability to disease, ocean abundance, distribution, and threat lichtensteini occurs in 54 Indo-Pacific susceptibilities. We developed our acidification, trophic effects of fishing, ecoregions that encompass 35 countries’ assessment of the species’ vulnerability and nutrients, low vulnerability to EEZs. The 35 countries are Australia, to extinction using all the available sedimentation, sea level rise, and Brunei, China, Egypt, Federated States information. As explained in the Risk collection and trade, and unknown of Micronesia, Fiji, France (French Analyses section, our assessment in this vulnerability to predation. Pacific Island Territories), India final rule emphasizes the ability of the Public comments did not provide any (including Andaman and Nicobar species’ spatial and demographic traits new or supplemental information on P. Islands), Indonesia, Israel, Japan, Jordan, to moderate or exacerbate its lichtensteini’s threat susceptibilities. We Kenya, Madagascar, Malaysia, Maldives, vulnerability to extinction, as opposed gathered supplemental information, Marshall Islands, Mauritius, Myanmar, to the approach we used in the which provided the following species- Palau, Papua New Guinea, Philippines, proposed rule, which emphasized the specific and genus-level information on Saudi Arabia, Seychelles, Solomon species’ susceptibility to threats. this species’ threat susceptibilities. Islands, Sri Lanka, Sudan, Taiwan, The following characteristics of P. Physogyra lichtensteini was not rated as Tanzania, Thailand, Timor-Leste, lichtensteini, in conjunction with the moderately or highly susceptible to United Kingdom (British Indian Ocean information described in the Corals and bleaching and coral disease by Territory), United States (PRIAs), Coral Reefs section, Coral Habitat sub- Carpenter et al. (2008), but they did not Vanuatu, and Vietnam. The regulatory section, and Threats Evaluation section have species-specific data. In the mechanisms relevant to P. lichtensteini, above, affect its vulnerability to western Indian Ocean in 1998–2005, the described first as the percentage of the extinction currently and over the genus Physogyra (which only includes above countries that utilize them to any foreseeable future. Its geographic P. lichtensteini) had a bleaching index degree and second, as the percentages of distribution includes most of the coral of 16.7 for eight countries, which was those countries whose regulatory reef ecoregions in the Indian Ocean and 19th highest of the 45 genera recorded, mechanisms may be limited in scope, western and central Pacific Ocean. Its and 45 percent of the highest value. In are as follows: General coral protection geographic distribution moderates this study, P. lichtensteini was (29 percent with 9 percent limited in vulnerability to extinction because some scope), coral collection (57 percent with identified as vulnerable to extinction areas within its range are projected to 29 percent limited in scope), pollution have less than average warming and due to its high bleaching rate, low control (43 percent with 9 percent acidification over the foreseeable future, diversity of its genus, and narrow limited in scope), fishing regulations on including the western Indian Ocean, the habitat range, and the genus Physogyra reefs (89 percent with 20 percent central Pacific, and other areas, so was rated as having the fifth highest limited in scope), managing areas for portions of the population in these areas extinction risk of the 45 genera in the protection and conservation (97 percent will be less exposed to severe study (McClanahan et al., 2007a). In with 11 percent limited in scope). The conditions. Its depth range is one to 20 Palau in 2000, P. lichtensteini most common regulatory mechanisms in meters. This moderates vulnerability to experienced very high levels of place for P. lichtensteini are reef fishing extinction over the foreseeable future bleaching and mortality. In that event, regulations and area management for because deeper areas of its range will 48 percent of all coral colonies of all protection and conservation. Coral usually have lower irradiance, and species were bleached, with bleaching collection and pollution control laws acidification is generally predicted to of different genera and species ranging are also somewhat utilized for the accelerate most in waters that are deeper from none to very high, and mortality species, but 29 percent of coral and cooler than those in which the from none to near 100 percent (Bruno et collection laws are limited in scope and species occurs. Its habitat includes both al., 2001). There are no other studies of may not provide substantial protection. turbid and clear upper reef