82_FR_3702 82 FR 3694 - 12-Month Finding on a Petition To List Giant and Reef Manta Rays as Threatened or Endangered Under the Endangered Species Act

82 FR 3694 - 12-Month Finding on a Petition To List Giant and Reef Manta Rays as Threatened or Endangered Under the Endangered Species Act

DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration

Federal Register Volume 82, Issue 8 (January 12, 2017)

Page Range3694-3715
FR Document2017-00370

We, NMFS, announce a 12-month finding on a petition to list the giant manta ray (Manta birostris) and reef manta ray (Manta alfredi) as threatened or endangered under the Endangered Species Act (ESA). We have completed a comprehensive status review of both species in response to this petition. Based on the best scientific and commercial information available, including the status review report (Miller and Klimovich 2016), and after taking into account efforts being made to protect these species, we have determined that the giant manta ray (M. birostris) is likely to become an endangered species within the foreseeable future throughout a significant portion of its range. Therefore, we propose to list the giant manta ray as a threatened species under the ESA. Any protective regulations determined to be necessary and advisable for the conservation of the proposed threatened giant manta ray under ESA section 4(d) would be proposed in a subsequent Federal Register announcement. Should the proposed listing be finalized, we would also designate critical habitat for the species, to the maximum extent prudent and determinable. We solicit information to assist this proposed listing determination, the development of proposed protective regulations, and designation of critical habitat in the event the proposed threatened listing for the giant manta ray is finalized. Additionally, we have determined that the reef manta ray (M. alfredi) is not currently in danger of extinction throughout all or a significant portion of its range and is not likely to become so within the foreseeable future. Therefore, we find that the reef manta ray does not warrant listing under the ESA at this time.

Federal Register, Volume 82 Issue 8 (Thursday, January 12, 2017)
[Federal Register Volume 82, Number 8 (Thursday, January 12, 2017)]
[Proposed Rules]
[Pages 3694-3715]
From the Federal Register Online  [www.thefederalregister.org]
[FR Doc No: 2017-00370]


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DEPARTMENT OF COMMERCE

National Oceanic and Atmospheric Administration

50 CFR Part 223

[Docket No. 160105011-6999-02]
RIN 0648-XE390


12-Month Finding on a Petition To List Giant and Reef Manta Rays 
as Threatened or Endangered Under the Endangered Species Act

AGENCY: National Marine Fisheries Service (NMFS), National Oceanic and 
Atmospheric Administration (NOAA), Commerce.

ACTION: Proposed rule; 12-month petition finding; request for comments.

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SUMMARY: We, NMFS, announce a 12-month finding on a petition to list 
the giant manta ray (Manta birostris) and reef manta ray (Manta 
alfredi) as threatened or endangered under the Endangered Species Act 
(ESA). We have completed a comprehensive status review of both species 
in response to this petition. Based on the best scientific and 
commercial information available, including the status review report 
(Miller and Klimovich 2016), and after taking into account efforts 
being made to protect these species, we have determined that the giant 
manta ray (M. birostris) is likely to become an endangered species 
within the foreseeable future throughout a significant portion of its 
range. Therefore, we propose to list the giant manta ray as a 
threatened species under the ESA. Any protective regulations determined 
to be necessary and advisable for the conservation of the proposed 
threatened giant manta ray under ESA section 4(d) would be proposed in 
a subsequent Federal Register announcement. Should the proposed listing 
be finalized, we would also designate critical habitat for the species, 
to the maximum extent prudent and determinable. We solicit information 
to assist this proposed listing determination, the development of 
proposed protective regulations, and

[[Page 3695]]

designation of critical habitat in the event the proposed threatened 
listing for the giant manta ray is finalized. Additionally, we have 
determined that the reef manta ray (M. alfredi) is not currently in 
danger of extinction throughout all or a significant portion of its 
range and is not likely to become so within the foreseeable future. 
Therefore, we find that the reef manta ray does not warrant listing 
under the ESA at this time.

DATES: Comments on the proposed rule to list the giant manta ray must 
be received by March 13, 2017. Public hearing requests must be made by 
February 27, 2017.

ADDRESSES: You may submit comments on this document, identified by 
NOAA-NMFS-2016-0014, by either of the following methods:
     Electronic Submissions: Submit all electronic public 
comments via the Federal eRulemaking Portal. Go to www.regulations.gov/#!docketDetail;D=NOAA-NMFS-2016-0014. Click the ``Comment Now'' icon, 
complete the required fields, and enter or attach your comments.
     Mail: Submit written comments to Maggie Miller, NMFS 
Office of Protected Resources (F/PR3), 1315 East West Highway, Silver 
Spring, MD 20910, USA.
    Instructions: Comments sent by any other method, to any other 
address or individual, or received after the end of the comment period, 
may not be considered by NMFS. All comments received are a part of the 
public record and will generally be posted for public viewing on 
www.regulations.gov without change. All personally identifying 
information (e.g., name, address, etc.), confidential business 
information, or otherwise sensitive information submitted voluntarily 
by the sender will be publicly accessible. NMFS will accept anonymous 
comments (enter ``N/A'' in the required fields if you wish to remain 
anonymous).
    You can find the petition, status review report, Federal Register 
notices, and the list of references electronically on our Web site at 
www.fisheries.noaa.gov/pr/species/fish/manta-ray.html.

FOR FURTHER INFORMATION CONTACT: Maggie Miller, NMFS, Office of 
Protected Resources, (301) 427-8403.

SUPPLEMENTARY INFORMATION: 

Background

    On November 10, 2015, we received a petition from Defenders of 
Wildlife to list the giant manta ray (M. birostris), reef manta ray (M. 
alfredi) and Caribbean manta ray (M. c.f. birostris) as threatened or 
endangered under the ESA throughout their respective ranges, or, as an 
alternative, to list any identified distinct population segments (DPSs) 
as threatened or endangered. The petitioners also requested that 
critical habitat be designated concurrently with listing under the ESA. 
On February 23, 2016, we published a positive 90-day finding (81 FR 
8874) announcing that the petition presented substantial scientific or 
commercial information indicating that the petitioned action may be 
warranted for the giant manta ray and reef manta ray, but that the 
Caribbean manta ray is not a taxonomically valid species or subspecies 
for listing, and explained the basis for that finding. We also 
announced the initiation of a status review of the giant manta ray and 
reef manta ray, as required by section 4(b)(3)(a) of the ESA, and 
requested information to inform the agency's decision on whether these 
species warrant listing as endangered or threatened under the ESA.

Listing Species Under the Endangered Species Act

    We are responsible for determining whether giant and reef manta 
rays are threatened or endangered under the ESA (16 U.S.C. 1531 et 
seq.). To make this determination, we first consider whether a group of 
organisms constitutes a ``species'' under section 3 of the ESA, then 
whether the status of the species qualifies it for listing as either 
threatened or endangered. Section 3 of the ESA defines species to 
include ``any subspecies of fish or wildlife or plants, and any 
distinct population segment of any species of vertebrate fish or 
wildlife which interbreeds when mature.'' On February 7, 1996, NMFS and 
the U.S. Fish and Wildlife Service (USFWS; together, the Services) 
adopted a policy describing what constitutes a DPS of a taxonomic 
species (61 FR 4722). The joint DPS policy identified two elements that 
must be considered when identifying a DPS: (1) The discreteness of the 
population segment in relation to the remainder of the species (or 
subspecies) to which it belongs; and (2) the significance of the 
population segment to the remainder of the species (or subspecies) to 
which it belongs.
    Section 3 of the ESA defines an endangered species as ``any species 
which is in danger of extinction throughout all or a significant 
portion of its range'' and a threatened species as one ``which is 
likely to become an endangered species within the foreseeable future 
throughout all or a significant portion of its range.'' Thus, in the 
context of the ESA, the Services interpret an ``endangered species'' to 
be one that is presently at risk of extinction. A ``threatened 
species'' is not currently at risk of extinction, but is likely to 
become so in the foreseeable future. The key statutory difference 
between a threatened and endangered species is the timing of when a 
species may be in danger of extinction, either now (endangered) or in 
the foreseeable future (threatened).
    Additionally, as the definition of ``endangered species'' and 
``threatened species'' makes clear, the determination of extinction 
risk can be based on either assessment of the range wide status of the 
species, or the status of the species in a ``significant portion of its 
range.'' The Services published a final policy to clarify the 
interpretation of the phrase ``significant portion of the range'' in 
the ESA definitions of ``threatened species'' and ``endangered 
species'' (79 FR 37577; July 1, 2014) (SPR Policy). The policy consists 
of the following four components:
    (1) If a species is found to be endangered or threatened in only an 
SPR, and the SPR is not a DPS, the entire species is listed as 
endangered or threatened, respectively, and the ESA's protections apply 
across the species' entire range.
    (2) A portion of the range of a species is ``significant'' if its 
contribution to the viability of the species is so important that 
without that portion, the species would be in danger of extinction or 
likely to become so in the foreseeable future.
    (3) The range of a species is considered to be the general 
geographical area within which that species can be found at the time 
USFWS or NMFS makes any particular status determination. This range 
includes those areas used throughout all or part of the species' life 
cycle, even if they are not used regularly (e.g., seasonal habitats). 
Lost historical range is relevant to the analysis of the status of the 
species, but it cannot constitute an SPR.
    (4) If a species is not endangered or threatened throughout all of 
its range but is endangered or threatened within an SPR, and the 
population in that significant portion is a valid DPS, we will list the 
DPS rather than the entire taxonomic species or subspecies.
    The statute also requires us to determine whether any species is 
endangered or threatened throughout all or a significant portion of its 
range as a result of any one or a combination of the following five 
factors: the present or threatened destruction, modification, or

[[Page 3696]]

curtailment of its habitat or range; overutilization for commercial, 
recreational, scientific, or educational purposes; disease or 
predation; the inadequacy of existing regulatory mechanisms; or other 
natural or manmade factors affecting its continued existence (ESA 
section 4(a)(1)(A)-(E)). Section 4(b)(1)(A) of the ESA requires us to 
make listing determinations based solely on the best scientific and 
commercial data available after conducting a review of the status of 
the species and after taking into account efforts being made by any 
State or foreign nation or political subdivision thereof to protect the 
species. In evaluating the efficacy of existing domestic protective 
efforts, we rely on the Services' joint Policy on Evaluation of 
Conservation Efforts When Making Listing Decisions (``PECE''; 68 FR 
15100; March 28, 2003) for any conservation efforts that have not been 
implemented, or have been implemented but not yet demonstrated 
effectiveness.

