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(x) Have disinfecting supplies, gloves, The revision and addition read as Dated: December 9, 2016. masks, and plastic for containing follows: Andrew M. Slavitt, contaminated materials. Acting Administrator, Centers for Medicare (xi) Have a fabrication facility § 424.58 Requirements for DMEPOS & Medicaid Services. accreditation organizations. information system, paper or digital, * * * * * Dated: December 22, 2016. that can track the production, list Sylvia M. Burwell component part number (and serial (c) Additional requirements for accrediting qualified suppliers. To Secretary, Department of Health and Human number if available), quantity, that is Services. accredit qualified suppliers that linked to patient information and be [FR Doc. 2017–00425 Filed 1–11–17; 8:45 am] Health Insurance Portability and fabricate or bill Medicare for prosthetics BILLING CODE 4120–01–P Accountability Act compliant. Such a and custom-fabricated orthotics as system must allow facility staff and specified in § 424.57(c)(22)(ii), an management, including those independent accreditation organization DEPARTMENT OF COMMERCE fabricating, to identify any parts that must be one of the following: could be recalled at a later date. (1) American Board for Certification National Oceanic and Atmospheric (xii) Have parallel bars, a full-length in Orthotics and Prosthetics, Administration mirror, and other appropriate Incorporated (ABC). assessment tools. (2) Board for Orthotist/Prosthetist 50 CFR Part 223 (xiii) Have a process using Certification International, Incorporated precautions to handle used patient (BOC). [Docket No. 160105011–6999–02] devices that are contaminated. (3) An organization that— RIN 0648–XE390 (xiv) Have repair and disinfecting (i) Employs or contracts with an areas clearly labeled. orthotist, prosthetist, occupational 12-Month Finding on a Petition To List (xv) Have the ability to handle all therapist or physical therapist who— Giant and Reef Manta Rays as potentially hazardous materials in (A) Meets the definition of qualified Threatened or Endangered Under the facility properly. practitioner specified in § 424.57(a); and Endangered Species Act (xvi) Have an emergency management (B) Is utilized for the purpose of AGENCY: National Marine Fisheries plan and a safety management plan. surveying the supplier or practitioner Service (NMFS), National Oceanic and (xvii) Have policy for detecting/ for compliance; and Atmospheric Administration (NOAA), reporting counterfeit supplies. (ii) Has the authority granted by CMS Commerce. (xviii) Have the proper tools, to approve or deny the accreditation of ACTION: equipment, and computers commonly Proposed rule; 12-month qualified suppliers as defined in petition finding; request for comments. used in the fabrication of particular § 424.57(a) based on a determination items and typically associated with the that the organization has standards SUMMARY: We, NMFS, announce a 12- particular technical approach (negative equivalent to the ABC or BOC. month finding on a petition to list the impression/positive model, CAD–CAM, * * * * * giant (Manta birostris) and or direct formed), as applicable: These ■ reef manta ray (Manta alfredi) as tools and equipment would include, but 4. Section § 424.535 is amended as follows: threatened or endangered under the are not limited to the following Endangered Species Act (ESA). We have ■ a. Revising the section heading. (A) Computers with appropriate completed a comprehensive status ■ b. In paragraph (a)(2) introductory text graphics/modeling capacity and review of both species in response to by removing the phrase ‘‘the provider or technology. this petition. Based on the best scientific supplier is—’’ and adding in its place (B) Band saw. and commercial information available, ‘‘the provider or supplier is any of the (C) Disc sander. including the status review report following:’’. (D) Sanding paper. (Miller and Klimovich 2016), and after ■ (E) Flexible shaft sander. c. In paragraph (a)(2)(ii) by removing taking into account efforts being made (F) Lathe. the phrase ‘‘Is debarred, suspended, or’’ to protect these species, we have (G) Drill press. and adding in its place the phrase determined that the giant manta ray (M. (H) Sewing machine. ‘‘Debarred, suspended or’’. birostris) is likely to become an (I) Grinding equipment. ■ d. Adding paragraph (a)(2)(iii). endangered species within the (J) Paint-spraying equipment. The revision and addition reads as foreseeable future throughout a (K) Welding equipment. follows: significant portion of its range. (L) Alignment jig. § 424.535 Revocation of enrollment and Therefore, we propose to list the giant (M) Ovens capable of heating plastics billing privileges in the Medicare program. manta ray as a threatened species under for molding. the ESA. Any protective regulations (a) * * * (N) Computer controlled milling determined to be necessary and machine. (2) * * * advisable for the conservation of the (O) Lockable storage areas for raw (iii) A qualified supplier as defined in proposed threatened giant manta ray materials and finished devices. § 424.57(a) that submitted a claim for under ESA section 4(d) would be (P) Air compressor. payment for a prosthetic or custom- proposed in a subsequent Federal * * * * * fabricated orthotic that was not— Register announcement. Should the ■ 3. Section 424.58 is amended as (A) Furnished by a qualified proposed listing be finalized, we would follows: practitioner; and also designate critical habitat for the ■ a. Revising the section heading. (B) Fabricated by a qualified species, to the maximum extent prudent ■ b. Redesignating paragraphs (c) practitioner or qualified supplier as and determinable. We solicit through (e) as paragraphs (d) through (f) defined in § 424.57(a) at a fabrication information to assist this proposed respectively. facility as defined in § 424.57(a). listing determination, the development ■ c. Adding a new paragraph (c). * * * * * of proposed protective regulations, and

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designation of critical habitat in the Caribbean manta ray (M. c.f. birostris) as significant portion of its range.’’ Thus, event the proposed threatened listing for threatened or endangered under the in the context of the ESA, the Services the giant manta ray is finalized. ESA throughout their respective ranges, interpret an ‘‘endangered species’’ to be Additionally, we have determined that or, as an alternative, to list any one that is presently at risk of the reef manta ray (M. alfredi) is not identified distinct population segments extinction. A ‘‘threatened species’’ is currently in danger of extinction (DPSs) as threatened or endangered. The not currently at risk of extinction, but is throughout all or a significant portion of petitioners also requested that critical likely to become so in the foreseeable its range and is not likely to become so habitat be designated concurrently with future. The key statutory difference within the foreseeable future. Therefore, listing under the ESA. On February 23, between a threatened and endangered we find that the reef manta ray does not 2016, we published a positive 90-day species is the timing of when a species warrant listing under the ESA at this finding (81 FR 8874) announcing that may be in danger of extinction, either time. the petition presented substantial now (endangered) or in the foreseeable scientific or commercial information future (threatened). DATES: Comments on the proposed rule indicating that the petitioned action Additionally, as the definition of to list the giant manta ray must be may be warranted for the giant manta ‘‘endangered species’’ and ‘‘threatened received by March 13, 2017. Public ray and reef manta ray, but that the species’’ makes clear, the determination hearing requests must be made by Caribbean manta ray is not a of extinction risk can be based on either February 27, 2017. taxonomically valid species or assessment of the range wide status of ADDRESSES: You may submit comments subspecies for listing, and explained the the species, or the status of the species on this document, identified by NOAA– basis for that finding. We also in a ‘‘significant portion of its range.’’ NMFS–2016–0014, by either of the announced the initiation of a status The Services published a final policy to following methods: • review of the giant manta ray and reef clarify the interpretation of the phrase Electronic Submissions: Submit all manta ray, as required by section ‘‘significant portion of the range’’ in the electronic public comments via the 4(b)(3)(a) of the ESA, and requested ESA definitions of ‘‘threatened species’’ Federal eRulemaking Portal. Go to information to inform the agency’s and ‘‘endangered species’’ (79 FR 37577; www.regulations.gov/ decision on whether these species July 1, 2014) (SPR Policy). The policy #!docketDetail;D=NOAA-NMFS-2016- warrant listing as endangered or consists of the following four 0014. Click the ‘‘Comment Now’’ icon, threatened under the ESA. components: complete the required fields, and enter (1) If a species is found to be or attach your comments. Listing Species Under the Endangered endangered or threatened in only an • Mail: Submit written comments to Species Act SPR, and the SPR is not a DPS, the Maggie Miller, NMFS Office of We are responsible for determining entire species is listed as endangered or Protected Resources (F/PR3), 1315 East whether giant and reef manta rays are threatened, respectively, and the ESA’s West Highway, Silver Spring, MD threatened or endangered under the protections apply across the species’ 20910, USA. ESA (16 U.S.C. 1531 et seq.). To make entire range. Instructions: Comments sent by any this determination, we first consider (2) A portion of the range of a species other method, to any other address or whether a group of organisms is ‘‘significant’’ if its contribution to the individual, or received after the end of constitutes a ‘‘species’’ under section 3 viability of the species is so important the comment period, may not be of the ESA, then whether the status of that without that portion, the species considered by NMFS. All comments the species qualifies it for listing as would be in danger of extinction or received are a part of the public record either threatened or endangered. Section likely to become so in the foreseeable and will generally be posted for public 3 of the ESA defines species to include future. viewing on www.regulations.gov ‘‘any subspecies of fish or wildlife or (3) The range of a species is without change. All personally plants, and any distinct population considered to be the general identifying information (e.g., name, segment of any species of vertebrate fish geographical area within which that address, etc.), confidential business or wildlife which interbreeds when species can be found at the time USFWS information, or otherwise sensitive mature.’’ On February 7, 1996, NMFS or NMFS makes any particular status information submitted voluntarily by and the U.S. Fish and Wildlife Service determination. This range includes the sender will be publicly accessible. (USFWS; together, the Services) adopted those areas used throughout all or part NMFS will accept anonymous a policy describing what constitutes a of the species’ life cycle, even if they are comments (enter ‘‘N/A’’ in the required DPS of a taxonomic species (61 FR not used regularly (e.g., seasonal fields if you wish to remain 4722). The joint DPS policy identified habitats). Lost historical range is anonymous). two elements that must be considered relevant to the analysis of the status of You can find the petition, status when identifying a DPS: (1) The the species, but it cannot constitute an review report, Federal Register notices, discreteness of the population segment SPR. and the list of references electronically in relation to the remainder of the (4) If a species is not endangered or on our Web site at species (or subspecies) to which it threatened throughout all of its range www.fisheries.noaa.gov/pr/species/fish/ belongs; and (2) the significance of the but is endangered or threatened within manta-ray.html. population segment to the remainder of an SPR, and the population in that FOR FURTHER INFORMATION CONTACT: the species (or subspecies) to which it significant portion is a valid DPS, we Maggie Miller, NMFS, Office of belongs. will list the DPS rather than the entire Protected Resources, (301) 427–8403. Section 3 of the ESA defines an taxonomic species or subspecies. SUPPLEMENTARY INFORMATION: endangered species as ‘‘any species The statute also requires us to which is in danger of extinction determine whether any species is Background throughout all or a significant portion of endangered or threatened throughout all On November 10, 2015, we received its range’’ and a threatened species as or a significant portion of its range as a a petition from Defenders of Wildlife to one ‘‘which is likely to become an result of any one or a combination of the list the giant manta ray (M. birostris), endangered species within the following five factors: the present or reef manta ray (M. alfredi) and foreseeable future throughout all or a threatened destruction, modification, or

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curtailment of its habitat or range; reflect concepts that are well-founded in The genus Manta has a long and overutilization for commercial, conservation biology and that convoluted taxonomic history due recreational, scientific, or educational individually and collectively provide partially to the difficulty of preserving purposes; disease or predation; the strong indicators of extinction risk such large specimens and conflicting inadequacy of existing regulatory (NMFS 2015). historical reports of taxonomic mechanisms; or other natural or The draft status review report was characteristics (Couturier et al. 2012; manmade factors affecting its continued subjected to independent peer review as Kitchen-Wheeler 2013). All manta rays existence (ESA section 4(a)(1)(A)–(E)). required by the Office of Management were historically categorized as Manta Section 4(b)(1)(A) of the ESA requires us and Budget (OMB) Final Information birostris, but Marshall et al. (2009) to make listing determinations based Quality Bulletin for Peer Review (M– presented new data that supported the solely on the best scientific and 05–03; December 16, 2004). The draft splitting of the monospecific Manta commercial data available after status review report was peer reviewed genus into two species: M. birostris and conducting a review of the status of the by independent specialists selected M. alfredi. species and after taking into account from the academic and scientific Both Manta species have diamond- efforts being made by any State or community, with expertise in manta ray shaped bodies with wing-like pectoral foreign nation or political subdivision biology, conservation, and management. fins; the distance over this wingspan is thereof to protect the species. In The peer reviewers were asked to termed disc width (DW). There are two evaluating the efficacy of existing evaluate the adequacy, appropriateness, distinct color types in both species: domestic protective efforts, we rely on and application of data used in the chevron and black (melanistic). Most of the Services’ joint Policy on Evaluation status review, including the extinction the chevron variants have a black dorsal of Conservation Efforts When Making risk analysis. All peer reviewer surface and a white ventral surface with Listing Decisions (‘‘PECE’’; 68 FR 15100; comments were addressed prior to distinct patterns on the underside that March 28, 2003) for any conservation dissemination and finalization of the can be used to identify individuals efforts that have not been implemented, draft status review report and (Marshall et al. 2008; Kitchen-Wheeler or have been implemented but not yet publication of this finding. 2010; Deakos et al. 2011). While these demonstrated effectiveness. We subsequently reviewed the status markings are assumed to be permanent, there is some evidence that the Status Review review report, its cited references, and peer review comments, and believe the pigmentation pattern of M. birostris may A NMFS biologist in the Office of status review report, upon which this actually change over the course of Protected Resources led the status 12-month finding and proposed rule is development (based on observation of review for the giant manta ray and reef based, provides the best available two individuals in captivity), and thus manta ray (Miller and Klimovich 2016). scientific and commercial information caution may be warranted when using The status review examined both on the two manta ray species. Much of color markings for identification species’ statuses throughout their the information discussed below on purposes in the wild (Ari 2015). The respective ranges and also evaluated if manta ray biology, distribution, black color variants of both species are any portion of their range was abundance, threats, and extinction risk entirely black on the dorsal side and significant as defined by the Services’ is attributable to the status review almost completely black on the ventral SPR Policy (79 FR 37578; July 1, 2014). report. However, in making the 12- side, except for areas between the gill- In order to complete the status review, month finding determination and slits and the abdominal area below the information was compiled on each proposed rule, we have independently gill-slits (Kitchen-Wheeler 2013). species’ biology, ecology, life history, applied the statutory provisions of the threats, and status from information Range, Distribution and Habitat Use ESA, including evaluation of the factors contained in the petition, our files, a Manta rays are circumglobal in range, set forth in section 4(a)(1)(A)–(E) and comprehensive literature search, and but within this broad distribution, our regulations regarding listing consultation with experts. We also individual populations are scattered and determinations. The status review report considered information submitted by highly fragmented (CITES 2013). The the public in response to our petition is available on our Web site (see ranges of the two manta species finding. In assessing the extinction risk ADDRESSES section) and the peer review sometimes overlap; however, at a finer report is available at http:// of both species, we considered the _ spatial scale, the two species generally demographic viability factors developed www.cio.noaa.gov/services programs/ appear to be allopatric within those by McElhany et al. (2000). The approach prplans/PRsummaries.html. Below is a habitat areas (Kashiwagi et al. 2011) and of considering demographic risk factors summary of the information from the exhibit different habitat use and to help frame the consideration of status review report and our analysis of movement patterns (inshore versus extinction risk has been used in many the status of the giant manta ray and reef offshore reef habitat use) (Marshall and of our status reviews, including for manta ray. Further details can be found Bennett 2010b; Kashiwagi et al. 2011). Pacific salmonids, Pacific hake, walleye in Miller and Klimovich (2016). Clark (2010) suggests that the larger M. pollock, Pacific cod, Puget Sound Description, Life History, and Ecology birostris may forage in less productive rockfishes, Pacific herring, scalloped, of the Petitioned Species pelagic waters and conduct seasonal great, and smooth hammerhead sharks, migrations following prey abundance, and black abalone (see Species Description whereas M. alfredi is more of a resident www.nmfs.noaa.gov/pr/species/ for Manta rays are large bodied, species in areas with regular coastal links to these reviews). In this approach, planktivorous rays, considered part of productivity and predictable prey the collective condition of individual the subfamily that appears to abundance. Kashiwagi et al. (2010) populations is considered at the species have diverged from Rhinoptera around observed that even in areas where both level according to four viable 30 million years ago (Poortvliet et al. species are found in large numbers at population descriptors: abundance, 2015). Manta species are distinguished the same feeding and cleaning sites, the growth rate/productivity, spatial from other rays in that they tend two species do not interact with each structure/connectivity, and diversity. to be larger, with a terminal mouth, and other (e.g., they are not part of the same These viable population descriptors have long cephalic fins (Evgeny 2010). feeding group, and males of one species