slopes, mid- the effects of threats on this genus or General coral protection laws are less slopes, lower reef crests, reef flats, species. Based on the species-specific common regulatory mechanisms for the lagoons, and caves. This moderates information above, P. lichtensteini is management of P. lichtensteini. vulnerability to extinction over the likely highly susceptible to ocean foreseeable future because the species is warming. Based on the threat Vulnerability to Extinction not limited to one habitat type but susceptibility information for other reef- As explained above in the Risk occurs in numerous types of reef building coral genera in this final rule, Analyses section, a species’ environments that will, on local and P. lichtensteini likely has some vulnerability to extinction results from regional scales, experience highly susceptibility to disease, ocean the combination of its spatial and variable thermal regimes and ocean acidification, trophic effects of fishing, demographic characteristics, threat chemistry at any given point in time. Its sedimentation, nutrients, sea-level rise, susceptibilities, and consideration of the abundance of at least tens of millions of predation, and collection and trade. The baseline environment and future colonies, combined with spatial available information does not support projections of threats. The SRR stated variability in ocean warming and more precise ratings of the factors that increase the potential acidification across the species range,

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moderates vulnerability to extinction millions of colonies providing buffering longer be warranted. Finally, section because the increasingly severe capacity in the form of absolute 4(b)(1)(B) of the ESA requires us to give conditions expected in the foreseeable numbers of colonies and variation in consideration to species which (1) have future will be non-uniform and susceptibility between individual been designated as requiring protection therefore will likely be a large number colonies. As discussed in the Corals and from unrestricted commerce by any of colonies that are either not exposed Coral Reefs section above, the more foreign nation, or (2) have been or do not negatively respond to a threat colonies a species has, the lower the identified as in danger of extinction, or at any given point in time. proportion of colonies that are likely to likely to become so within the be exposed to a particular threat at a Listing Determination foreseeable future, by any state agency particular time, and all individuals that or by any agency of a foreign nation. All In the proposed rule using the are exposed will not have the same stony corals are listed under Appendix determination tool formula approach, P. response; and II of the Convention on International lichtensteini was proposed for listing as Notwithstanding the projections Trade in Endangered Species of Wild threatened because of: High through 2100 that indicate increased Fauna and Flora, which regulates vulnerability to ocean warming (ESA severity over time of the three high international trade of species to ensure Factor E); moderate vulnerability to importance threats, the combination of survival. Dendrogyra cylindrus, which disease (C) and acidification (E); these biological and environmental we are listing as threatened, is also common generalized range wide characteristics indicates that the species listed as threatened by the State of abundance (E); wide overall distribution possesses sufficient buffering capacity Florida and all stony corals are (based on wide geographic distribution to avoid being in danger of extinction protected under the U.S. Virgin Islands and moderate depth distribution (E); within the foreseeable future throughout Indigenous and Endangered Species Act and inadequacy of existing regulatory its range. It is possible that this species’ of 1990. All of the corals in this final mechanisms (D). extinction risk may increase in the rule, including those we are listing In this final rule, we changed the future if global threats continue and under the ESA, are listed in the IUCN listing determination for P. lichtensteini increase in severity and the species Red List of Threatened Species as from threatened to not warranted. We exposure to threats increases throughout vulnerable, endangered, or critically made this determination based on a its range. Should the species experience endangered. The final rule takes into more species-specific and holistic reduced abundance or range consideration this information in its assessment of whether this species constriction of a certain magnitude, the listing determinations. meets the definition of either a