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Vol. 79 Tuesday, No. 241 December 16, 2014

Part IV

Department of Commerce

National Oceanic and Atmospheric Administration 50 CFR Parts 223 and 224 Endangered and Threatened Wildlife and Plants; 12-Month Finding for the Eastern Taiwan Strait Indo-Pacific Humpback Dolphin, Dusky Sea , Banggai Cardinalfish, Harrisson’s Dogfish, and Three Corals Under the Endangered Act; Proposed Rule

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DEPARTMENT OF COMMERCE DATES: Comments on our proposed rule of status reviews for each of the 27 to list eight species must be received by species (78 FR 63941, October 25, 2013; National Oceanic and Atmospheric February 17, 2015. Public hearing 78 FR 66675, November 6, 2013; 78 FR Administration requests must be made by January 30, 69376, November 19, 2013; 79 FR 9880, 2015. February 21, 2014; and 79 FR 10104, 50 CFR Parts 223 and 224 ADDRESSES: You may submit comments February 24, 2014). This document [Docket No. 140707555–4999–01] on this document, identified by NOAA– addresses the findings for 7 of those 27 NMFS–2014–0083, by any of the species: the Eastern Taiwan Strait RIN 0648–XD370 following methods: population of Indo-Pacific humpback • dolphin (Sousa chinensis), dusky sea Endangered and Threatened Wildlife Electronic Submissions: Submit all electronic public comments via the snake ( fuscus), Banggai and Plants; 12-Month Finding for the cardinalfish (Pterapogon kauderni), Eastern Taiwan Strait Indo-Pacific Federal eRulemaking Portal. Go to www.regulations.gov/ Harrisson’s dogfish (Centrophorus Humpback Dolphin, Dusky , harrissoni), and the corals Cantharellus Banggai Cardinalfish, Harrisson’s #!docketDetail;D=NOAA-NMFS-2014- 0083. Click the ‘‘Comment Now’’ icon, noumeae, Siderastrea glynni, and Dogfish, and Three Corals Under the Tubastraea floreana. The remaining 20 Endangered Species Act complete the required fields, and enter or attach your comments. species will be addressed in subsequent findings. AGENCY: National Marine Fisheries • Mail: Submit written comments to, We are responsible for determining Service (NMFS), National Oceanic and Lisa Manning, NMFS Office of Protected whether species are threatened or Atmospheric Administration (NOAA), Resources (F/PR3), 1315 East West endangered under the ESA (16 U.S.C. Commerce. Highway, Silver Spring, MD 20910, USA. 1531 et seq.). To make this ACTION: Proposed rule; 12-month determination, we consider first petition finding; request for comments. Instructions: You must submit comments by one of the above methods whether a group of organisms constitutes a ‘‘species’’ under the ESA, SUMMARY: We, NMFS, have completed to ensure that we receive, document, then whether the status of the species comprehensive status reviews under the and consider them. Comments sent by qualifies it for listing as either Endangered Species Act (ESA) for seven any other method, to any other address threatened or endangered. Section 3 of foreign marine species in response to a or individual, or received after the end of the comment period, may not be the ESA defines a ‘‘species’’ to include petition to list those species. These ‘‘any of fish or wildlife or seven species are the Eastern Taiwan considered. All comments received are a part of the public record and will plants, and any distinct population Strait population of Indo-Pacific segment of any species of vertebrate fish humpback dolphin (Sousa chinensis), generally be posted for public viewing on http://www.regulations.gov without or wildlife which interbreeds when dusky sea snake (), mature.’’ On February 7, 1996, NMFS Banggai cardinalfish (Pterapogon change. All personal identifying information (e.g., name, address, etc.), and the U.S. Fish and Wildlife Service kauderni), Harrisson’s dogfish (USFWS; together, the Services) adopted confidential business information, or (Centrophorus harrissoni), and the a policy describing what constitutes a otherwise sensitive information corals Cantharellus noumeae, distinct population segment (DPS) of a submitted voluntarily by the sender will Siderastrea glynni, and Tubastraea taxonomic species (the DPS Policy; 61 be publicly accessible. We will accept floreana. We have determined that the FR 4722). The DPS Policy identified two anonymous comments (enter ‘‘N/A’’ in Eastern Taiwan Strait Indo-Pacific elements that must be considered when the required fields if you wish to remain humpback dolphin is not a distinct identifying a DPS: (1) The discreteness anonymous). Attachments to electronic population segment and therefore does of the population segment in relation to comments will be accepted in Microsoft not warrant listing. We have determined the remainder of the species (or Word, Excel, or Adobe PDF file formats that, based on the best scientific and subspecies) to which it belongs; and commercial data available, and after only. (2) the significance of the population You can obtain the petition, status taking into account efforts being made segment to the remainder of the species review reports, the proposed rule, and to protect the species, Pterapogon (or subspecies) to which it belongs. As the list of references electronically on kauderni, and Centrophorus harrissoni stated in the DPS Policy, Congress our NMFS Web site at http:// meet the definition of a threatened expressed its expectation that the www.nmfs.noaa.gov/pr/species/ species; and Aipysurus fuscus, Services would exercise authority with petition81.htm. Cantharellus noumeae, Siderastrea regard to DPSs sparingly and only when glynni, and Tubastraea floreana meet FOR FURTHER INFORMATION CONTACT: Lisa the biological evidence indicates such the definition of an endangered species. Manning, NMFS, Office of Protected action is warranted. Therefore, we propose to list these six Resources (OPR), (301) 427–8403. Section 3 of the ESA defines an species under the ESA. We are not SUPPLEMENTARY INFORMATION: endangered species as ‘‘any species proposing to designate critical habitat which is in danger of extinction for any of the species proposed for Background throughout all or a significant portion of listing, because the geographical areas On July 15, 2013, we received a its range’’ and a threatened species as occupied by these species are entirely petition from WildEarth Guardians to one ‘‘which is likely to become an outside U.S. jurisdiction, and we have list 81 marine species as threatened or endangered species within the not identified any unoccupied areas that endangered under the Endangered foreseeable future throughout all or a are currently essential to the Species Act (ESA). This petition significant portion of its range.’’ We conservation of any of these species. We included species from many different interpret an ‘‘endangered species’’ to be are soliciting comments on our taxonomic groups, and we prepared our one that is presently in danger of proposals to list the six species. We are 90-day findings in batches by taxonomic extinction. A ‘‘threatened species,’’ on also proposing related administrative group. We found that the petitioned the other hand, is not presently in changes to our lists of threatened and actions may be warranted for 27 of the danger of extinction, but is likely to endangered species. 81 species and announced the initiation become so in the foreseeable future (that

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is, at a later time). In other words, the of our status reviews, including for biology, ecology, life history, threats, primary statutory difference between a Pacific salmonids, Pacific hake, walleye and conservation status from threatened and endangered species is pollock, Pacific cod, Puget Sound information contained in the petition, the timing of when a species may be in rockfishes, Pacific herring, scalloped our files, a comprehensive literature danger of extinction, either presently hammerhead sharks, and black abalone search, and consultation with experts. (endangered) or in the foreseeable future (see http://www.nmfs.noaa.gov/pr/ We also considered information (threatened). species/ for links to these reviews). In submitted by the public in response to When we consider whether species this approach, the collective condition our petition findings. Draft status review might qualify as threatened under the of individual populations is considered reports were also submitted to ESA, we must consider the meaning of at the species level according to four independent peer reviewers; comments the term ‘‘foreseeable future.’’ It is demographic viability factors: and information received from peer appropriate to interpret ‘‘foreseeable Abundance, growth rate/productivity, reviewers were addressed and future’’ as the horizon over which spatial structure/connectivity, and incorporated as appropriate before predictions about the conservation diversity. These viability factors reflect finalizing the draft reports. status of the species can be reasonably concepts that are well-founded in Each status review report provides a relied upon. The foreseeable future conservation biology and that thorough discussion of demographic considers the life history of the species, individually and collectively provide risks and threats to the particular habitat characteristics, availability of strong indicators of extinction risk. species. We considered all identified data, particular threats, ability to predict We then assess efforts being made to threats, both individually and threats, and the reliability to forecast the protect the species, to determine if these cumulatively, to determine whether the effects of these threats and future events conservation efforts are adequate to species responds in a way that causes on the status of the species under mitigate the existing threats. Section actual impacts at the species level. The consideration. Because a species may be 4(b)(1)(A) of the ESA requires the collective condition of individual susceptible to a variety of threats for Secretary, when making a listing populations was also considered at the which different data are available, or determination for a species, to take into species level, according to the four which operate across different time consideration those efforts, if any, being demographic viability factors discussed scales, the foreseeable future is not made by any State or foreign nation to above. necessarily reducible to a particular protect the species. We also evaluate The status review reports are available number of years. Discussions of the conservation efforts that have not yet on our Web site (see ADDRESSES considerations for each relevant species been fully implemented or shown to be section). Below we summarize are in the species-specific sections effective using the criteria outlined in information from those reports and the below. the joint NMFS/USFWS Policy for status of each species. Section 4(a)(1) of the ESA requires us Evaluating Conservation Efforts (PECE; Eastern Taiwan Strait Population of the to determine whether any species is 68 FR 15100, March 28, 2003), to Indo-Pacific Humpback Dolphin endangered or threatened due to any determine their certainty of one or a combination of the following implementation and effectiveness. The The following section describes our five threat factors: The present or PECE is designed to ensure consistent analysis of the status of the Eastern threatened destruction, modification, or and adequate evaluation of whether any Taiwan Strait (ETS) population of the curtailment of its habitat or range; conservation efforts that have been Indo-Pacific Humpback dolphin, Sousa overutilization for commercial, recently adopted or implemented, but chinensis. recreational, scientific, or educational not yet demonstrated to be effective, Species Description purposes; disease or predation; the will result in recovering the species to inadequacy of existing regulatory the point at which listing is not The Indo-Pacific humpback dolphin, mechanisms; or other natural or warranted or contribute to forming the Sousa chinensis (Osbeck, 1765), within manmade factors affecting its continued basis for listing a species as threatened the Sousa, family Delphinidae, existence. We are also required to make rather than endangered. The two basic and order Cetacea, is broadly listing determinations based solely on criteria established by the PECE are: (1) distributed. The of the genus the best scientific and commercial data The certainty that the conservation is unresolved and has historically been available, after conducting a review of efforts will be implemented; and (2) the based on morphology, but genetic the species’ status and after taking into certainty that the efforts will be analyses have recently been used. account efforts being made by any state effective. We consider these criteria in Current taxonomic hypotheses identify or foreign nation to protect the species. each species-specific section, as Sousa chinensis as one of two (Jefferson In making a listing determination, we applicable, below. Finally, we re-assess et al., 2001), three (Rice, 1998), or four first determine whether a petitioned the extinction risk of the species in light (Mendez et al., 2013) species within the species meets the ESA definition of a of the existing conservation efforts. genus. Each species is associated with a ‘‘species.’’ Next, using the best available unique geographic range, though the information gathered during the status Status Reviews species’ defined ranges vary depending review for the species, we complete a Status reviews for the petitioned on how many species are recognized. status and extinction risk assessment. In species addressed in this finding were Rice (1998) recognizes Sousa teuzii in assessing extinction risk, we consider conducted by NMFS OPR staff. Separate the eastern Atlantic, Sousa plumbea in the demographic viability factors status reviews were done for the Eastern the western Indo-Pacific, and Sousa developed by McElhany et al. (2000) Taiwan Strait Indo-Pacific humpback chinensis in the eastern Indo-Pacific. and the risk matrix approach developed dolphin (Whittaker, 2014), dusky sea Mendez et al. (2013) recently identified by Wainwright and Kope (1999) to snake (Manning, 2014), Banggai an as-yet unnamed potential new organize and summarize extinction risk cardinalfish (Conant, 2014), Harrison’s species in waters off of northern considerations. The approach of dogfish (Miller, 2014), and the three . Currently, the International considering demographic risk factors to corals (Meadows, 2014). In order to Union for Conservation of Nature help frame the consideration of complete the status reviews, we (IUCN) and International Whaling extinction risk has been used in many compiled information on the species’ Commission (IWC) Scientific Committee

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recognize only two species, Sousa lagoons, and sandy beaches (Ross et al., opportunistic piscivore (Barros et al., chinensis in the Indo-Pacific, and Sousa 1994). In Thailand, Malaysia, and 2004). As is common to the species as teuzii in the eastern Atlantic. Here, we , nearshore ecosystems are a whole, the ETS population uses follow a similar two-species taxonomy associated with tropical seagrass, coral, echolocation and passive listening to in our consideration of the genus and and mangrove lagoons (Beasley et al., find its prey. While little is known identification of the species Sousa 1997; Smith et al., 2003; Adulyanukosol about the specific diet and feeding of chinensis. Under that taxonomy, Sousa et al., 2006; Jaroensutasinee et al., 2011; the ETS population, diet can be inferred chinensis’ range includes nearshore Cherdsukai et al., 2013). In India, the from that of other humpback dolphin tropical and subtropical habitats in species is associated with nearshore populations (Barros et al., 2004; Chen et southern Africa, the Indian Ocean, habitat consisting of mangroves, corals, al., 2009). In Chinese waters off Hong North Australia, southern mainland and tidal mudflat, heavily influenced by Kong, the species consumes both China, Hong Kong, and Taiwan monsoons that regulate the influx of bottom-dwelling and pelagic fish (Jefferson et al., 2001; Mendez et al., freshwater to the system (Sutaria et al., species, including croakers (Sciaenidae), 2013). We chose to follow a two-species 2004). The coast of mainland China is mullets (Mugilidae), threadfins taxonomy as it provides the clearest thought to host at least eight (Polynemidae), and herring (Clupeidae) genetic, morphological, and geographic populations of the species, primarily (Barros et al., 2004). Part of the feeding delineation of the species and is well occurring in estuarine systems at the strategy for this population may be to supported by the current data available. mouths of large rivers (Jefferson et al., induce shoaling of fish by physically While growing genetic and 2001; Jefferson et al., 2004a). Two corralling them, allowing individuals to phylogeographic evidence suggests that coastal Chinese populations, in close forage and feed successfully, even Sousa chinensis is associated with proximity to the population in the within murky nearshore waters (Sheehy, further genetic subdivisions, more data Eastern Taiwan Strait, are relatively 2009). In general, the prey species of the are needed to clarify the taxonomy and well-studied. These are the Pearl River humpback dolphin include small fish delineate the geographic boundaries and Estuary/Hong Kong population and the which are generally not commercially ranges of these additional genetic units Jiulong River Estuary/Xaimen valuable to local fisheries (Barros et al., (Cockroft et al., 1997; Jefferson et al., population, both of which depend upon 2004; Sheehy, 2009). 2004b; Fre`re et al., 2008; Fre`re et al., ecosystem productivity associated with Little is known about the life history 2011; Lin et al., 2012; Mendez et al., the nutrient output supplied by large and reproduction of ETS humpback 2013). rivers (Chen et al., 2008; Chen et al., dolphin. In some cases, comparison of The Indo-Pacific humpback dolphin 2010). is easy to distinguish from other The Eastern Taiwan Strait population the ETS population with other dolphin species in its range, as it is of Sousa chinensis (henceforth referred populations may be appropriate, but one characterized by a robust body, a long, to as the ETS humpback dolphin), for needs to be cautious about making these distinct beak, a short dorsal fin atop a which we were petitioned, was first comparisons, as environmental factors wide dorsal hump, and round-tipped, described in 2002 during an exploratory such as food availability and habitat broad flippers and flukes (Jefferson et survey of coastal waters off of western status may affect important rates of al., 2001). The Indo-Pacific humpback Taiwan (Wang et al., 2004). Prior to reproduction and generation time in dolphin is medium-sized, up to 2.8 m in these coastal surveys, there are few different populations. A recent analysis length, weighing 250–280 kg (Ross et records mentioning the species in this of life history patterns for individuals in al., 1994). Morphological plasticity region, save two strandings, a few the Pearl River Estuary (PRE) population exists among populations of the species photographs, and anecdotal reports is the best proxy for the ETS population. and is correlated with their geographic (Wang, 2004), so their history in the Like the ETS population, the PRE distributions (Ross et al., 1994). For region is unclear. Since the first survey population inhabits estuarine and example, the Eastern Taiwan Strait in 2002, researchers have confirmed freshwater-influenced environments in population, which occurs at the eastern their year-round presence in the Eastern similar proximity to anthropogenic portion of the species’ range, has a short Taiwan Strait (Wang et al., 2011), activity (Jefferson et al., 2012). dorsal fin with a wide base; the base of inhabiting estuarine and coastal waters Maximum longevity for the PRE the fin measures 5–10 percent of the of central-western Taiwan. population is estimated to be greater body length and slopes gradually into The ETS humpback dolphin habitat is than 38 years (Jefferson et al., 2012). the surface of the body. This differs most similar to that of the populations Evidence from multi-year photo- from individuals in the western portion located off the coast of mainland China. analysis of the ETS population of the range, which have a larger hump Individuals of the ETS humpback demonstrated that adult survivorship is that comprises about 30 percent of body dolphin population are thought to be high, 0.985, suggesting that this width, and forms the base of an even restricted to water less than 30 meters population also has a relatively long smaller dorsal fin (Ross et al., 1994). deep, and most observed sightings have lifespan (Wang et al., 2012). In general, Males and females from the Pearl River occurred in estuarine habitat with it is inferred that the population has Estuary population, and in other significant freshwater input (Wang et long calving intervals, between 3 and 5 populations of Southeast Asia, do not al., 2007b). Across the ETS humpback years (Jefferson et al., 2012). Gestation exhibit sexual dimorphism in size, dolphin habitat, bottom substrate lasts 10–12 months (Jefferson et al., growth patterns, or morphology consists of soft-sloping muddy sediment 2012). Weaning may take up to 2 years, (Jefferson et al., 2001; Jefferson et al., with elevated nutrient inputs, primarily and strong female-calf association may 2012). In contrast, individuals from influenced by river deposition (Sheehy, last 3–4 years (Karczmarski et al., 1997; South Africa exhibit sexual dimorphism 2010). These nutrient inputs support Karczmarski, 1999). Peak calving in terms of size and dorsal hump high primary production, which fuels activity most likely occurs in the morphology (Ross et al., 1994; upper trophic levels, contributing to the warmer months, but exact peak of Karczmarski et al., 1997). dolphin’s source of food (Jefferson, calving time may vary geographically The species occurs in a range of 2000). (Jefferson et al., 2012). Age at sexual nearshore habitats, including estuaries, The Indo-Pacific humpback dolphin maturity is late, estimated at between 12 mangroves, seagrass meadows, coastal is considered a generalist and and 14 years (Jefferson et al., 2012).

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DPS Analysis pigmentation can be used to reliably The best available data suggest that The following section provides our differentiate between the ETS the ETS humpback dolphin population analysis, based on the best available humpback dolphin and nearby Chinese is discrete from all other populations of science and the DPS Policy, to populations (Wang et al., 2008). Thus, the species based on its morphological determine whether the ETS humpback we consider these significant differences differences. Although limited, the best dolphin population qualifies as a DPS of in pigmentation of the ETS humpback available data also suggest that the ETS the taxon. dolphin as evidence of its discreteness. humpback dolphin population is Several researchers have suggested geographically isolated from other Discreteness that the ETS population of the populations. The morphological The Services’ joint DPS Policy states humpback dolphin is physically and differences and geographic isolation set that a population segment of a geographically isolated from other this population apart from other vertebrate species may be considered populations, based on the fact that populations of the Indo-Pacific discrete if it satisfies either one of the individuals have not been observed humpback dolphin, and thus, we following conditions: (1) It is markedly crossing or to have crossed the Strait of conclude that the ETS humpback separated from other populations of the Taiwan, despite repeated surveys of dolphin population meets the same taxon as a consequence of Chinese and Taiwanese populations discreteness criterion of the DPS Policy. physical, physiological, ecological, or using photo-identification techniques Significance (Wang et al., 2004; Wang et al., 2007b; behavioral factors (quantitative When the discreteness criterion is met Chen et al., 2010; Wang et al., 2011; measures of genetic or morphological for a potential DPS, as it is for the ETS Wang et al., 2012). For instance, a discontinuity may provide evidence of humpback dolphin population, the detailed analysis of more than 450 this separation); or (2) it is delimited by second element that must be considered individually-recognizable dolphins international governmental boundaries under the DPS Policy is the significance catalogued for Taiwanese and Chinese within which differences in control of of the DPS to the taxon as a whole. populations revealed no matches among exploitation, management of habitat, Significance is evaluated in terms of the them (Wang et al., 2008). Movement of conservation status, or regulatory importance of the population segment to Sousa chinensis is thought to be limited mechanisms exist that are significant in the taxon to which it belongs, in this to shallow water and nearshore habitat light of section 4(a)(1)(D) of the ESA (61 case the species Sousa chinensis. Some FR 4722; February 7, 1996). (Karczmarski et al., 1997; Hung et al., of the considerations that can be used Individuals from the ETS population 2004). Water depth and fast-moving under the DPS Policy to determine a exhibit pigmentation that differs currents within the Eastern Taiwan discrete population segment’s significantly from nearby populations Strait are thought to isolate the ETS significance to the taxon as a whole along the mainland coast of China, and population from Chinese populations, include: (1) Persistence of the evidence suggests that pigmentation despite their relatively close geographic population segment in an unusual or varies geographically across the species’ proximity (Wang et al., 2004; Wang et unique ecological setting; (2) evidence range (Jefferson et al., 2001; Jefferson et al., 2008; Wang et al., 2011; Wee et al., that loss of the population segment al., 2004a; Wang et al., 2008). Across the 2011; Wang et al., 2012). In fact, the ETS would result in a significant gap in the species, pigmentation changes as population has never been observed in range of the taxon; and (3) evidence that individuals mature. When young, waters greater than 30 meters depth the population segment differs markedly dolphins appear dark grey with no or (Wang et al., 2007b). Evidence suggests from other populations of the species in few light-colored spots; as they age, they that the ETS population of the its genetic characteristics. transform to mostly white (appearing humpback dolphin has a narrow home The ETS humpback dolphin pinkish), as dark spots decrease with range, and does not migrate seasonally population occurs in an ecological age. In particular, the developmental or mix with Chinese populations (Wang setting similar to populations occurring transformation of pigment differs et al., 2011). The population has been along the coast of mainland China, and significantly between ETS and nearby shown to inhabit the shallow, narrow many features of its habitat and ecology Chinese humpback dolphin habitat on the western coast of Taiwan are similar to those of populations populations; specifically, the spotting throughout the year, and exhibits strong throughout the range of the species, as intensity (density of spots) on the dorsal site fidelity (Wang et al., 2011). discussed above. Throughout its range, fin of the ETS population is The evidence for geographic isolation the Indo-Pacific humpback dolphin is significantly greater than that of four is based on limited survey data consistently associated with coastal mainland Chinese populations, collected since 2002, which focused river output and is found in shallow including the other nearby populations only on nearshore waters at certain nearshore waters (Jefferson et al., 2001). in the Pearl River Estuary and Jiulong times of year and did not survey the It displays no apparent preference for River estuaries (Wang et al., 2008). Strait waters between mainland China clear or turbid waters (Karczmarski et Significantly greater spotting intensity and Western Taiwan (Wang et al., 2004; al., 2000). The habitat and ecosystem on the dorsal fin of the ETS population Wang et al., 2011; Wang et al., 2012). use of the species differ in some ways is consistent, regardless of age (Wang et Thus, the possibility for Indo-Pacific geographically, but evidence suggests al., 2008). Further, the ETS humpback humpback dolphin migration or that the dolphin is an opportunistic dolphin never loses the dark dorsal fin emigration across the Strait cannot be piscivore, and thus does not exhibit spots completely, as has been observed eliminated entirely. However, the best unique or restricted feeding ecology in older individuals of other humpback available scientific information across its range (Jefferson et al., 2001). dolphin populations (Wang et al., 2008). indicates that the species is found In Thailand, Malaysia, and Indonesia, In contrast, dorsal fins of Chinese primarily in shallow nearshore habitat, the species occurs in tropical seagrass, populations are strikingly devoid of and the ETS population has never been coral, and mangrove lagoons not present spots, compared to their bodies, observed in waters greater than 30 in ETS humpback dolphin habitat throughout most of their lives, except meters, and thus migration or (Beasley et al., 1997; Smith et al., 2003; when they are very young or very old emigration across the deeper Strait is Adulyanukosol et al., 2006; (Wang et al., 2008). These differences in thought to occur rarely, if ever. Jaroensutasinee et al., 2011; Chersukjai