Status Review

    A NMFS biologist in the Office of Protected Resources led the 
status review for the giant manta ray and reef manta ray (Miller and 
Klimovich 2016). The status review examined both species' statuses 
throughout their respective ranges and also evaluated if any portion of 
their range was significant as defined by the Services' SPR Policy (79 
FR 37578; July 1, 2014).
    In order to complete the status review, information was compiled on 
each species' biology, ecology, life history, threats, and status from 
information contained in the petition, our files, a comprehensive 
literature search, and consultation with experts. We also considered 
information submitted by the public in response to our petition 
finding. In assessing the extinction risk of both species, we 
considered the demographic viability factors developed by McElhany et 
al. (2000). The approach of considering demographic risk factors to 
help frame the consideration of extinction risk has been used in many 
of our status reviews, including for Pacific salmonids, Pacific hake, 
walleye pollock, Pacific cod, Puget Sound rockfishes, Pacific herring, 
scalloped, great, and smooth hammerhead sharks, and black abalone (see 
www.nmfs.noaa.gov/pr/species/ for links to these reviews). In this 
approach, the collective condition of individual populations is 
considered at the species level according to four viable population 
descriptors: abundance, growth rate/productivity, spatial structure/
connectivity, and diversity. These viable population descriptors 
reflect concepts that are well-founded in conservation biology and that 
individually and collectively provide strong indicators of extinction 
risk (NMFS 2015).
    The draft status review report was subjected to independent peer 
review as required by the Office of Management and Budget (OMB) Final 
Information Quality Bulletin for Peer Review (M-05-03; December 16, 
2004). The draft status review report was peer reviewed by independent 
specialists selected from the academic and scientific community, with 
expertise in manta ray biology, conservation, and management. The peer 
reviewers were asked to evaluate the adequacy, appropriateness, and 
application of data used in the status review, including the extinction 
risk analysis. All peer reviewer comments were addressed prior to 
dissemination and finalization of the draft status review report and 
publication of this finding.
    We subsequently reviewed the status review report, its cited 
references, and peer review comments, and believe the status review 
report, upon which this 12-month finding and proposed rule is based, 
provides the best available scientific and commercial information on 
the two manta ray species. Much of the information discussed below on 
manta ray biology, distribution, abundance, threats, and extinction 
risk is attributable to the status review report. However, in making 
the 12-month finding determination and proposed rule, we have 
independently applied the statutory provisions of the ESA, including 
evaluation of the factors set forth in section 4(a)(1)(A)-(E) and our 
regulations regarding listing determinations. The status review report 
is available on our Web site (see ADDRESSES section) and the peer 
review report is available at http://www.cio.noaa.gov/services_programs/prplans/PRsummaries.html. Below is a summary of the 
information from the status review report and our analysis of the 
status of the giant manta ray and reef manta ray. Further details can 
be found in Miller and Klimovich (2016).

Description, Life History, and Ecology of the Petitioned Species

Species Description

    Manta rays are large bodied, planktivorous rays, considered part of 
the Mobulidae subfamily that appears to have diverged from Rhinoptera 
around 30 million years ago (Poortvliet et al. 2015). Manta species are 
distinguished from other Mobula rays in that they tend to be larger, 
with a terminal mouth, and have long cephalic fins (Evgeny 2010). The 
genus Manta has a long and convoluted taxonomic history due partially 
to the difficulty of preserving such large specimens and conflicting 
historical reports of taxonomic characteristics (Couturier et al. 2012; 
Kitchen-Wheeler 2013). All manta rays were historically categorized as 
Manta birostris, but Marshall et al. (2009) presented new data that 
supported the splitting of the monospecific Manta genus into two 
species: M. birostris and M. alfredi.
    Both Manta species have diamond-shaped bodies with wing-like 
pectoral fins; the distance over this wingspan is termed disc width 
(DW). There are two distinct color types in both species: chevron and 
black (melanistic). Most of the chevron variants have a black dorsal 
surface and a white ventral surface with distinct patterns on the 
underside that can be used to identify individuals (Marshall et al. 
2008; Kitchen-Wheeler 2010; Deakos et al. 2011). While these markings 
are assumed to be permanent, there is some evidence that the 
pigmentation pattern of M. birostris may actually change over the 
course of development (based on observation of two individuals in 
captivity), and thus caution may be warranted when using color markings 
for identification purposes in the wild (Ari 2015). The black color 
variants of both species are entirely black on the dorsal side and 
almost completely black on the ventral side, except for areas between 
the gill-slits and the abdominal area below the gill-slits (Kitchen-
Wheeler 2013).

Range, Distribution and Habitat Use

    Manta rays are circumglobal in range, but within this broad 
distribution, individual populations are scattered and highly 
fragmented (CITES 2013). The ranges of the two manta species sometimes 
overlap; however, at a finer spatial scale, the two species generally 
appear to be allopatric within those habitat areas (Kashiwagi et al. 
2011) and exhibit different habitat use and movement patterns (inshore 
versus offshore reef habitat use) (Marshall and Bennett 2010b; 
Kashiwagi et al. 2011). Clark (2010) suggests that the larger M. 
birostris may forage in less productive pelagic waters and conduct 
seasonal migrations following prey abundance, whereas M. alfredi is 
more of a resident species in areas with regular coastal productivity 
and predictable prey abundance. Kashiwagi et al. (2010) observed that 
even in areas where both species are found in large numbers at the same 
feeding and cleaning sites, the two species do not interact with each 
other (e.g., they are not part of the same feeding group, and males of 
one species

[[Page 3697]]

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

Diet and Feeding

    As previously mentioned, manta feeding habits appear to be 
influenced by the movement and accumulation of zooplankton (Armstrong 
et al. 2016). Both manta species primarily feed on planktonic organisms 
such as euphausiids, copepods, mysids, decapod larvae and shrimp, but 
some studies have noted their consumption of small and moderate sized 
fishes as well (Bertolini 1933; Bigelow and Schroeder 1953; Carpenter 
and Niem 2001; The Hawaii Association for Marine Education and Research 
Inc. 2005). Mantas appear to be primarily nocturnal feeders, consistent 
with the upward migration of zooplankton at night, increasing their 
accessibility (Cushing 1951; Forward 1988). Known manta feeding areas 
that have been reported in the literature are summarized in Table 1 of 
Miller and Klimovich (2016); however, it is likely that additional 
feeding areas exist throughout both species' respective ranges.

[[Page 3698]]

Growth and Reproduction

    Manta rays are viviparous (i.e., give birth to live young), with a 
gestation period of around one year (Matsumoto and Uchida 2008; Uchida 
et al. 2008), and a reproductive periodicity of anywhere from 1 to 5 
years (see Table 3 in Miller and Klimovich (2016)). Generally, not much 
is known about manta ray growth and development. Free swimming wild 
mantas have been observed as small as 1.02 m DW and 1.22 m DW (Kitchen-
Wheeler 2013), with size at birth estimates ranging from 0.9 m DW to 
1.92 m DW (see Tables 2 and 3 in Miller and Klimovich (2016)); however, 
the lack of observations of small manta rays throughout the species' 
respective ranges may indicate that manta rays segregate by size, with 
different habitats potentially used by neonates and juveniles (Deakos 
2010b). While these habitats have yet to be identified, Erdmann (2014) 
presents a hypothesis, based on tagging data of a juvenile M. alfredi 
(~1.5m DW), that mantas likely give birth in protected areas, such as 
lagoons, that provide protection from larger predators.
    In M. alfredi, Deakos (2012) observed that sexual maturity was 
delayed until growth had reached 90 percent of maximum size, pointing 
to large body size providing a reproductive advantage. Deakos (2010) 
concluded that the minimum size at sexual maturity was 3.37 DW for 
female M. alfredi and 2.80 m DW for males in Maui. There is no evidence 
that male size affects mating success of M. alfredi in any way, but 
larger females were observed to have higher rates of pregnancy than 
smaller females (Deakos 2012). Homma et al. (1999) hypothesized that 
age at sexual maturity was 8-13 years in mantas and the data of Uchida 
et al. (2008), Marshall et al. (2011a) and Marshall and Bennett (2010b) 
confirmed this estimate. However, a population of female M. alfredi in 
the Maldives displayed late maturity (15 years or more) and lower 
reproductive rates than previously reported (one pup every five years, 
instead of biennially) (G. Stevens in prep. as cited in CITES (2013)). 
In contrast, Clark (2010) described a rapid transition to maturity for 
M. alfredi in Kona, Hawaii, with estimates of males reaching sexual 
maturity as early as 3-4 years.
    In terms of mating behavior, during courting, manta rays are 
commonly observed engaging in ``mating chains,'' where multiple males 
will pursue a single female. The mating displays can last hours or 
days, with the female swimming rapidly ahead of the males and 
occasionally somersaulting or turning abruptly (Deakos et al. 2011). 
Sexual dimorphism is present in manta rays, with female M. alfredi as 
much as 18 percent larger than males, so it is unlikely that a male 
could force a female to mate against her will (Deakos 2010; Marshall 
and Bennett 2010b). Additionally, males have never been observed to 
compete with each other directly for the attention of the female, so 
these mating chains may function as a kind of endurance rivalry 
(Andersson 1994; Deakos 2012). No copulations have been observed in the 
wild, so it is difficult to determine which males have a mating 
advantage, but this kind of endurance trial usually selects for the 
success of larger males (Andersson and Iwasa 1996; Deakos 2012).
    Although mantas have been reported to live to at least 40 years old 
(Marshall and Bennett 2010b; Marshall et al. 2011b; Kitchen-Wheeler 
2013) with low rates of natural mortality (Couturier et al. 2012), the 
time needed to grow to maturity and the low reproductive rates mean 
that a female will be able to produce only 5-15 pups in her lifetime 
(CITES 2013). Generation time for both species (based on M. alfredi 
life history parameters) is estimated to be 25 years (Marshall et al. 
2011a; Marshall et al. 2011b). Known life history characteristics of M. 
birostris and M. alfredi are summarized in Tables 2 and 3 in Miller and 
Klimovich (2016).