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do not attempt to mate with females of 2011a). In a tracking study of six M. capable of traveling long distances, the other species). Additional studies on birostris individuals from off Mexico’s similar to M. birostris (Yano et al. 1999; habitat use for both species are needed, Yucatan peninsula, Graham et al. (2012) Germanov and Marshall 2014), reef particularly investigating how these calculated a maximum distance manta rays are considered a more individuals influence their environment travelled of 1,151 km (based on resident species than giant manta rays as studies have shown that the removal cumulative straight line distance (Homma et al. 1999; Dewar et al. 2008; of large plankton feeders, like manta between locations; tag period ranged Clark 2010; Kitchen-Wheeler 2010; rays, from the ecosystem can cause from 2 to 64 days). Similarly, Hearn et Anderson et al. 2011a; Deakos et al. significant changes in species al. (2014) report on a tagged M. birostris 2011; Marshall et al. 2011b; McCauley et composition (Springer et al. 2003). that was tracked from Isla de la Plata al. 2014), with residencies estimated at The giant manta ray can be found in (Ecuador) to west of Darwin Island (tag up to 1.5 years (Clark 2010). For all ocean basins. In terms of range, was released after 104 days), a straight- example, along the east coast of within the Northern Hemisphere, the line distance of 1,500 km, further Australia, mark-recapture methods and species has been documented as far confirming that the species is capable of north as southern California and New fairly long distance migrations but also photographic identification of reef Jersey on the United States west and demonstrating connectivity between manta rays from 1982 to 2012 revealed east coasts, respectively, and Mutsu mainland and offshore islands. a re-sighting rate of more than 60 Bay, Aomori, Japan, the Sinai Peninsula However, a recent study by Stewart et percent (with females more likely to be and Arabian Sea, Egypt, and the Azores al. (2016a) suggests that the species may re-sighted than males), suggesting high Islands (Gudger 1922; Kashiwagi et al. not be as highly migratory as previously site fidelity to aggregation sites, 2010; Moore 2012; CITES 2013). In the thought. Using pop-up satellite archival including several locations within a Southern Hemisphere, the species tags in combination with analyses of range of up to 650 km (Couturier et al. occurs as far south as Peru, Uruguay, stable isotope and genetic data, the 2014). In , 76 percent of 105 M. South Africa, New Zealand and French authors found evidence that M. birostris alfredi individuals observed over 15 Polynesia (Mourier 2012; CITES 2013). may actually exist as well-structured years of surveys were re-sighted along Despite this large range, sightings are subpopulations off Mexico’s coast that the Kona coast, also confirming the high often sporadic. The timing of these exhibit a high degree of residency site fidelity behavior of the species sightings also varies by region (for (Stewart et al. 2016a). Additional (Clark 2010). Additionally, predictable example, the majority of sightings in research is required to better understand seasonal aggregations of M. alfredi, Brazil occur during June and September, the distribution and movement of the largely thought to be feeding-related and while in New Zealand sightings mostly species throughout its range. influenced by the seasonal distribution occur between January and March) and In terms of range of the reef manta of prey (Anderson et al. 2011a), have seems to correspond with the movement ray, M. alfredi, the species is currently been documented off the Maldives of , current circulation and only observed in the Indian Ocean and (Anderson et al. 2011a), Maui, Hawaii tidal patterns, seawater temperature, the western and south Pacific. The (Deakos et al. 2011), Lady Elliott Island, and possibly mating behavior (Couturier northern range limit for the species in Australia (Couturier et al. 2014), et al. 2012; De Boer et al. 2015; the western Pacific is presently known Ningaloo Reef, Western Australia Armstrong et al. 2016). to be off Kochi, Japan (32°48′ N., 132°58′ Within its range, M. birostris inhabits E.), and its eastern limit in the Pacific (McGregor et al. 2008), and southern tropical, subtropical, and temperate is known to be Fatu Hiva in French (Marshall et al. 2011c; bodies of water and is commonly found Polynesia (10°29′ S.; 138°37′ W.) Rohner et al. 2013). offshore, in oceanic waters, and near (Kashiwagi et al. 2010; Mourier 2012). Diet and Feeding productive coastlines (Marshall et al. However, it is difficult to estimate the 2009; Kashiwagi et al. 2011). As such, historical range of M. alfredi due to As previously mentioned, manta giant manta rays can be found in cooler confusion until recently about its feeding habits appear to be influenced water, as low as 19 °C, although identification (Marshall et al. 2009). For by the movement and accumulation of temperature preference appears to vary example, prior to the splitting of the zooplankton (Armstrong et al. 2016). by region (Duffy and Abbott 2003; genus, it was assumed that all manta Both manta species primarily feed on Marshall et al. 2009; Freedman and Roy rays found in the Philippines were M. planktonic organisms such as 2012; Graham et al. 2012). Additionally, birostris; however, based on recent euphausiids, copepods, mysids, giant manta rays exhibit a high degree survey efforts, it has been confirmed decapod larvae and shrimp, but some of plasticity in terms of their use of that both M. birostris and M. alfredi studies have noted their consumption of depths within their habitat, with tagging occur in these waters (Verdote and small and moderate sized fishes as well studies that show the species Ponzo 2014; Aquino et al. 2015; (Bertolini 1933; Bigelow and Schroeder conducting night descents of 200–450 m Rambahiniarison et al. 2016). This may 1953; Carpenter and Niem 2001; The depths (Rubin et al. 2008; Stewart et al. be the case elsewhere through its range Hawaii Association for Marine 2016b) and capable of diving to depths and underscores the need for Education and Research Inc. 2005). exceeding 1,000 m (A. Marshall et al. concentrated survey effort in order to Mantas appear to be primarily nocturnal unpubl. data 2011 cited in Marshall et better understand the distribution of al. (2011a)). these two manta ray species. feeders, consistent with the upward The giant manta ray is considered to Manta alfredi is commonly seen migration of zooplankton at night, be a migratory species, with satellite inshore near coral and rocky reefs and increasing their accessibility (Cushing tracking studies using pop-up satellite appears to avoid colder waters (<21 °C) 1951; Forward 1988). Known manta archival tags registering movements of (Rohner et al. 2013; Braun et al. 2014). feeding areas that have been reported in the giant manta ray from Mozambique to Reef manta rays prefer habitats along the literature are summarized in Table South Africa (a distance of 1,100 km), productive nearshore environments 1 of Miller and Klimovich (2016); from Ecuador to Peru (190 km), and (such as island groups or near upwelling however, it is likely that additional from the Yucatan, Mexico, into the Gulf events), and while recent tracking feeding areas exist throughout both of Mexico (448 km) (Marshall et al. studies indicate that M. alfredi is species’ respective ranges.

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Growth and Reproduction turning abruptly (Deakos et al. 2011). , Ningaloo Reef, Hawaii, , Manta rays are viviparous (i.e., give Sexual dimorphism is present in manta , and eastern Australia birth to live young), with a gestation rays, with female M. alfredi as much as (Dewar et al. 2008; Clark 2010; period of around one year (Matsumoto 18 percent larger than males, so it is Couturier et al. 2011; Deakos et al. 2011; and Uchida 2008; Uchida et al. 2008), unlikely that a male could force a Cerutti-Pereyra et al. 2012; Couturier et and a reproductive periodicity of female to mate against her will (Deakos al. 2014). The population structure for the anywhere from 1 to 5 years (see Table 2010; Marshall and Bennett 2010b). wider-ranging M. birostris is less clear. 3 in Miller and Klimovich (2016)). Additionally, males have never been While Clark (2010), using photo- Generally, not much is known about observed to compete with each other identification survey data collected manta ray growth and development. directly for the attention of the female, between 1992 and 2007 along the Kona, Free swimming wild mantas have been so these mating chains may function as Hawaii, coast, found low site-fidelity for observed as small as 1.02 m DW and a kind of endurance rivalry (Andersson 1994; Deakos 2012). No copulations M. birostris and high rate of 1.22 m DW (Kitchen-Wheeler 2013), have been observed in the wild, so it is immigration, indicative of a population with size at birth estimates ranging from difficult to determine which males have that is pelagic rather than coastal or 0.9 m DW to 1.92 m DW (see Tables 2 a mating advantage, but this kind of island-associated, Stewart et al. (2016a) and 3 in Miller and Klimovich (2016)); endurance trial usually selects for the provided recent evidence to show that however, the lack of observations of success of larger males (Andersson and the giant manta rays off Pacific Mexico small manta rays throughout the Iwasa 1996; Deakos 2012). may exist as isolated subpopulations, species’ respective ranges may indicate Although mantas have been reported with distinct home ranges. Additionally, that manta rays segregate by size, with to live to at least 40 years old (Marshall researchers are presently investigating different habitats potentially used by and Bennett 2010b; Marshall et al. whether there is a potential third manta neonates and juveniles (Deakos 2010b). 2011b; Kitchen-Wheeler 2013) with low ray species resident to the Yucata´n While these habitats have yet to be rates of natural mortality (Couturier et coastal waters of the Gulf of Mexico identified, Erdmann (2014) presents a al. 2012), the time needed to grow to (previously identified as M. birostris) hypothesis, based on tagging data of a ∼ maturity and the low reproductive rates (Hinojosa-Alvarez et al. 2016). Using the juvenile M. alfredi ( 1.5m DW), that mean that a female will be able to mitochondrial ND5 region (maternally- mantas likely give birth in protected produce only 5–15 pups in her lifetime inherited DNA), Hinojosa-Alvarez et al. areas, such as lagoons, that provide (CITES 2013). Generation time for both (2016) found shared haplotypes between protection from larger predators. species (based on M. alfredi life history Yucata´n manta ray samples and known In M. alfredi, Deakos (2012) observed parameters) is estimated to be 25 years M. birostris samples from Mozambique, that sexual maturity was delayed until (Marshall et al. 2011a; Marshall et al. Indonesia, Japan, and Mexico, but growth had reached 90 percent of 2011b). Known life history discovered four new manta ray maximum size, pointing to large body characteristics of M. birostris and M. haplotypes, exclusive to the Yucata´n size providing a reproductive advantage. alfredi are summarized in Tables 2 and samples. While analysis using the Deakos (2010) concluded that the 3 in Miller and Klimovich (2016). nuclear RAG1 gene (bi-parentally- minimum size at sexual maturity was inherited DNA) showed the Yucata´n Population Structure 3.37 DW for female M. alfredi and 2.80 samples to be consistent with identified m DW for males in Maui. There is no Since the splitting of the Manta M. birostris samples, the authors suggest evidence that male size affects mating genus, most of the recent research has that the ND5 genetic evidence indicates success of M. alfredi in any way, but examined the genetic discreteness, the potential for a third, distinctive larger females were observed to have phylogeny, and the evolutionary manta genetic group or possibly M. higher rates of pregnancy than smaller speciation in manta rays (Cerutti- birostris subspecies. At this time, females (Deakos 2012). Homma et al. Pereyra et al. 2012; Kashiwagi et al. additional studies, including in-depth (1999) hypothesized that age at sexual 2012; Poortvliet et al. 2015). Very few taxonomic studies and additional maturity was 8–13 years in mantas and studies have focused on the population genetic sampling, are needed to better the data of Uchida et al. (2008), structure within each species. However, understand the population structure of Marshall et al. (2011a) and Marshall and based on genetic sampling, photo- both species throughout their respective Bennett (2010b) confirmed this estimate. identification, and tracking studies, ranges. However, a population of female M. preliminary results tend to indicate that alfredi in the Maldives displayed late reef manta rays exist in isolated and Population Demographics maturity (15 years or more) and lower potentially genetically divergent Given their large sizes, manta rays are reproductive rates than previously populations. For example, using genetic assumed to have fairly high survival reported (one pup every five years, sequencing of mitochondrial DNA rates after maturity (e.g., low natural instead of biennially) (G. Stevens in (which is maternally-inherited) Cerutti- predation rates). Using estimates of prep. as cited in CITES (2013)). In Pereyra et al. (2012) found low genetic known life history parameters for both contrast, Clark (2010) described a rapid divergence (<1 percent) but giant and reef manta rays, and plausible transition to maturity for M. alfredi in ‘‘phylogeographic disjunction’’ between range estimates for the unknown life Kona, Hawaii, with estimates of males the M. alfredi samples from Australia history parameters, Dulvy et al. (2014) reaching sexual maturity as early as 3– (n = 2; Ningaloo Reef) and Indonesia calculated a maximum population 4 years. (n = 2), suggesting biogeographic factors growth rate of Manta spp. and found it In terms of mating behavior, during may be responsible for population to be one of the lowest values when courting, manta rays are commonly differentiation within the species. compared to 106 other shark and ray observed engaging in ‘‘mating chains,’’ Although based on very few samples (4 species. After taking into consideration where multiple males will pursue a total), these findings are consistent with different model assumptions, and the single female. The mating displays can photo-identification and tracking criteria for assessing productivity in last hours or days, with the female studies, which suggest high site-fidelity Musick (1999), Dulvy et al. (2014) swimming rapidly ahead of the males and residency for M. alfredi in many estimated realized productivity (r) for and occasionally somersaulting or portions of its range, including manta rays to be 0.029 (Dulvy et al.