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et al., 2013). In India, the species is portion of the entire range of the demonstrated that the population makes associated with nearshore habitat species, and its loss would not inhibit a significant contribution to the consisting of mangroves, corals, and population movement or gene flow adaptive, ecological, or genetic diversity tidal mudflat, heavily influenced by among other populations of the species of the taxon. As such, based on the best monsoons that regulate the influx of (Lin et al., 2012). The ETS humpback available data, we conclude that the ETS freshwater to the system (Sutaria et al., dolphin is distributed throughout only humpback dolphin population is not a 2004). The ETS humpback dolphin 512 square kilometers of coastal waters DPS and thus does not qualify for listing habitat is most similar to that of coastal off Western Taiwan; this small range is under the ESA. This is a final action, Chinese populations, with more not geographically significant in and, therefore, we do not solicit temperate water, soft muddy substrate, comparison to the taxon’s range comments on it. and consistent input from river systems. throughout the coastal Indo-Pacific and Dusky Sea Snake The ETS humpback dolphin habitat Indian Oceans. differs from the habitat occupied by There are no data to show that the The section below presents our mainland Chinese populations in some genetic characteristics of the ETS analysis of the status of the dusky sea ways, with nearby rivers generally humpback dolphin population differ snake, Aipysurus fuscus. Further details smaller than those in mainland China, markedly from other populations in a can be found in Manning (2014). and with warmer waters in the winter significant way. While pigmentation of Species Description due to the influence of the Kuroshio the ETS population is significantly Current, which periodically moves into different from other populations within The dusky sea snake, Aipysurus the Strait of Taiwan (Chern et al., 1990; the taxon (Wang et al., 2008), whether fuscus, is a species within the family Jan et al., 2002; Wang et al., 2008). the pattern is adaptive or has genetic , which is a very diverse family However, feeding ecology, prey underpinnings is unknown. In other of venomous . The genus availability, and prey preference are cetacean species, differences in Aipysurus contains seven species, six of thought to be similar in mainland China pigmentation have been hypothesized to which are restricted to Australasian and Taiwan (Barros et al., 2004; Wang relate to several adaptive responses, waters. The dusky sea snake is brown, et al., 2007a), so these small differences allowing individuals to hide from blackish-brown, or purplish-brown with in habitat do not seem to have predators, communicate with wide ventral scales and diamond- significant effects on the species’ conspecifics (promoting group shaped body scales that are smooth and ecology. cohesion), and disorient and corral prey imbricate (i.e., overlapping). There are The presumed habitat of the ETS (Caro et al., 2011). However, the generally 19 scale rows around the neck, humpback dolphin is narrower in differences in ETS humpback dolphin 19 around the mid-body, and 155 to 180 offshore width than that of other studied pigmentation may be a result of a ventral scales (Rasmussen, 2000). The populations of the taxon. For instance, genetic bottleneck from the small size of dusky sea snake is completely aquatic the ETS population is thought to inhabit this population (less than 100 and, like all sea snakes, has a paddle- a small area of coastal shallow waters individuals) and the possibility that it like tail for swimming. Its maximum within 3 km from the shore (Wang et al., represents a single social and/or family total length is about 90 cm (Rasmussen, 2007b). In contrast, Chinese populations group. Such small populations are more 2000). Growth rates for the dusky sea inhabit a broader shallow area ranging heavily influenced by genetic drift than snake have not been documented, but tens of kilometers offshore, where large populations (Frankham, 1996). reported growth rates for other sea dolphins can range farther from the Insufficient data exist to determine snakes range from 0.07–1.0 mm per day coastline without moving into deeper whether significant differences in ETS and decline with age (Heatwole, 1997). water (Hung et al., 2004; Chen et al., humpback dolphin pigmentation relate The maximum lifespan for dusky sea 2011). While the ETS population to the functional divergence of the snakes has been assumed to be about 10 exhibits some behavioral differences, population, or are simply a product of years, and age at first maturity has been such as increased cooperative calf- genetic drift and a genetic bottleneck. assumed to be about 3–4 years rearing and social connectivity, as The best data available thus lead us to (Lukoschek et al., 2010). Generation compared to Chinese populations conclude that loss of the ETS humpback length is thought to be approximately 5 (Dungan et al., 2011), it is uncertain dolphin population would not result in years (Lukoschek et al., 2010). whether or not these differences are significant loss of overall genetic or Despite its aquatic existence, and like adaptive or facultative, and simply ecological diversity of the taxon as a all , the dusky sea snake lacks based on the population’s low whole. gills and must surface to breathe air. abundance. Thus, insufficient evidence Dive durations vary by species, but most DPS Conclusion and Proposed exists to suggest significant differences sea snakes typically stay submerged for Determination in the dolphin’s ecology or adaptation about 30 minutes, and some for up to have derived from the differences in the According to our analysis, the ETS 1.5–2.5 hours (Heatwole and Seymour, physical parameters of its environment. humpback dolphin population is 1975). Maximum dive depth for dusky Therefore, differences in the habitat and considered discrete based on its unique sea snakes is unknown, but co-occurring ecological setting of the ETS humpback pigmentation patterns, which set it apart members of this genus are considered dolphin do not set it apart from the rest morphologically from the rest of the ‘‘shallow’’ and ‘‘intermediate’’ depth of the taxon, and do not appear to relate taxon, and evidence for its geographic species that dive no deeper than 20 m to significant selection pressures isolation. However, while discrete, the or 50 m, respectively (Heatwole and affecting the population’s foraging, ETS humpback dolphin population does Seymour, 1975). behavior, or ecology. not meet any criteria for significance to The dusky sea snake is viviparous, There is no evidence to suggest that the taxon as a whole. The ecological meaning embryos develop internally loss of the ETS humpback dolphin setting it occupies is similar to that of and young undergo live birth. Because population would result in a significant the rest of the species, loss of the this species never ventures on land, gap in the range of the taxon. The ETS population would not constitute a mating occurs at sea and young are born humpback dolphin population significant gap in the taxon’s extensive alive in the water. Within the genus constitutes a small and peripheral range, and no genetic or other data have Aipysurus, the number of young per

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brood is small, usually less than four, heavy coral growth, but they were also Reef after 2005, despite considerable and young are relatively large at birth observed to congregate in sandy- effort (Lukoschek et al., 2013; Table 1, (Cogger, 1975). Timing and seasonality bottomed gullies and channels (Minton Manning, 2014). Based on reef area data of the dusky sea snake’s breeding cycles and Heatwole, 1975). Home-range size reported in Skewes et al. (1999), are unknown, and very little is known and site fidelity of individual dusky sea Ashmore Reef represents about 40 about the juvenile life stage. snakes has not been evaluated. percent of the dusky sea snake’s The dusky sea snake preys mainly on However, a short-term (6–9 days), historical reef habitat. Extirpation from labrid (e.g., ) and gobiid (e.g., telemetry study on the sympatric olive this reef would represent a substantial gobies) fishes, and to a lesser extent, fish sea snakes (A. laevis) and a long-term (8- change in the species’ distribution and eggs (McCosker, 1975). Food year), mark-recapture study on the abundance. competition among sympatric sea turtle-headed sea snake A survey in 2005 at Hibernia Reef snakes is thought to be minimal, based ( annulatus) suggest that indicated a relatively low abundance of on examinations of diet composition for home-ranges of sea snakes are small, A. fuscus, and the most recent surveys, sympatric sea snakes (McCosker, 1975; movement of adults is very limited, and conducted in 2012 and 2013, have failed Voris and Voris, 1983). Feeding longer-distance dispersal may be due to detect any dusky sea snakes despite behavior of dusky sea snakes has not mainly to passive transport, such as by extensive survey effort (Guinea, 2005; been thoroughly investigated; however, currents and storms (Burns and Guinea, 2013). Dusky sea snakes were during surveys at Ashmore Reef, Heatwole, 1998; Lukoschek and Shine observed in surveys conducted at Scott Australia, Guinea and Whiting (2005) 2012). While it is very plausible that Reef in 1972/73, 2006, 2012 and 2013; commonly saw dusky sea snakes over adult A. fuscus are similar to these other however, their relative abundance varies sand bottom habitat and watched one species, research to evaluate adult and across the surveys, and no trends are snake actually force its head and about juvenile A. fuscus habitat use and detectable given the limited data (see 15 percent of its body into the sand. movement is needed. Table 1, Manning, 2014). For example, However, because it emerged without a Sea snakes typically have patchy Guinea (2012) visited Scott Reef in prey item (Guinea and Whiting, 2005), distributions and can be found in very February, 2006, and reported that dusky it is unclear whether this was foraging dense aggregations in certain locations sea snakes, as the third-most abundant or some other behavior. Like their within their ranges (Heatwole, 1997). species, made up 15 percent of the total terrestrial relatives, sea snakes swallow This patchiness complicates efforts to sea snake sightings (Guinea, 2013). their prey whole and therefore must understand habitat use patterns, as Portions of Scott Reef were surveyed have some strategy for subduing them. seemingly suitable habitat can remain again in 2012 and 2013, and dusky sea McCosker (1975) hypothesized that the unoccupied. On a smaller spatial scale, snakes made up only 3.2 percent and highly toxic venom of sea snakes is distributions of sea snake fauna on 7.4 percent of the total sightings probably more of a feeding adaptation Australian reefs appear to be influenced respectively for each year (Guinea, than a defensive one. by water depth, substrate type, and 2013). At Seringapatam Reef and Cartier The dusky sea snake is a benthic, feeding strategies (McCosker, 1975; Island, A. fuscus is rare or potentially coral reef-associated species endemic to Heatwole, 1975b). Other biotic factors, absent. Overall, while these limited several shallow emergent reefs of the such as limited juvenile dispersal, may abundance data are very difficult to Sahul Shelf off the coast of Western also contribute to the observed patchy interpret, they indicate that dusky sea Australia in the Timor Sea, between distributions (Lukoschek et al., 2007a). snakes have not been present in high Timor and Australia. These reefs are Overall, however, causative factors for numbers in any recent reef surveys relatively isolated and lie at the edge of observed distributions are not (Table 1, Manning, 2014). the continental shelf over several completely understood. The dusky sea snake has a restricted hundred kilometers from the mainland. range, and structure and connectivity of The dusky sea snake has been reported Population Abundance, Distribution, populations is uncertain. Assuming that to occur at Ashmore, Scott, and Structure A. fuscus is extirpated from Ashmore Seringapatam, and Hibernia Reefs and There are no historical or current Reef, Sanders et al. (2014) recently Cartier Island; however, individual population estimates for the dusky sea estimated that the dusky sea snake’s surveys have not consistently recorded snake. However, multiple reefs have range is now less than 262 sq km. dusky sea snakes at all of these been surveyed repeatedly, and although Although structure and connectivity of locations. For example, in transect survey methodologies have varied, the reef populations of A. fuscus have not surveys conducted by Minton and data provide some indication of been studied directly, some information Heatwole (1975) over several weeks population trends for some locations. may be gleaned from several studies on during December 1972 and January 1973 For Ashmore Reef in particular, the the olive sea snake, A. laevis, a at Ashmore, Scott, and Hibernia Reefs survey data provide a strong indication sympatric congener that is larger in size, and Cartier Island, dusky sea snakes of severe population decline and more common, and more widely were recorded at Scott and Ashmore possible extirpation. Older surveys distributed than A. fuscus, but is very reefs only. Extensive surveys conducted dating from 1972 to 2002 by various closely related to A. fuscus (Sanders et more recently at Ashmore Reef, where researchers indicate that the relative al., 2013b). As mentioned above, a dusky sea snakes were once relatively abundance of A. fuscus was fairly short-term (6–9 days) tracking study on common, have located no specimens consistent and represented about 10–23 A. laevis suggests that adults of this (Guinea, 2013; Lukoschek et al., 2013). percent of the sea snakes observed (see species have small home ranges (1,500– Lukoschek et al. (2010) estimated that Table 1, Manning, 2014). A footnote in 1,800 sq m) and undergo limited active the area of occurrence of dusky sea Smith (1926) also indicates that a dispersal (Burns and Heatwole, 1998). snakes is probably less than 500 km2. sample of 27 dusky sea snakes (out of Results of that study are somewhat During their surveys, Minton and an ∼100-specimen sea snake collection) supported by analyses by Lukoschek et Heatwole (1975) observed dusky sea had recently been collected for him at al. (2007b) of mitochondrial DNA snakes in shallow water (<10 m) as well Ashmore Reef. The dusky sea snake, (mtDNA) from 354 olive sea snakes as in the 12 to 25 m depth-zone. They however, has not been recorded in a collected across its range, including were observed in areas of moderate to single survey conducted at Ashmore some samples from Hibernia, Scott, and

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Ashmore reefs and Cartier Island. Based coral loss following the 1998 event has A comprehensive understanding of on their results, Lukoschek et al. not been quantified. Widespread the relationship between live coral (2007b) concluded that gene flow among mortality of corals was documented in cover and dusky sea snake abundance the reefs of the Timor Sea is low, and response to the 2003 bleaching event, likely requires more detailed that olive sea snakes at these reefs have and average live coral coverage was information regarding coral species been diverging for some time. A reduced to 10 percent (Kospartov et al., composition, habitat complexity, and subsequent analysis of microsatellite 2006; as cited in Lukoschek et al., 2013). coral and prey fish resiliency relative to DNA from the same specimens indicates Surveys conducted in 2005 and 2009 both the 1998 and 2003 bleaching that two of the most distant Timor reef indicated that recovery of corals at events. Such an analysis might offer populations of A. laevis are significantly Ashmore Reef was rapid but delayed by further insights into the differing diverged (Lukoschek et al., 2008). about 7 years (Ceccarelli et al., 2011). response patterns at the two reefs, and However, the degrees of divergence of Overall, there has been an eight-fold an indication of whether sea snake other reef populations were not increase in hard coral coverage from abundance is driven by live coral statistically significant, and there was 1998 to 2009 (Hale and Butcher, 2013), coverage over timescales relevant to no clear isolation-by-distance with all of the recorded recovery these disturbances. At this time, relationship (Lukoschek et al., 2008). occurring after 2005. Meanwhile, survey however, because a clear or consistent Although not conclusive, the available data suggest complete loss of dusky sea pattern does not emerge from the information for the olive sea snake and snakes at Ashmore Reef after 2005. available data regarding dusky sea snake the fact that dusky sea snakes also lack Existing survey data also show sharp abundances at Ashmore and Scott reefs a dispersive larval phase, suggest declines in total sea snake abundance in relationship to these two bleaching connectivity of A. fuscus may be limited and species diversity at Ashmore Reef events, we cannot conclude that loss of among some reefs within the region. following both the 1998 and 2003 live coral is contributing to the decline Limited inter-population exchange bleaching events (Lukoschek et al., of the dusky sea snake. would increase the extinction risk and 2013). These patterns are consistent The reefs where dusky sea snakes are reduce the recovery potential for local with a hypothesis that loss of live corals found lie more than several hundred populations that have experienced affects reef-associated sea snakes. kilometers offshore and thus enjoy a severe declines or have been lost. considerable degree of protection from The patterns at Ashmore Reef are human activities and land-based sources Summary of Factors Affecting the Dusky contrasted, however, by those observed of pollution. Despite this remoteness, Sea Snake at Scott Reef. Following the 1998 the reefs may experience some Available information regarding bleaching event, a greater than 80 degradation as a result of vessel traffic. current, historical, and potential threats percent loss of hard and soft coral cover Anchor damage, pollution from to the dusky sea snake was thoroughly occurred, which translated into a contaminated bilge water, and marine reviewed (Manning, 2014). Although reduction of live coral coverage to a debris are among the potential issues causes for observed declines in dusky total of roughly 10 percent (Smith et al., identified at Ashmore Reef, which sea snake have not been conclusively 2008). The 1998 El Nin˜ o event experiences a relatively high level of determined, we found that the species is represents the most extreme traffic from Indonesian fishers, yachts, being threatened by hybridization. temperature anomaly recorded for Scott merchant ships, and illegal entry vessels Other possible threats include vessels, Reef, and involved a rapid rise in water (Whiting, 2000; Lukoschek et al., 2013). pollution, climate change, and temperatures that remained above The mechanisms for and extent to inadequate regulatory mechanisms. We normal for two months (NOAA, 2013). which these boat-based habitat threats summarize information regarding each Almost 6 years after the bleaching event are impacting dusky or any other sea of these threats below according to the (in 2004), the hard corals had partially snake species of the Timor Sea reefs are factors specified in section 4(a)(1) of the recovered to 40 percent of their pre- unknown. ESA. Available information does not bleaching cover, the soft corals showed The extensive oil and gas industry indicate that disease, predation, or no sign of recovery, and community activity in this region may also be a overutilization (including bycatch) are composition of corals remained possible source of disturbance affecting operative threats on this species; significantly altered (Smith et al., 2008). dusky sea snakes and their habitat. therefore, we do not discuss those Within 12 years after the event (by Exploration and extraction activities further here. See Manning (2014) for 2010), coral cover, recruitment, within the Ashmore Platform began in additional discussion of all ESA Section community composition, and generic 1968 (Geoscience Australia, 2012) and 4(a)(1) threat categories. diversity were similar to pre-bleaching are expected to continue for some time, years (Gilmour et al., 2010). Several given the significant resources within The Present or Threatened Destruction, lesser disturbances, including two this region. Ashmore Reef and Cartier Modification, or Curtailment of Its cyclones and the 2003 El Nin˜ o event, Islands lie about 50–80 km west of the Habitat or Range occurred during this time period and main offshore wells in the Timor Sea, Aipysurus fuscus is dependent on may have slowed the rate of recovery to and the closest exploration wells are 36 coral reefs for prey and shelter, and loss some extent (Gilmour et al., 2013). km away (Russell et al., 2004). However, of live coral is a possible mechanism Available sea snake survey data, Scott Reef lies directly above a contributing to the decline of A. fuscus spanning 1972–2013, with surveys in significant portion of the Torosa at locations such as Ashmore Reef. Coral 1972–73, 2006, 2012, and 2013, do not Reservoir, where drilling for natural gas reefs of the Sahul Shelf experienced appear to indicate a major decline in is expected to start by 2017. The widespread bleaching in response to El abundance of dusky sea snakes at Scott development of the natural gas facility Nin˜ o events in 1998 and 2003. Ashmore Reef, which were relatively common in this area will mean increased vessel Reef experienced bleaching in 1998 and during the surveys conducted by Guinea traffic and potentially light, sound, and again, to an apparently greater extent, in (2012) in 2006. However, the temporal chemical pollution. The area is also 2003 (Lukoschek et al., 2013). However, gaps in these survey data, especially expected to experience minor because there are no estimates of coral from 1973 to 2006, could conceal subsidence or compaction as the gas is coverage prior to 1998, the extent of shorter-term patterns. removed (Woodside Energy LTD, 2013).