Population Structure

    Since the splitting of the Manta genus, most of the recent research 
has examined the genetic discreteness, phylogeny, and the evolutionary 
speciation in manta rays (Cerutti-Pereyra et al. 2012; Kashiwagi et al. 
2012; Poortvliet et al. 2015). Very few studies have focused on the 
population structure within each species. However, based on genetic 
sampling, photo-identification, and tracking studies, preliminary 
results tend to indicate that reef manta rays exist in isolated and 
potentially genetically divergent populations. For example, using 
genetic sequencing of mitochondrial DNA (which is maternally-inherited) 
Cerutti-Pereyra et al. (2012) found low genetic divergence (<1 percent) 
but ``phylogeographic disjunction'' between the M. alfredi samples from 
Australia (n = 2; Ningaloo Reef) and Indonesia (n = 2), suggesting 
biogeographic factors may be responsible for population differentiation 
within the species. Although based on very few samples (4 total), these 
findings are consistent with photo-identification and tracking studies, 
which suggest high site-fidelity and residency for M. alfredi in many 
portions of its range, including Indonesia, Ningaloo Reef, Hawaii, 
Fiji, New Caledonia, and eastern Australia (Dewar et al. 2008; Clark 
2010; Couturier et al. 2011; Deakos et al. 2011; Cerutti-Pereyra et al. 
2012; Couturier et al. 2014).
    The population structure for the wider-ranging M. birostris is less 
clear. While Clark (2010), using photo-identification survey data 
collected between 1992 and 2007 along the Kona, Hawaii, coast, found 
low site-fidelity for M. birostris and high rate of immigration, 
indicative of a population that is pelagic rather than coastal or 
island-associated, Stewart et al. (2016a) provided recent evidence to 
show that the giant manta rays off Pacific Mexico may exist as isolated 
subpopulations, with distinct home ranges. Additionally, researchers 
are presently investigating whether there is a potential third manta 
ray species resident to the Yucat[aacute]n coastal waters of the Gulf 
of Mexico (previously identified as M. birostris) (Hinojosa-Alvarez et 
al. 2016). Using the mitochondrial ND5 region (maternally-inherited 
DNA), Hinojosa-Alvarez et al. (2016) found shared haplotypes between 
Yucat[aacute]n manta ray samples and known M. birostris samples from 
Mozambique, Indonesia, Japan, and Mexico, but discovered four new manta 
ray haplotypes, exclusive to the Yucat[aacute]n samples. While analysis 
using the nuclear RAG1 gene (bi-parentally-inherited DNA) showed the 
Yucat[aacute]n samples to be consistent with identified M. birostris 
samples, the authors suggest that the ND5 genetic evidence indicates 
the potential for a third, distinctive manta genetic group or possibly 
M. birostris subspecies. At this time, additional studies, including 
in-depth taxonomic studies and additional genetic sampling, are needed 
to better understand the population structure of both species 
throughout their respective ranges.

Population Demographics

    Given their large sizes, manta rays are assumed to have fairly high 
survival rates after maturity (e.g., low natural predation rates). 
Using estimates of known life history parameters for both giant and 
reef manta rays, and plausible range estimates for the unknown life 
history parameters, Dulvy et al. (2014) calculated a maximum population 
growth rate of Manta spp. and found it to be one of the lowest values 
when compared to 106 other shark and ray species. After taking into 
consideration different model assumptions, and the criteria for 
assessing productivity in Musick (1999), Dulvy et al. (2014) estimated 
realized productivity (r) for manta rays to be 0.029 (Dulvy et al.

[[Page 3699]]

2014). This value is similar to the productivity estimate from 
Kashiwagi (2014) who empirically determined an r value of 0.023 using 
capture-mark-recapture analyses. Ward-Paige et al. (2013) calculated 
slightly higher estimates for the intrinsic rate of population 
increase, with r = 0.05 for M. alfredi and r = 0.042 for M. birostris; 
however, these estimates still place both manta ray species into or at 
the very edge of the ``very low'' productivity category (r <0.05), 
based on the productivity parameters and criteria in Musick (1999).
    In order to determine how changes in survival may affect 
populations, Smallegange et al. (2016) modeled the demographics of reef 
manta rays. Results showed that increases in yearling or adult annual 
survival rates resulted in much greater responses in population growth 
rates, mean lifetime reproductive success, and cohort generation time 
compared to similar increases in juvenile annual survival rates 
(Smallegange et al. 2016). Based on the elasticity analysis, population 
growth rate was most sensitive to changes in the survival rate of 
adults (Smallegange et al. 2016). In other words, in order to prevent 
populations from declining further, Smallegange et al. (2016) found 
that adult survival rates should be increased, such as through 
protection of adult aggregation sites or a reduction in fishing of 
adult manta rays (Smallegange et al. 2016). For those populations that 
are currently stable, like the Yaeyama Islands (Japan) population 
(where adult annual survival rate is estimated at 0.95; noted above), 
Smallegange et al. (2016) note that any changes in adult survival may 
significantly affect the population.
    Overall, given their life history traits and productivity 
estimates, particularly their low reproductive output and sensitivity 
to changes in adult survival rates, giant and reef manta ray 
populations are inherently vulnerable to depletions, with low 
likelihood of recovery.

Historical and Current Distribution and Population Abundance

    There are no current or historical estimates of the global 
abundance of M. birostris. Despite their larger range, they are 
encountered with less frequency than M. alfredi. Most estimates of 
subpopulations are based on anecdotal diver or fisherman observations, 
which are subject to bias. These populations seem to potentially range 
from around 100 to1,500 individuals (see Table 4 in Miller and 
Klimovich (2016)). In the proposal to include manta rays on the 
appendices of the Convention on International Trade in Endangered 
Species of Wild Fauna and Flora (CITES), it states that because 10 
populations of M. birostris have been actively studied, 25 other 
aggregations have been anecdotally identified, and all other sightings 
are rare, the total global population may be small (CITES 2013). The 
greatest number of M. birostris identified in the four largest known 
aggregation sites ranges from 180 to 1,500. Ecuador is thought to be 
home to the largest identified population of M. birostris in the world, 
with large aggregation sites within the waters of the Machalilla 
National Park and the Galapagos Marine Reserve (Hearn et al. 2014). 
Within the Indian Ocean, numbers of giant manta rays identified through 
citizen science in Thailand's waters (primarily on the west coast, off 
Khao Lak and Koh Lanta) have been increasing over the past few years, 
from 108 in 2015 to 288 in 2016. These numbers reportedly surpass the 
estimate of identified giant mantas in Mozambique (n = 254), possibly 
indicating that Thailand may be home to the largest aggregation of 
giant manta rays within the Indian Ocean (MantaMatcher 2016). In the 
Atlantic, very little information on M. birostris populations is 
available, but there is a known, protected population within the Flower 
Garden Banks National Marine Sanctuary in the Gulf of Mexico. However, 
researchers are still trying to determine whether the manta rays in 
this area are only M. birostris individuals or potentially also 
comprise individuals of a new, undescribed species (Marshall et al. 
2009; Hinojosa-Alvarez et al. 2016).
    In areas where the species is not subject to fishing, populations 
may be stable. For example, Rohner et al. (2013) report that giant 
manta ray sightings remained constant off the coast of Mozambique over 
a period of 8 years. However, in regions where giant manta rays are (or 
were) actively targeted or caught as bycatch, such as the Philippines, 
Mexico, Sri Lanka, and Indonesia, populations appear to be decreasing 
(see Table 5 in Miller and Klimovich (2016)). In Indonesia, declines in 
manta ray landings are estimated to be on the order of 71 to 95 
percent, with potential extirpations noted in certain areas (Lewis et 
al. 2015). Given the migratory nature of the species, population 
declines in waters where mantas are protected have also been observed 
but attributed to overfishing of the species in adjacent areas within 
its large home range. For example, White et al. (2015) provide evidence 
of a substantial decline in the M. birostris population in Cocos Island 
National Park, Costa Rica, where protections for the species have 
existed for over 20 years. Using a standardized time series of 
observations collected by dive masters on 27,527 dives conducted from 
1993 to 2013, giant manta ray relative abundance declined by 
approximately 89 percent. Based on the frequency of the species' 
presence on dives (4 percent), with a maximum of 15 individuals 
observed on a single dive, the authors suggest that Cocos Island may 
not be a large aggregating spot for the species, and suggest that the 
decline observed in the population is likely due to overfishing of the 
species outside of the National Park (White et al. 2015).
    Given that all manta rays were identified as M. birostris prior to 
2009, information on the historical abundance and distribution of M. 
alfredi is scarce. In the proposal to include the reef manta ray on the 
appendices of the Convention on the Conservation of Migratory Species 
of Wild Animals (CMS), it states that current global population numbers 
are unknown and no historical baseline data exist (CMS 2014). Local 
populations of M. alfredi have not been well assessed either, but 
appear generally to be small, sparsely distributed, and isolated. 
Photo-identification studies in Hawaii, Yap, Japan, Indonesia, and the 
eastern coast of Australia suggest these subpopulations range from 100 
to 350 individuals (see Table 6 in Miller and Klimovich (2016)), 
despite observational periods that span multiple decades. However, in 
the Maldives, population estimates range from 3,300 to 9,677 
individuals throughout the 26 atolls in the archipelago (Kitchen-
Wheeler et al. 2012; CITES 2013; CMS 2014), making it the largest 
identified population of M. alfredi in the world. Other larger 
populations may exist off southern Mozambique (superpopulation estimate 
of 802-890 individuals; Rohner et al. (2013); CITES (2013)) and Western 
Australia (metapopulation estimate = 1,200-1,500; McGregor (2009) cited 
in CITES (2013)).
    In terms of trends, studies report that the rate of population 
reduction appears to be high in local areas, from 50-88 percent, with 
areas of potential local extirpations of M. alfredi populations (Homma 
et al. 1999; Rohner et al. 2013; Lewis et al. 2015). In the portions of 
range where reef manta rays are experiencing anthropogenic pressures, 
including Indonesia and Mozambique, encounter rates have dropped 
significantly over the last 5 to 10 years (CMS 2014). However, where M. 
alfredi receives some kind of protection, such as in Australia, Hawaii, 
Guam, Japan,

[[Page 3700]]

the Maldives, Palau, and Yap, CITES (2013) reports that subpopulations 
are likely to be stable. For example, in Hawaii, based on photo-
identification survey data collected between 1992 and 2007 along the 
Kona Coast, Clark (2010) used a discovery curve to estimate that an 
average of 4.27 new pups were entering the population per year. Off the 
Yaeyama Islands, Japan, Kashiwagi (2014) conducted quantitative 
analyses using encounter records, biological observations, and photo-ID 
of manta rays over the period of 1987 to 2009 and found that the 
apparent population size increased steadily but slowly over the 23-year 
period, with a population growth rate estimate of 1.02-1.03. Based on 
aerial surveys of Guam conducted from 1963 to 2012, manta ray 
observations were infrequent but showed an increase over the study 
period (Martin et al. 2015). Off Lady Elliott Island, Australia, 
Couturier et al. (2014) modeled annual population sizes of M. alfredi 
from 2009 to 2012 and found an annual increase in abundance for both 
sexes, but cautioned that the modeled increase could be an artifact of 
improvements in photo-identification by observers over the study 
period. Within Ningaloo Marine Park, the status of reef manta rays was 
assessed as ``Good'' in 2013, but with low confidence in the ratings 
(Marine Parks & Reserves Authority 2013). Overall, however, the reef 
manta ray population of Australia is deemed to be one of the world's 
healthiest (Australian Government 2012).