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2014). This value is similar to the International Trade in Endangered M. birostris population in Cocos Island productivity estimate from Kashiwagi Species of Wild Fauna and Flora National Park, Costa Rica, where (2014) who empirically determined an r (CITES), it states that because 10 protections for the species have existed value of 0.023 using capture-mark- populations of M. birostris have been for over 20 years. Using a standardized recapture analyses. Ward-Paige et al. actively studied, 25 other aggregations time series of observations collected by (2013) calculated slightly higher have been anecdotally identified, and dive masters on 27,527 dives conducted estimates for the intrinsic rate of all other sightings are rare, the total from 1993 to 2013, giant manta ray population increase, with r = 0.05 for M. global population may be small (CITES relative abundance declined by alfredi and r = 0.042 for M. birostris; 2013). The greatest number of M. approximately 89 percent. Based on the however, these estimates still place both birostris identified in the four largest frequency of the species’ presence on manta ray species into or at the very known aggregation sites ranges from 180 dives (4 percent), with a maximum of 15 edge of the ‘‘very low’’ productivity to 1,500. Ecuador is thought to be home individuals observed on a single dive, category (r <0.05), based on the to the largest identified population of M. the authors suggest that Cocos Island productivity parameters and criteria in birostris in the world, with large may not be a large aggregating spot for Musick (1999). aggregation sites within the waters of the species, and suggest that the decline In order to determine how changes in the Machalilla National Park and the observed in the population is likely due survival may affect populations, Galapagos Marine Reserve (Hearn et al. to overfishing of the species outside of Smallegange et al. (2016) modeled the 2014). Within the Indian Ocean, the National Park (White et al. 2015). demographics of reef manta rays. numbers of giant manta rays identified Given that all manta rays were Results showed that increases in through citizen science in Thailand’s identified as M. birostris prior to 2009, yearling or adult annual survival rates waters (primarily on the west coast, off information on the historical abundance resulted in much greater responses in Khao Lak and Koh Lanta) have been and distribution of M. alfredi is scarce. population growth rates, mean lifetime increasing over the past few years, from In the proposal to include the reef reproductive success, and cohort 108 in 2015 to 288 in 2016. These manta ray on the appendices of the generation time compared to similar numbers reportedly surpass the estimate Convention on the Conservation of increases in juvenile annual survival of identified giant mantas in Migratory Species of Wild rates (Smallegange et al. 2016). Based on Mozambique (n = 254), possibly (CMS), it states that current global the elasticity analysis, population indicating that Thailand may be home population numbers are unknown and growth rate was most sensitive to to the largest aggregation of giant manta no historical baseline data exist (CMS changes in the survival rate of adults rays within the Indian Ocean 2014). Local populations of M. alfredi (Smallegange et al. 2016). In other (MantaMatcher 2016). In the Atlantic, have not been well assessed either, but words, in order to prevent populations very little information on M. birostris appear generally to be small, sparsely from declining further, Smallegange et populations is available, but there is a distributed, and isolated. Photo- al. (2016) found that adult survival rates known, protected population within the identification studies in Hawaii, Yap, should be increased, such as through Flower Garden Banks National Marine Japan, Indonesia, and the eastern coast protection of adult aggregation sites or Sanctuary in the Gulf of Mexico. of Australia suggest these a reduction in fishing of adult manta However, researchers are still trying to subpopulations range from 100 to 350 rays (Smallegange et al. 2016). For those determine whether the manta rays in individuals (see Table 6 in Miller and Klimovich (2016)), despite observational populations that are currently stable, this area are only M. birostris like the Yaeyama Islands (Japan) periods that span multiple decades. individuals or potentially also comprise population (where adult annual survival However, in the Maldives, population individuals of a new, undescribed rate is estimated at 0.95; noted above), estimates range from 3,300 to 9,677 species (Marshall et al. 2009; Hinojosa- Smallegange et al. (2016) note that any individuals throughout the 26 atolls in Alvarez et al. 2016). changes in adult survival may the archipelago (Kitchen-Wheeler et al. significantly affect the population. In areas where the species is not 2012; CITES 2013; CMS 2014), making Overall, given their life history traits subject to fishing, populations may be it the largest identified population of M. and productivity estimates, particularly stable. For example, Rohner et al. (2013) alfredi in the world. Other larger their low reproductive output and report that giant manta ray sightings populations may exist off southern sensitivity to changes in adult survival remained constant off the coast of Mozambique (superpopulation estimate rates, giant and reef manta ray Mozambique over a period of 8 years. of 802–890 individuals; Rohner et al. populations are inherently vulnerable to However, in regions where giant manta (2013); CITES (2013)) and Western depletions, with low likelihood of rays are (or were) actively targeted or Australia (metapopulation estimate = recovery. caught as bycatch, such as the 1,200–1,500; McGregor (2009) cited in Philippines, Mexico, Sri Lanka, and CITES (2013)). Historical and Current Distribution and Indonesia, populations appear to be In terms of trends, studies report that Population Abundance decreasing (see Table 5 in Miller and the rate of population reduction appears There are no current or historical Klimovich (2016)). In Indonesia, to be high in local areas, from 50–88 estimates of the global abundance of M. declines in manta ray landings are percent, with areas of potential local birostris. Despite their larger range, they estimated to be on the order of 71 to 95 extirpations of M. alfredi populations are encountered with less frequency percent, with potential extirpations (Homma et al. 1999; Rohner et al. 2013; than M. alfredi. Most estimates of noted in certain areas (Lewis et al. Lewis et al. 2015). In the portions of subpopulations are based on anecdotal 2015). Given the migratory nature of the range where reef manta rays are diver or fisherman observations, which species, population declines in waters experiencing anthropogenic pressures, are subject to bias. These populations where mantas are protected have also including Indonesia and Mozambique, seem to potentially range from around been observed but attributed to encounter rates have dropped 100 to1,500 individuals (see Table 4 in overfishing of the species in adjacent significantly over the last 5 to 10 years Miller and Klimovich (2016)). In the areas within its large home range. For (CMS 2014). However, where M. alfredi proposal to include manta rays on the example, White et al. (2015) provide receives some kind of protection, such appendices of the Convention on evidence of a substantial decline in the as in Australia, Hawaii, Guam, Japan,

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the Maldives, Palau, and Yap, CITES inadequacy of existing regulatory Plastics within the marine (2013) reports that subpopulations are mechanisms; or other natural or man- environment may also be a threat to the likely to be stable. For example, in made factors affecting its continued manta ray species, as the animals may Hawaii, based on photo-identification existence. We evaluated whether and ingest microplastics (through filter- survey data collected between 1992 and the extent to which each of the feeding) or become entangled in plastic 2007 along the Kona Coast, Clark (2010) foregoing factors contribute to the debris, potentially contributing to used a discovery curve to estimate that overall extinction risk of both manta ray increased mortality rates. Jambeck et al. an average of 4.27 new pups were species, with a ‘‘significant’’ (2015) found that the Western and Indo- entering the population per year. Off the contribution defined, for purposes of Pacific regions are responsible for the Yaeyama Islands, Japan, Kashiwagi this evaluation, as increasing the risk to majority of plastic waste. These areas (2014) conducted quantitative analyses such a degree that the factor affects the also happen to overlap with some of the using encounter records, biological species’ demographics (i.e., abundance, largest known aggregations for manta observations, and photo-ID of manta productivity, spatial structure, diversity) rays. For example, in Thailand, where rays over the period of 1987 to 2009 and either to the point where the species is recent sightings data have identified found that the apparent population size strongly influenced by stochastic or over 288 giant manta rays increased steadily but slowly over the depensatory processes or is on a (MantaMatcher 2016), mismanaged 23-year period, with a population trajectory toward this point. This plastic waste is estimated to be on the growth rate estimate of 1.02–1.03. Based section briefly summarizes our findings order of 1.03 million tonnes annually, on aerial surveys of Guam conducted and conclusions regarding threats to the with up to 40 percent of this entering from 1963 to 2012, manta ray giant and reef manta rays and their the marine environment (Jambeck et al. observations were infrequent but impact on the overall extinction risk of 2015). Approximately 1.6 million showed an increase over the study the species. More details can be found tonnes of mismanaged plastic waste is period (Martin et al. 2015). Off Lady in the status review report (Miller and being disposed of in Sri Lanka, again Elliott Island, Australia, Couturier et al. Klimovich 2016). with up to 40 percent entering the (2014) modeled annual population sizes marine environment (Jambeck et al. The Present or Threatened Destruction, of M. alfredi from 2009 to 2012 and 2015), potentially polluting the habitat Modification, or Curtailment of Its found an annual increase in abundance used by the nearby Maldives aggregation Habitat or Range for both sexes, but cautioned that the of manta rays. While the ingestion of modeled increase could be an artifact of Due to their association with plastics is likely to negatively impact improvements in photo-identification nearshore habitats, manta rays are at the health of the species, the levels of by observers over the study period. elevated risk for exposure to a variety of microplastics in manta ray feeding Within Ningaloo Marine Park, the status contaminants and pollutants, including grounds and frequency of ingestion are of reef manta rays was assessed as brevotoxins, heavy metals, presently being studied to evaluate the ‘‘Good’’ in 2013, but with low polychlorinated biphenyls, and plastics. impact on these species (Germanov confidence in the ratings (Marine Parks Many pollutants in the environment 2015b; Germanov 2015a). & Reserves Authority 2013). Overall, Because manta rays are migratory and however, the reef manta ray population have the ability to bioaccumulate in fish of Australia is deemed to be one of the species; however, only a few studies considered ecologically flexible (e.g., world’s healthiest (Australian have specifically examined the low habitat specificity), they may be less Government 2012). accumulation of heavy metals in the vulnerable to the impacts of climate tissues of manta rays (Essumang 2010; change compared to other sharks and Species Finding Ooi et al. 2015), with findings that rays (Chin et al. 2010). However, as Based on the best available scientific discuss human health risks from the manta rays frequently rely on coral reef and commercial information described consumption of manta rays. For habitat for important life history above, we find that M. birostris and M. example, Essumang (2010) found functions (e.g., feeding, cleaning) and alfredi are currently considered platinum levels within M. birostris depend on planktonic food resources for taxonomically-distinct species and, samples taken off the coast of Ghana nourishment, both of which are highly therefore, meet the definition of that exceeded the United Kingdom (UK) sensitive to environmental changes ‘‘species’’ pursuant to section 3 of the dietary intake recommendation levels, (Brainard et al. 2011; Guinder and ESA. Below, we evaluate whether these and Ooi et al. (2015) reported Molinero 2013), climate change is likely species warrant listing as endangered or concentrations of lead in M. alfredi to have an impact on the distribution threatened under the ESA throughout tissues from Lady Elliot Island, and behavior of both M. birostris and M. all or a significant portion of their Australia, that exceeded maximum alfredi. Currently, coral reef degradation respective range. allowable level recommendations for from anthropogenic causes, particularly fish consumption per the European climate change, is projected to increase Summary of Factors Affecting Giant Commission and the Codex through the future. Specifically, annual, and Reef Manta Rays Alimentarius Commission (WHO/FAO). globally averaged surface ocean As described above, section 4(a)(1) of While consuming manta rays may temperatures are projected to increase the ESA and NMFS’ implementing potentially pose a health risk to by approximately 0.7 °C by 2030 and 1.4 regulations (50 CFR 424.11(c)) state that humans, there is no information on the °C by 2060 compared to the 1986–2005 we must determine whether a species is lethal concentration limits of these average (IPCC 2013), with the latest endangered or threatened because of metals or other toxins in manta rays. climate models predicting annual coral any one or a combination of the Additionally, at this time, there is no bleaching for almost all reefs by 2050 following factors: The present or evidence to suggest that current (Heron et al. 2016). As declines in coral threatened destruction, modification, or concentrations of these environmental cover have been shown to result in curtailment of its habitat or range; pollutants are causing detrimental changes in coral reef fish communities overutilization for commercial, physiological effects to the point where (Jones et al. 2004; Graham et al. 2008), recreational, scientific, or educational either species may be at an increased the projected increase in coral habitat purposes; disease or predation; risk of extinction. degradation may potentially lead to a

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decrease in the abundance of manta ray circulation, remedying throat and skin 1970s prompted the commercial trade of cleaning fish (e.g., Labroides spp., ailments, curing male kidney issues, manta ray products, with gill plates Thalassoma spp., and Chaetodon spp.) and helping with fertility problems generally sent to Bali, Surabaya (East and an overall reduction in the number (Heinrichs et al. 2011). The use of gill Java), Ujung Pandant (Sulawasi), or of cleaning stations available to manta rakers as a remedy, which was Jakarta (West Java) for export to Hong rays within these habitats. This widespread in Southern China many Kong, Taiwan, Singapore and other potential decreased access to cleaning years ago, has recently gained renewed places in Asia (Dewar 2002; White et al. stations may negatively impact the popularity over the past decade as 2006; Marshall and Conradie 2014). fitness of the mantas by hindering their traders have increased efforts to market This economic incentive, coupled with ability to reduce parasitic loads and its healing and immune boosting emerging technological advances (e.g., dead tissue, which could lead to properties directly to consumers motorized vessels) and an increase in increases in diseases and declines in (Heinrichs et al. 2011). As a result, the number of boats in the fishery, reproductive fitness and survival rates. demand has significantly increased, greatly increased fishing pressure and However, these scenarios are currently incentivizing fishermen who once harvest of manta rays in the 1990s and speculative, as there is insufficient avoided capture of manta rays to 2000s (Dewar 2002). In Lamakera, information to indicate how and to what directly target these species (Heinrichs Indonesia, one of the main landing sites extent changes in reef community et al. 2011; CITES 2013). According to for mobulids, and particularly manta structure will affect the status of both Heinrichs et al. (2011), it is primarily rays, Dewar (2002) estimates that the manta ray species. the older population in Southern China total average harvest of ‘‘mantas’’ during Changes in climate and oceanographic as well as Macau, Singapore, and Hong the 2002 fishing season was 1,500 conditions, such as acidification, are Kong, that ascribes to the belief of the individuals (range 1,050–2,400), which also known to affect zooplankton healing properties of the gill rakers; is a significant increase from the structure (size, composition, diversity), however, unlike products like shark estimated historical harvest levels of phenology, and distribution (Guinder fins, the gill rakers are not considered around 200–300 mantas per season. and Molinero 2013). As such, the ‘‘traditional’’ or ‘‘prestigious’’ items and However, Lewis et al. (2015) note that migration paths and locations of both many consumers and sellers are not this estimate likely represents all resident and seasonal aggregations of even aware that gill rakers come from mobulid rays, not just manta rays. manta rays, which depend on these manta or mobula rays. Meat, cartilage, However, given these amounts, it is animals for food, may similarly be and skin of manta rays are also utilized, perhaps unsurprising that anecdotal altered (Australian Government 2012; but valued significantly less than the reports from fishermen indicate possible Couturier et al. 2012). It is likely that gill rakers, and usually enter local trade local population declines, with those M. alfredi populations that exhibit or are kept for domestic consumption fishermen noting that they have to travel site-fidelity behavior will be most (Heinrichs et al. 2011; CITES 2013). farther to fishing grounds as manta rays affected by these changes. For example, Indonesia, Sri Lanka, and India are no longer present closer to the resident manta ray populations may be presently represent the largest manta ray village (Dewar 2002; Lewis et al. 2015). forced to travel farther to find available exporting range state countries; In fact, using the records from Dewar food or randomly search for new however, Chinese gill plate vendors (2002) and community (local) catch productive areas (Australian have also reported receiving mobulid records, Lewis et al. (2015) show that Government 2012; Couturier et al. gill plates from other countries and there has been a steady decline in manta 2012). As research to understand the regions as well, including Malaysia, landings at Lamakera since 2002 exact impacts of climate change on Vietnam, South Africa, South America, (despite relatively unchanged fishing marine phytoplankton and zooplankton the Middle East, and the South China effort), with estimated landings in 2013– communities is still ongoing, the Sea (CMS 2014). To examine the impact 2014 comprising only 25 percent of the severity of this threat to both species of of this growing demand for gill rakers estimated numbers from 2002–2006. manta rays has yet to be fully on manta ray populations, information These declines in manta landings are determined. on landings and trends (identified by not just limited to Lamakera, but also appear to be the trend throughout Overutilization for Commercial, species where available) are evaluated Indonesia at the common mobulid Recreational, Scientific or Educational for both fisheries that target mantas and landing sites. For example, Lewis et al. Purposes those that catch mantas as bycatch. (2015) reports a 95 percent decline in Manta rays are both targeted and Targeted Fisheries manta landings in Tanjung Luar caught as bycatch in fisheries Indonesia is reported to be one of the (between 2001–2005 and 2013–2014), a worldwide. In fact, according to Lawson countries that catch the most mobulid decrease in the average size of mantas et al. (2016), manta ray catches have rays (Heinrichs et al. 2011). Manta and being caught, and a 71 percent decline been recorded in at least 30 large and mobula ray fisheries span the majority in manta landings in the Cilacap gillnet small-scale fisheries covering 25 of the Indonesian archipelago, with fishery between 2001–2005 and 2014. countries. The majority of fisheries that most landing sites along the Indian Areas in Indonesia where manta rays target mobulids are artisanal (Croll et al. Ocean coast of East and West Nusa have potentially been fished to 2015) and target the rays for their meat; Tenggara and Java (Lewis et al. 2015). extirpation, based on anecdotal reports however, since the 1990s, a market for Manta rays (presumably M. birostris, but (e.g., diver sightings data and fishermen mobulid gill rakers has significantly identified prior to the split of the genus) interviews), include Lembeh Strait in expanded, increasing the demand for have traditionally been harvested in northeast Sulawesi, Selayer Islands in manta ray products, particularly in Indonesia using harpoons and boats South Sulawesi, and off the west coast China. The gill rakers of mobulids are powered by paddles or sails, with manta of Alor Island (which may have been a used in Asian medicine and are thought fishing season lasting from May through local M. alfredi population) (Lewis et al. to have healing properties, such as October. Historically, the harvested 2015). curing diseases from chicken pox to manta rays would be utilized by the Although fishing for manta rays was cancer, boosting the immune system, village, but the advent of the banned within the Indonesian exclusive purifing the body, enhancing blood international gill raker market in the economic zone (EEZ) in February 2014