ability of these characteristics to threatened or endangered coral largely moderate exposure to threats will In the proposed rule we determined in response to public comments, diminish. However, the species is not that 12 species warranted listing as including more appropriate likely to become of such low abundance endangered: five in the Caribbean consideration of the buffering capacity or so spatially fragmented as to be in (Dendrogyra cylindrus, Orbicella of this species’ spatial and demographic danger of extinction due to depensatory annularis, Orbicella faveolata, Orbicella traits to lessen its vulnerability to processes, the potential effects of franksi, and Mycetophyllia ferox); and threats. Thus, based on the best environmental stochasticity, or the seven in the Indo-Pacific (Millepora available information above on P. potential for mortality from catastrophic foveolata, Pocillopora elegans (eastern lichtensteini’s spatial structure, events within the foreseeable future Pacific), Acropora jacquelineae, demography, threat susceptibilities, and throughout its range. Therefore, P. Acropora lokani, Acropora rudis, management, none of the five ESA lichtensteini is not warranted for listing Anacropora spinosa, and Euphyllia listing factors, alone or in combination, at this time under any of the listing paradivisa). We also determined that 54 are causing this species to be likely to factors. species warranted listing as threatened: become endangered throughout its range two in the Caribbean (Agaricia lamarcki within the foreseeable future, and thus Summary of Determinations and Dichocoenia stokesii); and 52 in the it is not warranted for listing at this In this final rule, we are responsible Indo-Pacific (Millepora tuberosa, time, because: for determining whether each of the Pocillopora danae, Pocillopora elegans (1) Physogyra lichtensteini’s proposed coral species meet the (Indo-Pacific), Seriatopora aculeata, distribution across the Red Sea, Indian definition of either threatened or Acropora aculeus, Acropora acuminata, Ocean and most of the Pacific is spread endangered under the ESA based on the Acropora aspera, Acropora dendrum, over a very large area. While some areas best available information including Acropora donei, Acropora globiceps, within its range are projected to be that which supported the proposed rule, Acropora horrida, Acropora listeri, affected by warming and acidification, and public comments received and Acropora microclados, Acropora other areas are projected to have less information we gathered since the palmerae, Acropora paniculata, than average warming and acidification, proposed rule was published. Section Acropora pharaonis, Acropora including the western Indian Ocean, the 4(b)(1)(A) of the ESA requires us to polystoma, Acropora retusa, Acropora central Pacific, and other areas. This make listing determinations based speciosa, Acropora striata, Acropora distribution and the heterogeneous solely on the best scientific and tenella, Acropora vaughani, Acropora habitats it occupies reduce exposure to commercial data available after verweyi, Anacropora puertogalerae, any given threat event or adverse conducting reviews of the statuses of the Astreopora cucullata, Isopora condition that does not occur uniformly species and after taking into account crateriformis, Isopora cuneata, throughout the species range. As efforts being made by any state or Montipora angulata, Montipora explained above in the Threats foreign nation to protect the species. We australiensis, Montipora calcarea, Evaluation section, we have not conclude that conservation efforts are Montipora caliculata, Montipora identified any threat that is expected to not protecting any of the coral species dilatata/flabellata/turgescens, occur uniformly throughout the species determined to be warranted for listing in Montipora lobulata, Montipora patula/ range within the foreseeable future); this final rule in a way that would verrilli, Alveopora allingi, Alveopora (2) Physogyra lichtensteini’s total reduce extinction risk such that a fenestrata, Alveopora verrilliana, Porites absolute abundance is at least tens of threatened determination would no horizontalata, Porites napopora, Porites