Species Finding

    Based on the best available scientific and commercial information 
described above, we find that M. birostris and M. alfredi are currently 
considered taxonomically-distinct species and, therefore, meet the 
definition of ``species'' pursuant to section 3 of the ESA. Below, we 
evaluate whether these species warrant listing as endangered or 
threatened under the ESA throughout all or a significant portion of 
their respective range.

Summary of Factors Affecting Giant and Reef Manta Rays

    As described above, section 4(a)(1) of the ESA and NMFS' 
implementing regulations (50 CFR 424.11(c)) state that we must 
determine whether a species is endangered or threatened because of any 
one or a combination of the following factors: The present or 
threatened destruction, modification, or curtailment of its habitat or 
range; overutilization for commercial, recreational, scientific, or 
educational purposes; disease or predation; inadequacy of existing 
regulatory mechanisms; or other natural or man-made factors affecting 
its continued existence. We evaluated whether and the extent to which 
each of the foregoing factors contribute to the overall extinction risk 
of both manta ray species, with a ``significant'' contribution defined, 
for purposes of this evaluation, as increasing the risk to such a 
degree that the factor affects the species' demographics (i.e., 
abundance, productivity, spatial structure, diversity) either to the 
point where the species is strongly influenced by stochastic or 
depensatory processes or is on a trajectory toward this point. This 
section briefly summarizes our findings and conclusions regarding 
threats to the giant and reef manta rays and their impact on the 
overall extinction risk of the species. More details can be found in 
the status review report (Miller and Klimovich 2016).

The Present or Threatened Destruction, Modification, or Curtailment of 
Its Habitat or Range

    Due to their association with nearshore habitats, manta rays are at 
elevated risk for exposure to a variety of contaminants and pollutants, 
including brevotoxins, heavy metals, polychlorinated biphenyls, and 
plastics. Many pollutants in the environment have the ability to 
bioaccumulate in fish species; however, only a few studies have 
specifically examined the accumulation of heavy metals in the tissues 
of manta rays (Essumang 2010; Ooi et al. 2015), with findings that 
discuss human health risks from the consumption of manta rays. For 
example, Essumang (2010) found platinum levels within M. birostris 
samples taken off the coast of Ghana that exceeded the United Kingdom 
(UK) dietary intake recommendation levels, and Ooi et al. (2015) 
reported concentrations of lead in M. alfredi tissues from Lady Elliot 
Island, Australia, that exceeded maximum allowable level 
recommendations for fish consumption per the European Commission and 
the Codex Alimentarius Commission (WHO/FAO). While consuming manta rays 
may potentially pose a health risk to humans, there is no information 
on the lethal concentration limits of these metals or other toxins in 
manta rays. Additionally, at this time, there is no evidence to suggest 
that current concentrations of these environmental pollutants are 
causing detrimental physiological effects to the point where either 
species may be at an increased risk of extinction.
    Plastics within the marine environment may also be a threat to the 
manta ray species, as the animals may ingest microplastics (through 
filter-feeding) or become entangled in plastic debris, potentially 
contributing to increased mortality rates. Jambeck et al. (2015) found 
that the Western and Indo-Pacific regions are responsible for the 
majority of plastic waste. These areas also happen to overlap with some 
of the largest known aggregations for manta rays. For example, in 
Thailand, where recent sightings data have identified over 288 giant 
manta rays (MantaMatcher 2016), mismanaged plastic waste is estimated 
to be on the order of 1.03 million tonnes annually, with up to 40 
percent of this entering the marine environment (Jambeck et al. 2015). 
Approximately 1.6 million tonnes of mismanaged plastic waste is being 
disposed of in Sri Lanka, again with up to 40 percent entering the 
marine environment (Jambeck et al. 2015), potentially polluting the 
habitat used by the nearby Maldives aggregation of manta rays. While 
the ingestion of plastics is likely to negatively impact the health of 
the species, the levels of microplastics in manta ray feeding grounds 
and frequency of ingestion are presently being studied to evaluate the 
impact on these species (Germanov 2015b; Germanov 2015a).
    Because manta rays are migratory and considered ecologically 
flexible (e.g., low habitat specificity), they may be less vulnerable 
to the impacts of climate change compared to other sharks and rays 
(Chin et al. 2010). However, as manta rays frequently rely on coral 
reef habitat for important life history functions (e.g., feeding, 
cleaning) and depend on planktonic food resources for nourishment, both 
of which are highly sensitive to environmental changes (Brainard et al. 
2011; Guinder and Molinero 2013), climate change is likely to have an 
impact on the distribution and behavior of both M. birostris and M. 
alfredi. Currently, coral reef degradation from anthropogenic causes, 
particularly climate change, is projected to increase through the 
future. Specifically, annual, globally averaged surface ocean 
temperatures are projected to increase by approximately 0.7 [deg]C by 
2030 and 1.4 [deg]C by 2060 compared to the 1986-2005 average (IPCC 
2013), with the latest climate models predicting annual coral bleaching 
for almost all reefs by 2050 (Heron et al. 2016). As declines in coral 
cover have been shown to result in changes in coral reef fish 
communities (Jones et al. 2004; Graham et al. 2008), the projected 
increase in coral habitat degradation may potentially lead to a

[[Page 3701]]

decrease in the abundance of manta ray cleaning fish (e.g., Labroides 
spp., Thalassoma spp., and Chaetodon spp.) and an overall reduction in 
the number of cleaning stations available to manta rays within these 
habitats. This potential decreased access to cleaning stations may 
negatively impact the fitness of the mantas by hindering their ability 
to reduce parasitic loads and dead tissue, which could lead to 
increases in diseases and declines in reproductive fitness and survival 
rates. However, these scenarios are currently speculative, as there is 
insufficient information to indicate how and to what extent changes in 
reef community structure will affect the status of both manta ray 
species.
    Changes in climate and oceanographic conditions, such as 
acidification, are also known to affect zooplankton structure (size, 
composition, diversity), phenology, and distribution (Guinder and 
Molinero 2013). As such, the migration paths and locations of both 
resident and seasonal aggregations of manta rays, which depend on these 
animals for food, may similarly be altered (Australian Government 2012; 
Couturier et al. 2012). It is likely that those M. alfredi populations 
that exhibit site-fidelity behavior will be most affected by these 
changes. For example, resident manta ray populations may be forced to 
travel farther to find available food or randomly search for new 
productive areas (Australian Government 2012; Couturier et al. 2012). 
As research to understand the exact impacts of climate change on marine 
phytoplankton and zooplankton communities is still ongoing, the 
severity of this threat to both species of manta rays has yet to be 
fully determined.

Overutilization for Commercial, Recreational, Scientific or Educational 
Purposes

    Manta rays are both targeted and caught as bycatch in fisheries 
worldwide. In fact, according to Lawson et al. (2016), manta ray 
catches have been recorded in at least 30 large and small-scale 
fisheries covering 25 countries. The majority of fisheries that target 
mobulids are artisanal (Croll et al. 2015) and target the rays for 
their meat; however, since the 1990s, a market for mobulid gill rakers 
has significantly expanded, increasing the demand for manta ray 
products, particularly in China. The gill rakers of mobulids are used 
in Asian medicine and are thought to have healing properties, such as 
curing diseases from chicken pox to cancer, boosting the immune system, 
purifing the body, enhancing blood circulation, remedying throat and 
skin ailments, curing male kidney issues, and helping with fertility 
problems (Heinrichs et al. 2011). The use of gill rakers as a remedy, 
which was widespread in Southern China many years ago, has recently 
gained renewed popularity over the past decade as traders have 
increased efforts to market its healing and immune boosting properties 
directly to consumers (Heinrichs et al. 2011). As a result, demand has 
significantly increased, incentivizing fishermen who once avoided 
capture of manta rays to directly target these species (Heinrichs et 
al. 2011; CITES 2013). According to Heinrichs et al. (2011), it is 
primarily the older population in Southern China as well as Macau, 
Singapore, and Hong Kong, that ascribes to the belief of the healing 
properties of the gill rakers; however, unlike products like shark 
fins, the gill rakers are not considered ``traditional'' or 
``prestigious'' items and many consumers and sellers are not even aware 
that gill rakers come from manta or mobula rays. Meat, cartilage, and 
skin of manta rays are also utilized, but valued significantly less 
than the gill rakers, and usually enter local trade or are kept for 
domestic consumption (Heinrichs et al. 2011; CITES 2013). Indonesia, 
Sri Lanka, and India presently represent the largest manta ray 
exporting range state countries; however, Chinese gill plate vendors 
have also reported receiving mobulid gill plates from other countries 
and regions as well, including Malaysia, Vietnam, South Africa, South 
America, the Middle East, and the South China Sea (CMS 2014). To 
examine the impact of this growing demand for gill rakers on manta ray 
populations, information on landings and trends (identified by species 
where available) are evaluated for both fisheries that target mantas 
and those that catch mantas as bycatch.
Targeted Fisheries
    Indonesia is reported to be one of the countries that catch the 
most mobulid rays (Heinrichs et al. 2011). Manta and mobula ray 
fisheries span the majority of the Indonesian archipelago, with most 
landing sites along the Indian Ocean coast of East and West Nusa 
Tenggara and Java (Lewis et al. 2015). Manta rays (presumably M. 
birostris, but identified prior to the split of the genus) have 
traditionally been harvested in Indonesia using harpoons and boats 
powered by paddles or sails, with manta fishing season lasting from May 
through October. Historically, the harvested manta rays would be 
utilized by the village, but the advent of the international gill raker 
market in the 1970s prompted the commercial trade of manta ray 
products, with gill plates generally sent to Bali, Surabaya (East 
Java), Ujung Pandant (Sulawasi), or Jakarta (West Java) for export to 
Hong Kong, Taiwan, Singapore and other places in Asia (Dewar 2002; 
White et al. 2006; Marshall and Conradie 2014). This economic 
incentive, coupled with emerging technological advances (e.g., 
motorized vessels) and an increase in the number of boats in the 
fishery, greatly increased fishing pressure and harvest of manta rays 
in the 1990s and 2000s (Dewar 2002). In Lamakera, Indonesia, one of the 
main landing sites for mobulids, and particularly manta rays, Dewar 
(2002) estimates that the total average harvest of ``mantas'' during 
the 2002 fishing season was 1,500 individuals (range 1,050-2,400), 
which is a significant increase from the estimated historical harvest 
levels of around 200-300 mantas per season. However, Lewis et al. 
(2015) note that this estimate likely represents all mobulid rays, not 
just manta rays.
    However, given these amounts, it is perhaps unsurprising that 
anecdotal reports from fishermen indicate possible local population 
declines, with fishermen noting that they have to travel farther to 
fishing grounds as manta rays are no longer present closer to the 
village (Dewar 2002; Lewis et al. 2015). In fact, using the records 
from Dewar (2002) and community (local) catch records, Lewis et al. 
(2015) show that there has been a steady decline in manta landings at 
Lamakera since 2002 (despite relatively unchanged fishing effort), with 
estimated landings in 2013-2014 comprising only 25 percent of the 
estimated numbers from 2002-2006. These declines in manta landings are 
not just limited to Lamakera, but also appear to be the trend 
throughout Indonesia at the common mobulid landing sites. For example, 
Lewis et al. (2015) reports a 95 percent decline in manta landings in 
Tanjung Luar (between 2001-2005 and 2013-2014), a decrease in the 
average size of mantas being caught, and a 71 percent decline in manta 
landings in the Cilacap gillnet fishery between 2001-2005 and 2014. 
Areas in Indonesia where manta rays have potentially been fished to 
extirpation, based on anecdotal reports (e.g., diver sightings data and 
fishermen interviews), include Lembeh Strait in northeast Sulawesi, 
Selayer Islands in South Sulawesi, and off the west coast of Alor 
Island (which may have been a local M. alfredi population) (Lewis et 
al. 2015).
    Although fishing for manta rays was banned within the Indonesian 
exclusive economic zone (EEZ) in February 2014