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(see The Inadequacy of Existing (2) 1970s to 2013 (present), when boats and Tull 2016). Acebes and Tull (2016) Regulatory Mechanisms), in May 2014, became bigger and motorized and the monitored the numbers of manta rays manta rays were still being caught and fishing technique switched to drift landed at Bunga Mar over a period of processed at Lamakera, with M. birostris gillnets, with the manta hunting season 143 days from April 2010 to December the most commonly targeted species extending from November to June. In 2011 (during which there were around (Marshall and Conradie 2014). Around the earlier period, the manta fishing 16–17 active fishing boats targeting 200 fishing vessels targeting mantas rays grounds were fairly close to the shore mobulids), and in total, 40 M. birostris are in operation (Marshall and Conradie (<5 km), noted along the coasts of were caught. In 2013, records from a 2014). Most of the fishing occurs in the southern Bohol, northwestern and single village (location not identified) Solor Sea and occasionally in the southern coasts of Camiguin and eastern showed over 2,000 mobuilds landed Lamakera Strait, with landings generally coasts of Limasawa. Boats would from January to May, of which 2 percent comprising around one to two dozen usually catch around one manta per (n = 51 individuals) were M. birostris manta rays per day. Taking into account day, with catches of 5–10 mantas for a (Verdote and Ponzo 2014). As there is the manta ray fishing season in fishing village considered a ‘‘good day’’ little evidence of enforcement of current Lamakera (June to October), Marshall (Acebes and Tull 2016). As the fishery prohibitions on manta ray hunting, and and Conradie (2014) estimate that became more mechanized in the 1970s, no efforts to regulate the mobulid between 625 and 3,125 manta rays transitioning to larger and motorized fisheries, with mobulid fishing (likely majority M. birostris) may be boats, and as the primary gear changed providing the greatest profit to landed each season. Lewis et al. (2015), from harpoons to non-selective fishermen, it is unlikely that fishing for however, report a much smaller driftnets, fishermen were able to access mantas, of which the majority appears number, with 149 estimated as landed previously unexplored offshore fishing to be M. birostris, will decrease in the in 2014. grounds, stay out for longer periods of future. It is unlikely that fishing effort and time, and catch more manta rays Manta rays are also reportedly associated utilization of the species will (Acebes and Tull 2016). Additionally, it targeted in fisheries in India, Ghana, significantly decrease in the foreseeable was during this time that the Peru, Thailand, Mozambique, Tonga, future because interviews with international gill raker market opened , possibly the Republic of fishermen indicate that many are up, increasing the value of gill rakers, Maldives, and previously in Mexico. In excited for the new prohibition on particularly for manta species. By 1997, India, Ghana, Peru, and Thailand, little manta rays in Indonesian waters, as it is there were 22 active mobulid ray fishing information is available on the actual expected to drive up the price of manta sites in the Bohol Sea (Acebes and Tull level of take of manta rays. In India, ray products and significantly increase 2016). In Pamilacan, 18 boats were manta rays are mainly landed as bycatch the current income of resident fishing for mobulids in 1993, increasing in tuna gillnetting and trawl fisheries; fishermen (Marshall and Conradie to 40 by 1997, and in Jagna, at least 20 however, a harpoon fishery at Kalpeni, 2014). Based on unpublished data, boats were engaged in mobulid hunting off Lakshadweep Islands, is noted for O’Malley et al. (2013) estimate that the in the 1990s (Acebes and Tull 2016). ‘‘abundantly’’ landing mantas (likely M. total annual income from the manta ray Catches from this time period, based on alfredi; A.M. Kitchen-Wheeler pers. fisheries in Indonesia is around the recollection of fishermen from comm. 2016) during peak season (from $442,000 (with 94 percent attributed to Pamilacan and Baclayon, Bohol, were June–August) (Raje et al. 2007). In Ghana, there is no available data on the the gill plate trade). Dharmadi et al. around 8 manta rays (for a single boat) (2015) noted that there are still many amount of manta rays landed in in 1995 and 50 manta rays (single boat) fishermen, particularly in Raja Ampat, Ghanaian fisheries; however, Debrah et in 1996 (Alava et al. 2002). However, it Bali, and Komodo, whose livelihoods al. (2010) observed that giant manta rays should be noted that the mobulid depend on shark and ray fishing. were targeted using wide-mesh drift fishery ended in Lila and Limasawa Without an alternative for income, it is gillnets in artisanal fisheries between Island in the late 1980s and in Sagay in unlikely that these fishing villages will 1995 and 2010, and D. Berces (pers. 1997, around the time that the whale stop their traditional fishing practices. comm. 2016) confirmed that manta rays fishery closed and a local ban in manta Additionally, enforcement of existing are taken during artisanal fishing for ray fishing was imposed (Acebes and laws appears to be lacking in this region pelagic sharks, and not ‘‘infrequently,’’ Tull 2016). (Marshall and Conradie 2014). The high with manta rays consumed locally. In market prices for manta products, where Despite increases in fishing effort, Peru, Heinrichs et al. (2011), citing to a a whole manta (∼5 m DW) will sell for catches of manta rays began to decline rapid assessment of the mobulid anywhere from $225–$450 (Lewis et al. in Philippine waters, likely due to a fisheries in the Tumbes and Piura 2015), drives the incentive to continue decrease in the abundance of the regions, reported estimated annual fishing the species, and evidence of population, prompting fishermen to landings of M. birostris on the order of continued targeted fishing despite shift their fishing grounds farther east 100–220 manta rays for one family of prohibitions suggests that and north. Although a ban on hunting fishermen. As such, total landings for overutilization of the Indonesian manta and selling giant manta rays was Peru are likely to be much larger. ray populations (primarily M. birostris, implemented in the Philippines in 1998 According to Heinrichs et al. (2011), based on the data) is likely to continue (see The Inadequacy of Existing dive operators in the Similan Islands, to occur into the foreseeable future. Regulatory Mechanisms), this has not Thailand, have also observed an In the Philippines, fishing for manta seemed to impact the mobulid fishery in increase in fishing for manta rays, rays mainly occurs in the Bohol Sea. any way. In Pamilacan, there were 14 including in protected Thai national According to Acebes and Tull (2016), mobulid hunting boats reported to be in marine parks, and while information on the manta ray fishery can be divided operation in 2011 (Acebes and Tull catches is unavailable, sightings of into two distinct periods based on 2016). In the village of Bunga Mar, Manta spp. (likely M. birostris) technology and fishing effort: (1) 1800s Bohol, there were 15 boats targeting decreased by 76 percent between 2006 to 1960s, when mantas were mainly mobulids in 2012, and out of 324 and 2012 (CITES 2013b). hunted in small, non-motorized boats registered fishermen, over a third were In southern Mozambique, reef manta using harpoons from March to May; and actively engaged in ray fishing (Acebes rays are targeted by fishermen, with

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estimates of around 20–50 individuals proportion of ray bycatch in the purse fishermen note that they generally tend taken annually from only a 50 km seine fisheries operating in the Indian to avoid deploying nets near large section of studied coastline (Rohner et Ocean (specifically M. birostris; ∼40 aggregations of manta rays or regularly al. 2013). As annual estimates of this M. percent) and especially the Eastern release them when caught, as recently as alfredi population range only from 149 Pacific Ocean (identified as Manta spp.; 2011, giant manta rays were observed to 454 individuals (between 2003 and ∼100 percent, but would be M. birostris being sold at Sri Lanka fish markets 2007), this take is equivalent to as well), but were not large components (Fernando and Stevens 2011). removing anywhere from 4 percent to 34 of the ray bycatch in the longline, trawl, Additionally, although Sri Lankan percent of the population per year. This or gillnet fisheries in any of the ocean fishermen state that they try to release removal rate is potentially basins. pregnant and young manta rays alive, unsustainable for a species with such a In the Atlantic Ocean, bycatch of giant based on 40 observed M. birostris being low productivity, and has likely manta rays has been observed in purse sold at markets (from May through contributed to the estimated 88 percent seine, trawl, and longline fisheries; August 2011), 95 percent were juveniles decline that has already been observed however, M. birostris does not appear to or immature adults (Fernando and in the local reef manta ray population be a significant component of the Stevens 2011). Extrapolating the (Rohner et al. 2013). Manta birostris, on bycatch. For example, in the European observed market numbers to a yearly the other hand, has not exhibited a purse seine fishery, which primarily value, Fernando and Stevens (2011) decline off Mozambique, represents operates in the Eastern Atlantic off estimated total annual landings for M. only 21 percent of the identified manta western Africa, observer data collected birostris in Sri Lanka to be around 1,055 rays in this area, and is rarely observed over the period of 2003–2007 (27 trips, individuals, which they concluded in the local fishery (one observed caught 598 sets; observer coverage averaged would likely result in a population over an 8-year period), indicating that 2.93 percent) showed only 11 M. crash (Fernando and Stevens 2011). fishing pressure is likely low for this birostris caught, with an equivalent Additionally, more recent data from the species (Rohner et al. 2013; Marine weight of 2.2 mt (Amande` et al. 2010). Indian Ocean Tuna Commission (IOTC) Megafauna Foundation 2016). In the U.S. bottom longline and gillnet database (http://www.iotc.org/iotc- Opportunistic hunting of manta rays fisheries operating in the western online-data-querying-service) covering (likely M. alfredi) has been reported in Atlantic, M. birostris is also a very rare the time period of 2012–2014 indicate Tonga and Micronesia (B. Newton and occurrence in the elasmobranch catch, that over 2,400 mt of M. birostris were J. Hartup pers. comms. cited in CMS with the vast majority that are caught recorded caught by the Sri Lankan 2014), and in the Maldives, Anderson released alive (see NMFS Reports gillnet and longline fleets primarily and Hafiz (2002) note that very small available at http://www.sefsc.noaa.gov/ engaged in artisanal fishing. This catches of manta rays occur in the labs/panama/ob/bottomline amount is almost double the 1,413 mt traditional fisheries, with meat used for observer.htm and http:// total catch that was reported in Clarke bait for shark fishing and skin used for www.sefsc.noaa.gov/labs/panama/ob/ and IOTC Secretariat (2014) by both Sri musical drums. Given the available gillnet.htm). Overall, given the present Lanka and Sudan fleets from a time information, it is unlikely that fishing low fishing pressure on giant manta period that was more than twice as long pressure on either manta ray species is rays, and evidence of minimal bycatch (2008–2013). Using the maximum significant in these areas. of the species (see Miller and Klimovich observed weight of M. birostris in the In Mexico, giant manta rays and (2016) for additional discussion), it is Indian Ocean (2,000 kg; which was mobula rays were historically targeted unlikely that overutilization as a result described as ‘‘unusually large’’ for their meat in the Gulf of California. of bycatch mortality is a significant (Kunjipalu and Boopendranath 1982)), In 1981, Notarbartolo di Sciara (1988) threat to M. birostris in the Atlantic this translates to a minimum of around observed a seasonally-active mobulid Ocean. However, information is severely 400 giant manta rays caught annually in fishery located near La Paz, Baja lacking on both population sizes and recent years by Sri Lankan fishing fleets. California Sur. Mobulids were fished in distribution of the giant manta ray as Given that fishermen have already noted the Gulf of California using both gillnets well as current catch and fishing effort a decrease in catches of manta rays over and harpoons, with their meat either on the species throughout this portion the past 5 years, it is likely that the fileted for human consumption or used of its range. as shark bait. The giant manta ray was In the Indian Ocean, manta rays continued and heavy fishing pressure characterized as ‘‘occasionally (primarily M. birostris) are mainly on M. birostris, and associated bycatch captured’’ by the fishery, and while it is caught as bycatch in purse seine and mortality, is significantly contributing to unclear how abundant M. birostris was gillnet fisheries. In the western Indian the overutilization of the species in this in this area, by the early 1990s, Homma Ocean, data from the pelagic tuna purse portion of its range. et al. (1999) reported that the entire seine fishery suggests that manta and Manta ray landings have also become mobulid fishery had collapsed. mobula rays, together, are an a more common occurrence in the insignificant portion of the bycatch, bycatch of fishermen operating off India. Bycatch comprising less than one percent of the Here, mobulids, including mantas, are Given the global distribution of manta total non-tuna bycatch per year landed as bycatch during tuna rays, they are frequently caught as (Romanov 2002; Amande` et al. 2008). gillnetting and trawling operations and bycatch in a number of commercial and However, in the eastern Indian Ocean, are auctioned off for their gill plates, artisanal fisheries worldwide. In a study manta rays appear at higher risk of while the meat enters the local markets. of elasmobranch bycatch patterns in capture from the fisheries operating Historical reports (from 1961–1995) commercial longline, trawl, purse seine throughout this area, with two of the top indicate that manta rays were only and gillnet fisheries, Oliver et al. (2015) three largest Manta spp. fishing and sporadically caught by fishermen along presented information on species- exporting range states (Sri Lanka and the east and west coasts of India, likely specific composition of ray bycatch in India) located in this region (Heinrichs due to the fact that the species was 55 fisheries worldwide. Based on the et al. 2011). In Sri Lanka, manta rays are rarely found near the shore (Pillai 1998). available data, Oliver et al. (2015) found primarily caught as bycatch in the However, based on available that manta rays comprised the greatest artisanal gillnet fisheries. While information, it appears that landings