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nigrescens, Acanthastrea brevis, determinable due to taxonomic be designated to the maximum extent Acanthastrea hemprichii, Acanthastrea uncertainty (Pocillopora danae, prudent and determinable, for species ishigakiensis, Acanthastrea regularis, Pocillopora elegans (eastern Pacific), that occur in U.S. jurisdiction. Pachyseris rugosa, Pectinia alcicornis, Pocillopora elegans (Indo-Pacific)). Protective regulations for threatened Barabattoia laddi, Pavona diffluens, As described previously in the Risk corals may be developed for the Caulastrea echinulata, Euphyllia Analyses section, in this final rule we conservation of the species. Federal, cristata, Euphyllia paraancora, and took a more holistic approach in state and private sector cooperation and Physogyra lichtensteini). Finally, we response to public comments and participation will be necessary to determined that two species in the reconsidered these coral species’ effectively and efficiently conserve the Caribbean currently listed as threatened demographic and distribution traits that listed coral species and the ecosystems (Acropora palmata and Acropora buffer or moderate exposure to threats, upon which they depend. cervicornis) warranted reclassification and the resulting capacity to respond to changing conditions into the foreseeable Identifying Section 7 Consultation as endangered. Requirements In this final rule we have determined future. This approach led to changes in Section 7(a)(2) of the ESA and NMFS/ that no species warrants listing as listing status from the proposed rule for FWS regulations require Federal endangered. We have determined the 58 of the 68 species while agencies to consult with us on any following 20 species warrant listing as determinations for 10 species remained actions they authorize, fund, or carry threatened: five in the Caribbean the same. While in some cases, a warranted species possesses one out if those actions may affect the listed (Dendrogyra cylindrus, Orbicella particularly compelling characteristic species or designated critical habitat. annularis, Orbicella faveolata, Orbicella that increases its vulnerability to Based on currently available franksi, and Mycetophyllia ferox); and extinction (e.g., a small effective information, examples of Federal 15 in the Indo-Pacific (Acropora population size, a depth restriction to actions that may affect the 22 coral globiceps, Acropora jacquelineae, shallow waters, or a highly constrained species listed as threatened include, but Acropora lokani, Acropora pharaonis, geographic range), no one factor in are not limited to: Energy projects, Acropora retusa, Acropora rudis, isolation led to a species being discharge of pollution from point Acropora speciosa, Acropora tenella, warranted for listing and the final sources, non-point source pollution, Anacropora spinosa, Euphyllia determinations are all based on the suite dredging, pile-driving, setting of water paradivisa, Isopora crateriformis, of demographic, spatial, and quality standards, vessel traffic, Montipora australiensis, Pavona susceptibility components that aquaculture facilities, military activities, diffluens, Porites napopora, and influence the species’ vulnerability to and fisheries management practices. Seriatopora aculeata). For the two extinction in the face of continuing Critical Habitat species in the Caribbean currently listed threats over the foreseeable future. as threatened (Acropora cervicornis and Similarly, many of the not warranted Critical habitat is defined in section 3 Acropora palmata), through this final species either lack one compelling of the ESA as: ‘‘(i) the specific areas rule we have conducted an updated characteristic that increases within the geographical area occupied status review and threats assessment, vulnerability to extinction or possess by the species, at the time it is listed in and determined they still warrant listing one or more compelling characteristics accordance with the provisions of as threatened. We also determined that that reduce vulnerability to extinction section 1533 of this title, on which are 43 proposed species do not warrant (e.g., a vast geographic distribution, low found those physical or biological listing as endangered or threatened: two susceptibility to high importance features (I) essential to the conservation in the Caribbean (Agaricia lamarcki, threats, a depth range extending into of the species and (II) which may Dichocoenia stokesii); and 41 in the deeper waters, or a large absolute require special management Indo-Pacific (Acanthastrea brevis, abundance estimate), but no one factor considerations or protection; and (ii) Acanthastrea hemprichii, Acanthastrea in isolation led to a species being not specific areas outside the geographical ishigakiensis, Acanthastrea regularis, warranted for listing and the final area occupied by the species at the time Acropora aculeus, Acropora acuminata, determinations are all based on the suite it is listed in accordance with the Acropora aspera, Acropora dendrum, of demographic, spatial, and provisions of 1533 of this title, upon a Acropora donei, Acropora horrida, susceptibility components that determination