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Whether, and the degree to which, any Voris, 1983). The necropsy indicated emissions is expected to continue (IPCC, of these threats or a combination of that the snake had fed recently and that 2013), and elevated sea surface these threats will impact dusky sea the stomach contents were temperatures are expected to rise at an snakes is not yet known. contaminated with oil (Gagnon, 2009). accelerated rate (Lough et al., 2012), loss Unfortunately, extremely limited Relatively high levels of polycyclic of corals through bleaching events is information also exists regarding the aromatic hydrocarbons were also expected to increase. The expansion of toxic effects of oil exposure on sea detected in the lungs, trachea, and Australia’s oil and gas exploration and snakes. Oil spills, which occur more muscle tissue (Gagnon, 2009). Neither of extraction in the Timor Sea may also frequently as a result of vessel or two dispersant chemicals used to treat result in an increased risk of oil spills pipeline incidents rather than the spill were detected in lung samples and additional habitat threats for dusky exploration and drilling activities (Gagnon, 2009). The necropsy report sea snakes. (www.amsa.gov.au), have also not concluded that the likely cause of death Inadequacy of Existing Regulatory occurred very often in this region. Some for this specimen was exposure to Mechanisms information is available from the August petroleum hydrocarbons (Gagnon, 2009 explosion of the West Atlas oil rig 2009). The dusky sea snake and its habitat on the Montara Well, which leaked oil In 2012 and 2013, Guinea (2013) receive a significant degree of regulatory and gas uncontrollably into the Timor conducted surveys to evaluate the protections. The largest potential gap in Sea for 74 days until the well was potential impacts of the Montara leak on existing regulatory mechanism may be finally capped in November 2009. species of marine reptiles. Potentially for threats related to climate change. Oil Considered one of the worst oil-related impacted areas surveyed included spills, while rare and unpredictable, and spills to have ever occurred in Australia, Ashmore Reef, Cartier Island, and other oil and gas industry activities may the Montara leak was analogous in Hibernia Reef; Scott and Seringapatam also pose threats to the species as a nature to the Deepwater Horizon reefs were surveyed as control reefs consequence of inadequate management disaster of April 2010 in the Gulf of (Guinea, 2013). Ashmore Reef and and regulation. We summarize the Mexico. In an effort to rapidly assess Cartier Island are 167 km west-north- available information regarding related impacts to multiple taxa, Watson et al. west and 108 km west from the Montara regulatory protections below; a more in- (2009) conducted ship-based transect well, respectively. Seringapatam and depth discussion is available in surveys in areas around the Atlas Scott reefs are several hundred km Manning (2014). drilling platform in September 2009. south-east of the Montara well and far Along with all of Australia’s other They did not observe or identify any from modeled oil trajectories (Guinea, hydrophiine sea snakes, dusky sea dusky sea snakes; however, they did 2013). The extensive survey efforts of snakes are listed under the observe ‘‘lethargic sea snakes lying in Guinea (2013) did not indicate any Commonwealth Environment Protection thick oil (i.e., not moving much when impact of the hydrocarbon release on and Biodiversity Conservation Act 1999 approached, unable to dive)’’ and marine reptiles (sea turtles and sea (EPBC Act). The EPBC Act provides a collected a dead horned sea snake snakes) of the potentially affected reefs. legal framework to protect and manage (Acalyptophis peronii) from oil-affected Of the reefs surveyed, Hibernia Reef and Australia’s nationally and waters for further analysis (Watson et Cartier Island had the highest sea snake internationally important flora, fauna, al., 2009). The necropsy report density; however, no sea snakes were ecological communities, and heritage indicated that this snake was in good observed at Ashmore Reef, where sea places that are of national physical condition, with no visible snake abundance and diversity had environmental significance. Under the external or internal pathologies, and no already declined to very low levels prior EPBC Act, no one may ‘‘kill, injure, oil was detected in swab samples of the to the 2009 incident (Guinea, 2013). take, trade, keep or move a member of skin (Gagnon and Rawson, 2010). Overall, these data suggest that while a native species’’ within any reserve Chemical analysis of tissues clearly there are likely to be acute impacts to without a permit (Commonwealth of indicated that exposure to crude oil sea snakes in response to major spills, Australia, 2000). The EPBC Act requires occurred through ingestion of prey and it is unlikely that pollution stemming that surveys be conducted for listed not through inhalation (Gagnon and from oil and gas industry activities has marine species. The EPBC Act also Rawson, 2010). Acalyptophis peronii is contributed to the observed declines of provides that the Australian considered more of a diet specialist than the dusky sea snake. Government Minister for the the dusky sea snake and primarily Overall, based on the existing Environment may make or adopt a consumes burrowing gobies (McCosker, information, we conclude that there is a recovery plan for a listed species, to set 1975; Voris and Voris, 1983). Because low likelihood that these habitat-related out the research and management they saw no physical damage to the gut threats have contributed to the observed actions needed to stop the decline of the structure and no contamination of the decline of the dusky sea snake. At this species and support its recovery. There tissues, Gagnon and Rawson (2010) time, there is insufficient information to are no recovery plans in place for any concluded it was unlikely that oil indicate whether and how the dusky sea sea snake species, however ingestion was the primary cause of snake will be affected by these habitat (www.environment.gov.au/topics/ death. Tests for presence of chemical issues in the future. We do expect that biodiversity/threatened-species- dispersants used during the spill- each of the various habitat-related issues ecological-communities/recovery-plans). response were not conducted. summarized above will continue well Thus, while the dusky snake receives A necropsy was also performed on a into the future, and some may worsen. substantial protection under the EPBC dead sea snake landed by a commercial Given that El Nin˜ o and its associated Act, without a recovery plan, that fisherman operating in the vicinity of warming of equatorial Pacific Ocean protection may not be enough to help the West Atlas spill on September 14, waters is a natural and reoccurring stabilize and recover the species. 2009 (Gagnon, 2009). This specimen climate phenomenon, coral bleaching in Two of the five main reefs within the was identified as elegans, response to sufficiently strong El Nin˜ o dusky sea snake’s historical range, which is a relatively widespread and events will continue. Furthermore, Ashmore Reef and Cartier Island, are abundant species that preys on and because climate warming as a protected reserves. Ashmore Reef other fishes (McCosker, 1975; Voris and consequence of carbon dioxide National Nature Reserve was established

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in 1983, under the National Parks and rare, and there is insufficient predictions of worsening damage to Wildlife Conservation Act 1975 (a information to indicate that the existing coral reefs in Australia in response to predecessor to the EPBC Act), and later regulatory mechanisms are inadequate climate change (IPCC, 2013), the largest listed as a Ramsar Site in 2000, under or that they have contributed to the potential future gap in the existing the Ramsar Convention, which is an decline of this species. regulatory mechanisms appears to be intergovernmental treaty on sustainable Potential threats to dusky sea snakes related to climate change. use of wetlands. In Australia, Ramsar stemming from anthropogenic climate change include elevated sea surface Other Natural or Manmade Factors Sites receive protection under the EPBC Affecting Their Continued Existence Act: Any action that will have or is temperature, ocean acidification, and likely to have a significant impact on a increased coral bleaching events (see Elevated sea surface temperature as a Ramsar Site requires an environmental below). Impacts of climate change on consequence of climate change has been assessment and approval. The EPBC Act the marine environment are already proposed as a possible threat to sea also sets forth national standards for being observed in Australia and snakes, and we have addressed habitat- managing, planning, monitoring, elsewhere (Melillo et al., 2014; related effects above. The IUCN Red List involving the community in, and Poloczanska et al., 2012), and the most assessment for A. fuscus, suggests that conducting environmental assessments recent United Nations climate-induced increases in water of Ramsar Sites to insure consistent Intergovernmental Panel on Climate temperature may actually exceed the compliance with the Ramsar Change (IPCC) assessment provides a upper lethal limit for A. fuscus, and Convention. Cartier Island, a former high degree of certainty that human thereby pose a threat to the species sources of greenhouse gases are (Lukoschek et al., 2010). These authors British Air Force bombing range, was ° designated as a Marine Reserve in 2000. contributing to global climate change assumed an upper lethal limit of 36 C, These two reserves cover a combined (IPCC, 2013). Ocean temperatures based on data for the pelagic sea snake, area of 750 km2 and are both assigned around Australia have increased by 0.68 Pelamis platurus. Experiments to ° to IUCN category Ia—strict nature C since 1910–1929 (Poloczanska et al., measure the thermal tolerances of A. reserve. IUCN category Ia areas are 2012), and carbon dioxide inputs have fuscus have not been conducted. Sea snakes, like all reptiles, are protected to preserve biodiversity and lowered ocean pH by 0.1 units since ectotherms, and thus to a great extent maintain the areas for the benefit of 1750 (Howard et al., 2009). Australia are physiologically affected by scientific research. Human access to and other countries have responded to temperature. On a large geographic such areas is tightly controlled and climate change through various scale, the distribution of sea snakes is limited. A small section of Ashmore international and national mechanisms. Australia signed on to the Kyoto considered to be dictated by ocean Reserve is managed as IUCN category temperatures: Sea snakes generally do II—national park. Such areas are Protocol in 2007 and has active domestic and international programs to not occur in waters below about 18 °C managed to protect ecosystems and (Davenport, 2011). Most sea snakes can biodiversity, and while still restricted, lower greenhouse gas emissions (www.climatechange.gov.au/). However, tolerate temperatures up to a mean of human visitation is not as limited as for about 39–40 °C, but tolerances may vary category Ia areas. No fishing or harvest in Australia, there appear to be no specific actions to address potential with the size of the snake and the rate of any biota is allowed within the of temperature change (Heatwole et al., reserves, with the limited exception of climate change effects on marine reptiles beyond monitoring (Fuentes et 2012). Also, although sea snakes are finfish fishing within the category II al., 2012). Because climate change able to dive to avoid extreme area of Ashmore Reef, and then only as related threats have not been clearly or temperatures of surface waters, they long as the fish are used for relatively mechanistically linked to decline of have limited capacity to acclimate and immediate consumption. Given the lack dusky sea snakes, the adequacy of cannot thermoregulate (Heatwole et al., of clearly identified habitat-related or existing or developing measures to 2012). human-disturbance-related threats to control climate change threats is not Sea surface temperatures vary the dusky sea snake, there is no possible to fully assess, nor are seasonally within the Timor Sea. The indication that these reserves and area sufficient data available to determine highest recorded oceanic water protections are inadequate such that what regulatory measures would be temperature in the Ashmore region is 31 ° they have contributed to the observed needed to adequately protect this C, and the highest recorded lagoon ° decline of the species. species from climate change. While it is water temperature is 35.4 C According to the Australia not possible to conclude that the current (Commonwealth of Australia, 2002). Department of Sustainability, efforts have been inadequate, such that These temperatures are below the Environment, Water, Population, and they have contributed to the decline of assumed upper lethal temperature limit Communities (DSEWPC) 2012 Report this species, we consider it likely that for dusky sea snakes; but Australia’s Card for marine reptiles listed under the dusky sea snakes will be negatively average ocean temperatures have EPBC Act, pollution from offshore oil impacted by climate change, given the increased by over half a degree since rigs and operations is a potential predictions of widespread and 1910–1929, and the rate of warming has concern for sea snakes (DSEWPC, 2012). potentially permanent damage to coral accelerated since the mid-20th century This report also states that Australia has reefs in Australia (IPCC, 2013). (Poloczanska et al., 2012). Given the a strong system for regulating the oil Overall, we do not find there is thermal tolerances of other sea snakes and gas industry and that this system substantial evidence indicating that A. and the ocean temperatures currently was strengthened further in the wake of fuscus is currently threatened by the experienced by A. fuscus at present, it the Montara oil spill. Details on how lack of adequate regulatory mechanisms. is very unlikely that elevated ocean any particular processes or regulations Beyond the direct protection the species temperature has been a source of were strengthened are not provided in receives through its listing under the mortality. However, it is plausible that this report and could not be found. EPBC Act, the dusky sea snake receives a continuation of the observed rate of Although oil spills pose a potential additional direct and indirect protection ocean warming would, in the distant threat to the health and status of the within the Ashmore Reef and Cartier future, result in negative physiological dusky sea snake, oil spills are relatively Island Marine Reserves. Given the consequences for A. fuscus.

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Hybridization and introgression have evidence indicating that this species Butcher, 2013). Indonesians have fished recently been identified by Sanders et currently faces a high risk of extinction. this site for centuries and subsistence al. (2014) as a threat to the continued The probable extirpation of the dusky fishing is allowed in only the IUCN existence of A. fuscus. Hybridization, or sea snake from Ashmore Reef, which category II portion of the reserve (Hale the production of viable offspring constitutes about 40 percent of the and Butcher, 2013). No commercial through the crossing of genetically historical reef habitat, represents a fishing is allowed in any part of the distinct taxa or groups, occurs in the contraction of an already limited range Reserve. The relatively pristine state of wild for about 10 percent of for this species. Loss of dusky sea the site makes it attractive for the long- species (Mallet, 2005). Hybridization snakes from Ashmore Reef and low term monitoring and other scientific can lead to introgression, or the relative abundances at all other reefs, projects that are conducted there (Hale integration of foreign genetic material coupled with high rates of hybridization and Butcher, 2013). Starting in the late into a genome. The conservation throughout the range and a presumed 1980’s, Environment Australia (EA) concern in this particular case is that low rate of dispersal, suggest that the contracted a private vessel and crew to reproductive barriers between the olive species is declining and unlikely to undertake on-site management at the sea snake, A. laevis, and the dusky sea recover without intervention. The Reserve; however, as of 2000, Australian snake, A. fuscus, appear to be breaking interaction of the threats of low and Customs Service took over this down, potentially allowing A. fuscus to declining abundance, limited dispersal, responsibility (Whiting, 2000). undergo reverse speciation. and high rates of hybridization all Enforcement of protections at the The dusky sea snake co-occurs with suggest a high risk of extinction in the Reserve depends largely on the presence the closely-related olive sea snake near term. of Customs officials, which is not quite throughout its range, and the two continuous (Lukoschek et al., 2013; Protective Efforts species are thought to have shared a Whiting, 2000). common ancestor approximately As mentioned previously, all of The Cartier Island Commonwealth 500,000 years ago (Sanders et al., Australia’s hydrophiine sea snakes are Marine Reserve, designated in 2000 2013b). The olive sea snake is a listed and protected under the EPBC under the EPBC Act, is completely relatively abundant and much more Act, making it illegal to kill, injure, take, closed to the public. No commercial or widely distributed species compared to trade, or move dusky sea snakes in recreational fishing is allowed. General the dusky sea snake. Although similar Commonwealth waters without a permit access and several specific activities, in appearance, the two species can be (DSEWPC, 2012a). The EPBC Act also such as scientific research, photography distinguished based on body scale rows, requires that surveys be conducted for and tourism, may be allowed with prior body size, and color pattern. Sanders et listed marine species. approval from the Director of National al. (2014) analyzed 11 microsatellite Sea snakes are also identified as a Parks issued under the EPBC Act (see markers for A. fuscus and A. laevis ‘‘conservation value’’ in Australia’s http://www.environment.gov.au/topics/ across four reefs (Ashmore, Hibernia, North-west Marine Bioregional Plan marine/marine-reserves/north-west/ Scott, and Seringapatam) to assess inter- (DSEWPC, 2012b). Marine bioregional cartier-activities). specific gene flow and introgression. plans are meant to improve the way Since the early 18th century, Results of their genetic analyses indicate decisions are made under the EPBC Act, Indonesian fishers have visited and significant and asymmetric gene flow, particularly with respect to balancing fished reefs within the Timor Sea, with higher rates of introgression from protection of marine biodiversity with mainly in search of trepang, trochus, A. laevis into the smaller A. fuscus the sustainable use of natural resources. turtle, shark fin, and reef fishes population (Sanders et al., 2014). A high The North-west Plan identifies activities (Commonwealth of Australia, 2002). In frequency of hybrids was also found at that may affect sea snakes and thus 1974, a Memorandum of Understanding each of the four reefs included in the require prior approval. National heritage (MOU) was established between study area. Forty-three percent of the places are also listed and protected Australia and Indonesia that set out snakes sampled (n=7) at Ashmore, 55 under the EPBC Act. Ashmore, Scott, arrangements by which traditional percent of the snakes sampled (n= 42) and Seringapatam reefs are all listed on fishers may access resources in at Scott Reef, and 42 percent of the Australia’s Commonwealth Heritage Australia’s territorial sea. Because of its snakes sampled (n=12) at Seringapatam List, and under the EPBC Act, approval shape, the area covered by this MOU is Reef were identified as hybrids (Sanders must be obtained before any action takes often referred to as the MOU Box. The et al., 2014). At Hibernia Reef, 95 place that could have a significant MOU Box, which covers an area of percent of the snakes sampled (n=19) impact on the national heritage values about 50,000 km2, includes the five were hybrids (Sanders et al., 2014). of these areas. main reefs where the dusky sea snake Phenotypically, the majority of hybrids Also mentioned previously were the occurs (Skewes et al., 1999). The marine resembled the olive sea snake (Sanders various habitat protections currently in resources within this area are managed et al., 2014). Whether the observed place that directly and indirectly protect by the Australian Government, and hybridization is a purely natural process the coral reefs within the dusky sea traditional fishing by Indonesian fishers or has human causes is not yet known. snake’s range. For example, the is allowed. However, as discussed Regardless, the high rates of Ashmore Commonwealth Marine above, certain restrictions apply within hybridization of A. fuscus with another Reserve, which includes 583 km2 of the Marine Reserves. Traditional species across its range may lead to the sandy islands, coral reefs, and Indonesian fishers may access parts of eventual disappearance of this surrounding waters up to 50 m deep the Ashmore Reserve for shelter and taxonomic species and is a threat to its (Commonwealth of Australia, 2002), is freshwater and to visit grave sites, but, survival. almost completely closed to the general as mentioned previously, fishing is public. Permits may be issued to prohibited in both the Cartier Island and Extinction Risk authorize visits for tourism or Ashmore Marine Reserves, with the Although accurate and precise data recreation. There are 1–2 visits per year limited exception for fishing for for many demographic characteristics of by commercial tourism vessels to view immediate consumption within the dusky sea snakes are lacking, the best wildlife, and about 15–20 recreational category II area of the Ashmore Reserve. available data provide multiple lines of yachts that visit each year (Hale and There is no evidence that sea snakes

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have been targeted by Indonesian fishers aware of any additional, planned or not- ecosystems upon which these species (Hale and Butcher, 201; Lukoschek et yet-implemented conservation measures depend, we consider the natural range al., 2013). that would protect this species; thus, we to be biologically and ecologically Because sea snakes are listed under did not conduct an analysis under the important to the species’ viability to the EPBC Act, all Australian fisheries PECE. We seek additional information persist in the face of threats. Distances are required to demonstrate that direct on other conservation efforts in our between non-introduced populations and indirect interactions with sea public comment process (see below). range from less than 1 km (Vagelli, snakes are sustainable (Zhou et al., 2011) up to 153 km (Vagelli et al., 2009). Proposed Determination 2012). Commercial trawls take over a Distribution of populations is dozen species of sea snakes (Heatwole Based on our consideration of the best discontinuous, with deep water, strong 1997; Wassenberg et al., 2001; Zhou et available data, as summarized here and currents, or coast exposed to severe al., 2012), and in the absence of bycatch in Manning (2014), and protective weather serving as effective ecological reduction devices (BRDs), an estimated efforts being made to protect the barriers to migration (Bernardi and 48.5 percent of all incidentally captured species, we conclude that the dusky sea Vagelli, 2004; Ndobe et al., 2012; Ndobe sea snakes will die (Wassenberg et al., snake, A. fuscus, is currently at high risk and Moore, 2013). The Banggai 2001). BRDs are required in the prawn of extinction throughout its range. We cardinalfish exhibits the highest known trawl fishery to minimize bycatch therefore propose to list it as degree of genetic structure of any mortality and help conserve protected endangered under the ESA. marine fish (Bernardi and Vagelli, 2004; species. The only trawl fishery that Banggai Cardinalfish Hoffman et al., 2005; Vagelli et al., operates within the range of the dusky 2009). Populations occurring on the sea snake is the North West Slope Trawl The following section describes our same reef, separated by only a few Fishery (NWSTF). The Australian analysis of the status of the Banggai kilometers, are genetically isolated from Fisheries Management Authority cardinalfish, Pterapogon kauderni. More one another (Bernardi and Vagelli, 2004; (AFMA) reports that the NWSTF, which details can be found in Conant (2014). Hoffman et al., 2005; Vagelli et al., targets three scampi species (lobsters), is Species Description 2009). a low effort fishery with a very low level The Banggai cardinalfish is generally of bycatch and no documented The Banggai cardinalfish is a species found in calm waters of sheltered bays interactions with threatened, within the family Apogonidae and or on the leeward side of islands (Allen endangered, or protected species genus Pterapogon. It was discovered in and Donaldson, 2007). It inhabits a (AFMA, 2012). The NWSTF is also a 1920 by Walter Kaudern and described variety of shallow (from about 0.5 to 6 deep-water fishery, and thus unlikely to by Koumans (1933). The genus m) habitats including coral reefs, encounter the reef-associated dusky sea Pterapogon contains one other species, seagrass beds, and less commonly, open snake (Fry et al., 2001; Lukoschek et al., P. mirifica, from northwestern Australia areas of low branching coral and rubble. 2007a; Lukoschek et al., 2013). As (Allen and Donaldson, 2007). To avoid predators, it associates with discussed here and in further detail in The Banggai cardinalfish is a microhabitats such as sea urchins and the status review report (Manning, relatively small marine fish. Adults anemones (Vagelli, 2011). Banggai 2014), there is no indication that direct generally do not exceed 55 to 57 mm cardinalfish are found in waters ranging harvest or incidental capture poses a standard length (Vagelli, 2011). The from 26–31 °C, but averaging 28 °C threat to the dusky sea snake. species is distinguished from all other (Ndobe et al., 2013). Sea snake products have been traded apogonids by its tasseled first dorsal fin, The Banggai cardinalfish, like many internationally since the 1930s (Marsh elongated anal and second dorsal fin apogonids, exhibits reversed sex roles, et al., 1994), but no sea snake species is rays, and deeply forked caudal fin where males provide parental care and currently listed under the Convention (Allen, 2000). It is brilliantly colored, brood eggs in their mouths. It lacks a on International Trade in Endangered with contrasting black and light bars planktonic larval stage and extends the Species of Wild Fauna and Flora with whitish spots over a silvery body. brooding of larvae for about 7 days after (CITES). Australia’s Wildlife Protection The Banggai cardinalfish has an hatching, which results in the release of Act 1982 restricts the export of sea exceptionally restricted natural range fully formed juveniles. Spawning occurs snake products out of Australia (Marsh (approximately 5,500 km2) within the year round but peaks around September et al., 1994). There are no data to suggest Banggai Archipelago, Indonesia. through October, which is a period of that the dusky sea snake is threatened Populations have been introduced in fewer storms in the region (Ndobe et al., by past, present, or future trade. areas of Indonesia outside of the 2013). The Banggai cardinalfish has the Despite their apparent Banggai Archipelago, including Luwuk lowest fecundity reported for any substantiveness, these existing and Harbor (Bernardi and Vagelli, 2004), apogonid (Vagelli, 2011). Generation ongoing conservation efforts seem Palu Bay (Moore and Ndobe, 2007), length (the age at which half of total unlikely to prevent further decline of Lembeh Strait (Erdmann and Vagelli, reproductive output is achieved by an the dusky sea snake, because they have 2001), Tumbak (Ndobe and Moore, individual) is estimated to be 1.5 years failed to prevent the decline of the 2005), Kendari Bay (Moore et al., 2011), (Vagelli, New Jersey Academy for species to date. For example, decades of and north Bali (Lilley, 2008). These Aquatic Sciences (NJAAS), personal protections at Ashmore Reef, while introductions are a result of discards communication cited in Allen and maintaining this as a relatively pristine from the ornamental live reef aquarium Donaldson (2007)) to 2 years (Ndobe et reef (Hale and Butcher, 2013), have not trade and introductions by dive-resort al., 2013). Its lifespan in the wild has prevented the severe decline and likely operators to support the tourist industry been estimated at approximately 2.5–3 extirpation of dusky sea snakes there. (Vagelli, 2011). The introduced years (Vagelli, 2011), with a maximum Furthermore, the threat posed by populations are an artifact of the lifespan up to 3–5 years (Ndobe et al., hybridization is beyond the scope of commercial ornamental live reef trade 2013). Based on a conservative estimate, existing protections. We are thus not and are not part of any conservation a male could incubate/brood able to conclude that the existing program to benefit the native approximately 400 to 640 offspring over protective efforts alter the extinction populations. Because we interpret the his lifespan (Vagelli, personal risk for the dusky sea snake. We are not ESA as conserving species and the communication, 2014), of which less