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have increased in recent years, caught per year from 1993–2015 in the rays. Manta rays are frequently observed particularly on the southwest coast. For eastern Pacific purse seine fishery by congregating in inshore cleaning the years 2003 and 2004, Raje et al. IATTC vessels (Hall unpublished data). stations, often associated with coral (2007) reported 647 mt of M. birostris While the impact of these bycatch levels reefs, where small remove from the southwest coast of India by the on giant manta ray populations is parasites and dead tissue from their trawl fisheries. In a snapshot of the uncertain, effort in the fishery appears bodies (Marshall and Bennett 2010a; Indian tuna gillnet fishery, Nair et al. to coincide with high productivity O’Shea et al. 2010; CITES 2013). They (2013) documented 5 individuals of M. areas, such as the Costa Rica Thermal may remain at these cleaning stations birostris that were landed by fishermen Dome, west of the Galapagos, off the for large periods of time, sometimes up off the coast of Vizhinjam, Kovalam and Guayas River estuary (Ecuador), and off to 8 hours a day, and may visit daily Colachel over the course of only 7 days. central and northern Peru, where giant (Duinkerken 2010; Kitchen-Wheeler On the east coast of India, Raje et al. mantas are likely to aggregate and have 2013; Rohner et al. 2013). While there (2007) documented 43 mt of M. birostris been observed caught in sets (Hall and is no information on manta ray diseases, landed in 2003 and 2004 at the Chennai Roman 2013). If effort is concentrated in or data to indicate that disease is fishing harbor. The apparent increase in manta ray aggregation areas, this could contributing to population declines in landings since the sporadic reports of lead to substantial declines and either species, impacts to these cleaning the species in the mid-1990s is likely potential local extirpations of giant stations (such as potential loss through due to the demand for the species’ gill manta ray populations. Already, habitat degradation) may negatively rakers, with M. birostris gill plates evidence of declines in this portion of impact the fitness of the mantas by characterized as ‘‘First Grade’’ and the giant manta ray’s range is apparent, decreasing their ability to reduce their fetching the highest price at auction at with White et al. (2015) estimating an 89 parasite load. However, at this time, the the major fishing port of Cochin percent decline in the relative impact and potential loss of cleaning Fisheries Harbour (Nair et al. 2013). abundance of M. birostris off Cocos stations is highly speculative. While Manta spp. are rarely reported Island, Costa Rica. Presently, the largest In terms of predation, manta rays are in the catch from the western Pacific, population of M. birostris is thought to frequently sighted with non-fatal with Hall and Roman (2013) noting that reside within the waters of the injuries consistent with shark attacks, M. japonica represents the most Machalilla National Park and the although the prevalence of these abundant mobulid in the fisheries data, Galapagos Marine Reserve (Hearn et al. sightings varies by location (Homma et the available information still suggests 2014); however, given the distribution al. 1999; Ebert 2003; Mourier 2012). For the potential for bycatch mortality and of purse seine fishing effort, and the example, Deakos et al. (2011) reported indicates declining trends within this migratory nature of the species, it is that scars from shark predation, mostly region. For example, based on observer likely that individuals from this on the posterior part of the body or the data from the Western and Central population are highly susceptible to the wing tip, were evident in 24 percent of Pacific Fisheries Commission (WCPFC) purse seine fisheries operating in the M. alfredi individuals observed at a fisheries, M. birostris is observed at a area. manta ray aggregation site off Maui, rate of 0.0017 individuals per associated Overall, given that the majority of Hawaii. At Lady Elliott Island, off set and 0.0076 individuals per observed declines in landings and eastern Australia, Couturier et al. (2014) unassociated set in the purse seine sightings of manta rays originate from observed 23 percent of individuals had fisheries, and at a rate of 0.001–0.003 the Indo-Pacific and eastern Pacific shark scars. In contrast, in southern individuals per 1,000 hooks in the portions of their range (see Table 5 in Mozambique, between 2003 and 2006, longline fisheries (Tremblay-Boyer and Miller and Klimovich 2016), additional 76.3 percent of the M. alfredi identified Brouwer 2016). The longline pressure on these species through by Marshall and Bennett (2010a) standardized catch-per-unit-effort data, bycatch mortality may have significant exhibited shark-inflicted bite marks, the while covering observations from only negative effects on local populations majority of which were already healed. the past decade, indicates that M. throughout this area. This is particularly Rohner et al. (2013) found a lower rate birostris is observed less frequently in a risk for M. birostris, which appears to for M. birostris, with only 35 percent of recent years compared to 2000–2005 be the species most frequently observed individuals observed with bite marks. (Tremblay-Boyer and Brouwer 2016). in the fisheries catch and bycatch, with Marshall and Bennett (2010a) also Additionally, a sharp decline in the this pressure already contributing to recorded two mid-pregnancy abortions catches of manta rays off Papua New declines in the species (of up to 95 by pregnant female M. alfredi attributed Guinea, where WCPFC fishing effort is percent) throughout many areas (i.e., to damage from shark attacks. The high, was observed in Papua New Indonesia, Philippines, Sri Lanka, authors observed that the rate of shark- Guinea purse seiner bycatch in 2005– Thailand, Madagascar, Costa Rica). As inflicted bites in southern Mozambique 2006, after a previously steady rise in such, we find that current fisheries- appears to be higher than predation manta ray catches from 1994–2005 (C. related mortality rates are a threat rates in other manta ray populations, Rose pers. comm. cited in Marshall et al. significantly contributing to the which is generally noted at less than 2011b). overutilization of M. birostris five percent (Ito 2000; Kitchen-Wheeler In the eastern Pacific, giant manta throughout this portion of its range. et al. 2012), but it is unknown why this rays are frequently reported as bycatch Additionally, given the high market difference exists. in the purse seine fisheries; however, prices for manta ray gill plates, we find Because the damage from a shark bite identification to species level is that the practice of landing these species usually occurs in the posterior region of difficult, and, as such, most manta and as valuable bycatch will likely continue the manta ray, there may be mobula ray captures are pooled together through the foreseeable future. disfigurement leading to difficult (Hall and Roman 2013). Based on clasper insertion during mating or reported M. birostris catch to the Inter- Disease or Predation inhibited waste excretion (Clark and American Tropical Tuna Commission No information has been found to Papastamatiou 2008). Given the already (IATTC), including available national indicate that disease or predation is a low reproductive ability of these observer program data, an average of factor that is significantly and species, attacks by sharks (or 135 giant manta rays were estimated negatively affecting the status of manta occasionally killer whales, see Fertl et

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al. (1996) and Visser and Bonoccorso alternative source of income, are and within specific marine parks of (2003)) may pose a threat to the species unlikely to stop their traditional fishing Western Australia. Given the declines by further impairing the manta rays’ practices, including the targeting of observed in the species throughout the ability to rebuild after depletion. manta rays. Additionally, in interviews Indian Ocean, and the migratory nature However, at this time, the impact of with fishermen, many viewed the of the , with the potential for the shark bites on manta ray reproduction, prohibition positively because it would species to move out of protected areas or predation mortality rates on the likely drive up the market price of into active fishing zones (e.g., from the status of either species, is highly manta ray products (Marshall and Maldives to Sri Lanka—a distance of speculative. Conradie 2014). Given the size of the ∼820 km, well within the ability of M. Indonesian archipelago, and current birostris), it is likely that existing The Inadequacy of Existing Regulatory resources, Dharmadi et al. (2015) note regulatory measures within this portion Mechanisms there are many issues with current of the species’ range are inadequate to Protections for manta rays are enforcement of regulations. For protect it from overutilization. increasing, yet there are still a number example, the collection of data is In the eastern Pacific portion of the of areas where manta rays are targeted difficult due to insufficient fisheries species’ range, the IATTC recently or allowed to be landed as bycatch. In officers trained in species identification implemented a prohibition on the fact, only one of the Regional Fishery and the large number of landing sites retention, transshipment, storage, Management Organizations (RFMOs) that need to be monitored (over 1,000). landing, and sale of all devil and manta has prohibited retention of bycaught Catch data are typically not accurately (mobula and manta) rays taken in its manta rays. Additionally, because both recorded at the smaller landing sites large-scale fisheries (Resolution C–15– manta species were identified as M. either, with coastal waters heavily 04). This regulation went into force on birostris prior to 2009, some national fished by artisanal fishermen using non- August 1, 2016. Cooperating members protections that were implemented selective gear (Dharmadi et al. 2015). must report mobulid catch data and before 2009 are specific only to giant Given the issues with enforcement and ensure safe release; however, manta rays, despite both species being evidence of illegal fishing, existing developing countries were granted an present in that nation’s waters. Below regulatory mechanisms are inadequate exception for small-scale and artisanal we provide an analysis of the adequacy to protect the species from further fisheries that catch these species for of measures in terms of controlling declines due to overutilization. domestic consumption. Given that M. threats to each species where available In the Philippines, legal protection for birostris is primarily caught as bycatch data permit. A list of current protections manta rays was introduced in 1998; in the IATTC purse seine fisheries, the for manta rays can be found in the however, similar to the situation in adequacy of this prohibition in Appendix of Miller and Klimovich Indonesia, enforcement of the protecting the species from (2016). prohibitions is lacking and illegal overutilization depends on the post- Overutilization of M. birostris fishing of the species is evident. For release survival rate of the species. example, in a random sampling of 11 While injuries from entanglements in Based on the available data, M. dried products of sharks and rays fishing gear (e.g., gillnets and longlines) birostris appears to be most at risk of confiscated for illegal trading, Asis et al. have been noted (Heinrichs et al. 2011), overutilization in the Indo-Pacific and (2016) found that four of the products at this time, at-vessel and post-release eastern Pacific portions of its range. could be genetically identified as mortality rates for manta rays in purse Targeted fishing and incidental capture belonging to M. birostris. Dried manta seine nets are unknown. For other of the species in Indonesia, Philippines, meat and gill rakers were frequently Mobula species, Francis and Jones Sri Lanka, and India, and throughout observed in markets between 2010 and (2016) provided preliminary evidence the eastern Pacific, has led to observed 2012, and fishing boats specifically that may indicate a potential for declines in the M. birostris populations. targeting mobulids (including manta significant post-release mortality of the Despite national protections for the rays) were identified in a number of spinetail devilray (Mobula japanica) in species, poor enforcement and illegal local fishing villages in the Philippines, purse seine fisheries; however, the fishing have essentially rendered the with landings consisting of M. birostris study was based on only seven observed existing regulatory mechanisms individuals. Fishing for mobulids is a individuals and, because of this, the inadequate to achieve their purpose of ‘‘way of life’’ and the primary source of authors caution that it is ‘‘premature to protecting the giant manta ray from income for many fishermen, and with draw conclusions about survival rates.’’ fishing mortality. the high prices for manta gill rakers in In fact, based on observer data in the In Indonesia, M. birostris and M. the Philippine markets (where an New Zealand purse seine fishery, alfredi were provided full protection in average manta ray of around 3 m DW mentioned in Francis and Jones (2016), the nation’s waters in 2014 (4/ could fetch up to $808; Acebes and Tull rays that were caught during sets and KEPMEN–KP/2014), with the creation of (2016)), it is unlikely that pressure on released were ‘‘usually lively’’ and the world’s largest manta ray sanctuary the species will decrease. With swam away from the vessel and judged at around 6 million km2. Fishing for the essentially no efforts to regulate the by the observers as ‘‘likely to survive.’’ species and trade in manta ray parts are mobulid fisheries in the Philippines, Although decreasing purse seine fishing banned. Despite this prohibition, fishing and a severe lack of enforcement of the effort in manta ray hotspots would for manta rays continues, with evidence current manta ray hunting prohibition, significantly decrease the likelihood of of the species being landed and traded current regulations to protect M. bycatch mortality, without further in Indonesian markets (AFP 2014; birostris from overutilization in the information on post-release survival Marshall and Conradie 2014; Dharmadi Philippines are inadequate. rates, it is highly uncertain if the et al. 2015). As mentioned previously In the eastern and central Indian prohibition will be adequate in (see Overutilization for commercial, Ocean, very few national protections decreasing the mortality of the species. recreational, scientific, or educational have been implemented for M. birostris. Additionally, in 2016, prohibitions on purposes), many fishermen throughout Essentially, fishing for the species and the fishing and sale of M. birostris and Indonesia rely on shark and ray fishing retention of bycatch is allowed except requirement for immediate release of for their livelihoods, and without an within the Republic of Maldives EEZ mantas caught as bycatch were

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implemented in Peru. Ecuador banned seamounts in the Leyte Gulf. In 2010, Tourism Impacts the fishing, landing and sale of manta there were 4 active fishing boats in this Codes of conduct have been rays in its waters back in 2010. Given fishery, supplying manta ray products to developed by a number of organizations that the largest population of M. Bohol during the ‘‘off season’’ (Acebes and used by dive operators to promote birostris is found in the waters between and Tull 2016). While it is uncertain the safe viewing of manta rays and Peru and Ecuador (with the Isla de la whether fishing pressure on M. alfredi reduce the potential negative impacts of Plata population estimated at around will increase in the future (given that these activities on manta rays (see Other 1,500 individuals), these prohibitions the majority of effort is presently Natural or Man-Made Factors Affecting should provide some protection to the concentrated outside of their Its Continued Existence for discussion species from fishing mortality when in distribution), current regulations in the of this threat). The Manta Trust, a UK- these waters. However, illegal fishing Philippines only prohibit fishing of M. registered charity, has developed a still occurs in these waters. For birostris, and, as such, are inadequate to number of guidelines for divers, example, in Ecuador’s Machalilla protect the species from potential snorkelers, tour group operators, and in- National Park (a major M. birostris declines in the future. water tourists, based on studies of aggregation site), researchers have In Indonesia, while the majority of interaction effects conducted by the observed large numbers of manta rays landings data is reported as M. birostris, organization from 2005–2013 (available with life-threatening injuries as a result anecdotal reports from fishermen note here: http://www.mantatrust.org/ of incidental capture in illegal wahoo that M. alfredi used to be caught as awareness/resources/). The Hawaii (Acanthocybium solandri) trawl and bycatch in drift gillnets. Evidence of Association for Marine Education and drift gillnet fisheries operating within declines and extirpations of local reef the park (Heinrichs et al. 2011; Marshall manta ray populations suggest that the Research Inc. (2014) notes that codes of et al. 2011a). Depending on the extent species is at risk of overutilization by conduct for manta ray dive operators of the activities, illegal fishing could fisheries in these local, inshore areas, have been implemented in a number of potentially contribute to local declines despite a lack of records. As such, the popular manta ray diving locales, in the population if not adequately inadequacy of existing mechanisms including Kona, Hawaii, Western controlled. Also, given the migratory (discussed previously) may pose a threat Australia, Mozambique, Bora Bora, and nature of the species, national to the remaining local reef manta ray in the Maldives; however, information protections may not be adequate to populations in Indonesia. on the adherence to, effectiveness, or protect the species from overutilization In the Indian Ocean, M. alfredi is adequacy of these codes of conduct in throughout its range, particularly when subject to targeted fishing in the western minimizing potential negative impacts the species crosses boundary lines Indian Ocean (off Mozambique) where of tourism activities on the populations where protections no longer exist, as declines of up to 88 percent have been could not be found. evidenced by the significant decline in observed but no fishery protections or Other Natural or Man-Made Factors M. birostris observed in Cocos Island regulatory measures are in place. While Affecting Its Continued Existence National Park, Costa Rica (White et al. the Commonwealth of Australia has 2015). now listed both species of Manta on its Manta rays are known to aggregate in list of migratory species under its various locations around the world, in Overutilization of M. alfredi Environment Protection and groups usually ranging from 100–1,000 Despite a significant overlap in range Biodiversity Conservation Act 1999, for M. birostris and 100–700 for M. with M. birostris in the Indian and which means that any action that may alfredi (Notarbartolo-di-Sciara and Pacific Oceans, and the more nearshore have a significant impact on the species Hillyer 1989; Graham et al. 2012; and reef-associated resident behavior, must undergo an environmental Venables 2013). These sites function as M. alfredi is rarely identified in assessment and approval process, there feeding sites, cleaning stations, or sites commercial and artisanal fisheries are no specific regulatory protections for where courtship interactions take place catch. While the prior lumping of all the species throughout Western (Heinrichs et al. 2011; Graham et al. manta rays as M. birostris may account Australian waters. Manta spp. are only 2012; Venables 2013), with the for these findings, in certain portions of explicitly protected from targeted appearance of manta rays at these the species’ range, the distribution of M. fishing within Ningaloo Marine Park locations generally predictable and alfredi may not overlap with the areas and, collectively, with all species in related to food availability of fishing operations. For example, in small designated zones along the (Notarbartolo-di-Sciara and Hillyer the Philippines, Rambahiniarison et al. Western Australian coast; however, it is 1989; Heinrichs et al. 2011; Jaine et al. (2016) explains that capture of reef important to note that neither species is 2012). Additionally, manta rays exhibit manta rays is unusual, as the main subject to directed fishing in these learned behaviors, with diving spots mobulid fishing ground in the Bohol waters. In fact, in those portions of the using artificial lights to concentrate Sea lies offshore in deeper waters, species’ range where populations are plankton and attract manta rays (Clark where the presence of the more coastal either not fished and/or are afforded 2010). These behavioral traits, including M. alfredi is unlikely. Additionally, protection and appear stable, we find the predictable nature of manta ray while M. alfredi are known to make existing regulatory measures to be appearances, combined with their slow night time deep-water dives offshore for adequate in protecting the species from swimming speeds, large size, and lack of foraging (≤150 m; Braun et al. (2014)), overutilization. These areas include fear towards humans, may increase their the driftnets deployed by the mobulid waters of Australia, Hawaii, Guam, vulnerability to other threats, such as fishermen are set at night at much Japan, the Republic of Maldives, Palau, overfishing, which was previously shallower maximum depths of 40 m and and Yap. Given the more coastal and discussed, and tourism (O’Malley et al. thus are unlikely to catch the species resident behavior of M. alfredi, national 2013; CMS 2014). (Rambahiniarison et al. 2016). However, measures prohibiting fishing of manta Tourism was identified as a potential Acebes and Tull (2016) did observe a rays are likely to provide adequate threat to the species, given that new, active mobulid fishery off Dinagat protection to the species from interacting (i.e., swimming) with manta Island in northern Mindanao that overutilization through the foreseeable rays is a significant tourist attraction appears to target M. alfredi around future. throughout the range of both species. In