[[Page 3702]]

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

[[Page 3703]]

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

[[Page 3704]]

have increased in recent years, particularly on the southwest coast. 
For the years 2003 and 2004, Raje et al. (2007) reported 647 mt of M. 
birostris from the southwest coast of India by the trawl fisheries. In 
a snapshot of the Indian tuna gillnet fishery, Nair et al. (2013) 
documented 5 individuals of M. birostris that were landed by fishermen 
off the coast of Vizhinjam, Kovalam and Colachel over the course of 
only 7 days. On the east coast of India, Raje et al. (2007) documented 
43 mt of M. birostris landed in 2003 and 2004 at the Chennai fishing 
harbor. The apparent increase in landings since the sporadic reports of 
the species in the mid-1990s is likely due to the demand for the 
species' gill rakers, with M. birostris gill plates characterized as 
``First Grade'' and fetching the highest price at auction at the major 
fishing port of Cochin Fisheries Harbour (Nair et al. 2013).
    While Manta spp. are rarely reported in the catch from the western 
Pacific, with Hall and Roman (2013) noting that M. japonica represents 
the most abundant mobulid in the fisheries data, the available 
information still suggests the potential for bycatch mortality and 
indicates declining trends within this region. For example, based on 
observer data from the Western and Central Pacific Fisheries Commission 
(WCPFC) fisheries, M. birostris is observed at a rate of 0.0017 
individuals per associated set and 0.0076 individuals per unassociated 
set in the purse seine fisheries, and at a rate of 0.001-0.003 
individuals per 1,000 hooks in the longline fisheries (Tremblay-Boyer 
and Brouwer 2016). The longline standardized catch-per-unit-effort 
data, while covering observations from only the past decade, indicates 
that M. birostris is observed less frequently in recent years compared 
to 2000-2005 (Tremblay-Boyer and Brouwer 2016). Additionally, a sharp 
decline in the catches of manta rays off Papua New Guinea, where WCPFC 
fishing effort is high, was observed in Papua New Guinea purse seiner 
bycatch in 2005-2006, after a previously steady rise in manta ray 
catches from 1994-2005 (C. Rose pers. comm. cited in Marshall et al. 
2011b).
    In the eastern Pacific, giant manta rays are frequently reported as 
bycatch in the purse seine fisheries; however, identification to 
species level is difficult, and, as such, most manta and mobula ray 
captures are pooled together (Hall and Roman 2013). Based on reported 
M. birostris catch to the Inter-American Tropical Tuna Commission 
(IATTC), including available national observer program data, an average 
of 135 giant manta rays were estimated caught per year from 1993-2015 
in the eastern Pacific purse seine fishery by IATTC vessels (Hall 
unpublished data). While the impact of these bycatch levels on giant 
manta ray populations is uncertain, effort in the fishery appears to 
coincide with high productivity areas, such as the Costa Rica Thermal 
Dome, west of the Galapagos, off the Guayas River estuary (Ecuador), 
and off central and northern Peru, where giant mantas are likely to 
aggregate and have been observed caught in sets (Hall and Roman 2013). 
If effort is concentrated in manta ray aggregation areas, this could 
lead to substantial declines and potential local extirpations of giant 
manta ray populations. Already, evidence of declines in this portion of 
the giant manta ray's range is apparent, with White et al. (2015) 
estimating an 89 percent decline in the relative abundance of M. 
birostris off Cocos Island, Costa Rica. Presently, the largest 
population of M. birostris is thought to reside within the waters of 
the Machalilla National Park and the Galapagos Marine Reserve (Hearn et 
al. 2014); however, given the distribution of purse seine fishing 
effort, and the migratory nature of the species, it is likely that 
individuals from this population are highly susceptible to the purse 
seine fisheries operating in the area.
    Overall, given that the majority of observed declines in landings 
and sightings of manta rays originate from the Indo-Pacific and eastern 
Pacific portions of their range (see Table 5 in Miller and Klimovich 
2016), additional pressure on these species through bycatch mortality 
may have significant negative effects on local populations throughout 
this area. This is particularly a risk for M. birostris, which appears 
to be the species most frequently observed in the fisheries catch and 
bycatch, with this pressure already contributing to declines in the 
species (of up to 95 percent) throughout many areas (i.e., Indonesia, 
Philippines, Sri Lanka, Thailand, Madagascar, Costa Rica). As such, we 
find that current fisheries-related mortality rates are a threat 
significantly contributing to the overutilization of M. birostris 
throughout this portion of its range. Additionally, given the high 
market prices for manta ray gill plates, we find that the practice of 
landing these species as valuable bycatch will likely continue through 
the foreseeable future.

Disease or Predation

    No information has been found to indicate that disease or predation 
is a factor that is significantly and negatively affecting the status 
of manta rays. Manta rays are frequently observed congregating in 
inshore cleaning stations, often associated with coral reefs, where 
small cleaner fish remove parasites and dead tissue from their bodies 
(Marshall and Bennett 2010a; O'Shea et al. 2010; CITES 2013). They may 
remain at these cleaning stations for large periods of time, sometimes 
up to 8 hours a day, and may visit daily (Duinkerken 2010; Kitchen-
Wheeler 2013; Rohner et al. 2013). While there is no information on 
manta ray diseases, or data to indicate that disease is contributing to 
population declines in either species, impacts to these cleaning 
stations (such as potential loss through habitat degradation) may 
negatively impact the fitness of the mantas by decreasing their ability 
to reduce their parasite load. However, at this time, the impact and 
potential loss of cleaning stations is highly speculative.
    In terms of predation, manta rays are frequently sighted with non-
fatal injuries consistent with shark attacks, although the prevalence 
of these sightings varies by location (Homma et al. 1999; Ebert 2003; 
Mourier 2012). For example, Deakos et al. (2011) reported that scars 
from shark predation, mostly on the posterior part of the body or the 
wing tip, were evident in 24 percent of M. alfredi individuals observed 
at a manta ray aggregation site off Maui, Hawaii. At Lady Elliott 
Island, off eastern Australia, Couturier et al. (2014) observed 23 
percent of individuals had shark scars. In contrast, in southern 
Mozambique, between 2003 and 2006, 76.3 percent of the M. alfredi 
identified by Marshall and Bennett (2010a) exhibited shark-inflicted 
bite marks, the majority of which were already healed. Rohner et al. 
(2013) found a lower rate for M. birostris, with only 35 percent of 
individuals observed with bite marks. Marshall and Bennett (2010a) also 
recorded two mid-pregnancy abortions by pregnant female M. alfredi 
attributed to damage from shark attacks. The authors observed that the 
rate of shark-inflicted bites in southern Mozambique appears to be 
higher than predation rates in other manta ray populations, which is 
generally noted at less than five percent (Ito 2000; Kitchen-Wheeler et 
al. 2012), but it is unknown why this difference exists.
    Because the damage from a shark bite usually occurs in the 
posterior region of the manta ray, there may be disfigurement leading 
to difficult clasper insertion during mating or inhibited waste 
excretion (Clark and Papastamatiou 2008). Given the already low 
reproductive ability of these species, attacks by sharks (or 
occasionally killer whales, see Fertl et

[[Page 3705]]

al. (1996) and Visser and Bonoccorso (2003)) may pose a threat to the 
species by further impairing the manta rays' ability to rebuild after 
depletion. However, at this time, the impact of shark bites on manta 
ray reproduction, or predation mortality rates on the status of either 
species, is highly speculative.