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than 5 percent may survive to adulthood over time, in density and abundance. baseline for historical abundance. (Vagelli 2007 as cited in CITES (2007)). Ndobe (et al., in press) stated that their However, even without that data, it is High mortality occurs during the first 2011–2012 estimate of 1.5–1.7 million clear that population abundance days after release from the brood pouch represented 62–71 percent of the estimates at sites throughout the due to predation, including parental and abundance estimate of 2.4 million from Banggai Archipelago declined non-parental cannibalism (Vagelli, the 2004 survey. A total abundance significantly between 2004 and 2011– 1999). estimate was not provided for the 2007 2012. Banggai cardinalfish form stable survey, however mean observed density Declines and extirpations of local groups. Natural group size is difficult to decreased approximately 38 percent populations have been observed across know because group size decreases with between 2007 (0.08 fishes per m2) and years, likely due to directed harvest and, fishing pressure, and most populations 2011–2012 (0.05 fishes per m2). more recently, habitat destruction. In are not pristine. However, one bay Historical data on abundance are the 2001 survey, Bakakan Island had (oyster pearl farm) in private ownership lacking, as surveys were done after about 6,000 fish, but by the 2004 census, in the Banggai Islands had, until 2006, harvest began in the early to mid-1990s. only 17 fish remained (Vagelli, 2008). In never been fished, and group size The private oyster pearl farm mentioned the 2007 survey, 350 individuals were averaged about 13 fish, but varied from above is thought to represent a proxy for found at Bakakan Island, but this was 2–33 fish per group (Lunn and Moreau, historical abundance by several still well below the 6,000 fish found in 2002). At the same site in 2004, group researchers, though others disagree that the 2001 survey (Vagelli, 2008). In 2014, Moore (personal communication) size varied from 1 to over 200 fish per the site is representative of historical group (Moore, unpublished data, 2014). reported that local fishers characterize abundance. The private oyster farm Group size is typically less than 25 the cardinalfish population on Bakakan exists within a privately owned bay in individuals, although smaller groups are Island as small and declining. Between Banggai Island, and fishing has been common and vary by age class and the 2001 and 2004 surveys, the prohibited there since trade began, habitat type (Vagelli, 2011). population density at Masoni Island although illegal poaching in the bay was The first scientific surveys of Banggai doubled from 0.03 to 0.06 fish per m2 reported in 2006 (Talbot et al., 2013). cardinalfish estimated population (an increase of approximately 150 fish The habitat in the bay may be similar to abundance and density between 1.7 in 3 years) (Vagelli, 2005). This increase other sites that support the Banggai million, with a mean density of 0.03 is thought to have occurred in response cardinalfish; thus, several researchers fishes per m2, based on a census at three to a collecting ban that the local people sites in 2001 (Vagelli, 2002; Vagelli and claim this population can be used as a imposed in early 2003. However, in the Erdmann, 2002), and 2.4 million, with proxy for a baseline of population 2007 survey, the population was found a mean density of 0.07 fishes per m2, abundance (Allen and Donaldson, 2007; to have declined to 0.008 fish per m2, based on an expanded census of 34 sites Vagelli, 2008). In 2001, densities of fish with 38 fish recorded over the entire conducted in 2004 (CITES, 2007). In in the private oyster pearl farm averaged census site (the largest group consisted ± 2 2007, population the density estimate of 0.63 0.39 fishes per m (1 standard of 2 individuals). An extensive search the expanded survey sites indicated a deviation, SD) (range: 0.28 to 1.22 fishes around the entire island identified only 2 mean density of 0.08 fishes per m2 per m ) (Lunn and Moreau 2002) and 150 fish (Vagelli, 2008). A population in 2 (Vagelli, 2008); however, overall 0.58 fishes per m in 2004 (Vagelli southeast Peleng Island had 159 and 207 population abundance was not reported 2005). When these densities are fish in 2002 and 2004, respectively for the 2007 survey. By 2011–2012, compared to the densities found in the (Vagelli, 2005). However, by 2007, it Ndobe et al. (in press) estimated the 2001 and 2004 survey data discussed had been practically extirpated, with population abundance at 1.5–1.7 above, they indicate that the Banggai only 27 fish found (Vagelli, 2008). million, with a mean observed density cardinalfish abundance has declined up Overharvest of microhabitat, such as of 0.05 fishes per m2, reportedly for the to 90% from historical levels (Allen and Diadema sea urchins and sea anemones, 24 of the 34 sites that were surveyed in Donaldson, 2007; Vagelli, 2008). and coral mining have resulted in local 2004 and 2007. The 2011–2012 However, several researchers (Moore, population depletions on an island off estimates does not include locations in Sekolah Tinggi Perikanan dan Kelautan Liang, which was surveyed in 2004, and Toado where the habitat was limited (STPL), personal communication 2014; was extirpated by 2012 (Ndobe et al., and density was very high (Ndobe et al., Ndobe, Tadulako University, personal 2013). Extirpation of local populations in press); thus, the population communication 2014) caution against has been documented in areas with abundance estimate likely is biased low. the use of this bay as a baseline for increased harvest of microhabitat, However, 7 of the major sites first population trends. Banggai cardinalfish combined with fishing pressure on surveyed in 2004 have declined in population distribution is inherently Banggai cardinalfish. Interviews with abundance and mean density (Ndobe et patchy, and density is highly variable locals and visits to several sites in 2011 al., in press), indicating the population between and within sites of the Banggai and 2012 indicate populations are has likely decreased from the 2.4 Archipelago, including this bay (Moore, declining in the Banggai Archipelago million estimated in 2004. Although the unpublished data, 2004). The (Ndobe et al., 2013). mean observed density estimate of 0.03 researchers also question whether the fishes per m2 found in the 2001 survey habitat in the bay is comparable to other Summary of Factors Affecting the (Vagelli, 2002; Vagelli and Erdmann, sites. The bay has been protected from Banggai Cardinalfish 2002) is less than the 2011–2012 survey, degradation because it is privately Next we consider whether any one or the 2001 survey was based on only three owned and contains significant amounts a combination of the five threat factors sites, while the 2011–2012 survey was of sheltered habitat and good quality specified in section 4(a)(1) of the ESA based on 24 sites of the 34 sites. Ndobe microhabitat/habitat, with limited are contributing to the extinction risk of (et al., in press) selected the expanded suitable habitat for predators of the the Banggai cardinalfish. We discuss survey sites from 2004 and 2007 for cardinalfish, such as groupers and other each of the five factors below, as all their 2011–2012 survey based on the larger reef fish. We acknowledge the factors pose some degree of extinction author’s previous work on habitat debate regarding the use of the data risk. More details are available in conditions and to better compare trends, from the private oyster farm as a Conant (2014).

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Present or Threatened Destruction, showed coral reef cover declined by lacking on the extent of impact the Modification, or Curtailment of Habitat more than half, from 25 percent to 11 disease poses to Banggai cardinalfish or Range percent (Moore et al., 2011; 2012). Major habitat. causes of the coral reef decline around The illegal use of fish bombs Overutilization for Commercial, Banggai Island were attributed to (typically made with fertilizer and Recreational, Scientific, or Educational destructive fishing methods and general phosphorus) and cyanide to catch fish Purposes has resulted in significant loss of coral fishing pressure, coastal development, The Banggai cardinalfish is traded reef habitat within the Banggai and the replacement of traditional internationally as a live marine cardinalfish range (Allen and Werner, homes with concrete and breeze-block ornamental reef fish. It has been 2002). Damage to coral reefs due to fish dwellings, which increases the demand for mined coral and sand. Loss of coral collected in the Banggai Islands, bombs is prevalent, even in protected Indonesia, since 1995 (Marini and areas (Talbot et al., 2013). Cyanide is reef cover may increase mortality of Banggai cardinalfish recruits due to Vagelli, 2007). The United States, used to catch fish for the live reef fish Europe, and Asia are the major trade, and the practice kills corals (e.g., cannibalism (Moore, personal communication, 2014; Ndobe et al., in importers of the Banggai cardinalfish for see Jones and Steven, 1997; Mous et al., the aquarium trade (CITES, 2007). The 2000). Boats have degraded the coral press). Climate change may also impact Banggai cardinalfish is the tenth most reefs in the area, and clear-cutting of Banggai cardinalfish habitat as a result common ornamental fish imported into wooded slopes and mangroves has of coral bleaching. Coral bleaching the United States (Rhyne et al., 2012). occurred, increasing sedimentation, events due to warming temperatures are Banggai cardinalfish exports for the which degrades coral reef habitat anticipated to increase by 2040 in areas ornamental live reef fish trade may be (Lilley, 2008). Other upland activities, of the Indian Ocean, including waters of decreasing, although systematic data are such as agriculture and human Indonesia (van Hooidonk et al., 2013). lacking. In 2001, up to 118,000 Banggai population growth, have increased the Coral bleaching due to elevated water cardinalfish were sold to trade centers amount of waste and nitrates in the temperatures has not been observed each month, with a total estimate of marine environment, promoting algal around Banggai Island up through 700,000–1.4 million fish traded (Lunn blooms (Lilley, 2008), which may December 2011; however, extensive and Moreau, 2002, 2004). From 2004 destroy coral reefs by outcompeting bleaching was observed in nearby through 2006, around 600,000–700,000 them for vital resources such as light Tomini Bay in 2010 (Moore et al., 2011; fish were traded yearly (Moore et al., and oxygen (reviewed by Fabricius, 2012). The Banggai cardinalfish is 2011). In 2008 and 2009, 236,373 and 2005). Significant plastic, styrofoam, restricted to shallow waters with 330,416 fish, respectively, were traded and other human-made debris occurs in ambient temperatures ranging from 28 at Bone Bone, Toropot, and Bone Baru the area (Lilley, 2008). This information to 31 °C. Thus, warming temperatures trade centers (Moore et al., 2011, 2012). indicates destruction of habitat is may render habitat unsuitable, but However, these numbers do not include occurring within the Banggai specific data on impacts to the Banggai trading data from Bone Bone in 2008 cardinalfish’s range. Although cardinalfish are lacking. and other active centers (e.g., Panapat quantitative data on impacts to Sea urchins and anemones are for 2008 and 2009). These collections cardinalfish populations are lacking, experiencing intensive and increasing centers each reported about 15,000 fish considerable qualitative information harvest pressure, which negatively per month in 2007 (Vagelli, 2008; 2011). exists indicating that where habitat has impacts the Banggai cardinalfish (Moore Vagelli (personal communication, 2014) been degraded (e.g., Tanjung Nggasuang et al., 2012; Ndobe et al., 2012). Sea estimates that 1,000,000 Banggai and Toropot surveyed in 2004 and 2012, anemones were once abundant but were cardinalfish are currently captured each and Mbuang-Mbuang, on Bokan Island, drastically reduced from Tinakin Laut, year for the ornamental live reef trade. surveyed in 2012), large and thriving Banggai Island, which resulted in a The ornamental live reef fish trade Banggai cardinalfish populations spread collapse of the Banggai cardinalfish has resulted in decreases in cardinalfish over large areas can be reduced to population in the area (Moore et al., population density and extirpation of isolated remnants crowded into small 2012). Heavy harvest of sea anemones at local populations. By 2000 (after less remaining patches of habitat with some Mamboro, Palu Bay, resulted in a drastic than a decade of trade), negative protective microhabitat (Ndobe, reduction of new recruits and juvenile impacts on the Banggai cardinalfish personal communication, 2014). Banggai cardinalfish (observed since from the trade were observed. The trade Coral reef conditions in the Central 2006) in 2008 (Moore et al., 2011). results in high mortality of cardinalfish Sulawesi Province, including the Moore et al. (2011; 2012) report that collected. Based on interviews with Banggai Archipelago, were examined intensive harvesting of shallow water collectors, Lilley (2008) estimated that from 2001 through 2007 in seven invertebrates, including sea anemones only one out of every four to five fish Districts in the region (Moore and and sea urchins, is increasing and is collected makes it to the buyer for Ndobe, 2008). Average condition of the linked to socio-economic trends export due to high mortality and discard reefs was poor, and major impacts associated with consumption by local practices. Density and group size of included coral mining, sedimentation, seaweed farmers and use as feed for cardinalfish and sea urchins are fishing, and predation (Moore and carnivorous fish destined for the negatively impacted by the trade (Kolm Ndobe, 2008). Population explosions of ornamental live reef trade. and Berglund, 2003). Ndobe and Moore the crown-of-thorns starfish In addition, a disease of unknown (2009) also found that populations were (Acanthaster planci), a coral predator, origin may be damaging hard corals in exploited, but observed high population have been observed in the area, habitat occupied by the Banggai density in areas where collection had indicating an ecological imbalance, cardinalfish. The disease affects the top been ongoing for some years with likely due to overharvest of natural sections of long-branched rotation between sites, indicating some predators and changes in hydrology and species as well as species of Porites, harvest sustainability. Unfortunately, water quality (Moore et al., 2012). both of which are important habitat destruction and collection and Surveys conducted at five sites around microhabitat for the Banggai destruction of microhabitat (unrelated to Banggai Island from 2004 through 2011 cardinalfish (Vagelli, 2011). Data are the Banggai cardinalfish fishery) have

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now greatly reduced cardinalfish pressure on the natural population, but Legislation is needed to establish populations at sites which had the concept requires further research fishing quotas and size limits; however, previously sustained periodic collection before it can be implemented at a local no legally binding regulations have been for more than a decade (Moore, personal community level (Ndobe, personal passed or implemented (Moore et al., communication, 2014). Decreases in communication, 2014). 2011). Indonesia prohibits the use of population density are also evidenced chemicals or explosives to catch fish Disease or Predation by significant declines in the catch per (Fisheries Law No. 31/2004, Article unit effort (Vagelli, personal Predation and cannibalism are high 8(1)). However, the practice continues communication, 2014). In Bone Baru, among new recruits (Moore et al., 2012). (Vagelli, 2011), and damage to coral from 1993–2000, fishers were catching However, specific data are lacking on reefs due to fish bombs is prevalent, an average of 1,000–10,000 fish per day, whether predation pressure is even in protected areas (Talbot et al., but by 2003 they only averaged 100– increasing or impacting the Banggai 2013). 1,000 per day, with most catching cardinalfish population growth beyond In 2011, Indonesia had proposed to between 200–300 fish (EC-Prep Project, natural levels. list the Banggai cardinalfish for 2005). Prior to 2003, collectors from A virus known as the Banggai restricted protected status under Bone Baru typically required one day to cardinalfish iridovirus (genus domestic law. But the proposal stalled capture approximately 2,000 specimens. Megalocytivirus) is linked to high when the Indonesian Institute for In 2007, they reported requiring one mortality of wild-caught fish imported Science argued that the introduced week to capture the same number for the ornamental live reef fish trade populations meant the species was no (Vagelli, 2011). Vagelli (2011) reports (Vagelli, 2008; Weber et al., 2009). The longer endemic, and thus did not meet similar declines for Banggai Island, virus causes necrosis of spleen and the criteria for protected status (Moore, where between 2000 and 2004, the renal tissue, which appears as darkened personal communication, 2014; Ndobe, reported mean catch declined from tissue. Other symptoms are lethargy and personal communication, 2014). In about 1,000 fish/hour to 25–330 fish/ lack of appetite. Surveys of wild 2007, the Banggai cardinalfish was hour. populations have not reported proposed for listing under CITES Information suggests the number of symptoms of the disease. Necropsies of Appendix II. However, the proposal active participants in the trade may over 100 fish collected in the wild and failed. The species is listed in Annex D have dropped. In 2001, there were 12 at holding facilities showed no of the European Wildlife Trade villages that collected the Banggai indication of the virus (Talbot et al., Regulations, which only requires cardinalfish, but only 3 were active in 2013). Thus, the virus is likely monitoring of European Union import 2011 (Moore et al., 2011, 2012), and at transmitted from other specimens at levels through import notifications. least 5 villages were active in 2014 containment centers, or is carried by the Based on the weaknesses discussed (Moore, personal communication, 2014). Banggai cardinalfish and is only above, regulatory mechanisms on the Reported as number of collectors, the expressed as a result of stress incurred commercial harvest industry do not data indicate a decline in participation during the long transport process appear adequate to ensure the as well, from about 130 in 2001 (Lunn (Weber et al., 2009; Talbot et al., 2013) population will be sustainable. and Moreau, 2004) to about 80 in 2007 and may not be a concern for wild fish. (Vagelli, 2011) and 2012 (Vagelli, Other Natural or Manmade Factors Inadequacy of Existing Regulatory Affecting Continued Existence personal communication, 2014). Mechanisms In 2012, a large-scale aquaculture Global averaged combined land and facility based in Thailand began to Current Indonesian legislation ocean surface temperatures show a breed Banggai cardinalfish in captivity requires that all trade in Banggai warming of 0.85 °C over the period 1880 for export, which may alleviate some of cardinalfish go through quarantine to 2012 (IPCC, 2013). As discussed the pressure to collect fish from wild procedures before crossing internal earlier (see Present or Threatened populations (Talbot et al., 2013; Rhyne, administrative borders or prior to export Destruction, Modification, or Roger Williams University, unpublished (Moore et al., 2011). Compliance Curtailment of Habitat or Range), data 2014). In 2013, approximately historically has been low, but is warming temperatures may destroy or 120,000 Banggai cardinalfish were improving (Moore, personal modify habitat, but data are lacking on imported into the United States from the communication, 2014; Moore et al., specific direct impacts to the Banggai Thailand facility. The volume 2011). However, reported collection cardinalfish. represents a significant portion of through the Fish Quarantine Data The Banggai Archipelago sits at the overall United States imports of the system, which records fish that go junction of three tectonic plates cardinalfish and may even exceed the through quarantine procedures, was (Eurasian, Indian-Australian, and number of wild fish currently imported well below the total reported collection Pacific-Philippine Sea) and is (Rhyne, unpublished data, 2014). Efforts from Bone Baru, Toropot, and Bone vulnerable to earthquakes. An to captive-breed the species in the Bone for 2008 and 2009. Bone Baru, earthquake measuring 7.6 on the Richter United States are also ongoing, which Toropot, and Bone Bone reported scale occurred in 2000 and destroyed may alleviate dependence on wild- collection of 236,373 fish in 2008 and coral reefs in the region (Vagelli, 2011). caught cardinalfish. In the United 330,416 fish in 2009. Whereas in 2008 Frequent earthquakes within the States, the Florida Department of and 2009, the Fish Quarantine Data Banggai Archipelago may have Agriculture and Consumer Services has reported collection of 83,200 and impacted localized Banggai cardinalfish certified eight aquaculture facilities that 215,950 fish, respectively (Moore et al., populations (CITES, 2007), but specific are beginning to culture and market 2011). Enforcement of the Fish data are lacking. farm-raised Banggai cardinalfish Quarantine procedures is weak, and (Knickerbocker, Florida Department of illegal, unregulated, and unreported Extinction Risk Agriculture and Consumer Services, capture and trade are still a major The life history characteristics (i.e., personal communication 2014). In-situ problem, especially in remote areas low fecundity, high degree of parental breeding by the fishing communities in (Ndobe, personal communication, care and energetic investment in the endemic area may also alleviate 2014). offspring, high new recruit mortality, no

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planktonic dispersal, high site fidelity) the foreseeable future, which negatively with ongoing and projected threats to of the Banggai cardinalfish render it less impacts the Banggai cardinalfish and its habitat and microhabitat, commercial resilient and more vulnerable to ability to avoid predators. use, inadequate regulatory mechanisms, stochastic events than marine species Overutilization from direct harvest for disease and predation, and additional that are able to disperse over large areas the ornamental live reef fish trade has natural or manmade factors, we and recolonize sites that have been lost significantly impacted the Banggai conclude that demographic risks and due to these events. Because the Banggai cardinalfish and remains a concern. the combination of threats to the species cardinalfish also has an exceptionally Trade continues resulting in high may contribute to the overall restricted natural range (approximately mortality, and in areas of heavy vulnerability and resiliency of the 5,500 km2), these demographic traits overexploitation, populations have been Banggai cardinalfish. The Banggai become more important in terms of the extirpated. However, an increase in cardinalfish has experienced a decline extent to which the threats appreciably compliance with the Fish Quarantine in abundance as evidenced by the reduce the fitness of the species. The regulations and improved trade decrease in mean density at survey sites Banggai cardinalfish lacks dispersal practices have occurred in recent years, between 2004 and 2012. Moreover, at ability and exhibits high site fidelity, and we anticipate compliance and trade least some researchers believe that the and new recruits stay within parental practices will likely continue to population may have experienced a habitat. Thus, recolonization is unlikely improve in the future, which may dramatic decline from historical once a local population is extirpated. mitigate impacts through sustainable abundance due to overharvest based on Local populations off Liang and Peleng trade. Participation in collection of comparisons between populations in a Island are reported extirpated, and Banggai cardinalfish for the live private bay and other populations. Most interviews with local fishermen indicate ornamental reef trade has dropped in of the species’ demographic extirpation of small local populations recent years. Captive-bred facilities have characteristics put it at a high risk of throughout the Banggai Archipelago. recently started in the United States and extinction. However, the threat of The Banggai cardinalfish also exhibits Thailand and are anticipated to decrease overharvest has been and will likely high genetic population substructuring; the threat of directed harvest of the wild continue to be reduced in the future. thus, extirpation of local populations populations in the future. Predation of Further, the overall population from overharvest and/or loss of habitat new recruits is high. Mortality from abundance (1.5 to 1.7 million) may can result in loss of genetic diversity disease in wild-caught fish imported for allow some resilience against stochastic and further fragmentation of spatial the ornamental live reef fish trade and events; thus, placing the Banggai distribution. In considering the disease affecting the Banggai cardinalfish at an overall moderate risk demographic risks to the species, its cardinalfish habitat are both plausible of extinction. threats. However, data are lacking on growth rate/productivity, spatial Protective Efforts structure/connectivity, and diversity are how these threats impact the population The Banggai cardinalfish is listed as assigned to the high risk of extinction and what, if any, impacts will occur and ‘endangered’ by the World Conservation category. However, the overall at what rate in the future. Climate Union (IUCN; Allen and Donaldson, population abundance (estimated at 1.5 change within the Banggai cardinalfish 2007). Although listing under the IUCN to 1.7 million) is assigned to the range will continue to affect coral reefs provides no direct conservation benefit, moderate risk of extinction category, in the future, and it is reasonable to expect that future earthquakes that may it raises awareness of the species. In because the abundance may allow some addition, the Banggai cardinalfish was resilience against stochastic events. destroy or modify habitat within the species’ range will occur at the current one of the first entrants into the Frozen In considering the threats, we rely on rate. Ark Project, which is a program to save the best available data to assess how the The Banggai cardinalfish is exposed, the genetic material of imperiled species threats are currently impacting or likely and negatively responds to some degree, (Williams, 2004; Clarke, 2009). to impact the species in the foreseeable to the five threat factors discussed In 2007, Indonesia developed a future. The best available data indicate above. Although quantitative analyses national multi-stakeholder Banggai that several threats to the Banggai are lacking, it is reasonable to expect cardinalfish action plan (BCF–AP), cardinalfish will continue and increase, that when these exposures are which focused on conservation, trade, with the species responding negatively, combined, synergistic effects may occur. and management issues (Ndobe and but other threats will decrease, with the For example, the ornamental live reef Moore, 2009). As part of the BCF–AP, species responding favorably. Habitat fish trade likely causes the expression of annual stakeholder meetings are held to degradation has occurred and is the iridovirus in the Banggai share data, review progress, and set anticipated to continue and increase in cardinalfish, which results in increased goals (Moore et al., 2011). The BCF–AP the foreseeable future. Although mortality. The indiscriminate harvest of called for biophysical and socio- Indonesia prohibits the use of chemicals sea anemones and sea urchins and economic monitoring of trade, or explosives to catch fish, historically, destruction of coral reefs eliminates population status, and habitat, and compliance has been low, and data important cardinalfish shelter and several organizations have begun to indicate compliance is not improving. substrate and increases the likelihood of report on these activities. However, Data also indicate that by 2007, harvest predation. Interactions among these there is no integrated or comprehensive of microhabitat (sea urchins and sea threats may lead to a higher extinction monitoring system, and long-term data anemones) had negatively impacted risk than predicted based on any sets are lacking (Moore et al., 2011). cardinalfish populations, and the individual threat. Several aspects of the BCF–AP appear to harvest had increased by 2011. Moore et In sum, based on the life history have improved the sustainability of the al. (2011, 2012) concluded that it would characteristics of the Banggai Banggai cardinalfish trade. Fishermen be difficult to establish and enforce cardinalfish, which indicate high groups have gained legal status local regulations for controlling the vulnerability to demographic risks (due (allowing them access to various overharvest of microhabitat. Thus, it is to trends in population growth/ benefits such as funding or loan reasonable to expect that microhabitat productivity, spatial structure and support), which has led to socialization harvest will continue and increase in connectivity, and diversity), coupled of sustainable harvest in Bone Baru. The