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fact, O’Malley et al. (2013) estimated time unknown, the results from the extinction risk for both manta ray that the manta ray tourism industry Venables (2013) study provide a species, the ‘‘foreseeable future’’ was provides $140 million annually in direct preliminary estimate of the potentially considered to extend out several revenue or economic impact. Regular minimum response of the species to decades (>50 years). Given both species’ manta ray concentrations off interactions with tourists, and indicates life history traits, with longevity Mozambique, parts of Indonesia, that these interactions can cause the estimated to be greater than 20–40 years, Australia, Philippines, Yap, southern species to alter (and even stop) maturity ranges from 3 to >15 years, Japan, Hawaii, and Mexico have all behaviors that serve critical biological reproductive periodicity anywhere from become tourist attractions where manta functions (such as feeding and an annual cycle to a 5-year cycle, with dives are common (Anderson et al. cleaning). Additional studies on both a litter of only 1 pup, and a generation 2011b). Estimates of the number of the short-term and long-term impact of time estimated to be around 25 years, it people interacting with manta rays per tourist interactions with manta rays are would likely take more than a few year at these popular dive sites are needed in order to evaluate if this decades (i.e., multiple generations) for significant, ranging from over 10,000 at interaction is a potential threat to the any recent management actions to be Ho’ona Bay (Hawaii; Clark (2010)) to at survival of the species. realized and reflected in population least 14,000 in the Maldives (Anderson In addition to tourism activities, abundance indices. Similarly, the et al. 2011b). another potential threat to both manta impact of present threats to both species While manta ray tourism is far less ray species is an increase in mortality could be realized in the form of damaging to the species than the impact from boat strikes and entanglements. noticeable population declines within of fisheries, this increasing demand to Because manta ray aggregation sites are this time frame, as demonstrated in the see and dive with the animals has the sometimes in areas of high maritime very limited available sightings time- potential to lead to other unintended traffic (such as Port Santos in Brazil or series data. As the main potential consequences that could harm the in the Caribbean (Marshall et al. 2011a; operative threat to the species is species. For example, Osada (2010) Graham et al. 2012)), manta rays are at overutilization by commercial and found that a popular manta dive spot in potential risk of being struck and killed artisanal fisheries, this time frame Kona, Hawaii, had fewer emergent by boats. Mooring and boat anchor line would allow for reliable predictions zooplankton and less diversity entanglement may also wound manta regarding the impact of current levels of compared to a less used dive spot, and rays or cause them to drown (Deakos et fishery-related mortality on the attributed the difference to potential al. 2011; Heinrichs et al. 2011). For biological status of the two species. inadvertent habitat destruction by example, in a Maui, Hawaii, M. alfredi Additionally, this time frame allows for divers. Tour groups may also be population (n = 290 individuals), consideration of the previously engaging in inappropriate behavior, Deakos et al. (2011) observed that 1 out discussed impacts on manta ray habitat such as touching the mantas. Given the of 10 reef manta rays had an amputated from climate change and the potential increasing demand for manta ray or disfigured non-functioning cephalic effects on the status of these two tourism, with instances of more than 10 fin, likely a result of line entanglement. species. tourism boats present at popular dive Internet searches also reveal sites with over 100 divers in the water photographs of mantas with injuries In determining the extinction risk of at once (Anderson et al. 2011b; Venables consistent with boat strikes and line a species, it is important to consider 2013), without proper tourism entanglements, and manta researchers both the demographic risks facing the protocols, these activities could have report that such injuries may affect species as well as current and potential serious consequences for manta ray manta fitness in a significant way (The threats that may affect the species’ populations. Hawaii Association for Marine status. To this end, a demographic Already, evidence of tourism Education and Research Inc. 2005; analysis was conducted for the giant activities potentially altering manta ray Deakos et al. 2011; Heinrichs et al. 2011; manta ray and the reef manta ray. A behavior has been observed. For Couturier et al. 2012; CMS 2014; demographic risk analysis is an example, from 2007–2008, low numbers Germanov and Marshall 2014; Braun et assessment of the manifestation of past of mantas were observed at normally al. 2015), potentially similar to the threats that have contributed to the popular manta dive sites in the impacts of shark or orca attacks. species’ current status and informs the Maldives while manta ray numbers However, there is very little quantitative consideration of the biological response remained stable at less visited sites information on the frequency of these of the species to present and future (Anderson et al. 2011b). Similarly, De occurrences and no information on the threats. This analysis evaluated the Rosemont (2008) noted the impact of these injuries on the overall population viability characteristics and disappearance of a resident manta ray health of the populations. trends available for the manta rays, such colony from a popular cleaning station as abundance, growth rate/productivity, in a Bora Bora lagoon in 2005, and Assessment of Extinction Risk spatial structure and connectivity, and attributed the absence to new hotel The ESA (section 3) defines an diversity, to determine the potential construction and increased tourism endangered species as ‘‘any species risks these demographic factors pose to activities; however, by 2007, the author which is in danger of extinction each species. The information from this notes that the mantas had returned to throughout all or a significant portion of demographic risk analysis was the site. In a study of the tourism its range.’’ A threatened species is considered alongside the information impacts on M. alfredi behavior in Coral defined as ‘‘any species which is likely previously presented on threats to these Bay, Western Australia, Venables (2013) to become an endangered species within species, including those related to the observed that mantas exhibited a variety the foreseeable future throughout all or factors specified by the ESA section of behavioral changes in response to a significant portion of its range.’’ For 4(a)(1)(A)–(E) (and summarized in a swim group interactions (i.e., their the term ‘‘foreseeable future,’’ we define separate Threats Assessment section response was different than their it as the time frame over which below) and used to determine an overall behavior prior to the approach of the identified threats could be reliably risk of extinction for M. birostris and M. swim group). Although the long-term predicted to impact the biological status alfredi. Because species-specific effects of tourism interactions are at this of the species. For the assessment of information is sporadic and sometimes

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uncertain (due to the prior lumping of Yet, given the reports of anecdotal species exhibiting migratory behavior the Manta genus), the qualitative declines in sightings and decreases in and distances tracked of up to 1,500 km. reference levels of ‘‘low risk,’’ M. birostris landings (of up to 95 However, a recent study of the M. ‘‘moderate risk’’ and ‘‘high risk’’ were percent) in areas subject to fishing birostris population found off Pacific used to describe the overall assessment (particularly the Indo-Pacific and Mexico suggests there may be a degree of extinction risk, with detailed eastern Pacific portions of the species’ of spatial structuring within the species. definitions of these risk levels found in range), with take estimates that At this time, it is unknown whether the status review report (Miller and currently exceed those subpopulation natural rates of dispersal among Klimovich 2016). and aggregation estimates (e.g., 50–3,125 populations are too low to prevent individuals), abundance of these Demographic Risk Analysis sufficient gene flow among populations. particular populations may be at levels Additionally, there is no information to Giant Manta Ray that place them at increased risk of indicate that M. birostris is composed of genetic drift and potentially at more Abundance conspicuous source-sink populations or immediate risks of inbreeding habitat patches. Current and accurate abundance depression and demographic estimates are unavailable for the giant stochasticity. Extirpations of these Diversity manta ray, as the species tends to be populations would inherently increase Rates of dispersal and gene flow are only sporadically observed. While the overall risk of extinction for the not known to have been altered in M. observations of individuals in local entire species. birostris. Presently, giant manta rays are aggregations range from around 40 Growth Rate/Productivity wide-ranging inhabitants of offshore, individuals to over 600, estimates of oceanic waters and productive coastline subpopulation size have only been The current net productivity of M. ecosystems and thus are continually calculated for Mozambique (n = 600 birostris is unknown due to the exposed to ecological variation at a individuals) and Isla de la Plata, imprecision or lack of available broad range of spatial and temporal Ecuador (n = 1,500 individuals). abundance estimates or indices. scales. As such, large-scale impacts that If a population is critically small in Fecundity, however, is extremely low, affect ocean temperatures, currents, and size, chance variations in the annual with one pup per litter and a potentially food chain dynamics, may number of births and deaths can put the reproductive periodicity of 1–2 years. pose a threat to this species. However, population at added risk of extinction. Using estimates of life history given the migratory behavior of the giant Demographic stochasticity refers to the parameters for both giant and reef manta manta ray and tolerance to both tropical variability of annual population change rays, Dulvy et al. (2014) calculated a and temperate waters, these animals arising from random birth and death median maximum population growth likely have the ability to shift their events at the individual level. When rate to be 0.116 (one of the lowest values range or distribution to remain in an populations are very small, chance compared to other shark and ray environment conducive to their demographic events can have a large species), and estimated productivity (r) physiological and ecological needs, impact on the population. The to be 0.029. Ward-Paige et al. (2013) providing the species with resilience to conservation biology ‘‘50/500’’ rule-of- calculated a slightly higher intrinsic rate these effects. At this time, there is no thumb suggests that the effective of population increase for M. birostris at information to suggest that natural population size (Ne; the number of r = 0.042; however, both these estimates processes that cause ecological variation reproducing individuals in a indicate that the giant manta ray has have been significantly altered to the population) in the short term should not very low productivity and, thus, is point where M. birostris is at risk. be <50 individuals in order to avoid extremely susceptible to decreases in its inbreeding depression and demographic abundance. Reef Manta Ray stochasticity (Franklin 1980; Harmon Given their large sizes, manta rays are Abundance and Braude 2010). In the long-term, Ne assumed to have a fairly high survival should not be <500 in order to decrease rate after maturity (e.g., low natural Current and accurate abundance the impact of genetic drift and potential predation), with estimated annual estimates are unavailable for the reef loss of genetic variation that will survival rates for M. alfredi populations manta ray. Observations of individuals prevent the population from adapting to supporting this assumption. Based on in local aggregations range from 35 environmental changes (Franklin 1980; modeling work on M. alfredi, adult individuals to over 2,400; however, Harmon and Braude 2010). Given the survival rate was found to be the most many are on the order of 100–600 two available subpopulation estimates, significant factor affecting the viability individuals. Subpopulation sizes range M. birostris is not likely to experience of the population. from 100 to 350 individuals, with the extreme fluctuations that could lead to Additionally, at this time, no changes exception of the Maldives at 3,300– depensation; however, data are severely in demographic or reproductive traits or 9,677 individuals. Meta-population lacking. The threshold for depensation barriers to the exploitation of requisite estimates for southern Mozambique and in giant manta rays is also unknown. habitats/niches/etc. have been observed Ningaloo Reef, Australia are 802–890 Additionally, the genetic diversity in in M. birostris. and 1,200–1,500 individuals, the giant manta ray has not been respectively. investigated. While a preliminary study Spatial Structure/Connectivity The rather low subpopulation suggests that the species may exist as The giant manta ray inhabits tropical, estimates for M. alfredi throughout most isolated subpopulations, available subtropical, and temperate bodies of of its range suggest that the species may tracking information indicates these water and is commonly found offshore, be at increased risk of genetic drift and manta rays are pelagic and migratory in oceanic waters, and near productive potential loss of genetic variation. and can likely travel large distances to coastlines. It occurs over a broad Unlike the giant manta ray, M. alfredi is reproduce. It is this more transient and geographic range and is found in all thought to be a more resident species, pelagic nature of the species that has ocean basins. Most tagging and tracking with populations that occur year-round made it difficult to estimate population studies indicate that the home range of at certain sites. This reproductive sizes. individuals is likely large, with the isolation further increases the risk of