The Inadequacy of Existing Regulatory Mechanisms

    Protections for manta rays are increasing, yet there are still a 
number of areas where manta rays are targeted or allowed to be landed 
as bycatch. In fact, only one of the Regional Fishery Management 
Organizations (RFMOs) has prohibited retention of bycaught manta rays. 
Additionally, because both manta species were identified as M. 
birostris prior to 2009, some national protections that were 
implemented before 2009 are specific only to giant manta rays, despite 
both species being present in that nation's waters. Below we provide an 
analysis of the adequacy of measures in terms of controlling threats to 
each species where available data permit. A list of current protections 
for manta rays can be found in the Appendix of Miller and Klimovich 
(2016).
Overutilization of M. birostris
    Based on the available data, M. birostris appears to be most at 
risk of overutilization in the Indo-Pacific and eastern Pacific 
portions of its range. Targeted fishing and incidental capture of the 
species in Indonesia, Philippines, Sri Lanka, and India, and throughout 
the eastern Pacific, has led to observed declines in the M. birostris 
populations. Despite national protections for the species, poor 
enforcement and illegal fishing have essentially rendered the existing 
regulatory mechanisms inadequate to achieve their purpose of protecting 
the giant manta ray from fishing mortality.
    In Indonesia, M. birostris and M. alfredi were provided full 
protection in the nation's waters in 2014 (4/KEPMEN-KP/2014), with the 
creation of the world's largest manta ray sanctuary at around 6 million 
km\2\. Fishing for the species and trade in manta ray parts are banned. 
Despite this prohibition, fishing for manta rays continues, with 
evidence of the species being landed and traded in Indonesian markets 
(AFP 2014; Marshall and Conradie 2014; Dharmadi et al. 2015). As 
mentioned previously (see Overutilization for commercial, recreational, 
scientific, or educational purposes), many fishermen throughout 
Indonesia rely on shark and ray fishing for their livelihoods, and 
without an alternative source of income, are unlikely to stop their 
traditional fishing practices, including the targeting of manta rays. 
Additionally, in interviews with fishermen, many viewed the prohibition 
positively because it would likely drive up the market price of manta 
ray products (Marshall and Conradie 2014). Given the size of the 
Indonesian archipelago, and current resources, Dharmadi et al. (2015) 
note there are many issues with current enforcement of regulations. For 
example, the collection of data is difficult due to insufficient 
fisheries officers trained in species identification and the large 
number of landing sites that need to be monitored (over 1,000). Catch 
data are typically not accurately recorded at the smaller landing sites 
either, with coastal waters heavily fished by artisanal fishermen using 
non-selective gear (Dharmadi et al. 2015). Given the issues with 
enforcement and evidence of illegal fishing, existing regulatory 
mechanisms are inadequate to protect the species from further declines 
due to overutilization.
    In the Philippines, legal protection for manta rays was introduced 
in 1998; however, similar to the situation in Indonesia, enforcement of 
the prohibitions is lacking and illegal fishing of the species is 
evident. For example, in a random sampling of 11 dried products of 
sharks and rays confiscated for illegal trading, Asis et al. (2016) 
found that four of the products could be genetically identified as 
belonging to M. birostris. Dried manta meat and gill rakers were 
frequently observed in markets between 2010 and 2012, and fishing boats 
specifically targeting mobulids (including manta rays) were identified 
in a number of local fishing villages in the Philippines, with landings 
consisting of M. birostris individuals. Fishing for mobulids is a ``way 
of life'' and the primary source of income for many fishermen, and with 
the high prices for manta gill rakers in the Philippine markets (where 
an average manta ray of around 3 m DW could fetch up to $808; Acebes 
and Tull (2016)), it is unlikely that pressure on the species will 
decrease. With essentially no efforts to regulate the mobulid fisheries 
in the Philippines, and a severe lack of enforcement of the current 
manta ray hunting prohibition, current regulations to protect M. 
birostris from overutilization in the Philippines are inadequate.
    In the eastern and central Indian Ocean, very few national 
protections have been implemented for M. birostris. Essentially, 
fishing for the species and retention of bycatch is allowed except 
within the Republic of Maldives EEZ and within specific marine parks of 
Western Australia. Given the declines observed in the species 
throughout the Indian Ocean, and the migratory nature of the animal, 
with the potential for the species to move out of protected areas into 
active fishing zones (e.g., from the Maldives to Sri Lanka--a distance 
of ~820 km, well within the ability of M. birostris), it is likely that 
existing regulatory measures within this portion of the species' range 
are inadequate to protect it from overutilization.
    In the eastern Pacific portion of the species' range, the IATTC 
recently implemented a prohibition on the retention, transshipment, 
storage, landing, and sale of all devil and manta (mobula and manta) 
rays taken in its large-scale fisheries (Resolution C-15-04). This 
regulation went into force on August 1, 2016. Cooperating members must 
report mobulid catch data and ensure safe release; however, developing 
countries were granted an exception for small-scale and artisanal 
fisheries that catch these species for domestic consumption. Given that 
M. birostris is primarily caught as bycatch in the IATTC purse seine 
fisheries, the adequacy of this prohibition in protecting the species 
from overutilization depends on the post-release survival rate of the 
species. While injuries from entanglements in fishing gear (e.g., 
gillnets and longlines) have been noted (Heinrichs et al. 2011), at 
this time, at-vessel and post-release mortality rates for manta rays in 
purse seine nets are unknown. For other Mobula species, Francis and 
Jones (2016) provided preliminary evidence that may indicate a 
potential for significant post-release mortality of the spinetail 
devilray (Mobula japanica) in purse seine fisheries; however, the study 
was based on only seven observed individuals and, because of this, the 
authors caution that it is ``premature to draw conclusions about 
survival rates.'' In fact, based on observer data in the New Zealand 
purse seine fishery, mentioned in Francis and Jones (2016), rays that 
were caught during sets and released were ``usually lively'' and swam 
away from the vessel and judged by the observers as ``likely to 
survive.'' Although decreasing purse seine fishing effort in manta ray 
hotspots would significantly decrease the likelihood of bycatch 
mortality, without further information on post-release survival rates, 
it is highly uncertain if the prohibition will be adequate in 
decreasing the mortality of the species.
    Additionally, in 2016, prohibitions on the fishing and sale of M. 
birostris and requirement for immediate release of mantas caught as 
bycatch were

[[Page 3706]]

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

Other Natural or Man-Made Factors Affecting Its Continued Existence

    Manta rays are known to aggregate in various locations around the 
world, in groups usually ranging from 100-1,000 for M. birostris and 
100-700 for M. alfredi (Notarbartolo-di-Sciara and Hillyer 1989; Graham 
et al. 2012; Venables 2013). These sites function as feeding sites, 
cleaning stations, or sites where courtship interactions take place 
(Heinrichs et al. 2011; Graham et al. 2012; Venables 2013), with the 
appearance of manta rays at these locations generally predictable and 
related to food availability (Notarbartolo-di-Sciara and Hillyer 1989; 
Heinrichs et al. 2011; Jaine et al. 2012). Additionally, manta rays 
exhibit learned behaviors, with diving spots using artificial lights to 
concentrate plankton and attract manta rays (Clark 2010). These 
behavioral traits, including the predictable nature of manta ray 
appearances, combined with their slow swimming speeds, large size, and 
lack of fear towards humans, may increase their vulnerability to other 
threats, such as overfishing, which was previously discussed, and 
tourism (O'Malley et al. 2013; CMS 2014).
    Tourism was identified as a potential threat to the species, given 
that interacting (i.e., swimming) with manta rays is a significant 
tourist attraction throughout the range of both species. In

[[Page 3707]]

fact, O'Malley et al. (2013) estimated that the manta ray tourism 
industry provides $140 million annually in direct revenue or economic 
impact. Regular manta ray concentrations off Mozambique, parts of 
Indonesia, Australia, Philippines, Yap, southern Japan, Hawaii, and 
Mexico have all become tourist attractions where manta dives are common 
(Anderson et al. 2011b). Estimates of the number of people interacting 
with manta rays per year at these popular dive sites are significant, 
ranging from over 10,000 at Ho'ona Bay (Hawaii; Clark (2010)) to at 
least 14,000 in the Maldives (Anderson et al. 2011b).
    While manta ray tourism is far less damaging to the species than 
the impact of fisheries, this increasing demand to see and dive with 
the animals has the potential to lead to other unintended consequences 
that could harm the species. For example, Osada (2010) found that a 
popular manta dive spot in Kona, Hawaii, had fewer emergent zooplankton 
and less diversity compared to a less used dive spot, and attributed 
the difference to potential inadvertent habitat destruction by divers. 
Tour groups may also be engaging in inappropriate behavior, such as 
touching the mantas. Given the increasing demand for manta ray tourism, 
with instances of more than 10 tourism boats present at popular dive 
sites with over 100 divers in the water at once (Anderson et al. 2011b; 
Venables 2013), without proper tourism protocols, these activities 
could have serious consequences for manta ray populations.
    Already, evidence of tourism activities potentially altering manta 
ray behavior has been observed. For example, from 2007-2008, low 
numbers of mantas were observed at normally popular manta dive sites in 
the Maldives while manta ray numbers remained stable at less visited 
sites (Anderson et al. 2011b). Similarly, De Rosemont (2008) noted the 
disappearance of a resident manta ray colony from a popular cleaning 
station in a Bora Bora lagoon in 2005, and attributed the absence to 
new hotel construction and increased tourism activities; however, by 
2007, the author notes that the mantas had returned to the site. In a 
study of the tourism impacts on M. alfredi behavior in Coral Bay, 
Western Australia, Venables (2013) observed that mantas exhibited a 
variety of behavioral changes in response to swim group interactions 
(i.e., their response was different than their behavior prior to the 
approach of the swim group). Although the long-term effects of tourism 
interactions are at this time unknown, the results from the Venables 
(2013) study provide a preliminary estimate of the potentially minimum 
response of the species to interactions with tourists, and indicates 
that these interactions can cause the species to alter (and even stop) 
behaviors that serve critical biological functions (such as feeding and 
cleaning). Additional studies on both the short-term and long-term 
impact of tourist interactions with manta rays are needed in order to 
evaluate if this interaction is a potential threat to the survival of 
the species.
    In addition to tourism activities, another potential threat to both 
manta ray species is an increase in mortality from boat strikes and 
entanglements. Because manta ray aggregation sites are sometimes in 
areas of high maritime traffic (such as Port Santos in Brazil or in the 
Caribbean (Marshall et al. 2011a; Graham et al. 2012)), manta rays are 
at potential risk of being struck and killed by boats. Mooring and boat 
anchor line entanglement may also wound manta rays or cause them to 
drown (Deakos et al. 2011; Heinrichs et al. 2011). For example, in a 
Maui, Hawaii, M. alfredi population (n = 290 individuals), Deakos et 
al. (2011) observed that 1 out of 10 reef manta rays had an amputated 
or disfigured non-functioning cephalic fin, likely a result of line 
entanglement. Internet searches also reveal photographs of mantas with 
injuries consistent with boat strikes and line entanglements, and manta 
researchers report that such injuries may affect manta fitness in a 
significant way (The Hawaii Association for Marine Education and 
Research Inc. 2005; Deakos et al. 2011; Heinrichs et al. 2011; 
Couturier et al. 2012; CMS 2014; Germanov and Marshall 2014; Braun et 
al. 2015), potentially similar to the impacts of shark or orca attacks. 
However, there is very little quantitative information on the frequency 
of these occurrences and no information on the impact of these injuries 
on the overall health of the populations.