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legally-established fishermen’s group It is uncertain whether the MPA will be populations). The STPL EAFM Learning Kelompok BCFLestari, in Bone Baru, changed in the foreseeable future to Centre team will be implementing this implemented collection practices better suit the species. component through January 2015. These designed to prevent capture of brooding Although no longer active, the Marine efforts are likely to introduce local males (Moore et al., 2011). Workshops Aquarium Council (MAC), an measures to sustain the Banggai have been held on improving capture international non-governmental cardinalfish trade (Moore, personal methods and post-harvest care, and organization, developed a certification communication, 2014; Ndobe, personal several community members have system to improve the management of communication, 2014). become active in conservation efforts. the marine aquarium trade. MAC Under the PECE, conservation efforts However, the BCF–AP officially ended developed best practices for collectors not yet implemented or not yet shown in 2012 and so did the funding. Some and exporters, including those in to be effective must have certainty of of the stakeholders are still active and Indonesia. Best practices include implementation and effectiveness before are likely to continue to be so, despite improvement of product quality, being considered as factors decreasing lack of government support (Moore, reduction in mortality rates, safer extinction risk. The effort described personal communication, 2014). practices for collectors, and fairer prices above does not satisfy the PECE criteria As discussed earlier, compliance with paid to collectors. By applying the MAC of having a certainty of implementation the Fish Quarantine regulations has standards, traders could be certified as and effectiveness. Although a pilot increased, which is largely due to the meeting these international standards project in Central Sulawesi Province development and implementation of the (Lilley, 2008). Building on the MAC under the ecosystems-based approach is BCF–AP (Moore et al., 2011). In 2004, efforts, the Yayasan Alam Indonesia underway with the Banggai cardinalfish one Banggai cardinalfish trader followed Lestari (LINI) has worked in the Banggai as one of five fisheries case studies, we Fish Quarantine procedures. By 2008, Islands to promote a sustainable fishery lack information on how this effort will there was a marked increase in legal for the Banggai cardinalfish and to yield measures that will be funded, trade, but unreported fishing still occurs protect habitat (Talbot et al., 2013). LINI regulated, or regularly practiced to (Moore et al., 2011). With the lapse of focuses on surveys, capacity building, sustain the Banggai cardinalfish trade in the BCF–AP, legislation is needed to and training of local suppliers and reef the future; thus, this effort cannot be support and restart the goals described restoration (Lilley, 2008). LINI’s training considered to alter the risk of extinction in the BCF–AP, and although efforts and education efforts may raise of the Banggai cardinalfish. We seek have been ongoing to establish fishing awareness of needed conservation additional information on other quotas and size limits, no legally efforts to benefit the Banggai conservation efforts in our public binding regulations have been passed or cardinalfish. For example, more benign comment process (see below). implemented (Moore et al., 2011). collection methods have been In 2007, the Banggai Cardinal Fish implemented at Bone Baru, the species Proposed Determination Centre (BCFC) was established in the has been adopted as a mascot, and local Based on the best available scientific Banggai Laut District to serve as a citizens craft and market items related and commercial information discussed central point for sharing information to the fish. LINI is also trying to set up above, we find that the Banggai and managing the species over a wider a mechanism for hobbyists to buy only cardinalfish is at a moderate risk of community area (Lilley, 2008; Moore et from distributors who use best practices extinction, but the nature of the threats al., 2011). As of 2011, the BCFC had no and are sustainable (Talbot et al., 2013). and demographic risks identified do not electricity, no operational budget, and However, continued funding for the suggest the species is presently in was operated on a voluntary basis program is a concern (Moore, personal danger of extinction, and therefore, it (Moore et al., 2011). Further inhibiting communication, 2014). does not meet the definition of an the continued operation of the BCFC is In addition to the protective efforts endangered species. We do find, that in 2013, the region was split into described above, Indonesia has however, that both the species’ risk of two Districts by constitutional law (UU committed to develop a comprehensive extinction and the best available No. 5/2013). The BCFC will need to be management plan for the Banggai information on the extent of and trends officially approved under the new cardinalfish under the auspices of in the major threats affecting this District to maintain its legal status Indonesia’s national plan of action species (habitat destruction and (Ndobe, personal communication, under the Coral Triangle Initiative on overutilization) make it likely this 2014). Coral Reefs, Fisheries, and Food species will become an endangered A marine protected area (MPA) Security (CTI–CFF). The CTI–CFF species within the foreseeable future consisting of 10 islands was declared by specifies a goal to use an ecosystems- throughout its range. We therefore Indonesia in 2007, with conservation of based approach to managing fisheries propose to list it as threatened under the the Banggai cardinalfish as the primary (EAFM), including a more sustainable ESA. goal of the Banggai and Togong Lantang trade in live reef fishes. In 2013, World Islands (Ndobe et al., 2012). However, Wide Fund for Nature (WWF), in Harrisson’s Dogfish Banggai cardinalfish populations are not partnership with STPL, implemented a The following section describes our found at Togong Lantang Island, while pilot project in Central Sulawesi analysis of the status of the gulper for three other islands within the Province under the ecosystems-based shark, Harrisson’s dogfish proposed MPA with known approach and chose the Banggai (Centrophorus harrissoni). More details populations, Banggai cardinalfish cardinalfish as one of five fisheries case can be found in Miller (2014). conservation is not included as a studies in Banggai Laut District. The conservation goal in the designation goal is to draft local regulations for an Species Description (Ndobe et al., 2012). In addition, based EAFM for two Districts—Banggai Laut Centrophorus harrissoni, or on genetic analysis, only 2 of 17 known District (which encompasses the Harrisson’s dogfish, is a shark belonging populations occur within the MPA, majority of the endemic Banggai to the family Centrophoridae (order which led Ndobe et al. (2012) to cardinalfish populations) and Banggai Squaliformes). The Centrophoridae conclude the MPA design was ill-suited Kepulauan District (which includes the contain two genera: Deania (long- for conserving the Banggai cardinalfish. Peleng Island Banggai cardinalfish snouted or bird-beak dogfishes) and

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Centrophorus, usually referred to as zones sampled (with the exception of genetically distinct, and tagging studies gulper sharks. ‘‘Gulper shark’’ is also the the two sites noted above) and juveniles are limited, with insufficient recapture common name for the largest species, C. evenly interspersed with adults across rates to make any determination granulosus (White et al., 2013). all depths. regarding the connectivity of the Harrisson’s dogfish is endemic to In terms of mating and reproductive populations. In addition, there are a subtropical and temperate waters off behavior, which could provide some number of other uncertainties associated eastern Australia and neighboring insight into potential spatial structuring, with the assumption of two separate seamounts. Specimens identified as C. very little information is available. It is Harrisson’s dogfish stocks, including harrissoni have also been collected known that Harrisson’s dogfish is necessary sex ratios and other along the Three Kings, Kermadec, and viviparous (i.e., gives birth to live successful reproduction requirements, Norfolk Ridges north of New Zealand, young), with a yolk-sac placenta. which are further discussed in Miller and it has also possibly been identified Females have litters of one or (more (2014). Due to these uncertainties, we off (Duffy, 2007). It is a commonly) two pups, with size at birth do not find conclusive evidence of demersal species, primarily found along around 35–40 cm TL (Graham and separate populations of Harrisson’s the upper- to mid-continental and Daley, 2011). Although the gestation dogfish. Therefore, we consider the insular slopes off eastern Australia, from period is unknown, a 2 to 3 year period available information for these two north of Evans Head in northern New has been estimated for other stocks, including estimates of depletion South Wales (NSW) to Cape Hauy on Centrophorus species, with continuous rates and protection benefits of the island of Tasmania, and on the breeding from maturity to maximum age management measures, together when Tasmantid Seamount Chain off NSW (Kyne and Simpfendorfer, 2007; Graham we determine the status of the entire and southern Queensland (hereafter and Daley, 2011). Female C. harrissoni species throughout its range. referred to as its ‘‘core range’’). It occurs mature at sizes around 98 cm TL and Because species-specific historical in depths of 180 to 1000 m, with a reach maximum sizes of 112–114 cm and current abundance estimates are not principal depth range of 200 to 900 m TL, while males mature around 75–85 available, Williams et al. (2013a) used a (White et al., 2008; Last and Stevens, cm TL and reach maximum sizes of 95– variety of methods and analyses to 2009; Williams et al., 2013a). However, 99 cm TL (Graham and Daley, 2011). estimate the pre-fishery (pre-1980s) and specimens have been collected in Female age at maturity is estimated current abundance (in biomass units) at deeper waters from the seamounts and between 23 and 36 years of age (Daley fishery stock and sub-regional scales ridges north of New Zealand and off et al., 2002; Wilson et al., 2009; Last and (detailed information on the data southeastern Australia and in shallower Stevens, 2009; Graham and Daley, sources and methods can be found in depths off eastern Bass Strait (Daley et 2011). Longevity is estimated at over 46 Williams et al. (2013a)). Results from al., 2002; Graham and Daley, 2011; years of age (Wilson et al., 2009). the various analyses revealed that Williams et al., 2013a). Gulper sharks, Current breeding sites for Harrisson’s Harrisson’s dogfish is currently including Harrisson’s dogfish, are dogfish are thought to include waters off estimated to be at 21 percent of its pre- thought to conduct diel vertical feeding eastern Australia, from Port Stephens to fishery population size throughout its migrations, whereby the sharks ascend 31 Canyon, areas off North Flinders and core range (with a lower estimate of 11 the continental slope near dusk to Cape Barren in southeastern Australia, percent and upper estimate of 31 around 200 m depths to feed and then and waters around Taupo Seamount percent). The authors note that this descend before dawn (Williams et al., (Williams et al., 2012). These are areas overall estimate of decline is strongly 2013a), which helps to explain the large where mature males, mature females, influenced by the small declines depth distribution for the species. Small and juveniles have been recorded, and estimated on seamounts (Williams et al. bathypelagic bony fishes (particularly thus are likely to be areas that support 2013a). The continental margin myctophids, lantern fishes), viable populations where mating and population is estimated to be at 11 cephalopods, and crustaceans have been pupping occur (Williams et al., 2012). percent of its pre-fishery population size found in the stomachs of C. harrissoni However, more extensive sampling, as (range of 4 to 20 percent; with the (Daley et al., 2002). well critical information regarding the estimate influenced by uncertainty Research studies indicate that C. aspects of the Harrisson’s dogfish surrounding the level of cumulative harrissoni may also exhibit spatial breeding cycle (including necessary sex fishing effort off the northern NSW sexual segregation (Graham and Daley, ratios for successful reproduction, slope). The seamount population is 2011), based on the evidence that males preferred mating and breeding grounds, estimated to be at 75 percent of its pre- tend to dominate the sex ratios on and mating and breeding behaviors), is fishery population size (range 50 survey grounds and assumption that needed to identify and fully percent to 100 percent). females must be more abundant comprehend the spatial dynamics of Summary of Factors Affecting elsewhere to compensate for the uneven Harrisson’s dogfish. sex ratios. Specifically, sex ratios varied For management purposes, Harrisson’s Dogfish from 1.5:1 to 4.9:1 along the east coast Harrisson’s dogfish in Australia have Available information regarding of Australia, illustrating the been separated into two stocks that are current, historical, and potential threats predominance of males (Graham and considered to be ‘‘distinct’’ populations: to Harrisson’s dogfish were thoroughly Daley, 2011). Two notable sites, A ‘‘continental slope’’ stock that occurs reviewed (Miller, 2014). We find that however, did show females continuously along the Australian the main threat to the species is outnumbering males and were located eastern continental margin, and a overutilization for commercial off northern NSW, from Newcastle to ‘‘seamount stock’’ that occurs on the purposes, with the species’ natural Danger Point, and off Taupo Seamount Tasmantid Seamount Chain off NSW biological vulnerability to (Graham and Daley, 2011), providing and southern Queensland, including the overexploitation exacerbating the some support for spatial sexual Fraser, Recorder, Queensland, Britannia, severity of the threat, and hence also segregation. Interestingly, Graham and Derwent Hunter, Barcoo, and Taupo identified as a secondary threat Daley (2011) found no evidence of Seamounts. However, to date, no genetic contributing to the species’ risk of sexual or age segregation by depth, with studies have been conducted to confirm extinction. We summarize information males dominating throughout all depth that these two populations are regarding these threats and their

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interactions below, according to the Daley et al. (2002) note that in the these species were separated in the later factors specified in section 4(a)(1) of the early 1990s significant quantities of 1976 surveys, and in 1977, southern ESA. Available information does not Centrophorus spp. were also caught off dogfish comprised around 75 percent indicate that habitat destruction, eastern Victoria by fishermen using and Harrisson’s dogfish comprised 25 modification, or curtailment, disease, or droplines targeting blue-eye trevalla percent of the combined catch. In 1976– predation are operative threats on this (Centrolophus antarctica) and ling 77, Harrisson’s and southern dogfishes species; therefore, we do not discuss (Genypterus blacodes). In addition, combined represented around 9 percent, those further here. Because new some Southern and Eastern Scalefish 18 percent, and 32 percent of the total regulatory measures were just recently and Shark Fishery (SESSF) operators off fish catches off Sydney, Ulladulla, and implemented, the adequacy and Victoria used deep-set gillnets to target Eden, respectively. The overall mean effectiveness of existing regulatory Centrophorus species for their livers in catch rate (for all grounds and depths) measures is discussed in the ‘‘Protective the 1990s (Daley et al., 2002). Squalene was 126 kg/hour. This is in stark Efforts’’ section below. See Miller (2014) oil, which is extracted from the liver of contrast to the 0.4 kg/h catch rate in for full discussion of all threat deep-sea sharks, is used in a number of 1996–1997, when only 14 southern and categories. cosmetics and health products, and the 8 Harrisson’s dogfishes were caught, livers of Centrophorus species have the comprising 0.18 percent of the total fish Overutilization for Commercial, highest squalene oil content (67–89 catch weight (Graham et al., 2001). For Recreational, Scientific, or Educational percent) of any deep-sea shark. the 1976–77 surveys where the two Purposes Fishermen would keep the livers of the species were separated, the mean catch Historically, Harrisson’s dogfish and Centrophorus spp. and discard the rate of Harrisson’s dogfish was 28.8 kg/ other gulper sharks were taken in both carcasses due to their mercury content. hr caught over the course of 173 tows. Australian Commonwealth-managed However, by the time the mercury In 1996–97, the mean catch rate of commercial trawl fisheries (those that restrictions were eased in 1995 Harrisson’s dogfish was 0.1 kg/hr over are managed by the Australian Federal (allowing for carcasses to also be sold), the course of 165 tows (Graham et al., Government, in coordination with very few Centrophorus species were 1997; 2001). These decreases in survey Australian State fisheries agencies, being caught off eastern Victoria, with catch rates provide compelling evidence through the Australian Fisheries targeting of these sharks having of declines of over 99.7 percent in Management Authority (AFMA) (Kyne essentially ceased (Daley et al., 2002). relative abundance of C. harrissoni on and Simpfendorfer, 2007)) and State- Since 2002, total catch of gulper sharks the upper-slope of NSW, a core part of managed commercial trawl fisheries by Commonwealth licensed vessels has their range, after 20 years of trawling operating on the upper slope off eastern been less than 15 t per year (Woodhams activity (Graham et al., 2001). Australia, within the core range of et al., 2013). In Australia, the commercial trawl Harrisson’s dogfish. Unfortunately, little In 2001, Graham et al. (2001) fisheries are still active, as are demersal information is available on the specific quantified the effects of the historical line fisheries, which also incidentally catch of these deep-water sharks, trawling on the abundance of gulper catch Harrisson’s dogfish. In terms of primarily due to the historical sharks off NSW using data from fishery- Commonwealth-managed fisheries, inaccuracy of data reporting and species independent surveys conducted along Harrisson’s dogfish are primarily caught identification issues. These the upper slope before and after the as bycatch by the SESSF, which Commonwealth and State-managed expansion of the commercial trawl- operates over an extensive area of the commercial trawl fisheries developed fishery (Andrews et al., 1997). The Australian Fishing Zone (AFZ) around off NSW in the 1970s and off Victoria initial pre-fishery survey was carried eastern, southern, and southwestern and Tasmania in the 1980s. By the early out during 1976 and 1977. There were Australia. The distribution of recent 1980s, more than 100 trawlers were three trawling survey grounds: (1) (2006–2010) commercial fishing effort operating off NSW, with around 60 Sydney-Newcastle, (2) Ulladulla- in the SESSF shows that there is still percent regularly fishing on the upper Batemans Bay, and (3) Eden-Gabo Island substantial fishing effort on slope. In fact, between 1977 and 1988, and eight depth zones (covering depths Commonwealth upper-slope grounds catches from these upper-slope trawl of 200–650 m). The two northern using demersal gears, specifically trawl operations comprised more than half of grounds (Sydney and Ulladulla) were and auto-longline operations (see Miller the total trawl landings in NSW surveyed twice in 1976 and twice in (2014) for more details). According to (Graham et al., 2001). Large numbers of 1977; the southern (Eden) ground was Graham (2013), around 30 trawlers and C. harrissoni were likely caught and surveyed three times in 1977. These 3 auto-longliners in the SESSF still discarded off NSW during this time, due surveys were repeated in 1996–1997, operate along the upper-slopes. Since to the absence of a market for deepwater (with two surveys conducted off Sydney auto-longline vessels, which deploy up shark carcasses (a result of mercury and Ulladulla and three off Eden) using to 15,000 hooks per vessel per day, can content regulations and preference for the same vessel and trawl gear and operate on the steep and rough ground more marketable bony fishes) (Daley et similar sampling protocols, to examine that would potentially be a refuge for C. al., 2002; Graham and Daley, 2011). the changes in relative abundances of harrissoni from trawling (R. Daley, Similarly, trawlers operating on the the main species (number and kg per Commonwealth Scientific and upper-slope off eastern Victoria reported trawling hour) after 20 years of trawling Industrial Research Organization minimal catches of Centrophorus (see Andrew et al., 1997; Graham et al., (CSIRO), personal communication, dogfishes, but also likely discarded 2001). Results from these surveys show 2014), the combined operation of both substantial numbers due to Victorian that Harrisson’s dogfish were present the trawl and auto-longline fisheries State restrictions on mercury content in and, at one time, were caught across all within the range of Harrisson’s dogfish shark flesh (Daley et al., 2002). Graham of the survey grounds and depth zones. significantly increases the likelihood of and Daley (2011) estimate that landings In 1976, catches of Harrisson’s dogfish incidental catch of the species. Catch of Centorphorus spp. were around were combined with southern dogfish rates of Harrisson’s dogfish in the several hundred tonnes per year during (C. zeehaani) in the initial two surveys SESSF have been minimal in recent the 1980s and early 1990s. off Sydney and one off Ulladulla. When years, likely due to their low abundance

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on the continental margin; however, the population that can be caught and still their life history parameters. Species combined operation of these demersal maintain sustainability of the with slow population growth rates, late gears on the upper-slope grounds may population; Forrest and Walters, 2009). age at maturity, long gestation times, further decrease abundance of the However, these harvest levels can only low fecundity, and higher longevity are remaining population. For the 2012– be sustained by a population in a especially sensitive to elevated fishing 2013 season, reported gulper shark (C. significantly less depleted state mortality (Musick, 1999; Garcı´a et al., harrissoni, C. moluccensis, C. zeehaani) (Woodhams et al., 2011). In the case of 2008; Hutchings et al., 2012). These life landings (in trunk weight) were 0.9 t Harrison’s dogfish, Woodhams et al. history traits increase the species’ with discards of 1.2 t (Woodhams et al., (2013) notes that even low levels of susceptibility to depletion by decreasing 2013). This is a decrease from the mortality can pose a risk because of its the species’ ability to rapidly recover previous year, which reported landings significantly depleted state. Although from exploitation. Harrisson’s dogfish of 3.8 t. Given the evidence of total fishing mortality on gulper sharks exhibits these same life history traits, substantial depletion of both Harrisson’s is unknown, the level of catch and with late maturity, long gestation times, and southern dogfishes in Australian observed discards in recent years was small litter sizes, and high longevity. waters over the years, high risk of deemed likely to result in further These life history traits have overfishing in the SESSF, with no population declines (Woodhams et al. exacerbated the overall impact of the current indication of recovery (based on 2011; 2012; 2013). In the 2012–13 historical overutilization of the species 2012–2013 season data), the Australian fishing season, discards actually on its extinction risk, leading to the Government Department of Agriculture outnumbered landings (1.2 t compared substantial decline in Harrisson’s classified the above three gulper sharks to 0.9 t; Woodhams et al., 2013). Thus, dogfish abundance, and will continue to as ‘‘overfished’’ in 2012, with the even with the prohibition on retention place the species at increased risk of current level of fishing mortality noted of the species, there is still a potential demographic stochasticity. as ‘‘uncertain’’ (Woodhams et al., 2013). for discards based on the significant Extinction Risk In fact, upper-slope gulper sharks have overlap of current fishing effort within been classified as overfished since they the core range of the species It is clear that the species faces were first included in Australia’s (Woodhams et al., 2013). This is a current demographic risks that greatly Fishery Status Reports in 2005 concern because Harrisson’s dogfish increase its susceptibility to extinction. (Woodhams et al., 2011). In February suffers from high at-vessel mortality in Due to the significant decline, the 2013, a zero retention limit was trawl gear and potentially high at-vessel species is no longer found in implemented for Harrisson’s dogfish mortality in auto-longline gear approximately 19 percent of its (Woodhams et al., 2013), along with (Williams et al., 2013a). Therefore, the Australian range and, furthermore, other management measures detailed in continued fishing effort on the upper- throughout the rest of its core range, is AFMA’s Upper-Slope Dogfish slope and potential for incidental estimated to be at 21 percent of its total Management Strategy (AFMA, 2012) capture of Harrisson’s dogfish in the virgin population size (with separate and evaluated in the ‘‘Protective Efforts’’ trawl and line fisheries described above, estimates of 11 percent for the section below. which will likely result in mortality of continental margin population and 75 In terms of state-managed fisheries, the species, is considered a threat that percent for the seamount population) the range of Harrisson’s dogfish extends is currently contributing to the (Williams et al., 2013a). Although the within NSW, Victoria, and Tasmania overutilization of the species and its risk population on the seamounts may be jurisdictions. In both Victorian and of extinction. less depleted, it also likely comprises a Tasmanian fisheries, catch records of In the areas off New Zealand where C. significantly smaller portion of the Harrisson’s dogfish are rare and harrissoni have been observed (Three entire Harrisson’s dogfish population, interactions with these fisheries are Kings Ridge, Norfolk Ridge, and based on the amount of available habitat considered to be unlikely, based on Kermadec Ridge), there is limited and corresponding carrying capacity. In their respective fishing operations fishing effort (Graham, 2013). The fact, the continental margin habitat, (Threatened Species Scientific fishing activities include trawling on the where the population is estimated to be Committee (TSSC), 2013). In NSW West Norfolk Ridge, drop-lining for at only 11 percent of its total virgin commercial fisheries, Harrisson’s large bony fishes on the Three Kings population size, represents 86 percent of dogfish may be caught by the Ocean Rise, West Norfolk Ridge, and Harrisson’s dogfish’s estimated extent of Trap and Line Fishery and the Ocean Wanganella Bank, and minimal occurrence and 84 percent of its Trawl Fishery. According to Graham longlining and close to no trawling on estimated area of occupancy (TSSC, (2013), there are up to five trawlers in the Kermadec Ridge. No bycatch of 2013), indicating significant depletion the Ocean Trawl Fishery that fish gulper sharks has been reported from throughout most of the species’ range. In seasonally between Newcastle and these fishing activities (based on a addition, the existing Harrisson’s Sydney and may incidentally catch personal communication from C. Duffy dogfish populations along the Harrisson’s dogfish, and only minimal in Graham (2013)). Given the continental margin and off the line fishing effort on the upper-slope (K. uncertainty surrounding the C. seamounts in Australia and New Graham, Australian Museum, personal harrissoni abundance in this area, it is Zealand are small and fragmented, with communication, 2014). In 2013, a zero currently unknown if these fishing only three identified remnant retention limit was implemented for activities are impacting Harrisson’s populations that are thought to be viable Harrisson’s dogfish (unless for scientific dogfish populations or significantly (due to presence of mature males, purposes as agreed by Fisheries NSW) contributing to its extinction risk females, and/or juveniles within the (NSW DPI, 2013). (Graham, 2013). same area). Two of these populations Because of their low productivity, are located off the continental margin sustainable harvest rates of gulper Other Natural or Manmade Factors and the third is off Taupo Seamount. It sharks are estimated to be less than five Affecting the Continued Existence of is unclear the extent to which these percent of their virgin biomass, and Harrisson’s Dogfish populations can help recover maybe even as low as one percent Many sharks are biologically Harrisson’s dogfish, as breeding (reflecting the proportion of total vulnerable to overexploitation due to behavior, stock structure, inter-