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inbreeding depression and potential barriers to the exploitation of requisite Threats Assessment inability of the population to respond to habitats/niches/etc. have been observed. Giant Manta Ray environmental variation or anthropogenic perturbations. For Spatial Structure/Connectivity The most significant and certain threat to the giant manta ray is example, Kashiwagi (2014) recently The reef manta ray is commonly seen overutilization for commercial estimated the effective population size inshore near coral and rocky reefs. The of the M. alfredi population off the purposes. Giant manta rays are both species is associated with warmer Yaeyama Islands to be Ne = 89, targeted and caught as bycatch in a waters (≤21 °C) and productive indicating that the population is not number of global fisheries throughout part of a large gene pool and may be nearshore habitats (such as island their range. Estimated take of giant close to a level where viability could be groups). It is considered a more resident manta rays, particularly in many jeopardized in the shorter term. Total species than M. birostris. While the portions of the Indo-Pacific, frequently population was estimated at 165–202 species has been tracked undertaking exceeds numbers of observed individuals, indicating long-term long-distance movements (≤700 km), individuals in those areas, and is viability vulnerability. With most usually to exploit offshore productive accompanied by observed declines in available subpopulation estimates areas, reef manta rays tend to return to sightings and landings of the species. ranging only from 100 to 600 known aggregation sites, indicating a Efforts to address overutilization of the individuals (with the exception of degree of site-fidelity. Based on photo- species through regulatory measures Western Australia, Maldives, and identification surveys of the M. alfredi appear inadequate, with evidence of Southern Mozambique), it is likely that population off Maui, Hawaii, Deakos et targeted fishing of the species despite these populations similarly have low al. (2011) suggested that geographic prohibitions (Indo-Pacific; Eastern effective population sizes that may barriers, such as deep channels, might Pacific) and only one regional measure increase their vulnerability to be barriers to movement between to address bycatch issues, with inbreeding depression, the loss of neighboring M. alfredi populations. uncertain effectiveness (Eastern Pacific). Additionally, given the migratory and genetic variants, or fixation of Collectively, this information suggests pelagic behavior, national protections deleterious mutations. that gene flow is likely limited among Overall, based on the information for the species are less likely to populations of M. alfredi, particularly above, the estimates of small and adequately protect the species from isolated subpopulations throughout those separated by deep ocean expanses. fisheries-related mortality. Giant manta most of the species’ range, with the With the exception of the Yaeyama, rays are not confined by national three exceptions off Mozambique, Japan population of M. alfredi, which boundaries and may, for example, lose Maldives, and Western Australia, Kashiwagi (2014) hypothesized may be certain protections as they conduct inherently place M. alfredi at an a ‘‘sink’’ population but is presently seasonal migrations or even as they increased risk of extinction from increasing with a population growth move around to feed if they cross environmental variation or rate of 1.02–1.03, there is no particular national jurisdictional anthropogenic perturbations. However, information to indicate that M. alfredi is boundaries (e.g., between the Maldives the trend in overall abundance of M. composed of conspicuous source-sink and Sri Lanka or India), move outside of alfredi is highly uncertain. populations or habitat patches whose established Marine Protected Areas, or enter into high seas. While the species Growth Rate/Productivity loss may pose a risk of extinction. recently has been added to CITES The current net productivity of M. Diversity Appendix II (added in March 2013 with alfredi is unknown due to the a delayed effectiveness of September imprecision or lack of available Given their tendency towards site 2014), which may curb targeted fishing abundance estimates or indices. fidelity, M. alfredi likely exists as as countries must ensure that manta ray Fecundity, however, is extremely low, isolated populations with low rates of products are legally obtained and trade with one to, rarely, two pups per litter dispersal and little gene flow among is sustainable, the species is still likely and a reproductive periodicity of populations. Currently, there is no to be caught as bycatch in the industrial anywhere from 1–5 years. Estimated information to suggest that natural fisheries and targeted by artisanal productivity (r) values range from 0.023 processes that cause ecological variation fisheries for domestic consumption. to 0.05, indicating that the reef manta have been significantly altered to the Other threats to M. birostris that ray has very low productivity and, thus, point where the species is at risk. Reef potentially contribute to long-term risk is extremely susceptible to decreases in manta rays also likely have the ability of the species include (micro) plastic its abundance. to shift their distribution to remain in an ingestion rates, increased parasitic loads Annual survival rate for reef manta environment conducive to their as a result of climate change effects, and rays is fairly high. Estimated survival physiological and ecological needs, potential disruption of important life rates for subpopulations range from 0.95 providing the species with resilience to history functions as a result of increased to 1 off Australia, Hawaii, and Japan these effects. For example, in response tourism; however, due to the significant (Deakos et al. 2011; Couturier et al. to changing ecological conditions, like data gaps, the likelihood and impact of 2014; Kashiwagi 2014). In Mozambique, the biannual reversal of monsoon these threats on the status of the species rates were lower, between 0.6–0.7; is highly uncertain. however shark attacks are also more currents, reef manta rays will migrate to common in this area (Marshall et al. the downstream side of atolls, Reef Manta Ray 2011c). Based on modeling work, potentially to remain in nutrient-rich Given their more inshore distribution Smallegange et al. (2016) showed that waters year-round (Anderson et al. and association with shallow coral and population growth rate was most 2011a). Presently, there is no rocky reefs, M. alfredi does not appear sensitive to changes in the survival of information to suggest that natural to be as vulnerable to commercial and adults. processes that cause ecological variation larger-scale artisanal fishing operations Additionally, no changes in have been significantly altered to the as M. birostris. These fisheries tend to demographic or reproductive traits or point where M. alfredi is at risk. operate in deeper and more pelagic

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waters, targeting migratory and coral reefs, are also likely to occur as a extinction throughout its entire range. commercially valuable species (like result of climate change, affecting the However, under the final Significant tunas, billfishes, and sharks), and, potential previous predictability of M. Portion of Its Range (SPR) policy, we hence, have a higher likelihood of alfredi food resources. Reef manta rays must consider whether the species may catching giant manta rays. In the may need to venture out farther to find be in danger of extinction, or likely to available information, only two available food or search for new become so within the foreseeable future, countries are reported to have targeted productive areas; however, given that in a significant portion of its range (79 artisanal fisheries for M. alfredi: The the species has been shown capable of FR 37577; July 1, 2014). Philippines (documented 4 fishing making long-distance foraging Significant Portion of Its Range (SPR) boats) and Mozambique. The species movements, the impact of this potential Analysis has been identified in bycatch from displacement or change in distribution Indonesia, Papua New Guinea, and of zooplankton may not be a significant To identify only those portions that Kiribati, with subsequent observed contributor to the species’ extinction warrant further consideration under the declines in sightings, and potential local risk. SPR Policy, we must determine whether extirpations; however, the extent of Other threats that potentially there is substantial information fishing mortality on the species contribute to long-term risk of the indicating that (1) the portions may be throughout its range is highly uncertain. species include (micro) plastic ingestion significant and (2) the species may be in Additionally, the lumping of both rates, and potential disruption of danger of extinction in those portions or species as M. birostris prior to 2009, as important life history functions or likely to become so within the well as the fact that much of the catch destruction of habitat as a result of foreseeable future. With respect to the is not reported down to species level, increased tourism; however, due to the second of those determinations, as also significantly contributes to this significant data gaps, the likelihood and mentioned previously, the best available uncertainty. However, based on the data impact of these threats on the status of information indicates that the giant available, many of the identified the species is highly uncertain. manta ray faces concentrated threats throughout the Indo-Pacific and eastern populations of M. alfredi throughout the Overall Risk Summary western and central Pacific are currently Pacific portion of its range. Estimated protected by regulations and appear Giant Manta Ray take of giant manta rays is frequently greater than the observed individuals in stable, indicating that these existing Given the extremely low reproductive those areas, with observed declines in regulatory measures are adequate at output and overall productivity of the sightings and landings of the species of protecting the species from declines due giant manta ray, it is inherently up to 95 percent. Efforts to address to fishing mortality. Within the Indian vulnerable to threats that would deplete overutilization of the species through Ocean, national protections exist for the its abundance, with a low likelihood of regulatory measures appear inadequate large population of M. alfredi off the recovery. While there is considerable in this portion of its range, with Maldives, and while specific protections uncertainty regarding the current evidence of targeted fishing of the for M. alfredi have not been abundance of M. birostris throughout its species despite prohibitions and implemented in Western Australia, the range, the best available information bycatch measures that may not species is not subject to directed fishing indicates that the species has significantly decrease fisheries-related (or prevalent in bycatch) and is experienced population declines of mortality rates of the species. Based on presently one of the largest identified potentially significant magnitude within the demographic risks and threats to the populations. areas of the Indo-Pacific and eastern species in this portion, we determined Climate change was identified as a Pacific portions of its range, primarily that the species has a moderate risk of potential threat contributing to the long- due to fisheries-related mortality. Yet, extinction in this portion of its range. term extinction risk of the species. larger subpopulations of the species still Next, we must evaluate whether this Because M. alfredi are more commonly exist, including off Mozambique (where portion is ‘‘significant.’’ As defined in associated with coral reefs compared to declines were not observed) and the SPR Policy, a portion of a species’ giant manta rays, frequently aggregating Ecuador. However, as giant manta rays range is ‘‘significant’’ ‘‘if the species is within these habitats and showing a are a migratory species and continue to not currently endangered or threatened high degree of site-fidelity and face fishing pressure, particularly from throughout its range, but the portion’s residency to these areas, we found the the industrial purse seine fisheries and contribution to the viability of the impact of climate change on coral reefs artisanal gillnet fisheries operating species is so important that, without the to be a potential risk to the species. within the Indo-Pacific and eastern members in that portion, the species Although the species itself is not Pacific portions of its range, would be in danger of extinction, or dependent on corals, which are most overutilization will continue to be a likely to become so in the foreseeable susceptible to the effects of climate threat to these remaining M. birostris future, throughout all of its range’’ (79 change, the manta rays rely on the reef populations through the foreseeable FR 37578; July 1, 2014). Without the community structure, like the future, placing them at a moderate risk Indo-Pacific and eastern Pacific portion abundance of cleaner fish, to carry out of extinction. of the species’ range, the species would important functions, such as removing While we assume that declining have to depend on only its members in parasite loads and dead tissue. Coral populations within the Indo-Pacific and the Atlantic for survival. While areas reef community structure is likely to be eastern Pacific portions of its range will exhibiting source-sink dynamics, which altered as a result of increasing events likely translate to overall declines in the could affect the survival of the species, of coral bleaching through the species throughout its entire range, are not known, the largest foreseeable future; however, what this there is very little information on the subpopulations and records of change will look like and its subsequent abundance, spatial structure, or extent individuals of the species come from the impact on the species is highly of fishery-related mortality of the Indo-Pacific and eastern Pacific portion. uncertain. Similarly, changes in species within the Atlantic portion of its The only data from the Atlantic on the zooplankton communities and range. As such, we cannot conclude that abundance of the species are records of distribution, including in and around the species is at a moderate risk of >70 individuals in the Flower Garden

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Banks Marine Sanctuary (Gulf of be discrete in relation to the remainder international governmental boundaries. Mexico) and 60 manta rays from waters of the taxon (species or subspecies) to As such, we find that the M. birostris off Brazil (see Table 4 in Miller and which it belongs; and (2) the population population in the Indo-Pacific and Klimovich (2016)). Given that the must be ‘‘significant’’ (as that term is eastern Pacific does not meet the species is rarely identified in the used in the context of the DPS policy, discreteness criteria of the DPS policy, fisheries data in the Atlantic, it may be which is different from its usage under and, thus, is not a valid DPS. assumed that populations within the the SPR policy) to the remainder of the Reef Manta Ray Atlantic are small and sparsely taxon to which it belongs. distributed. These demographic risks, in In terms of discreteness, a population Overall, the species’ life history conjunction with the species’ inherent segment of a vertebrate species may be characteristics increase its inherent vulnerability to depletion, indicate that considered discrete if it satisfies either vulnerability to depletion. Its tendency even low levels of mortality may one of the following conditions: (1) ‘‘It towards site fidelity and high residency portend drastic declines in the is markedly separated from other rates suggests that there may be little population. As such, without the Indo- populations of the same taxon as a gene flow between subpopulations, Pacific and eastern Pacific portion, the consequence of physical, physiological, meaning that reestablishment after minimal targeted fishing of the species ecological, or behavioral factors. depletion is unlikely. Additionally, by artisanal fishermen and bycatch Quantitative measures of genetic or because these aggregations tend to be mortality from the purse seine, trawl, morphological discontinuity may small, even light fishing may lead to and longline fisheries operating in the provide evidence of this separation’’; or population depletion. However, despite Atlantic becomes a significant (2) ‘‘it is delimited by international these inherent risks, the species does contributing factor to the extinction risk governmental boundaries within which not appear subjected to significant of the species. Based on the above differences in control of exploitation, threats that are causing declines, or findings, we conclude that the Indo- management of habitat, conservation likely to cause declines, to the point Pacific and eastern Pacific portion of the status, or regulatory mechanisms exist where the species would be at risk of giant manta ray’s range comprises a that are significant in light of section extinction. As mentioned in the threats significant portion of the range of the 4(a)(1)(D)’’ of the ESA (61 FR 4722; analysis, targeted fishing of the species species because this portion’s February 7, 1996). has only been observed in a select few contribution to the viability of M. Research on the genetics of the locations, and its identification in birostris is so important that, without species, which may provide evidence of bycatch is limited. The majority of the the members in this portion, the giant discreteness between populations, is known M. alfredi subpopulations, manta ray would likely become in ongoing. As discussed previously in this particularly throughout the western and danger of extinction within the finding, while there may be evidence of Central Pacific, while small, are foreseeable future, throughout all of its a potential M. birostris subspecies, or protected from fishing mortality and range. new manta species, found off the appear stable. Some of the larger known Under the SPR policy, we conclude Yucata´n coast in the Gulf of Mexico, the M. alfredi subpopulations, such as off that the Indo-Pacific and eastern Pacific study by Hinojosa-Alvarez et al. (2016) the Maldives (n = 3,300–9,677 portion of the giant manta ray’s range also showed that some of the Yucata´n individuals) and Western Australia (n = qualifies as a significant portion of the manta rays found in the area shared 1,200–1,500 individuals), are not subject species’ range. Additionally, based on haplotypes with M. birostris samples to directed fishing, with Australia’s the information above and further from the Indo-Pacific and eastern overall population considered to be one discussed in our demographic risks Pacific. Additionally, based on nuclear of the world’s healthiest. While climate analysis and threats assessment, as well DNA, the Yucata´n samples were change may alter aspects of the habitat as the information in the status review consistent with the M. birostris samples and food resources of the species, the report, we conclude that M. birostris is from the Indo-Pacific and eastern Pacific subsequent impact on the species is at a moderate risk of extinction within portions of its range. This is the only highly uncertain. Thus, based on the this significant portion of its range. study that we are aware of that has above evaluation of demographic risks compared potential genetic differences and threats to the species, we find that Distinct Population Segment (DPS) between ocean basins for giant manta the reef manta ray is likely to be at a low Analysis rays. Given the available data, we do not overall risk of extinction. In accordance with the SPR policy, if find evidence to indicate genetic SPR Analysis a species is determined to be threatened discreteness between M. birostris in the or endangered in a significant portion of Atlantic and M. birostris in the Indo- As was done for the giant manta ray, its range, and the population in that Pacific and eastern Pacific. we must conduct an SPR analysis to significant portion is a valid distinct In terms of physical, physiological, determine if the species is in danger of population segment (DPS), NMFS will morphological, ecological, behavioral, extinction, or likely to become so within list the DPS rather than the entire and regulatory factors, there is no the foreseeable future, in a significant taxonomic species or subspecies. evidence that the Indo-Pacific and portion of its range. In applying the Because the Indo-Pacific and eastern eastern Pacific population of M. birostris policy, we first examined where threats Pacific represents a significant portion is markedly separate from the are concentrated to evaluate whether the of the range of the species, and this population in the Atlantic. There is no species is at risk of extinction within portion is at a risk of extinction that is evidence of differences in the those portions. Targeted fishing and higher than ‘‘low,’’ we performed a DPS morphology or physiology between the subsequent declines in populations of analysis on the population within this populations, nor any information to M. alfredi are known from waters off portion to see if it qualifies as a valid indicate changes in habitat use or Mozambique and the Philippines, and DPS. behavior across ocean basins. Also, the species has also been identified in The Services’ policy on identifying given that the species is highly bycatch from Indonesia, Papua New DPSs (61 FR 4722; February 7, 1996) migratory and pelagic, with no Guinea, and Kiribati. However, with the identifies two criteria for DPS identified barriers to movement, these exception of the southern Mozambique designations: (1) The population must populations cannot be delimited by population, the extent of decline of the