Assessment of Extinction Risk

    The ESA (section 3) defines an endangered species as ``any species 
which is in danger of extinction throughout all or a significant 
portion of its range.'' A threatened species is defined as ``any 
species which is likely to become an endangered species within the 
foreseeable future throughout all or a significant portion of its 
range.'' For the term ``foreseeable future,'' we define it as the time 
frame over which identified threats could be reliably predicted to 
impact the biological status of the species. For the assessment of 
extinction risk for both manta ray species, the ``foreseeable future'' 
was considered to extend out several decades (>50 years). Given both 
species' life history traits, with longevity estimated to be greater 
than 20-40 years, maturity ranges from 3 to >15 years, reproductive 
periodicity anywhere from an annual cycle to a 5-year cycle, with a 
litter of only 1 pup, and a generation time estimated to be around 25 
years, it would likely take more than a few decades (i.e., multiple 
generations) for any recent management actions to be realized and 
reflected in population abundance indices. Similarly, the impact of 
present threats to both species could be realized in the form of 
noticeable population declines within this time frame, as demonstrated 
in the very limited available sightings time-series data. As the main 
potential operative threat to the species is overutilization by 
commercial and artisanal fisheries, this time frame would allow for 
reliable predictions regarding the impact of current levels of fishery-
related mortality on the biological status of the two species. 
Additionally, this time frame allows for consideration of the 
previously discussed impacts on manta ray habitat from climate change 
and the potential effects on the status of these two species.
    In determining the extinction risk of a species, it is important to 
consider both the demographic risks facing the species as well as 
current and potential threats that may affect the species' status. To 
this end, a demographic analysis was conducted for the giant manta ray 
and the reef manta ray. A demographic risk analysis is an assessment of 
the manifestation of past threats that have contributed to the species' 
current status and informs the consideration of the biological response 
of the species to present and future threats. This analysis evaluated 
the population viability characteristics and trends available for the 
manta rays, such as abundance, growth rate/productivity, spatial 
structure and connectivity, and diversity, to determine the potential 
risks these demographic factors pose to each species. The information 
from this demographic risk analysis was considered alongside the 
information previously presented on threats to these species, including 
those related to the factors specified by the ESA section 4(a)(1)(A)-
(E) (and summarized in a separate Threats Assessment section below) and 
used to determine an overall risk of extinction for M. birostris and M. 
alfredi. Because species-specific information is sporadic and sometimes

[[Page 3708]]

uncertain (due to the prior lumping of the Manta genus), the 
qualitative reference levels of ``low risk,'' ``moderate risk'' and 
``high risk'' were used to describe the overall assessment of 
extinction risk, with detailed definitions of these risk levels found 
in the status review report (Miller and Klimovich 2016).

Demographic Risk Analysis

Giant Manta Ray

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

Reef Manta Ray

Abundance
    Current and accurate abundance estimates are unavailable for the 
reef manta ray. Observations of individuals in local aggregations range 
from 35 individuals to over 2,400; however, many are on the order of 
100-600 individuals. Subpopulation sizes range from 100 to 350 
individuals, with the exception of the Maldives at 3,300-9,677 
individuals. Meta-population estimates for southern Mozambique and 
Ningaloo Reef, Australia are 802-890 and 1,200-1,500 individuals, 
respectively.
    The rather low subpopulation estimates for M. alfredi throughout 
most of its range suggest that the species may be at increased risk of 
genetic drift and potential loss of genetic variation. Unlike the giant 
manta ray, M. alfredi is thought to be a more resident species, with 
populations that occur year-round at certain sites. This reproductive 
isolation further increases the risk of

[[Page 3709]]

inbreeding depression and potential inability of the population to 
respond to environmental variation or anthropogenic perturbations. For 
example, Kashiwagi (2014) recently estimated the effective population 
size of the M. alfredi population off the Yaeyama Islands to be Ne = 
89, indicating that the population is not part of a large gene pool and 
may be close to a level where viability could be jeopardized in the 
shorter term. Total population was estimated at 165-202 individuals, 
indicating long-term viability vulnerability. With most available 
subpopulation estimates ranging only from 100 to 600 individuals (with 
the exception of Western Australia, Maldives, and Southern Mozambique), 
it is likely that these populations similarly have low effective 
population sizes that may increase their vulnerability to inbreeding 
depression, the loss of genetic variants, or fixation of deleterious 
mutations.
    Overall, based on the information above, the estimates of small and 
isolated subpopulations throughout most of the species' range, with the 
three exceptions off Mozambique, Maldives, and Western Australia, 
inherently place M. alfredi at an increased risk of extinction from 
environmental variation or anthropogenic perturbations. However, the 
trend in overall abundance of M. alfredi is highly uncertain.
Growth Rate/Productivity
    The current net productivity of M. alfredi is unknown due to the 
imprecision or lack of available abundance estimates or indices. 
Fecundity, however, is extremely low, with one to, rarely, two pups per 
litter and a reproductive periodicity of anywhere from 1-5 years. 
Estimated productivity (r) values range from 0.023 to 0.05, indicating 
that the reef manta ray has very low productivity and, thus, is 
extremely susceptible to decreases in its abundance.
    Annual survival rate for reef manta rays is fairly high. Estimated 
survival rates for subpopulations range from 0.95 to 1 off Australia, 
Hawaii, and Japan (Deakos et al. 2011; Couturier et al. 2014; Kashiwagi 
2014). In Mozambique, rates were lower, between 0.6-0.7; however shark 
attacks are also more common in this area (Marshall et al. 2011c). 
Based on modeling work, Smallegange et al. (2016) showed that 
population growth rate was most sensitive to changes in the survival of 
adults.
    Additionally, no changes in demographic or reproductive traits or 
barriers to the exploitation of requisite habitats/niches/etc. have 
been observed.
Spatial Structure/Connectivity
    The reef manta ray is commonly seen inshore near coral and rocky 
reefs. The species is associated with warmer waters (>21 [deg]C) and 
productive nearshore habitats (such as island groups). It is considered 
a more resident species than M. birostris. While the species has been 
tracked undertaking long-distance movements (>700 km), usually to 
exploit offshore productive areas, reef manta rays tend to return to 
known aggregation sites, indicating a degree of site-fidelity. Based on 
photo-identification surveys of the M. alfredi population off Maui, 
Hawaii, Deakos et al. (2011) suggested that geographic barriers, such 
as deep channels, might be barriers to movement between neighboring M. 
alfredi populations. Collectively, this information suggests that gene 
flow is likely limited among populations of M. alfredi, particularly 
those separated by deep ocean expanses.
    With the exception of the Yaeyama, Japan population of M. alfredi, 
which Kashiwagi (2014) hypothesized may be a ``sink'' population but is 
presently increasing with a population growth rate of 1.02-1.03, there 
is no information to indicate that M. alfredi is composed of 
conspicuous source[hyphen]sink populations or habitat patches whose 
loss may pose a risk of extinction.
Diversity
    Given their tendency towards site fidelity, M. alfredi likely 
exists as isolated populations with low rates of dispersal and little 
gene flow among populations. Currently, there is no information to 
suggest that natural processes that cause ecological variation have 
been significantly altered to the point where the species is at risk. 
Reef manta rays also likely have the ability to shift their 
distribution to remain in an environment conducive to their 
physiological and ecological needs, providing the species with 
resilience to these effects. For example, in response to changing 
ecological conditions, like the biannual reversal of monsoon currents, 
reef manta rays will migrate to the downstream side of atolls, 
potentially to remain in nutrient-rich waters year-round (Anderson et 
al. 2011a). Presently, there is no information to suggest that natural 
processes that cause ecological variation have been significantly 
altered to the point where M. alfredi is at risk.

Threats Assessment

Giant Manta Ray

    The most significant and certain threat to the giant manta ray is 
overutilization for commercial purposes. Giant manta rays are both 
targeted and caught as bycatch in a number of global fisheries 
throughout their range. Estimated take of giant manta rays, 
particularly in many portions of the Indo-Pacific, frequently exceeds 
numbers of observed individuals in those areas, and is accompanied by 
observed declines in sightings and landings of the species. Efforts to 
address overutilization of the species through regulatory measures 
appear inadequate, with evidence of targeted fishing of the species 
despite prohibitions (Indo-Pacific; Eastern Pacific) and only one 
regional measure to address bycatch issues, with uncertain 
effectiveness (Eastern Pacific). Additionally, given the migratory and 
pelagic behavior, national protections for the species are less likely 
to adequately protect the species from fisheries-related mortality. 
Giant manta rays are not confined by national boundaries and may, for 
example, lose certain protections as they conduct seasonal migrations 
or even as they move around to feed if they cross particular national 
jurisdictional boundaries (e.g., between the Maldives and Sri Lanka or 
India), move outside of established Marine Protected Areas, or enter 
into high seas. While the species recently has been added to CITES 
Appendix II (added in March 2013 with a delayed effectiveness of 
September 2014), which may curb targeted fishing as countries must 
ensure that manta ray products are legally obtained and trade is 
sustainable, the species is still likely to be caught as bycatch in the 
industrial fisheries and targeted by artisanal fisheries for domestic 
consumption.
    Other threats to M. birostris that potentially contribute to long-
term risk of the species include (micro) plastic ingestion rates, 
increased parasitic loads as a result of climate change effects, and 
potential disruption of important life history functions as a result of 
increased tourism; however, due to the significant data gaps, the 
likelihood and impact of these threats on the status of the species is 
highly uncertain.

Reef Manta Ray

    Given their more inshore distribution and association with shallow 
coral and rocky reefs, M. alfredi does not appear to be as vulnerable 
to commercial and larger-scale artisanal fishing operations as M. 
birostris. These fisheries tend to operate in deeper and more pelagic

[[Page 3710]]

waters, targeting migratory and commercially valuable species (like 
tunas, billfishes, and sharks), and, hence, have a higher likelihood of 
catching giant manta rays. In the available information, only two 
countries are reported to have targeted artisanal fisheries for M. 
alfredi: The Philippines (documented 4 fishing boats) and Mozambique. 
The species has been identified in bycatch from Indonesia, Papua New 
Guinea, and Kiribati, with subsequent observed declines in sightings, 
and potential local extirpations; however, the extent of fishing 
mortality on the species throughout its range is highly uncertain. 
Additionally, the lumping of both species as M. birostris prior to 
2009, as well as the fact that much of the catch is not reported down 
to species level, also significantly contributes to this uncertainty. 
However, based on the data available, many of the identified 
populations of M. alfredi throughout the western and central Pacific 
are currently protected by regulations and appear stable, indicating 
that these existing regulatory measures are adequate at protecting the 
species from declines due to fishing mortality. Within the Indian 
Ocean, national protections exist for the large population of M. 
alfredi off the Maldives, and while specific protections for M. alfredi 
have not been implemented in Western Australia, the species is not 
subject to directed fishing (or prevalent in bycatch) and is presently 
one of the largest identified populations.
    Climate change was identified as a potential threat contributing to 
the long-term extinction risk of the species. Because M. alfredi are 
more commonly associated with coral reefs compared to giant manta rays, 
frequently aggregating within these habitats and showing a high degree 
of site-fidelity and residency to these areas, we found the impact of 
climate change on coral reefs to be a potential risk to the species. 
Although the species itself is not dependent on corals, which are most 
susceptible to the effects of climate change, the manta rays rely on 
the reef community structure, like the abundance of cleaner fish, to 
carry out important functions, such as removing parasite loads and dead 
tissue. Coral reef community structure is likely to be altered as a 
result of increasing events of coral bleaching through the foreseeable 
future; however, what this change will look like and its subsequent 
impact on the species is highly uncertain. Similarly, changes in 
zooplankton communities and distribution, including in and around coral 
reefs, are also likely to occur as a result of climate change, 
affecting the potential previous predictability of M. alfredi food 
resources. Reef manta rays may need to venture out farther to find 
available food or search for new productive areas; however, given that 
the species has been shown capable of making long-distance foraging 
movements, the impact of this potential displacement or change in 
distribution of zooplankton may not be a significant contributor to the 
species' extinction risk.
    Other threats that potentially contribute to long-term risk of the 
species include (micro) plastic ingestion rates, and potential 
disruption of important life history functions or destruction of 
habitat as a result of increased tourism; however, due to the 
significant data gaps, the likelihood and impact of these threats on 
the status of the species is highly uncertain.