by the Secretary that such Acropora listeri, Acropora microclados, influence the species’ vulnerability to areas are essential for the conservation Acropora palmerae, Acropora extinction, in the face of continuing of the species’’ (16 U.S.C. 1532(5)(A)). paniculata, Acropora polystoma, threats over the foreseeable future. ‘‘Conservation’’ means the use of all Acropora striata, Acropora vaughani, methods and procedures needed to Acropora verweyi, Alveopora allingi, Effects of Listing bring the species to the point at which Alveopora fenestrata, Alveopora Conservation measures provided for listing under the ESA is no longer verrilliana, Anacropora puertogalerae, species listed as endangered or necessary (16 U.S.C. 1532(3)). Section Astreopora cucullata, Barabattoia laddi, threatened under the ESA may include 4(a)(3)(A) of the ESA requires that, to Caulastrea echinulata, Euphyllia recovery plans (16 U.S.C. 1553(f)), the maximum extent prudent and cristata, Euphyllia paraancora, Isopora critical habitat designations, Federal determinable, critical habitat be cuneata, Millepora foveolata, agency consultation requirements (16 designated concurrently with the final Millepora tuberosa, Montipora angulata, U.S.C. 1536), and prohibitions on taking listing of a species (16 U.S.C. Montipora calcarea, Montipora (16 U.S.C. 1538). Recognition of the 1533(a)(3)(A)(i)). Further, ESA caliculata, Montipora dilatata/ species’ plight through listing promotes implementing regulations at 50 CFR flabellata/turgescens, Montipora conservation actions by Federal and 424.12(h) specify that critical habitat lobulata, Montipora patula/verrilli, state agencies, private groups, and shall not be designated within foreign Pachyseris rugosa, Pectinia alcicornis, individuals, as well as the international countries or in other areas outside of Physogyra lichtensteini, Porites community. For listed species, a U.S. jurisdiction. horizontalata, and Porites nigrescens). recovery program could be The existing designated critical Three coral species were not implemented, and critical habitat will habitat for Acropora palmata and A.

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cervicornis in the Caribbean (50 CFR may include applying some or all of the life history characteristics within the 226.216) remains effective with this section 9 prohibitions to these species. following general categories of habitat final rule. The designation of critical Therefore, pursuant to ESA section 4(d), features: (1) Space for individual growth habitat is not determinable for any of subsequent to this rulemaking we will and for normal behavior; (2) food, water, the newly listed corals at this time due evaluate whether there are protective air, light, minerals, or other nutritional to the extremely complex biological and regulations necessary and advisable for or physiological requirements; (3) cover physical requirements of the species. the conservation of any of the 20 species or shelter; (4) sites for reproduction and Although we have gathered information newly-listed as threatened in this final development of offspring; and (5) through the status review and public rule, including application of some or habitats that are protected from comment processes on the habitats all of the take prohibitions. The existing disturbance or are representative of the occupied by these species, we currently 4(d) rule for Acropora palmata and A. historical, geographical, and ecological do not have enough information to cervicornis (50 CFR 223.208) will distributions of the species (50 CFR determine which of features within remain in effect for these threatened 424.12(b)). ESA implementing those habitats are essential to the species. regulations at 50 CFR 424.12(h) specify conservation of any of the listed corals Policies on Role of Peer Review that critical habitat shall not be and may require special management designated within foreign countries or considerations or protection. We will In December 2004, the Office of in other areas outside of U.S. continue to gather and review other Management and Budget (OMB) issued jurisdiction. Therefore, we request ongoing studies on the habitat use and a Final Information Quality Bulletin for information only on potential areas of requirements of the newly listed corals Peer Review establishing minimum peer critical habitat within waters in U.S. to attempt to identify these features. review standards, a transparent process jurisdiction. Additionally, we need more time to for public disclosure of peer review gather the information needed to planning, and opportunities for public For features and areas potentially perform the required analyses of the participation. The OMB