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species throughout these other areas has Protective Efforts conservation efforts in our public not been quantified. But while the rate comment process (see below). There are many conservation efforts of decline is unknown, fishing pressure Determination on the species continues in these presently ongoing to collect research on manta ray life history, ecology, and portions of range and, combined with Section 4(b)(1) of the ESA requires biology, and to raise awareness of the species’ demographic risks of that NMFS make listing determinations threats to manta rays (see Miller and isolated, small populations and based solely on the best scientific and Klimovich (2016) for detailed commercial data available after extremely low productivity, these discussion). The available research and conducting a review of the status of the threats are likely placing these citizen science data that have resulted species and taking into account those populations on a trajectory toward a from these conservation efforts have efforts, if any, being made by any state higher risk of extinction. already been considered in the above or foreign nation, or political The second question that needs to be analysis, and future research activities subdivisions thereof, to protect and addressed in the SPR analysis is will continue to provide valuable conserve the species. We have whether these portions can be information on these manta ray species. independently reviewed the best considered ‘‘significant.’’ Without these Additionally, the efforts by these available scientific and commercial portions, would the species be in danger organizations to educate the public, information including the petition, of extinction, or likely to become so in such as through awareness campaigns, public comments submitted on the 90- the foreseeable future, throughout all of could eventually lead to decreases in day finding (81 FR 8874; February 23, its range? We find that this is unlikely the demand for manta ray products. For 2016), the status review report (Miller to be the case. Even if these populations example, Lawson et al. (2016), citing and Klimovich 2016), and other were gone, the species would still exist unpublished data, noted an 18-month published and unpublished as small, isolated populations awareness-raising campaign conducted information, and have consulted with throughout the Indo-Pacific. There is no in 2015 in Guangzhou, China, that species experts and individuals familiar evidence of source-sink dynamics seemed to indicate a level of success in with manta rays. We considered each of between these portions and other areas, decreasing consumer demand for gill the statutory factors to determine whether it presented an extinction risk which could affect the survival of the rakers, which, in turn, decreased the to each species on its own, now or in species. In fact, the only indication of a interest of traders to carry gill plates in the foreseeable future, and also potential source-sink dynamic was the future. While more monitoring of trade and consumer behavior is required considered the combination of those hypothesized for the M. alfredi to evaluate the success of these efforts, factors to determine whether they population off Yaeyama, Japan, which it may indicate that awareness-raising collectively contributed to the Kashiwagi (2014) found is presently campaigns could be successful tools for extinction risk of the species, now or in increasing, indicating no risk of loss to influencing customer behavior. With the foreseeable future. this population. In fact, many of the M. demand reduction viewed as a potential Based on our consideration of the best alfredi populations outside of the avenue to indirectly reduce fishing available scientific and commercial portions identified above, while small pressure on manta rays, these information, as summarized here and in in size, are presently thought to be campaigns may ultimately help decrease Miller and Klimovich (2016), including stable or increasing. Additionally, these the main threat to the species (Lawson our SPR and DPS analyses, we find that populations, such as the largest et al. 2016). the giant manta ray (Manta birostris) is identified M. alfredi population, off the at a moderate risk of extinction within Awareness campaigns are also being Maldives, benefit from national a significant portion of its range, with used to educate the public on protections that prohibit the fishing, the species likely to become in danger appropriate tourist behavior during landing, or selling of the species. of extinction within the foreseeable manta ray dives, which can help Because these populations occur future throughout that portion. We did decrease potential negative impacts of nearshore, and the species exhibits high not find that the significant portion tourism activities on manta rays. As meets the criteria of a DPS. Therefore, residency rates and site-fidelity mentioned previously, best practice behavior, these protections will be we have determined that the giant codes of conduct have been developed manta ray meets the definition of a adequate to prevent overutilization of by a number of organizations and are the species through the foreseeable threatened species and, per the SPR increasingly being used by dive policy, propose to list it is as such future. As such, even without the operators at a number of popular manta portions identified above, the species throughout its range under the ESA. ray diving sites, including Kona, Based on our consideration of the best will unlikely be in danger of extinction Hawaii, Western Australia, throughout all of its range now or in the available scientific and commercial Mozambique, Bora Bora, and the information, as summarized here and in foreseeable future. Maldives, to promote the safe viewing of Miller and Klimovich (2016), we find Thus, under the SPR policy, we could manta rays. that the reef manta ray (Manta alfredi) not identify any portions of the species’ While we find that these efforts will faces an overall low risk of extinction range that meet both criteria (i.e., the help increase the scientific knowledge throughout its range. As previously portion is biologically significant and and promote public awareness about explained, we could not identify any the species may be in danger of manta rays, with the potential (but not portion of the species’ range that met extinction in that portion, or likely to certainty) to decrease the impacts of both criteria of the SPR policy. become so within the foreseeable specific threats in the future, we do not Accordingly, the reef manta ray does not future). Therefore, we find that our find that these efforts have significantly meet the definition of a threatened or conclusion about the species’ overall altered the extinction risk for the giant endangered species, and thus, the reef risk of extinction does not change and manta ray to where it would not be at manta ray does not warrant listing as conclude that M. alfredi is likely to be risk of extinction in the foreseeable threatened or endangered at this time. at a low risk of extinction throughout its future. However, we seek additional This is a final action on the range. information on these and other aforementioned petition to list the reef

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manta ray under the ESA, and, determination that such areas are opportunities for public participation. therefore, we do not solicit comments essential for the conservation of the The OMB Bulletin, implemented under on it. species. ‘‘Conservation’’ means the use the Information Quality Act (Pub. L. of all methods and procedures needed 106–554), is intended to enhance the Effects of Listing to bring the species to the point at quality and credibility of the Federal Conservation measures provided for which listing under the ESA is no government’s scientific information, and species listed as endangered or longer necessary. Section 4(a)(3)(a) of applies to influential or highly threatened under the ESA include the ESA (16 U.S.C. 1533(a)(3)(A)) influential scientific information recovery actions (16 U.S.C. 1533(f)); requires that, to the extent prudent and disseminated on or after June 16, 2005. concurrent designation of critical determinable, critical habitat be To satisfy our requirements under the habitat, if prudent and determinable (16 designated concurrently with the listing OMB Bulletin, we obtained independent U.S.C. 1533(a)(3)(A)); Federal agency of a species. Designations of critical peer review of the status review report. requirements to consult with NMFS habitat must be based on the best Independent specialists were selected under section 7 of the ESA to ensure scientific data available and must take from the academic and scientific their actions do not jeopardize the into consideration the economic, community for this review. All peer species or result in adverse modification national security, and other relevant reviewer comments were addressed or destruction of critical habitat should impacts of specifying any particular area prior to dissemination of the status it be designated (16 U.S.C. 1536); and as critical habitat. If we determine that review report and publication of this prohibitions on ‘‘taking’’ (16 U.S.C. it is prudent and determinable, we will proposed rule. 1538). Recognition of the species’ plight publish a proposed designation of Public Comments Solicited on Listing through listing promotes conservation critical habitat for the giant manta ray in actions by Federal and state agencies, a separate rule. Public input on features To ensure that the final action foreign entities, private groups, and and areas in U.S. waters that may meet resulting from this proposal will be as individuals. the definition of critical habitat for the accurate and effective as possible, we solicit comments and suggestions from Identifying Section 7 Conference and giant manta ray is invited. the public, other governmental agencies, Consultation Requirements Protective Regulations Under Section the scientific community, industry, Section 7(a)(2) (16 U.S.C. 1536(a)(2)) 4(d) of the ESA environmental groups, and any other of the ESA and NMFS/USFWS We are proposing to list the giant interested parties. Comments are regulations require Federal agencies to manta ray (Manta birostris) as a encouraged on this proposal (See DATES confer with us on actions likely to threatened species. In the case of and ADDRESSES). Specifically, we are jeopardize the continued existence of threatened species, ESA section 4(d) interested in information regarding: (1) species proposed for listing, or that leaves it to the Secretary’s discretion New or updated information regarding result in the destruction or adverse whether, and to what extent, to extend the range, distribution, and abundance modification of proposed critical the section 9(a) ‘‘take’’ prohibitions to of the giant manta ray; (2) new or habitat. If a proposed species is the species, and authorizes us to issue updated information regarding the ultimately listed, Federal agencies must regulations necessary and advisable for genetics and population structure of the consult on any action they authorize, the conservation of the species. Thus, giant manta ray; (3) habitat within the fund, or carry out if those actions may we have flexibility under section 4(d) to range of the giant manta ray that was affect the listed species or its critical tailor protective regulations, taking into present in the past but may have been habitat and ensure that such actions do account the effectiveness of available lost over time; (4) new or updated not jeopardize the species or result in conservation measures. The 4(d) biological or other relevant data adverse modification or destruction of protective regulations may prohibit, concerning any threats to the giant critical habitat should it be designated. with respect to threatened species, some manta ray (e.g., post-release mortality Examples of Federal actions that may or all of the acts which section 9(a) of rates, landings of the species, illegal affect the giant manta ray include, but the ESA prohibits with respect to taking of the species); (5) current or are not limited to: Alternative energy endangered species. We are not planned activities within the range of projects, discharge of pollution from proposing such regulations at this time, the giant manta ray and their possible point sources, non-point source but may consider potential protective impact on the species; (6) recent pollution, contaminated waste and regulations pursuant to section 4(d) for observations or sampling of the giant plastic disposal, dredging, pile-driving, the giant manta ray in a future manta ray; and (7) efforts being made to development of water quality standards, rulemaking. In order to inform our protect the giant manta ray. vessel traffic, military activities, and consideration of appropriate protective Public Comments Solicited on Critical fisheries management practices. regulations for the species, we seek Habitat information from the public on the Critical Habitat threats to giant manta rays and possible We request information describing the Critical habitat is defined in section 3 measures for their conservation. quality and extent of habitats for the of the ESA (16 U.S.C. 1532(3)) as: (1) giant manta ray, as well as information The specific areas within the Role of Peer Review on areas that may qualify as critical geographical area occupied by a species, The intent of peer review is to ensure habitat for the species in U.S. waters. at the time it is listed in accordance that listings are based on the best Specific areas that include the physical with the ESA, on which are found those scientific and commercial data and biological features essential to the physical or biological features (a) available. In December 2004, the Office conservation of the species, where such essential to the conservation of the of Management and Budget (OMB) features may require special species and (b) that may require special issued a Final Information Quality management considerations or management considerations or Bulletin for Peer Review establishing protection, should be identified. Areas protection; and (2) specific areas outside minimum peer review standards, a outside the occupied geographical area the geographical area occupied by a transparent process for public should also be identified, if such areas species at the time it is listed upon a disclosure of peer review planning, and themselves are essential to the

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conservation of the species. ESA information on occupied and under Executive Order 12866. This implementing regulations at 50 CFR unoccupied habitat areas; (2) the proposed rule does not contain a 424.12(g) specify that critical habitat reasons why any habitat should or collection-of-information requirement shall not be designated within foreign should not be determined to be critical for the purposes of the Paperwork countries or in other areas outside of habitat as provided by sections 3(5)(A) Reduction Act. U.S. jurisdiction. Therefore, we request and 4(b)(2) of the ESA; (3) information Executive Order 13132, Federalism information only on potential areas of regarding the benefits of designating critical habitat within waters under U.S. particular areas as critical habitat; (4) In accordance with E.O. 13132, we jurisdiction. current or planned activities in the areas determined that this proposed rule does Section 4(b)(2) of the ESA requires the that might be proposed for designation not have significant Federalism effects Secretary to consider the ‘‘economic and their possible impacts; (5) any and that a Federalism assessment is not impact, impact on national security, and foreseeable economic or other potential required. In keeping with the intent of any other relevant impact’’ of impacts resulting from designation, and the Administration and Congress to designating a particular area as critical in particular, any impacts on small provide continuing and meaningful habitat. Section 4(b)(2) also authorizes entities; (6) whether specific dialogue on issues of mutual state and the Secretary to exclude from a critical unoccupied areas may be essential to Federal interest, this proposed rule will habitat designation those particular provide additional habitat areas for the be given to the relevant governmental areas where the Secretary finds that the conservation of the species; and (7) agencies in the countries in which the benefits of exclusion outweigh the potential peer reviewers for a proposed species occurs, and they will be invited benefits of designation, unless critical habitat designation, including to comment. As we proceed, we intend excluding that area will result in persons with biological and economic to continue engaging in informal and extinction of the species. For features expertise relevant to the species, region, formal contacts with the states, and and areas potentially qualifying as and designation of critical habitat. other affected local, regional, or foreign entities, giving careful consideration to critical habitat, we also request References information describing: (1) Activities or all written and oral comments received. A complete list of the references used other threats to the essential features or List of Subjects in 50 CFR Part 223 activities that could be affected by in this proposed rule is available upon designating them as critical habitat; and request (see ADDRESSES). Endangered and threatened species. (2) the positive and negative economic, Classification Dated: January 5, 2017. national security and other relevant Samuel D. Rauch, III, impacts, including benefits to the National Environmental Policy Act Deputy Assistant Administrator for recovery of the species, likely to result The 1982 amendments to the ESA, in Regulatory Programs, National Marine if these areas are designated as critical section 4(b)(1)(A), restrict the Fisheries Service. habitat. We seek information regarding information that may be considered For the reasons set out in the the conservation benefits of designating when assessing species for listing. Based preamble, 50 CFR part 223 is proposed areas within waters under U.S. on this limitation of criteria for a listing to be amended as follows: jurisdiction as critical habitat. In decision and the opinion in Pacific keeping with the guidance provided by Legal Foundation v. Andrus, 675 F. 2d PART 223—THREATENED MARINE OMB (2000; 2003), we seek information 825 (6th Cir. 1981), NMFS has AND ANADROMOUS SPECIES that would allow the monetization of concluded that ESA listing actions are these effects to the extent possible, as not subject to the environmental ■ 1. The authority citation for part 223 well as information on qualitative assessment requirements of the National continues to read as follows: impacts to economic values. Environmental Policy Act (NEPA). Authority: 16 U.S.C. 1531–1543; subpart B, Data reviewed may include, but are § 223.201–202 also issued under 16 U.S.C. not limited to: (1) Scientific or Executive Order 12866, Regulatory 1361 et seq.; 16 U.S.C. 5503(d) for commercial publications; (2) Flexibility Act, and Paperwork § 223.206(d)(9). Reduction Act administrative reports, maps or other ■ 2. In § 223.102, in the table in graphic materials; (3) information As noted in the Conference Report on paragraph (e) add a new entry for ‘‘ray, received from experts; and (4) the 1982 amendments to the ESA, giant manta’’ in alphabetical order by comments from interested parties. economic impacts cannot be considered common name under the ‘‘Fishes’’ Comments and data particularly are when assessing the status of a species. subheading to read as follows: sought concerning: (1) Maps and Therefore, the economic analysis specific information describing the requirements of the Regulatory § 223.102 Enumeration of threatened amount, distribution, and use type (e.g., Flexibility Act are not applicable to the marine and anadromous species. foraging or migration) by the giant listing process. In addition, this * * * * * manta ray, as well as any additional proposed rule is exempt from review (e) * * *

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

******* Fishes

******* Ray, giant manta Manta birostris ... Entire species .... [Insert Federal Register page where the document begins], NA ...... NA. [Insert date of publication 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).

[FR Doc. 2017–00370 Filed 1–11–17; 8:45 am] BILLING CODE 3510–22–P

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