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population exchange, and general We evaluate these conservation efforts March 28, 2003), includes regulatory movement of individuals is currently using the criteria outlined in PECE. management measures designed to rebuild the Harrisson’s dogfish unknown. Due to their size and Protective Efforts isolation, these populations may be at population above a limit reference point an increased risk of random genetic drift The EPBC Act, the Australian of 25 percent of its unfished biomass and could experience the fixing of Government’s central piece of (B25). Setting a recovery time frame was recessive detrimental alleles that could environmental legislation, applies to deemed not feasible until further further contribute to the species’ any group or individual whose actions research on the species is completed; extinction risk (Musick, 2011). In may have a significant impact on a however, an interim time frame to reach ‘‘matter of national environmental addition, the patchy distribution of this reference point was estimated based significance.’’ Any proposed action that these populations throughout the solely on the biological characteristics meets this standard must then be species’ entire range increases of the species (three generation times) assessed to determine its environmental susceptibility to local extirpations from and equal to 85.5 years (SWG, 2012). impact. Species listed as ‘‘vulnerable,’’ The outcomes and the effectiveness of environmental and anthropogenic ‘‘endangered,’’ and ‘‘critically the Strategy are expected to be perturbations or catastrophic events. endangered’’ under the EPBC Act are measured on a biennial basis, as Given the apparent spatial structuring of considered to be matters of national detailed in AFMA’s ‘‘Upper-Slope the species and dominance of males in environmental significance and receive Dogfish Research and Monitoring the sex ratios at many locations, a these provisions. Workplan.’’ The workplan for the period further reduction in the numbers of In 2009, Harrisson’s dogfish was of 2014–2016 (Workplan 1) focuses on females at any given site may decrease nominated for listing under the EPBC the development of a cost-effective reproductive success and prevent Act. Its status was reviewed by the method for measuring baseline relative population replacement. The species Threatened Species Scientific abundance of gulper sharks and has extremely low fecundity (2–3 year Committee (TSSC), a committee recovery over time (AFMA, 2014). This gestation period resulting in 1 to 2 established under the EPBC Act to output will be assessed as part of the pups), slow growth rates, and late advise the Australian Minister for the Research and Monitoring Workplan maturity, all of which contribute to a Environment on the amendment and 2014–16 review (proposed time frame of long population doubling time. In a updating of lists of threatened species, July 2014-Dec 2016). Once the severely depleted state, these traits may threatened ecological communities, and methodology has been developed, the contribute to increasing the species’ key threatening processes, and with the next output (Workplan 2) is expected to extinction risk, especially if the species making or adoption of recovery plans produce baseline relative abundance is still subject to threats that further and threat abatement plans. In 2013, the estimates for Southern and Harrisson’s reduce its abundance. Thus, although TSSC concluded that Harrisson’s dogfish (proposed time frame for output: the species’ biological characteristics dogfish was eligible for listing as Jan 2017–Dec 2019). Subsequent have allowed it to successfully thrive in endangered under the EPBC Act because workplans will provide estimates of the past, under the current conditions of the species had suffered a severe rebuilding over time and will be severely fragmented populations and reduction in numbers, with a suspected periodically assessed to ensure that the low abundance throughout its range, population decline of between 74 and actions within the workplans are questionable population viability, and 82 percent (TSSC, 2013). However, the achieving the desired outputs. Hence, it risk of incidental mortality from TSSC concluded that the species was appears it will be a number of years fisheries, the species’ natural life history also eligible for listing as a conservation before the effectiveness of the Strategy traits are presently threatening its dependent species under the EPBC Act will be able to be quantified. As continued existence. Specific because it is the ‘‘focus of a plan of outlined in the PECE, we must evaluate information is lacking on interactions management [the Strategy] that provides these conservation efforts that have not among threats. for managed actions necessary to stop yet demonstrated effectiveness at the the decline of, and support the recovery time of listing to determine whether Without considering the effectiveness of, the species so that its chances of long these efforts are likely to be effective at of the recently implemented term survival in nature are maximized’’ reducing or eliminating threats and management measures in reducing the (TSSC, 2013). In May 2013, based on the improving the status of Harrisson’s threat of overutilization and improving TSSC recommendation, the Minister of dogfish. Below are the regulatory the status of Harrisson’s dogfish in the Environment officially listed measures from the Strategy that have Australian waters (discussed in the Harrisson’s dogfish as a conservation already been implemented by AFMA for ‘‘Protective Efforts’’ section below), dependent species under the EPBC Act. the conservation of the species (under Miller (2014) concluded that Harrisson’s This listing means that the species is not the legal authority of section 41A of the dogfish is presently at a high risk of considered a matter of national Australian Fisheries Management Act extinction due to threats of environmental significance in the 1991 and implemented under ‘‘SESSF overutilization exacerbated by its context of the EPBC Act, and, as such, Fishery Closures Direction No. 1 2013;’’ natural biological vulnerability to Harrisson’s dogfish are exempt from the satisfying the first criteria of the PECE) depletion, the interaction of which has EPBC Act protective provisions. and our subsequent evaluation of their resulted in significant demographic In 2012, AFMA published the Upper- likely effectiveness at improving the risks to the species. We agree with this Slope Dogfish Management Strategy (the status of Harrisson’s dogfish (the second analysis and find that the species is ‘‘Strategy’’; see AFMA, 2012) to satisfy criteria of the PECE). The figures and presently in danger of extinction the aforementioned management tables referenced below can be found in throughout its range. Below we evaluate requirements for a conservation the PECE supplement (Miller, 2014b). formalized conservation efforts that dependent listing of Harrisson’s Dogfish have yet to be implemented or to show and Southern Dogfish under Australia’s Prohibition on the Commercial effectiveness to determine whether EPBC Act. The Strategy, which we Retention of Gulper Sharks these efforts contribute to making listing evaluate below according to the The Strategy implements a complete the species as endangered unnecessary. guidelines in the PECE (68 FR 15100; prohibition on the commercial retention

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of all gulper sharks. However, even the habitat area’s ability to support of power-handline methods on before the prohibition, reported catch dogfish populations) and 5.5 percent of Harrisson’s dogfish in order to evaluate rates of Harrisson’s dogfish in the the continental margin habitat are the effectiveness of these closures. SESSF have been minimal in recent closed to all types of fishing (see Table Based on findings from Graham (2011) years, likely due to the low abundance 1; Figures 1 and 4 in Miller, 2014b). In and Williams et al. (2013b), there is a of the species on the continental margin terms of the areas that support high selectivity rate for target species where the fisheries operate. Harrisson’s Harrisson’s dogfish populations, this (and consequently low bycatch) when dogfish are not a targeted species, but coverage translates to protection for 26.3 using the power handline technique. rather taken as incidental catch. percent of the current biomass of the For example, in one of the experiments Although this prohibition will decrease seamount population (provided by the designed to replicate normal power- the numbers of sharks being landed, it new Derwent Hunter closure) and 19.1 handline fishing operations for is worth noting that discards have percent of the biomass of the harvesting blue-eye trevalla (the target outnumbered landings in recent years continental margin population. species for power-handline fishing), and at a rate that was deemed likely to Contributing to the protection of the results showed that Harrisson’s dogfish result in further declines of the species continental margin population are the could be successfully avoided. Out of a (Woodhams et al., 2011). Additionally, Strategy’s extension of the Flinders total of 1,435 individual line drops, in the latest Fishery Status Report for Research Zone closure and revision to 25,509 hooks, and over 10 fishing trips, Commonwealth-managed fish stocks, it the Harrisson’s Gulper closure that no Harrisson’s dogfish were taken as states: ‘‘[t]here is potential for prohibits fishing in the depth range of bycatch. This is in contrast to the 6,819 unreported or underestimated discards Harrisson’s dogfish. The fact that these blue-eye trevalla that were caught using (based on the large degree of overlap of closures encompass areas critical to the power-handline method (Williams current fishing effort with the core range population viability further increases et al., 2013b). Likely contributing to this of the species [Harrisson’s dogfish]), and the effectiveness of this regulation in high degree of selectivity using the low levels of mortality can pose a risk improving the status of the species. For power handline method and avoidance for such depleted populations’’ example, the Extended Flinders of Harrisson’s dogfish is the fact that (Woodhams et al., 2013). Based on the Research Zone (see Figures 2a and 2b in fishing for blue-eye trevalla is normally above discarding trends, the fact that it PECE supplement) protects the only conducted during daylight hours, in is the Commonwealth Trawl Sector of known potentially reproducing depths of 280–550 m. Based on the SESSF which is the main fishery population of Harrisson’s dogfish found Harrisson’s dogfish’s diel-migration operating within the species’ core south of Sydney. Specifically, this patterns, the species is normally found continental margin range, and the closure protects the mature male in depths greater than 550 m during evidence that Harrisson’s dogfish are population found around Babel Island, daylight hours, deeper than the normal not expected to survive after incidental the mature female population found power handline operating depths. capture in trawl gear (Rowling et al., around Cape Barren, and the likely Insight into post-release mortality was 2010), the new retention prohibition migration route between these two also provided from the Williams et al. may only have a minor impact on populations that is thought to support (2013b) study, as exploratory fishing for decreasing current fisheries-related mating activities (Middle Ground). Prior mortality. Harrisson’s dogfish was conducted to to this closure, only the Babel and Cape determine the occurrence of the species Network of Spatial/Area Closures Barren grounds were protected, leaving on the seamounts. A total of 105 Prior to the Strategy, a number of the closely adjacent Trawl Corridor and Harrisson’s dogfish were captured closures were implemented across the Middle Ground open to fishing during this exploratory component of SESSF operational area (AFMA, 2012); activities (and the potential for the survey and Williams et al. (2013b) however, there were concerns that these incidental catch). Now, this closure has observed that many of these sharks, closures were too small in relation to been extended and prohibits all fishing when brought to the surface, were in the historical distribution of the species methods from 200 to 1000 m deep, good physical condition. All but one to prevent further declines or recover covering the entire depth range of shark were released back into the water the species (Musick, 2011; Woodhams et Harrisson’s dogfish. alive and actively swam away. Williams al., 2011). Musick (2011) estimated that If we also consider closures that et al. (2013b) attribute this potentially the closures protected Harrisson’s prohibit all high-risk fishing methods low post-release mortality to the short dogfish from all forms of industrial (permitting only power hand-line), the soak times associated with power- fishing in only 9.8 percent of its habitat. protection coverage increases to 24 handline fishing. In addition, this type In response to these concerns, AFMA percent of Harrisson’s dogfish’s entire of fishing method consists of a high evaluated options for closures in the core habitat (see Table 1; Figures 1–4 in degree of spatial targeting and small Strategy and created a new network of Miller, 2014b). The effectiveness of gear size, which also likely contribute to spatial/area closures in 2013, taking into these regulations in improving the a high survival rate of Harrisson’s account the species’ distribution and status of Harrisson’s dogfish partly dogfish when caught on lines (Williams habitat potential, which would protect depends on the handling of the species et al., 2013b). Based on these findings, the species from various forms of fishing in fishing gear and subsequent post- we consider closures that prohibit all and prevent further declines. release mortality rates of the shark. In high-risk fishing methods (permitting Regulations that are the most effective other words, these regulations are only only power hand-line), as effectively in protecting the species from threats of likely to be effective in decreasing decreasing the threat of overutilization overutilization (i.e., incidental catch) threats if they reduce incidental catch (i.e., mortality from incidental catch) of are those that prohibit all types of altogether or reduce mortality rates of Harrisson’s dogfish (see Table 1; Figures fishing methods. An analysis of already Harrisson’s dogfish when incidentally 1–4 in Miller, 2014b). The coverage of implemented conservation efforts from caught. As these closures prohibit all these closures, when broken out by the Strategy estimates that 26.3 percent fishing with the exception of power- continental margin and seamount of the core Harrisson’s dogfish seamount handline methods, we need to consider proportions and weighted by carrying habitat (weighted by carrying capacity— the selectivity and post-release mortality capacity, translates to protection for

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Harrisson’s dogfish over 18.4 percent of However, preliminary tagging studies of threat of overutilization by prohibiting its core continental margin habitat and a closely related species, C. zeehaani, high-risk fishing methods, which 77.6 percent of its seamount habitat (see inside a fishery closure off southern decreases fishery-related mortality from Table 1 in Miller, 2014b). Contributing Australia suggest that the home ranges bycatch. Based on a prior review by to the protection of the continental of deep-water dogfish sharks may be Musick (2011), it was recommended margin population is the Strategy’s small, with evidence of resident female that closures include at least 20 to 35 extension of the Endeavour closure, and populations that can be effectively percent of important Harrisson’s dogfish for the seamount population, the newly protected by fishery closures (Daley et habitat in order to prevent further created Queensland and Britannia al., 2014). Furthermore, as new decline of the species and potentially seamount closures. information becomes available that support recovery. Overall, the closures If we look at the closures that prohibit improves the understanding of evaluated above appear to provide the trawling operations next, it is estimated Harrisson’s dogfish biology and stock species with effective protection from that 29.5 percent of the species’ core structure, the management arrangements high-risk fishing methods over 24 habitat range is protected from trawling in the Strategy can be adapted as percent of its core habitat range (see activities (see Table 1 in Miller, 2014b). necessary to ensure the effectiveness of Table 1 in Miller, 2014b). Specifically, With these regulations, almost all of the the Strategy over time. the core habitat of the much-less- Harrisson’s dogfish’s core seamount Compliance and Enforcement depleted seamount population is habitat would be protected. As significantly protected from high-risk Harrisson’s dogfish are not expected to In addition to the actual spatial extent fishing methods and almost entirely survive when caught in trawl gear, these of the closure network, the certainty of protected (98.2 percent) from trawling closures are likely to be effective in effectiveness of these regulatory activities (see Table 1 in Miller, 2014b). decreasing mortality rates from measures in decreasing threats to the In fact, 77.6 percent of the seamount incidental catch in trawls. In fact, there species also depends on the compliance population biomass is protected from all is already evidence of rebuilding in and enforcement of these closures. For high-risk fishing methods by the new areas that were extensively trawled but the Commonwealth fisheries, AFMA has closures created by the Strategy. These have seen significantly less activity created a compliance team to assist with conservation efforts are likely to recently. Graham and Daley (2011) note issues such as quota evasion and effectively improve and protect the the presence of a high numbers of balancing, Vessel Monitoring System status of this population so that it is no juveniles (<80 cm TL, including (VMS) requirements, and compliance longer presently in danger of extinction. with fisheries closures and interactions neonates) that were caught during a In terms of the continental margin with protected species. In terms of VMS 2009 long-line survey at sites off Port population, the new network of spatial requirements (a key monitoring Stephens NSW. This area had been closures provides protection from high- provision in the Strategy), compliance extensively trawled during the first 20 risk fishing methods over 18.4 percent rates have significantly increased over years of the upper-slope fishery, but of the core margin habitat. The closures the years, thanks to outreach material to over the last 10 years has seen protect 32.4 percent of the current vessel operators. Compliance rates for significantly less trawling activity biomass, including the only known the requirement for vessels to have an (Graham et al., 2001; Graham and Daley, viable population found south of operational VMS averaged around 97 2011). The authors of the study attribute Sydney, from all fishing activities, percent for the 2012–2013 year (AFMA, the increase in juvenile sightings as which will be critical for improving the potentially a re-establishment of the 2013a). status of the population (see Table 1; population in this area. Another key to the successful and Figure 1 in Miller, 2014b). Although NSW closures and regulations may effective conservation of the Harrisson’s also offer additional protection to the dogfish population so that it may incidental fishing mortality may occur species (TSSC, 2013). Specifically, the rebuild in the future is compliance with outside of these closures, based on the NSW ‘‘North of Sydney closure’’ (see fishing prohibitions inside closures. In best available information, we consider Figure 3 in Miller, 2014b) prohibits all 2010–2011, AFMA identified the the current network of closures effective fishing methods except for power- activity of fishing boats entering and/or in adequately decreasing the present handline, but allows trawling in depths fishing inside closures as an occasional threat of overutilization throughout the over 650 m (which overlaps with the but significant risk. To combat this, they species’ range to the point where the Harrisson’s dogfish depth range). The developed a ‘‘show cause’’ program species is not currently in danger of NSW trawl restriction areas 4 and 6 (see whereby breaches inside closures were extinction. Figure 5 in Miller, 2014b) also provide identified from VMS, and the operators As mentioned previously, these some protection by prohibiting trawling, of these vessels were sent a letter asking conservation efforts have been designed but are open to line methods. Overall, them to explain or ‘‘show cause’’ for with the explicit objective to stop the these additional regulations protect 2.4 their activity. Within a year of running decline of Harrisson’s dogfish and percent of the core habitat (and 3 the program, the incidence of fishing or rebuild the population above 25 percent percent of the core continental margin navigating inside fishery closures had of its unfished biomass. AFMA’s habitat), mainly from trawling, except at decreased from an average of 11 ‘‘Upper-Slope Dogfish Research and the shallowest depths (TSSC, 2013). breaches per month to less than 2 Monitoring Workplan’’ details the Many uncertainties surround these breaches per month (AFMA, 2013b). provisions for monitoring and reporting estimates. We currently do not know the progress on the objective and locations of important foraging grounds Conclusion effectiveness (based on evaluation of or nursery areas that are critical for After consideration of the evaluation quantifiable parameters and using population viability. In addition, we criteria for certainty of effectiveness principles of adaptive management) of have no information regarding the under the PECE, we find that these the implemented conservation efforts. movement of Harrisson’s dogfish in and existing regulatory measures are likely Specifically, the outcomes and the out of these protective closures, or the to be effective in improving the present effectiveness of the Strategy are connectivity between the seamounts status of the species. The network of expected to be measured on a biennial and continental margin populations. implemented closures addresses the basis. However, as noted below,