Bulletin, qualifying as critical habitat, we also impacts of the designation. Designations implemented under the Information request information describing: (1) of critical habitat must be based on the Quality Act (Public Law 106–554) is Activities or other threats to the best scientific data available and must intended to enhance the quality and essential features or activities that could take into consideration the economic, credibility of the Federal government’s be affected by designating them as national security, and other relevant scientific information, and applies to critical habitat, and (2) the positive and impacts of specifying any particular area influential or highly influential negative economic, national security as critical habitat. To the maximum scientific information disseminated on and other relevant impacts, including extent prudent and determinable, we or after June 16, 2005. To satisfy our benefits to the recovery of the species, will publish proposed designations of requirements under the OMB Bulletin, likely to result if these areas are critical habitat for the newly listed the BRT obtained independent peer designated as critical habitat. review of the draft Status Review corals in a separate rule or rules. Once Classification critical habitat is designated (only in Report, and NMFS obtained U.S. jurisdictions), section 7 of the ESA independent peer review of the draft National Environmental Policy Act requires Federal agencies to ensure that Management Report. Independent they do not fund, authorize, or carry out specialists were selected from the The 1982 amendments to the ESA, in any actions that are likely to destroy or academic and scientific community, section 4(b)(1)(A), restrict the adversely modify that habitat. This Federal and state agencies, and/or the information that may be considered requirement is in addition to the section private sector for this review. All peer when assessing species for listing. Based 7 requirement that Federal agencies reviewer comments were addressed on this limitation of criteria for a listing ensure that their actions are not likely prior to dissemination of the final SRR decision and NOAA Administrative to jeopardize the continued existence of and Management Report. Order 216–6 (Environmental Review listed species. We determined that the peer review Procedures for Implementing the conducted pursuant to the OMB National Environmental Policy Act), we ESA Section 9 Take Prohibitions Bulletin also satisfied the requirements have concluded that ESA listing actions ESA section 9(a) take prohibitions (16 of the Services’ 1994 policy for peer are not subject to requirements of the U.S.C. 1538(a)(1)(B)) apply to all species review of scientific data included in National Environmental Policy Act. listed as endangered. These section 9(a) listing decisions (59 FR 34270). Executive Order 12866, Regulatory prohibitions include prohibitions Flexibility Act, and Paperwork against importing, exporting, engaging Solicitation of Information Reduction Act in foreign or interstate commerce, or We are soliciting information on ‘‘taking’’ of the species. ‘‘Take’’ is features and areas that may support As noted in the Conference Report on defined under the ESA as ‘‘to harass, designations of critical habitat for the 20 the 1982 amendments to the ESA, harm, pursue, hunt, shoot, wound, kill, newly listed coral species. Information economic impacts cannot be considered trap, capture, or collect, or attempt to provided should identify the physical when assessing the status of a species. engage in any such conduct.’’ These and biological features essential to the Therefore, the economic analysis prohibitions apply to all persons subject conservation of the species and areas requirements of the Regulatory to the jurisdiction of the United States, that contain these features for the coral Flexibility Act are not applicable to including in the United States, its species proposed to be listed. Areas listing actions. territorial sea, or on the high seas. In the outside the occupied geographical area case of threatened species, section 9 should also be identified if such areas In addition, this final rule is exempt prohibitions do not automatically apply. themselves are essential to the from review under E.O. 12866. Section 4(d) of the ESA directs the conservation of the species. Essential This final determination does not Secretary to issue regulations she features may include, but are not contain a collection of information considers necessary and advisable for limited to, features specific to requirement for the purposes of the the conservation of the species, which individual species’ ranges, habitats and Paperwork Reduction Act.