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certainty that the above conservation term to the point where the species is describes our analysis of the status of efforts will remain in place after 5 years no longer presently in danger of the three species. Information on many cannot be predicted at this time. As it extinction. However, given that the of the species is sparse, so we cannot stands, the Strategy, and conservation implementation of these conservation provide complete descriptions of their efforts therein, are only a force under efforts is only certain for 5 years, a time natural history. More details can be Australian law if AFMA continues to frame that is insufficient to increase the found in Meadows (2014). implement the closures under section species’ chances of survival when faced Species Description of Cantharellus 41A of the Fisheries Management Act again with prior threats, we conclude noumeae 1991. These closures are implemented that the species will likely be in danger under ‘‘Directions’’ (for example, the of extinction in the foreseeable future. Cantharellus noumeae is a fungiid or current fishery closures to protect We specifically seek additional mushroom coral that was the first Harrisson’s dogfish have been information from the public comment described species of its genus, in 1984 implemented under ‘‘SESSF Fishery process on these conservation efforts (Hoeksema and Best, 1984). It received Closures Direction No. 1 2013’’). These and their certainty of implementation its own new genus name because, legal instruments are only in effect for and effectiveness (see below). unlike most other fungiid corals, it is 5 years, after which AFMA may choose stalked and not free-living as an adult. Proposed Determination to extend the closures by creating a new Other species in the genus have since Direction. If AFMA does not take action We assessed the ESA section 4(a)(1) been discovered and named, so the after 5 years, these closures will expire. factors and conclude that the species genus is no longer monotypic. Polyps Although the Upper-Slope Dogfish faces ongoing threats from are relatively small for a fungiid coral, Research and Monitoring Workplan overutilization, with the species’ natural ranging from 25 to 65 mm in diameter details AFMA’s commitment to stop the biological vulnerability to (Hoeksema and Best, 1984). The polyps decline of Harrisson’s dogfish and work overexploitation exacerbating the are cup-shaped when fully developed to rebuild the population, the protection severity of the threats. The species faces and have wavy margins (AIMS, 2013a). of the species is not required under the demographic risks, such as small and The primary septa are thin. The species EPBC Act since the species was listed as fragmented populations with low may be solitary or colonial; colonies conservation dependent instead of productivity, which make it likely to be consist of a few contorted polyps. Their endangered. In addition, in the case influenced by stochastic or depensatory typical color is mottled brown. where any part of this Strategy ceases to processes throughout its range and place Cantharellus noumeae was thought to exist or changes, the species would not the species in danger of extinction from occur only in a restricted area of less automatically be listed as endangered the aforementioned threats. We deem than 225 km 2 on reefs in sheltered bays under the EPBC Act. Rather, the TSSC ongoing conservation efforts as in New Caledonia, on the southern tip would be convened and asked to currently effective in decreasing the of the main island of Grand Terre evaluate how the changes impact the main threat of overutilization to the (Hoeksema et al., 2008). Recent research status of the species and provide point where the species is no longer by the French Institut de Recherche recommendations on listing eligibility presently in danger of extinction. pour le De´veloppement (IRD) has found to the Minister for the Environment, However, the time frame over which that the species also occurs on fringing with the ultimate decision on whether these conservation efforts will certainly reefs farther up the southeast coast at to list the species in a given category be in place is insufficient to increase the Noumea and at Balabaio in the made by the Minister. species’ chances of survival or prevent northeastern part of New Caledonia While we conclude that the present its extinction through the foreseeable (www.lagplon.ird.nc; Antoine Gilbert, conservation efforts are currently future. Therefore, based on the best Ginger Soproner, personal effective in preventing the extinction of available scientific and commercial communication, 2013). It is found in the species, we have no certainty that information as presented in the status waters 10 to 35 m deep, close to soft they will remain in place after 5 years. report and this finding, we find that C. sediment habitats that are in sheltered Taking into account the present state harrissoni is not currently in danger of bays and lagoons (Hoeksema and Best, and life history of the species, we do not extinction throughout its range, but is 1984). There are records of it in western, consider 5 years to be sufficient time for likely to become so in the foreseeable northern, and eastern parts of the island the status of the species to improve to future. We propose to list Harrisson’s of New Guinea that includes Papua New where it is no longer in danger of dogfish as a threatened species under Guinea and West Papua, Indonesia, with extinction without the continued the ESA. details likely to be published soon on a implementation of these efforts. In other new Web site (http:// Corals words, the removal of these coralsoftheworld.com; Charlie Veron, conservation efforts after 5 years will The three coral species considered personal communication). There are once again subject the species to the herein are all marine invertebrates in also reports of it from Papua New threats described previously, and based the phylum . The phylum is Guinea in the International Union for on the information from the extinction called Cnidaria because member species Conservation of Nature (IUCN) risk analysis (e.g., substantial depletion, use cnidae (capsules containing stinging assessment, but the assessment fragmented populations, extremely low nematocysts) for prey capture and questions the validity of this record productivity, sensitivity to low levels of defense. All are tropical, shallow water, (Hoeksema et al., 2008). The IUCN mortality), we find that the species will scleractinian (‘‘stony’’) corals that assessment and the researcher whose likely become in danger of extinction at secrete a calcium carbonate skeleton. published record is in question (Doug that time. Two of the three have the typical stony Fenner) suggest further confirmation is In conclusion, after consideration of coral symbiosis with zooxanthellae necessary (Hoeksema et al., 2008; the evaluation criteria under the PECE, (photosynthetic) algae that reside in Fenner, personal communication). we are sufficiently certain that the gastrodermal cells of the coral tissue. Fossil records from over 5 million years implemented conservation efforts will All are non-reef building corals that live ago indicate that this species was at one effectively decrease the threat of in small colonies or as solitary time found as far west as East overutilization by fisheries in the near individuals. The following section Kalimantan, on the island of Borneo,

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Indonesia (Hoeksema, 1989; Hoeksema, have recently passed through or been elsewhere in the wild and is yet 1993). carried across the Panama Canal to the undiscovered (Guzma´n and Edgar, Scleractinian corals have diverse Pacific Ocean side; or (2) the alternate 2008). There are no plans to re- reproductive strategies, including both possibility that S. glynni evolved from introduce the species, as existing asexual and sexual modes of S. siderea, likely about 2 to 2.3 million colonies are too small to survive, though reproduction (see Brainard et al., 2011). years ago during a period of high sea three of the fragments are being Individual reproductive modes for these level, when the Isthmus of Panama may considered for cryopreservation, which three species have not been studied. have been breached, allowing inter- would further reduce the population Cantharellus noumeae may be a basin transfer of the species’ ancestors. size (Guzma´n, personal communication, sequential sex-changing species like Because the available information to 2013). other members of its family. Because of reclassify the species is inconclusive, Species Description of Tubastraea their relationship with symbiotic we determine that S. glynni is a valid floreana zooxanthellae, C. noumeae needs to live and unique species. in shallow water to be exposed to light The range of S. glynni is a small area Tubastraea floreana was first the symbiotic algae use to of the Pacific Ocean near the small described by Wells (1982). It is an photsynthetically fix carbon. island of Uraba in Panama Bay, a few azooxanthellate species, which means it There is no quantitative species- kilometers from the opening of the lacks the symbiotic photosynthetic specific population or trend information Panama Canal (Guzma´n and Edgar, zooxanthellae that most scleractinians available for C. noumeae (Hoeksema et 2008). Identified colonies of S. glynni have. It has a bright pink color while al., 2008; Gilbert, personal were reported to be unattached and alive, but turns deep red-black when communication). The current and occur ‘‘along the upper sand-coral dead out of water. Corallites in the continuing presence of the species in rubble reef slope at a depth of 7 to 8.5 species are closely spaced (Cairns, 1991) New Caledonia was confirmed by Bert meters’’ (Budd and Guzma´n, 1994). All and about 4–6 mm in size (Wells, 1983). Hoeksema (personal communication) in the islands around the site, as well as Tubastraea floreana is endemic to a 2012 and in one murky location in another set of islands to the south, were few sites on a number of islands in the Prony Bay on the southern tip of Grand searched several times without finding Galapagos Islands chain. It is mostly Terre in 2013 (Andrew Bruckner, any additional colonies (Fenner, 2001). found in cryptic habitats, including on personal communication). In addition, The reproductive mode for this the ceilings of caves, and on ledges and Antoine Gilbert (personal species has also not been studied. rock overhangs (Hickman et al., 2007). communication) notes that from surveys Because of their relationship with It has been reported to occur at depths he has done over the past 4 years, the symbiotic zooxanthellae, S. glynni need of 2 to 46 m (Hickman et al., 2007). species is ‘‘uncommon and usually to live in shallow water to be exposed The reproductive mode of this species found in fringing reefs where to light the symbiotic algae use to has not been studied, but other sedimentation is quite intense.’’ He also photsynthetically fix carbon. Tubastraea species reproduce asexually. noted that the species is ‘‘usually found Only five colonies of S. glynni have Other Tubastraea species are invasive in low density, [but] it was observed in ever been found. All were found by and productive (Riul et al., 2013), so T. relative[ly] high density on the slope of Budd and Guzma´n (1994) when they floreana is also likely to be moderately artificial shores (embankment) in the discovered the species in 1992. All five productive. biggest (commercial and industrial) colonies occurred within a small area of According to Hickman et al. (2007), harbour of New Caledonia: la Grande less than 10 m 2, with each colony prior to the 1982–83 El Nin˜ o Southern Rade.’’ We found no information on within 1 m of another (Budd and Oscillation (ENSO) this species was abundance or trends on New Guinea. Its Guzma´n, 1994). Each colony was no known from six sites on four islands in presence at one site in Milne Bay more than 20 cm 2 in size. One colony the Galapagos. Since the 1982–83 (Fenner, 2003) is uncertain; Charlie was sacrificed in order to provide ENSO, specimens have only been Veron may publish information from material for the species’ description. observed at two sites. At one of these New Guinea on his Web site soon (see During the 1997–98 El Nin˜ o event, the two sites, the species has not been seen above). four surviving colonies started to since 2001, leaving only a single deteriorate, displaying signs of confirmed site with living specimens Species Description of Siderastrea bleaching and tissue loss. Due to their (Hickman et al., 2007). Recent reports glynni unhealthy state, the four colonies were indicate the species is still present in at Siderastrea glynni was described in moved to Smithsonian Tropical least one site (Stuart Banks, Charles 1994 (Budd and Guzma´n, 1994). It Research Institute (STRI) aquaria in Darwin Foundation, personal occurs in non-reef-forming spherical Panama City, Panama, where they communication, 2013). We know of no colonies that are 70 to 100 mm in remain to this day (Guzma´n and Edgar, other published information on diameter (AIMS, 2013b). They have 2008; Hector Guzma´n, STRI, personal distribution or abundance for this polygonal corallites that are 2.5 to 3.5 communication, 2013). According to species. mm in diameter (Budd and Guzma´n, Guzma´n (personal communication, 1994). The species is a light reddish- 2013) the colonies were fragmented to Summary of Factors Affecting the Three brown in color and occurs on coarse increase the number of specimens, but Species of Coral sand-rubble substrates. Recent genetic their growth rate has been very slow, Next we consider whether any one or work by Forsman et al. (2005) has and some fragments did not survive. a combination of the threat factors shown that S. glynni is genetically very From the original colonies, only one specified in section 4(a)(1) of the ESA similar to the Caribbean species S. survives, with less than 4 cm2 of living are contributing to the extinction risk of siderea, though there are differences tissue. Nine of the fragmented colonies these three corals. Available information between the species. Their study could also survive in the lab and all are less does not indicate that overutilization is not differentiate between two possible than 9 cm 2 in area (Guzma´n, personal an operative threat for these species; explanations of the species’ evolution: communication, 2013). No known therefore, we do not discuss this factor (1) that S. siderea and S. glynni are the colonies exist in the wild; however, further here. We discuss each of the same species and that S. glynni may there is a possibility that it still exists remaining four factors and their

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interaction in turn below, with species- Ocean acidification threatens to slow from climate change are largely species- specific information following a general or halt coral growth and reef building specific and must be examined on that discussion relevant to all of the species. entirely if the pH of the ocean becomes basis to fully assess extinction risk (79 A full review of all of the ESA section too low for corals to form their calcite FR 53851; September 10, 2014). 4(a)(1) threat factors can be found in skeletons, but tolerance appears to vary In addition to the general global Meadows (2014b) and our final rule by species for those that have been threats identified in our status review of listing 20 corals (20-coral listing rule) studied (see Brainard et al., 2011). In 82 corals and final rule listing 20 corals under the ESA (79 FR 53851; September addition, bioerosion of reefs is likely to under the ESA (Brainard et al., 2011; 79 10, 2014), which provides a general accelerate as coral skeletons become FR 53851; September 10, 2014), there global summary of threats facing corals. more fragile as a result of the effects of are some species-specific threats for Our 20-coral listing rule identified acidification, but effects are highly which we have detailed information at ocean warming, ocean acidification, sea- species-specific. Since the petitioned the scale of these species’ ranges that are level rise, disease, sedimentation, species are not reef-building, this effect discussed below. nutrient enrichment, and fishing as the is likely to be less significant. Cantharellus noumeae major global threats to coral reefs. The Sea-level is also likely to rise as a information about these threats and the result of climate change, but effects on Cantharellus noumeae is exposed to species’ responses to these threats is corals are highly uncertain, owing to deforestation, urbanization, and mining described in the 20-coral listing rule and uncertainty in both the likely rate and activity that causes sedimentation and incorporated herein by reference. extent of sea-level rise as well as the water pollution throughout its range in Species-specific information regarding ability of corals generally (or the New Caledonia (Hoeksema et al., 2008; applicability of these threats to the three petitioned species specifically) to keep David et al., 2010; McKenna et al., species considered here is discussed pace with the rise in sea level (Brainard 2011). The mining activity is a result of below, where available. The extent to et al., 2011; 79 FR 53851; September 10, nickel and smaller amounts of other which the risks discussed in the 20- 2014). metal mining (cobalt and chromium coral listing rule are similar to the risks While climate change effects are especially) on land throughout the main to these three corals is discussed for likely to be serious for many corals, island of Grand Terre (McKenna et al., each species. Brainard et al. (2011) and our final rule 2011; Hoeksema, personal listing 20 corals under the ESA (79 FR communication). Grand Terre holds 25 The Present or Threatened Destruction, 53851; September 10, 2014) show that percent of the world’s known nickel Modification, or Curtailment of Its adaptation and acclimatization of corals deposits (McKenna et al., 2011). Nickel Habitat or Range to increased ocean temperatures are mining started there in the 1870s. Habitat modification from climate possible, that there is intra-genus and Currently, most mining is done by open- change is a potential threat to all three inter-species variation in susceptibility cast strip mining, which has caused species of corals (79 FR 53851; to bleaching, ocean acidification, and deforestation and increased erosion and September 10, 2014). Coral bleaching sedimentation, that at least some species runoff of sediments leading to varying occurs when the photosynthetic have already expanded their range in degrees of sedimentation and light zooxanthellae symbionts of corals are response to climate change, and that not attenuation throughout the lagoon of damaged by light at higher than normal all species are seriously affected by Grand Terre, including in areas in and temperatures. The resulting damage ocean acidification. In addition, a more adjacent to the species’ range (Ouillon et leads to the expulsion of these recent paper by Logan et al. (2013) al., 2010). Labrosse et al. (2000) estimate important organisms from the coral examined the potential for coral that 300 million m 3 of soil has been host, depriving the host of the nutrients adaptation and acclimatization to displaced since the beginning of mining and energy provided by the climate change and found that these activities. Mines are located across the zooxanthellae. While corals can survive processes can reduce the frequency of country, including the large new Goro mild to moderate bleaching, repeated, mass bleaching events in the future. complex, which includes mines, severe, or prolonged bleaching can lead Their modeling results suggest some processing facilities, and a port. The to colony mortality. Bleaching events adaptation or acclimatization may even complex began production in late 2010 have been increasing both in intensity have already occurred. A study by and is very near the most abundant and geographic extent due to worldwide Wooldridge (2014) provides support population of C. noumeae. The Goro anthropogenic climate change (Hoegh- that a suite of morphological and complex has already had three incidents Guldberg, 2006; Eakin et al., 2009). physiological traits relate to bleaching affecting the environment, involving Certain genera and growth forms, vulnerability. These include symbionts’ spills or releases of sulfuric acid particularly branched species, are more type, metabolic rate, colony tissue solutions used in the processing of the sensitive to bleaching than others thickness, skeletal growth form, mucus nickel ore (Sulfuric Acid on the Web, (Wooldridge, 2013). Many corals are production rates, fluorescent pigment 2013). Runoff of heavy metals from the physiologically optimized to their local concentrations, and heterotrophic mining operations has greatly increased long-term seasonal variations in feeding capacity. According to concentrations of those metals in the temperatures and an increase of only 1– Wooldridge (2014), these traits tend to marine environment (Fichez et al., 2 °C above the normal local seasonal correlate with the ends of the dichotomy 2010). Nickel has been shown to affect maximum can induce bleaching of branching and plate corals with thin fertilization success of four reef coral (Brainard et al., 2011; Logan et al., tissue layers versus massive and species in the families Acroporidae and 2013). The United States NOAA Coral encrusting corals with thick tissue Faviidae (Reichelt-Brushett and Reef Watch satellite bleaching database layers. The species under consideration Harrison, 2005) and to affect settlement shows that the range of all three species here are not necessarily the most and cause mortality of larvae in the occurs in areas that frequently have vulnerable, based on those traits (see coral Pocillopora damicornis (Goh, bleaching alerts, with alerts being more below). Therefore, while climate change 1991). Gilbert (personal communication, frequent and severe in the ranges of S. is generally considered a potential 2013) reports that the species is glynni and T. floreana, than in the range threat to these candidate corals, the common in areas of high sedimentation of C. noumeae. likelihood and magnitude of threats and in the largest harbor, so it may be

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tolerant to environmental stressors like 2016 (Mate, 2003; Guzma´n and Edgar, found no species-specific information sedimentation. The species may have 2008). Almost continuous dredging and on the susceptibility of this species to the ability to actively remove sediments, release of oil-based compounds (bunker ocean acidification. as has been shown in some other oil, diesel, gasoline, etc.) that are spilled Disease and Predation fungiid corals (Bongaerts et al., 2012), from nearby port facilities and but this is uncertain. Mitigation commercial vessels anchored near the Coral disease has been linked to the measures for mining operations are species’ natural range are other reasons effects of climate change (see Brainard required by legislation and include reef why it was decided to transfer and then et al., 2011), especially indirectly as a monitoring requirements (UNESCO, keep in captivity the remaining known synergistic effect, as climate change and 2011; Gilbert, personal communication, colonies (Guzman, personal other threats potentially increase stress 2013), but this monitoring is not at the communication, 2013). ‘‘During the on corals, making them more species level (Gilbert, personal 1997–98 ENSO event, the four known susceptible to disease. Coral diseases communication, 2013). It is unclear how colonies of S. glynni began to also appear to be increasing worldwide effective the mitigation methods are, as deteriorate, displaying bleaching and (Roessig et al., 2004). Nevertheless, sedimentation and pollution remain tissue loss’’ (Guzma´n and Edgar, 2008). susceptibility of coral species to disease concerns (David et al., 2010). This suggests this species is vulnerable is highly species-specific and no Despite the frequency of bleaching to increased ocean temperatures, though generalizations can be made. We found alerts, heat-related bleaching is there is no specific research on this no species-specific information on apparently not a significant current point. As discussed above, the area of disease in C. noumeae or T. floreana. threat in the range of C. noumeae in the species’ range is subject to a high Black-band, dark spot, and white plague New Caledonia, as water temperatures frequency of bleaching warnings. We diseases in the Caribbean occur in S. there are relatively low (Hoeksema, have found no species-specific siderea, which is closely related to S. Naturalis Biodiversity Center, personal information on the susceptibility of this glynni (Sekar et al., 2008; Brandt and communication, 2013) and the ReefBase species to ocean acidification. McManus, 2009; Cardenas et al., 2012), coral bleaching database only reports suggesting S. glynni may be susceptible events with low bleaching severity as Tubastraea floreana to similar coral diseases, but we have no the worst past events to ever occur For T. floreana, there is a lack of solid information. there. We have found no species- information on thermal tolerances, but With respect to predation, we found specific information on the ‘‘the dramatic reduction in its no information on predation threats to susceptibility of this species to distribution immediately after the 1982– S. glynni or T. floreana. For C. noumeae, bleaching or ocean acidification; 83 [ENSO] event suggests that this one potential predation threat is however, its growth form suggests it is mortality resulted from the event’’ Acanthaster planci (crown-of-thorns not among the most susceptible species (Hickman et al., 2007). This is true starfish). Acanthaster planci does not (Wooldridge, 2014). despite the fact that this species is appear to be a major cause of coral Anthropogenic eutrophication occurs azooxanthellate, suggesting that other mortality in New Caledonia (Adjeroud, in the range of the species near the mechanisms besides loss of calorie 2012), but several remote reefs surveyed capital of Noumea and is attributed subsidy from symbionts are involved. during the Global Reef Expedition in mostly to inadequately treated sewage Edgar et al. (2010) document a series of November 2013 on the outer-slope of (Fichez et al., 2010), although 19 drastic ecosystem changes in the Guilbert’s atolls showed evidence of aquaculture farms on the west coast and Galapagos following the 1982–83 ENSO past outbreaks (LOF, 2013). event, including dramatic declines in island-wide agriculture may also play Inadequacy of Existing Regulatory dissolved nutrients and phytoplankton roles (David et al., 2010). Storm events Mechanisms and flooding have also recently productivity, leading to declines across occurred in the range of the species the food chain and resulting in heavily The petitioners discussed regulation (EMR, 2013), and there is concern that grazed reefs with crustose coralline of trade in corals under CITES as a climate change may make such events algae (‘‘urchin barrens’’) replacing threat to these species. All of the species more frequent in New Caledonia former macroalgal and coral habitats. A considered in this petition were listed (Gilbert, personal communication, total of 95–99 percent of reef coral cover in Appendix II of CITES in 1989, when 2013). was lost from the Galapagos between all scleractinian corals were listed. The biggest threats to New Guinea’s 1983 and 1985 (Edgar et al., 2010). All While only some scleractinians were in coral reef resources include known coral reefs based on calcareous trade at the time, the 1989 listing sedimentation and pollution from frameworks died and subsequently rationale for including all scleractinians inland sources (e.g., forest clearance, disintegrated to rubble and sand (Glynn, in Appendix II was because of sewage, and erosion), climate change, 1994). These changes led to large identification difficulties where non- and dynamite fishing (Burke et al., 2011; decreases in biodiversity. The urchin traded species resemble species in trade. PNG, 2009; PNG, 2012). There is little Eucidaris galapagensis now appears to According to Article II of CITES, species specific data on these threats in New be present in sufficient numbers to listed on Appendix II are those that are Guinea in the above references. prevent re-establishment of coral and ‘‘not necessarily now threatened with macroalgal habitat, thereby facilitating a extinction but may become so unless Siderastrea glynni regime shift in local benthic habitats trade in specimens of such species is Should S. glynni ever be restored to (Edgar et al., 2010). Moreover, the subject to strict regulation in order to the wild, it faces considerable habitat Galapagos Islands sit near the center of avoid utilization incompatible with degradation threats from coastal the most intense El Nin˜ o events in the their survival.’’ Based on the CITES development, oil production, region (Glynn and Ault, 2000) and are definitions and standards for listing sedimentation, eutrophication and other regularly included in bleaching threat species on Appendix II, the species’ pollution, and increased transportation warnings issued by NOAA (see above). listing on Appendix II is not itself an activities in the Panama City area, the Therefore, future ENSO events and inherent indication that these species Gulf of Panama, and the enlarged inhibition of recruitment are likely to may now warrant threatened or Panama Canal, which is due to open in remain threats to T. floreana. We have endangered status under the ESA. The