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Executive Order 13132, Federalism Executive Order 12898, Environmental PART 223—THREATENED MARINE In accordance with E.O. 13132, Justice AND ANADROMOUS SPECIES agencies are required to take into Executive Order 12898 requires that account any federalism impacts of Federal actions address environmental ■ 1. The authority citation for part 223 regulations under development. This justice in the decision-making process. continues to read as follows: Executive Order includes specific In particular, the environmental effects Authority: 16 U.S.C. 1531–1543; subpart B, consultation directives for situations of the actions should not have a § 223.201–202 also issued under 16 U.S.C. where a regulation will preempt state disproportionate effect on minority and 1361 et seq.; 16 U.S.C. 5503(d) for law, or impose substantial direct low-income communities. This final § 223.206(d)(9). compliance costs on state and local rule is not expected to have a governments (unless required by disproportionately high effect on ■ 2. In § 223.102, in the table, amend statute). Neither of those circumstances minority populations or low-income paragraph (e) by removing the two is applicable to this final listing populations. existing entries under the ‘‘Corals’’ determination. In keeping with the subheading and adding the following 22 intent of the Administration and List of Subjects in 50 CFR Part 223 entries to read as follows: Congress to provide continuing and Endangered and threatened species; meaningful dialogue on issues of mutual Exports; Imports; Transportation. § 223.102 Enumeration of threatened state and Federal interest, the proposed Dated: August 26, 2014. marine and anadromous species. rule was provided to the relevant * * * * * agencies in each state in which the Eileen Sobeck, subject species occurs, and these Assistant Administrator for Fisheries, (e) * * * agencies were invited to comment. National Marine Fisheries Service. Their comments were addressed with For the reasons set out in the other comments in the Summary of preamble, 50 CFR part 223 is amended Comments Received section. as follows:

Species 1 Citation(s) for listing Critical ESA rules Common name Scientific name Description of listed entity determination(s) habitat

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Corals

Coral, [no common name] .. Acropora globiceps ...... Entire species ...... [Insert FR citation] NA NA 9/10/2014 Coral, [no common name] .. Acropora jacquelineae ...... Entire species ...... [Insert FR citation] NA NA 9/10/2014 Coral, [no common name] .. Acropora lokani ...... Entire species ...... [Insert FR citation] NA NA 9/10/2014 Coral, [no common name] .. Acropora pharaonis ...... Entire species ...... [Insert FR citation] NA NA 9/10/2014 Coral, [no common name] .. Acropora retusa ...... Entire species ...... [Insert FR citation] NA NA 9/10/2014 Coral, [no common name] .. Acropora rudis ...... Entire species ...... [Insert FR citation] NA NA 9/10/2014 Coral, [no common name] .. Acropora speciosa ...... Entire species...... [Insert FR citation] NA NA 9/10/2014 Coral, [no common name] .. Acropora tenella ...... Entire species...... [Insert FR citation] NA NA 9/10/2014 Coral, [no common name] .. Anacropora spinosa ...... Entire species ...... [Insert FR citation] NA NA 9/10/2014 Coral, [no common name] .. Euphyllia paradivisa ...... Entire species ...... [Insert FR citation] NA NA 9/10/2014 Coral, [no common name] .. Isopora crateriformis ...... Entire species...... [Insert FR citation] NA NA 9/10/2014 Coral, [no common name] .. Montipora australiensis ...... Entire species...... [Insert FR citation] NA NA 9/10/2014 Coral, [no common name] .. Pavona diffluens ...... Entire species ...... [Insert FR citation] NA NA 9/10/2014 Coral, [no common name] .. Porites napopora ...... Entire species ...... [Insert FR citation] NA NA 9/10/2014 Coral, [no common name] .. Seriatopora aculeata ...... Entire species ...... [Insert FR citation] NA NA 9/10/2014 Coral, boulder star ...... Orbicella franksi ...... Entire species ...... [Insert FR citation] NA NA 9/10/2014 Coral, elkhorn ...... Acropora palmata ...... Entire species ...... [Insert FR citation] 226.216 223.208 9/10/2014 Coral, lobed star ...... Orbicella annularis ...... Entire species ...... [Insert FR citation] NA NA 9/10/2014

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Species 1 Citation(s) for listing Critical ESA rules Common name Scientific name Description of listed entity determination(s) habitat

Coral, mountainous star ...... Orbicella faveolata ...... Entire species ...... [Insert FR citation & NA NA date of publication in the Federal Reg- ister Coral, pillar ...... Dendrogyra cylindrus ...... Entire species ...... [Insert FR citation] NA NA 9/10/2014 Coral, rough cactus ...... Mycetophyllia ferox ...... Entire species ...... [Insert FR citation] NA NA 9/10/2014 Coral, staghorn ...... Acropora cervicornis ...... Entire species ...... [Insert FR citation] 226.216 223.208 9/10/2014

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* * * * * [FR Doc. 2014–20814 Filed 9–9–14; 8:45 am] BILLING CODE 3510–22–P

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