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significance of any threat from Caledonia submit Environmental Impact Reserve (1984), both designations of international trade would depend on the Assessments for the proposed UNESCO. The area was also designated amount of international trade relative to exploration and possible exploitation of a Gala´pagos Archipelago Particularly the population size of the species, as cobalt sands to the World Heritage Sensitive Area in 2005. This is a well as any other factors related to the Centre. We have no evidence this has designation by the International trade, such as habitat damage caused in occurred. The New Caledonian Mining Maritime Organization (IMO) that the collecting process, or synergistic Code prescribes mitigation measures to recognizes the area as having ecological, effects of other threats. We have no mitigate the impacts of mining activities socio-economic, or scientific attributes information any of these three species is (see above), and abandoned mines are that make the area vulnerable to damage traded internationally. being restored using indigenous plant by international shipping activities. Because each of the species species (UNESCO, 2011). Based on this designation, the IMO considered herein exists in small ranges In Papua New Guinea, there is a instituted special navigation rules in the that do not overlap with each other, and variety of legislation to protect area. In addition, Ecuador’s ‘‘Ley de they are not otherwise managed or biodiversity and habitat, including a Gestion Ambiental’’ (Law of regulated under any other common mandate to ensure marine resource Environmental Management) establishes international regimes, additional sustainability, and a plan of action principles and directives for discussion of this factor is left for the directed at coral reef conservation (PNG, environmental management, land-use species-specific entries for this section, 2009). However, as noted above, threats planning, zoning, sustainable use, and below. remain. Resources and capacity may not natural heritage conservation. Ecuador’s be adequate to ensure full Cantharellus noumeae fisheries law states that no harm may be implementation of the laws and plan caused to areas that are declared Since the Organic Law (No. 99–209) (PNG, 2009; PNG, 2012). protected, with corals included under on March 19, 1999, New Caledonia has Overall, we do not believe that the those protections (MCA Toolkit, 2013). been recognized as an ‘‘Overseas threat to C. noumeae from habitat While the above laws and protected area Country’’ of France. This status gives modification, destruction, and pollution designations provide a great deal of New Caledonia extensive autonomy is adequately addressed or mitigated by protection for resources in the area in with respect to France. In particular, the existing regulatory mechanisms. principal, in practice, illegal activities national laws in force within France are Siderastrea glynni and incomplete and difficult no longer applicable to New Caledonia, enforcement, as discussed in the status and New Caledonia now manages the A national law in Panama prohibits review report (Meadows, 2014), could ocean resources of its Exclusive coral extraction or mining (Guzma´n, threaten T. floreana. Moreover, the Economic Zone. The territorial sea and 2003), but enforcement is weak and the threats from climate change and ENSO the maritime public domain (coastal law may not fully protect rare species events are outside the scope of these terrestrial and nearshore aquatic zone (Guzma´n, personal communication, protections. originating under French colonial law) 2013). The range of S. glynni is adjacent depend on management from New to the Bay of Panama, which is Other Natural or Manmade Factors Caledonia’s three provinces (David et designated an internationally important Affecting Their Continued Existence al., 2010). In the two provinces where C. wetland under the Ramsar Convention The range of C. noumeae in New noumeae occurs, collection of live and contains extensive mangrove beds Caledonia is exposed to eight tropical corals (and other marine resources) is that are critical nursery grounds for storms per year on average (David et al., restricted to scientists and licensed many marine species. The Bay is a 2010). Specific effects of storms on this fishers who can only collect for a protected Wildlife Refuge under species are not documented, but the domestic market. Panamanian law. However, developers petitioner submitted an undated Web The range of C. noumeae is included seek to open the area for tourism, and page that claims Cyclone Erica in the United Nations Education, Panamanian authorities have requested destroyed between 10 and 80 percent of Scientific and Cultural Organization a reduction of the Ramsar area of the live coral in New Caledonia in 2003 (UNESCO) World Heritage Site bay (AIDA, 2013). We were not able to (EDGE, Undated; Guillemot et al., 2010). designation for the ‘‘Lagoons of New find any other species-specific We were not able to find any other Caledonia’’ site, specifically within the information on this threat. Based on the species-specific information available South Grand Lagoon area. The World available information, it is not clear that regarding this threat category for C. Heritage Site implementation is existing regulatory mechanisms would noumeae. Based on this information, we supported by specific legislation on be adequate to protect S. glynni, should consider tropical storms an additional fisheries, land and water use planning, it be reintroduced into the wild or found potential natural threat to the species, urban development, and mining (Morris in additional locations. for which we seek additional and Mackay, 2008). A wide monitoring Tubastraea floreana information (see below). program of the heritage site all around For S. glynni and T. floreana, both New Caledonia was created (Andre´foue¨t The Gala´pagos Marine Reserve was species have such a small number of 2008), but this suffers from a lack of established in 1986 and expanded to its colonies, they are susceptible to all of sampling at a species level (Gilbert, current size around all the islands in the problems of species with low personal communication, 2013). In 1998. The reserve has a zoning plan genetic diversity and population size, 2011, the World Heritage Committee of with both limited and multiple use including inbreeding depression, UNESCO (the organizing body for World zones. Rules prohibit removing or population bottlenecks, Allee effects, Heritage Sites) issued Decision 35Com disturbing any plant, animal, or remains and density-independent mortality, 7B.22, which expressed concern of such, or other natural objects. among others. regarding permits granted to the mining Tubastraea floreana also occurs inside company GEOVIC to explore for cobalt the Galapagos Island World Heritage Extinction Risk in mineral sands in areas adjacent to the Site (expanded to include Galapagos The extinction risk analyses of site and near the range of C. noumeae. Marine Reserve areas in 2001) and the Meadows (2014) found all three species The committee requested that New Gala´pagos Island Man and Biosphere to be at either a moderately high or high

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risk of extinction. The extinction risk for any of these three species. We seek increase the number of section 7 C. noumeae was found to be moderately additional information on other consultations, because these species high, based on the species’ small, conservation efforts in our public occur outside of the United States and restricted range, likely low growth rate comment process (see below). are unlikely to be affected by Federal and genetic diversity, and potential actions. Proposed Determination threats from development, water Critical Habitat pollution, possibly sedimentation at Based on the best available scientific some level, and potential illegal and commercial information as Critical habitat is defined in section 3 activities, mitigated by consideration of presented in the status report and this of the ESA (16 U.S.C. 1532(5)) as: (1) potential resilience to sedimentation finding, we find that all three species of The specific areas within the threats and uncertainty regarding coral are in danger of extinction geographical area occupied by a species, sensitivity to heavy metals. Based on the throughout all of their ranges. We at the time it is listed in accordance current information, this is the case assessed the ESA section 4(a)(1) factors with the ESA, on which are found those whether or not the species’ range and conclude that Cantharellus physical or biological features (a) includes New Guinea. The extinction noumeae, Siderastrea glynni, and essential to the conservation of the risk for S. glynni was found to be high, Tubastraea floreana all face ongoing species and (b) that may require special due to the lack of known populations in threats from habitat alteration, small management considerations or the wild, a small captive population in ranges and/or population sizes, and the protection; and (2) specific areas outside a single location, likely low growth rates inadequacy of existing regulatory the geographical area occupied by a and genetic diversity, and potential mechanisms throughout their ranges. C. species at the time it is listed upon a increased threats from El Nin˜ o, climate noumeae also faces risks from pollution determination that such areas are change, disease, and other development and S. glynni may be at risk from essential for the conservation of the and habitat degradation, should the disease. We therefore propose to list all species. ‘‘Conservation’’ means the use species be reintroduced to Panama. The three species as endangered. of all methods and procedures needed to bring the species to the point at extinction risk for T. floreana was found Effects of Listing to be high, based on its small, restricted which listing under the ESA is no range, documented declines, likely low Conservation measures provided for longer necessary. Section 4(a)(3)(A) of levels of genetic diversity, and threats species listed as endangered or the ESA (16 U.S.C. 1533(a)(3)(A)) from El Nin˜ o, climate change, threatened under the ESA include requires that, to the extent prudent and development, and illegal activities, recovery actions (16 U.S.C. 1533(f)); determinable, critical habitat be mitigated by potential for moderate concurrent designation of critical designated concurrently with the listing productivity. habitat, if prudent and determinable (16 of a species. However, critical habitat After reviewing the best available U.S.C. 1533(a)(3)(A)); Federal agency shall not be designated in foreign scientific data and the extinction risk requirements to consult with NMFS countries or other areas outside U.S. evaluations of the three species of coral, under section 7 of the ESA to ensure jurisdiction (50 CFR 424.12 (h)). we concur with Meadows (2014) and their actions do not jeopardize the The best available scientific and conclude that the risk of extinction for species or result in adverse modification commercial data as discussed above all three species is currently high. or destruction of critical habitat should identify the geographical areas occupied it be designated (16 U.S.C. 1536); and by Aipysurus fuscus, Cantharellus Protective Efforts prohibitions on taking (16 U.S.C. 1538). noumeae, Centrophorus harrissoni, We evaluated conservation efforts we Recognition of the species’ plight Pterapogon kauderni, Siderastrea are aware of to protect and recover coral through listing promotes conservation glynni, and Tubastraea floreana as being that are either underway but not yet actions by Federal and state agencies, entirely outside U.S. jurisdiction, so we shown to be effective, or are only foreign entities, private groups, and cannot designate critical habitat for planned. We were not able to find any individuals. The main effects of the these species. information on conservation efforts proposed endangered listings are We can designate critical habitat in specific to C. noumeae or T. floreana, or prohibitions on take, including export areas in the United States currently their habitat, that are not yet and import. unoccupied by the species, if the area(s) implemented or shown to be effective are determined by the Secretary to be and that would potentially alter the Identifying Section 7 Conference and essential for the conservation of the extinction risk for the species. For S. Consultation Requirements species. Regulations at 50 CFR 424.12(e) glynni, we are aware that Dr. Hector Section 7(a)(2) (16 U.S.C. 1536(a)(2)) specify that we shall designate as Guzma´n, who maintains the only of the ESA and NMFS/USFWS critical habitat areas outside the surviving colonies of this species in regulations require Federal agencies to geographical range presently occupied captivity at the STRI laboratories, is consult with us to ensure that activities by the species only when the planning to cryopreserve some they authorize, fund, or carry out are not designation limited to its present range specimens to provide an additional likely to jeopardize the continued would be inadequate to ensure the means to recover the species and existence of listed species or destroy or conservation of the species. The best preserve its genetic information. The adversely modify critical habitat. available scientific and commercial certainty that this effort will be Section 7(a)(4) (16 U.S.C. 1536(a)(4)) of information on these species does not implemented is unclear. Further, the the ESA and NMFS/USFWS regulations indicate that U.S. waters provide any effectiveness of a cryopreservation effort also require Federal agencies to confer specific essential biological function for for species recovery is largely unknown, with us on actions likely to jeopardize any of the species proposed for listing. and thus it is impossible to determine the continued existence of species Based on the best available information, whether this effort will be effective in proposed for listing, or that result in the we have not identified unoccupied conserving or improving the status of destruction or adverse modification of area(s) in U.S. water that are currently this species. We are thus not able to proposed critical habitat of those essential to the conservation of any of conclude that any current conservation species. It is unlikely that the listing of the corals proposed for listing. efforts would alter the extinction risk for these species under the ESA will Therefore, based on the available

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information, we do not intend to diseases or inappropriate genetic (4) Provision of care for live corals or designate critical habitat for Aipysurus mixing; sea snakes that were in captivity at the fuscus, Cantharellus noumeae, (6) Harming captive by, time of listing. These individuals are Centrophorus harrissoni, Pterapogon among other things, injuring or killing a still protected under the ESA and may kauderni, Siderastrea glynni, and captive animal, through experimental or not be killed or injured, or otherwise Tubastraea floreana. potentially injurious care or conducting harmed, and, therefore, must receive proper care. Normal care of captive Identification of Those Activities That research or sexual breeding activities on animals necessarily entails handling or Would Constitute a Violation of Section captive animals, outside the bounds of other manipulation of the animals, and 9 of the ESA normal animal husbandry practices. Captive sexual breeding of corals is we do not consider such activities to On July 1, 1994, NMFS and FWS considered potentially injurious. constitute take or harassment of the published a policy (59 FR 34272) that Furthermore, the production of coral animals so long as adequate care, requires us to identify, to the maximum progeny has conservation implications including veterinary care, when such extent practicable at the time a species (both positive and negative) for wild practices, procedures, or provisions are is listed, those activities that would or populations. Experimental or not likely to result in injury, is would not constitute a violation of potentially injurious care or procedures provided; and section 9 of the ESA. and research or sexual breeding (5) Any interstate and foreign Because we are proposing to list all activities of corals or dusky sea snakes commerce trade of animals already in three corals and the dusky sea snake as may, depending on the circumstances, captivity. Section 11(f) of the ESA gives endangered, all of the prohibitions of be authorized under an ESA 10(a)(1)(A) NMFS authority to promulgate section 9(a)(1) of the ESA will apply to permit for scientific research or the regulations that may be appropriate to these species. These include enhancement of the propagation or enforce the ESA. NMFS may promulgate prohibitions against the import, export, survival of the species. future regulations to regulate trade or use in foreign commerce, or ‘‘take’’ of holding of these species (if any), if the species. These prohibitions apply to Identification of Those Activities That necessary. NMFS will provide the all persons subject to the jurisdiction of Would Not Constitute a Violation of public with the opportunity to comment the United States, including in the Section 9 of the ESA on future proposed regulations. United States, its territorial sea, or on We will identify, to the extent known the high seas. Take is defined as ‘‘to Protective Regulations Under Section at the time of the final rule, specific 4(d) of the ESA harass, harm, pursue, hunt, shoot, activities that will not be considered We are proposing to list Pterapogon wound, kill, trap, capture, or collect, or likely to result in a violation of section to attempt to engage in any such kauderni, and Centrophorus harrissoni 9 of the ESA. Although not binding, we as threatened species. In the case of conduct.’’ The intent of this policy is to are considering the following actions, increase public awareness of the effects threatened species, ESA section 4(d) depending on the circumstances, as not leaves it to the Secretary’s discretion of this listing on proposed and ongoing being prohibited by ESA section 9: activities within the species’ range. whether, and to what extent, to extend (1) Take authorized by, and carried Activities that we believe could result in the section 9(a) ‘‘take’’ prohibitions to out in accordance with the terms and a violation of section 9 prohibitions for the species, and authorizes us to issue conditions of, an ESA section these species include, but are not regulations necessary and advisable for 10(a)(1)(A) permit issued by NMFS for limited to, the following: the conservation of the species. Thus, (1) Possessing, delivering, purposes of scientific research or the we have flexibility under section 4(d) to transporting, or shipping any individual enhancement of the propagation or tailor protective regulations, taking into or part (dead or alive) taken in violation survival of the species; account the effectiveness of available of section 9(a)(1); (2) Continued possession of parts that conservation measures. The 4(d) (2) Delivering, receiving, carrying, were in possession at the time of listing. protective regulations may prohibit, transporting, or shipping in interstate or Such parts may be non-commercially with respect to threatened species, some foreign commerce any individual or exported or imported; however the or all of the acts which section 9(a) of part, in the course of a commercial importer or exporter must be able to the ESA prohibits with respect to activity; provide evidence to show that the parts endangered species. These 9(a) (3) Selling or offering for sale in meet the criteria of ESA section 9(b)(1) prohibitions apply to all individuals, interstate commerce any part, except (i.e., held in a controlled environment at organizations, and agencies subject to antique articles at least 100 years old; the time of listing, in a non-commercial U.S. jurisdiction. We will consider (4) Importing or exporting; activity); potential protective regulations (5) Releasing captive animals into the (3) Continued possession of live pursuant to section 4(d) for the wild without a permit issued under corals or sea snakes that were in proposed threatened species. For section 10(a)(1)(A). Although animals captivity or in a controlled environment example, we may consider future held non-commercially in captivity at (e.g., in aquaria) at the time of this regulations on trade of wild-caught the time of listing are exempt from the listing, so long as the prohibitions under Banggai cardinalfish (see number 7 prohibitions of import and export, the ESA section 9(a)(1) are not violated. below). We seek public comment on individual animals are considered listed Facilities must provide evidence that potential 4(d) protective regulations (see and afforded most of the protections of the animals were in captivity or in a below). the ESA, including most importantly, controlled environment prior to listing. the prohibition against injuring or We suggest such facilities submit Public Comments Solicited killing. Release of a captive animal has information to us on the animals in their To ensure that any final action the potential to injure or kill the animal. possession (e.g., size, age, description of resulting from this proposed rule to list Of an even greater conservation animals, and the source and date of six species will be as accurate and concern, the release of a captive animal acquisition) to establish their claim of effective as possible, we are soliciting has the potential to affect wild possession (see FOR FURTHER comments and information from the populations through introduction of INFORMATION CONTACT); public, other concerned governmental

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agencies, the scientific community, comments on each of the status review proposed rule is exempt from review industry, and any other interested reports, including from: four scientists under Executive Order 12866. This parties on information in the status with expertise on sea snakes or the proposed rule does not contain a review and proposed rule. Comments dusky sea snake specifically, five collection-of-information requirement are encouraged on these proposals (See familiar with the Banggai cardinalfish, for the purposes of the Paperwork DATES and ADDRESSES). We must base five familiar with Harrisson’s dogfish, Reduction Act. our final determination on the best and ten scientists familiar with corals. Executive Order 13132, Federalism available scientific and commercial For these species, we received information when making listing comments from the scientists, and their In accordance with E.O. 13132, we determinations. We cannot, for example, comments are incorporated into the determined that this proposed rule does consider the economic effects of a draft status review reports for each not have significant Federalism effects listing determination. Final species and this 12-month finding. and that a Federalism assessment is not promulgation of any regulation(s) on Proposed Revisions to the NMFS Lists required. In keeping with the intent of these species’ listing proposals will take the Administration and Congress to into consideration the comments and We propose to revise and add table provide continuing and meaningful any additional information we receive, subheadings to accommodate the dialogue on issues of mutual state and proposed listings in our lists of and such communications may lead to Federal interest, this proposed rule will threatened and endangered species at 50 a final regulation that differs from this be given to the relevant governmental CFR 223.102 and 50 CFR 224.101, proposal or result in a withdrawal of agencies in the countries in which the respectively. We propose to revise the this listing proposal. We particularly species occurs, and they will be invited subheading of ‘‘Sea Turtles’’ in both seek: to comment. We will confer with the tables by changing the subheading to (1) Information concerning the threats U.S. Department of State to ensure ‘‘Reptiles.’’ This new subheading will to any of the six species proposed for appropriate notice is given to foreign encompass all currently listed sea listing; nations within the range of all three turtles as well as other marine reptiles (2) Taxonomic information on any of species. As the process continues, we like the dusky sea snake. In addition, we these species; intend to continue engaging in informal (3) Biological information (life propose to add the subheading ‘‘Corals’’ to our table at 50 CFR 224.101. This and formal contacts with the U.S. State history, genetics, population Department, giving careful connectivity, etc.) on any of these subheading has already been added to our table at 50 CFR 223.102 in a consideration to all written and oral species; comments received. (4) Efforts being made to protect any previous rulemaking (79 FR 20802; of these species throughout their current April 14, 2014). These revisions and List of Subjects in 50 CFR Parts 223 and ranges; additions are not substantive changes, 224 (5) Information on the commercial but having these headings will help the trade of any of these species; public identify and locate species of Administrative practice and (6) Historical and current distribution interest in a more efficient manner. procedure, Endangered and threatened species, Exports, Imports, Reporting and and abundance and trends for any of References these species; and record keeping requirements, (7) Information relevant to potential A complete list of the references used Transportation. ESA section 4(d) protective regulations in this proposed rule is available upon Dated: December 8, 2014. for any of the proposed threatened request (see ADDRESSES). Samuel D. Rauch, III. species, especially the application, if Classification Deputy Assistant Administrator for any, of the ESA section 9 prohibitions Regulatory Programs, National Marine on import, take, possession, receipt, and National Environmental Policy Act Fisheries Service. sale of the Banggai cardinalfish which is The 1982 amendments to the ESA, in For the reasons set out in the currently in international trade. section 4(b)(1)(A), restrict the preamble, 50 CFR parts 223 and 224 are We request that all information be information that may be considered proposed to be amended as follows: accompanied by: (1) Supporting when assessing species for listing. Based documentation, such as maps, on this limitation of criteria for a listing PART 223—THREATENED MARINE bibliographic references, or reprints of decision and the opinion in Pacific AND ANADROMOUS SPECIES pertinent publications; and (2) the Legal Foundation v. Andrus, 675 F. 2d submitter’s name, address, and any 825 (6th Cir. 1981), NMFS has ■ 1. The authority citation for part 223 association, institution, or business that concluded that ESA listing actions are continues to read as follows: the person represents. not subject to the environmental assessment requirements of the National Authority: 16 U.S.C. 1531–1543; subpart B, Role of Peer Review § 223.201–202 also issued under 16 U.S.C. Environmental Policy Act (NEPA) (See In December 2004, the Office of 1361 et seq.; 16 U.S.C. 5503(d) for NOAA Administrative Order 216–6). § 223.206(d)(9). Management and Budget (OMB) issued a Final Information Quality Bulletin for Executive Order 12866, Regulatory ■ 2. In § 223.102, amend the table in Peer Review establishing a minimum Flexibility Act, and Paperwork paragraph (e) by: peer review standard. Similarly, a joint Reduction Act ■ A. Revising the table subheading of NMFS/FWS policy (59 FR 34270; July 1, As noted in the Conference Report on ‘‘Sea Turtles 2’’ to ‘‘Reptiles 2’’; and 1994) requires us to solicit independent the 1982 amendments to the ESA, ■ B. Adding new entries for two species expert review from qualified specialists, economic impacts cannot be considered in alphabetical order under the ‘‘Fishes’’ concurrent with the public comment when assessing the status of a species. table subheading to read as follows: period. The intent of the peer review Therefore, the economic analysis policy is to ensure that listings are based requirements of the Regulatory § 223.102 Enumeration of threatened on the best scientific and commercial Flexibility Act are not applicable to the marine and anadromous species. data available. We solicited peer review listing process. In addition, this * * * * *

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(e) The threatened species under the jurisdiction of the Secretary of Commerce are:

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

******* REPTILES 2

******* FISHES Cardinalfish, Banggai ...... Pterapogon kauderni ...... Entire species ...... Insert Federal Register ci- NA NA tation and date when published as a final rule].

******* Shark, Harrisson’s dogfish Centrophorus harrissoni ... Entire species ...... Insert Federal Register ci- NA NA tation and date when published as a final rule]. 1 Species includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement, see 61 FR 4722, February 7, 1996), and evolutionarily significant units (ESUs) (for a policy statement, see 56 FR 58612, November 20, 1991). 2 Jurisdiction for sea turtles by the Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service, is limited to turtles while in the water.

PART 224—ENDANGERED MARINE ■ A. Revising the table subheading of name under the ‘‘Corals’’ table AND ANADROMOUS SPECIES ‘‘Sea Turtles 2’’ to ‘‘Reptiles 2’’; subheading to read as follows: ■ B. Adding an entry for the dusky sea ■ 3. The authority citation for part 224 snake in alphabetical order under the § 224.101 Enumeration of endangered continues to read as follows: new ‘‘Reptiles 2’’ table subheading; marine and anadromous species. ■ C. Adding a ‘‘Corals’’ table Authority: 16 U.S.C. 1531–1543 and 16 * * * * * subheading to follow the ‘‘Molluscs’’ U.S.C. 1361 et seq. (h) The endangered species under the table subheading; and ■ 4. In § 224.101, paragraph (h), amend ■ D. Adding entries for three species of jurisdiction of the Secretary of the table by: coral in alphabetical order by scientific Commerce are:

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

******* REPTILES 2 Sea snake, dusky ...... Aipysurus fuscus ...... Entire species ...... Insert Federal Register ci- NA NA tation and date when published as a final rule].

******* MOLLUSCS

******* CORALS Coral, [no common name] Cantharellus noumeae ...... Entire species ...... Insert Federal Register ci- NA NA tation and date when published as a final rule]. Coral, [no common name] Siderastrea glynni ...... Entire species ...... Insert Federal Register ci- NA NA tation and date when published as a final rule]. Coral, [no common name] Tubastraea floreana ...... Entire species ...... Insert Federal Register ci- NA NA tation and date when published as a final rule]. 1 Species includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement, see 61 FR 4722, February 7, 1996), and evolutionarily significant units (ESUs) (for a policy statement, see 56 FR 58612, November 20, 1991). 2 Jurisdiction for sea turtles by the Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service, is limited to turtles while in the water.

* * * * * [FR Doc. 2014–29203 Filed 12–15–14; 8:45 am] BILLING CODE 3510–22–P

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