Overall Risk Summary

Giant Manta Ray

    Given the extremely low reproductive output and overall 
productivity of the giant manta ray, it is inherently vulnerable to 
threats that would deplete its abundance, with a low likelihood of 
recovery. While there is considerable uncertainty regarding the current 
abundance of M. birostris throughout its range, the best available 
information indicates that the species has experienced population 
declines of potentially significant magnitude within areas of the Indo-
Pacific and eastern Pacific portions of its range, primarily due to 
fisheries-related mortality. Yet, larger subpopulations of the species 
still exist, including off Mozambique (where declines were not 
observed) and Ecuador. However, as giant manta rays are a migratory 
species and continue to face fishing pressure, particularly from the 
industrial purse seine fisheries and artisanal gillnet fisheries 
operating within the Indo-Pacific and eastern Pacific portions of its 
range, overutilization will continue to be a threat to these remaining 
M. birostris populations through the foreseeable future, placing them 
at a moderate risk of extinction.
    While we assume that declining populations within the Indo-Pacific 
and eastern Pacific portions of its range will likely translate to 
overall declines in the species throughout its entire range, there is 
very little information on the abundance, spatial structure, or extent 
of fishery-related mortality of the species within the Atlantic portion 
of its range. As such, we cannot conclude that the species is at a 
moderate risk of extinction throughout its entire range. However, under 
the final Significant Portion of Its Range (SPR) policy, we must 
consider whether the species may be in danger of extinction, or likely 
to become so within the foreseeable future, in a significant portion of 
its range (79 FR 37577; July 1, 2014).
Significant Portion of Its Range (SPR) Analysis
    To identify only those portions that warrant further consideration 
under the SPR Policy, we must determine whether there is substantial 
information indicating that (1) the portions may be significant and (2) 
the species may be in danger of extinction in those portions or likely 
to become so within the foreseeable future. With respect to the second 
of those determinations, as mentioned previously, the best available 
information indicates that the giant manta ray faces concentrated 
threats throughout the Indo-Pacific and eastern Pacific portion of its 
range. Estimated take of giant manta rays is frequently greater than 
the observed individuals in those areas, with observed declines in 
sightings and landings of the species of up to 95 percent. Efforts to 
address overutilization of the species through regulatory measures 
appear inadequate in this portion of its range, with evidence of 
targeted fishing of the species despite prohibitions and bycatch 
measures that may not significantly decrease fisheries-related 
mortality rates of the species. Based on the demographic risks and 
threats to the species in this portion, we determined that the species 
has a moderate risk of extinction in this portion of its range.
    Next, we must evaluate whether this portion is ``significant.'' As 
defined in the SPR Policy, a portion of a species' range is 
``significant'' ``if the species is not currently endangered or 
threatened throughout its range, but the portion's contribution to the 
viability of the species is so important that, without the members in 
that portion, the species would be in danger of extinction, or likely 
to become so in the foreseeable future, throughout all of its range'' 
(79 FR 37578; July 1, 2014). Without the Indo-Pacific and eastern 
Pacific portion of the species' range, the species would have to depend 
on only its members in the Atlantic for survival. While areas 
exhibiting source-sink dynamics, which could affect the survival of the 
species, are not known, the largest subpopulations and records of 
individuals of the species come from the Indo-Pacific and eastern 
Pacific portion. The only data from the Atlantic on the abundance of 
the species are records of >70 individuals in the Flower Garden

[[Page 3711]]

Banks Marine Sanctuary (Gulf of Mexico) and 60 manta rays from waters 
off Brazil (see Table 4 in Miller and Klimovich (2016)). Given that the 
species is rarely identified in the fisheries data in the Atlantic, it 
may be assumed that populations within the Atlantic are small and 
sparsely distributed. These demographic risks, in conjunction with the 
species' inherent vulnerability to depletion, indicate that even low 
levels of mortality may portend drastic declines in the population. As 
such, without the Indo-Pacific and eastern Pacific portion, the minimal 
targeted fishing of the species by artisanal fishermen and bycatch 
mortality from the purse seine, trawl, and longline fisheries operating 
in the Atlantic becomes a significant contributing factor to the 
extinction risk of the species. Based on the above findings, we 
conclude that the Indo-Pacific and eastern Pacific portion of the giant 
manta ray's range comprises a significant portion of the range of the 
species because this portion's contribution to the viability of M. 
birostris is so important that, without the members in this portion, 
the giant manta ray would likely become in danger of extinction within 
the foreseeable future, throughout all of its range.
    Under the SPR policy, we conclude that the Indo-Pacific and eastern 
Pacific portion of the giant manta ray's range qualifies as a 
significant portion of the species' range. Additionally, based on the 
information above and further discussed in our demographic risks 
analysis and threats assessment, as well as the information in the 
status review report, we conclude that M. birostris is at a moderate 
risk of extinction within this significant portion of its range.
Distinct Population Segment (DPS) Analysis
    In accordance with the SPR policy, if a species is determined to be 
threatened or endangered in a significant portion of its range, and the 
population in that significant portion is a valid distinct population 
segment (DPS), NMFS will list the DPS rather than the entire taxonomic 
species or subspecies. Because the Indo-Pacific and eastern Pacific 
represents a significant portion of the range of the species, and this 
portion is at a risk of extinction that is higher than ``low,'' we 
performed a DPS analysis on the population within this portion to see 
if it qualifies as a valid DPS.
    The Services' policy on identifying DPSs (61 FR 4722; February 7, 
1996) identifies two criteria for DPS designations: (1) The population 
must be discrete in relation to the remainder of the taxon (species or 
subspecies) to which it belongs; and (2) the population must be 
``significant'' (as that term is used in the context of the DPS policy, 
which is different from its usage under the SPR policy) to the 
remainder of the taxon to which it belongs.
    In terms of discreteness, a population segment of a vertebrate 
species may be considered discrete if it satisfies either one of the 
following conditions: (1) ``It is markedly separated from other 
populations of the same taxon as a consequence of physical, 
physiological, ecological, or behavioral factors. Quantitative measures 
of genetic or morphological discontinuity may provide evidence of this 
separation''; or (2) ``it is delimited by international governmental 
boundaries within which differences in control of exploitation, 
management of habitat, conservation status, or regulatory mechanisms 
exist that are significant in light of section 4(a)(1)(D)'' of the ESA 
(61 FR 4722; February 7, 1996).
    Research on the genetics of the species, which may provide evidence 
of discreteness between populations, is ongoing. As discussed 
previously in this finding, while there may be evidence of a potential 
M. birostris subspecies, or new manta species, found off the 
Yucat[aacute]n coast in the Gulf of Mexico, the study by Hinojosa-
Alvarez et al. (2016) also showed that some of the Yucat[aacute]n manta 
rays found in the area shared haplotypes with M. birostris samples from 
the Indo-Pacific and eastern Pacific. Additionally, based on nuclear 
DNA, the Yucat[aacute]n samples were consistent with the M. birostris 
samples from the Indo-Pacific and eastern Pacific portions of its 
range. This is the only study that we are aware of that has compared 
potential genetic differences between ocean basins for giant manta 
rays. Given the available data, we do not find evidence to indicate 
genetic discreteness between M. birostris in the Atlantic and M. 
birostris in the Indo-Pacific and eastern Pacific.
    In terms of physical, physiological, morphological, ecological, 
behavioral, and regulatory factors, there is no evidence that the Indo-
Pacific and eastern Pacific population of M. birostris is markedly 
separate from the population in the Atlantic. There is no evidence of 
differences in the morphology or physiology between the populations, 
nor any information to indicate changes in habitat use or behavior 
across ocean basins. Also, given that the species is highly migratory 
and pelagic, with no identified barriers to movement, these populations 
cannot be delimited by international governmental boundaries. As such, 
we find that the M. birostris population in the Indo-Pacific and 
eastern Pacific does not meet the discreteness criteria of the DPS 
policy, and, thus, is not a valid DPS.

Reef Manta Ray

    Overall, the species' life history characteristics increase its 
inherent vulnerability to depletion. Its tendency towards site fidelity 
and high residency rates suggests that there may be little gene flow 
between subpopulations, meaning that reestablishment after depletion is 
unlikely. Additionally, because these aggregations tend to be small, 
even light fishing may lead to population depletion. However, despite 
these inherent risks, the species does not appear subjected to 
significant threats that are causing declines, or likely to cause 
declines, to the point where the species would be at risk of 
extinction. As mentioned in the threats analysis, targeted fishing of 
the species has only been observed in a select few locations, and its 
identification in bycatch is limited. The majority of the known M. 
alfredi subpopulations, particularly throughout the western and Central 
Pacific, while small, are protected from fishing mortality and appear 
stable. Some of the larger known M. alfredi subpopulations, such as off 
the Maldives (n = 3,300-9,677 individuals) and Western Australia (n = 
1,200-1,500 individuals), are not subject to directed fishing, with 
Australia's overall population considered to be one of the world's 
healthiest. While climate change may alter aspects of the habitat and 
food resources of the species, the subsequent impact on the species is 
highly uncertain. Thus, based on the above evaluation of demographic 
risks and threats to the species, we find that the reef manta ray is 
likely to be at a low overall risk of extinction.
SPR Analysis
    As was done for the giant manta ray, we must conduct an SPR 
analysis to determine if the species is in danger of extinction, or 
likely to become so within the foreseeable future, in a significant 
portion of its range. In applying the policy, we first examined where 
threats are concentrated to evaluate whether the species is at risk of 
extinction within those portions. Targeted fishing and subsequent 
declines in populations of M. alfredi are known from waters off 
Mozambique and the Philippines, and the species has also been 
identified in bycatch from Indonesia, Papua New Guinea, and Kiribati. 
However, with the exception of the southern Mozambique population, the 
extent of decline of the

[[Page 3712]]

species throughout these other areas has not been quantified. But while 
the rate of decline is unknown, fishing pressure on the species 
continues in these portions of range and, combined with the species' 
demographic risks of isolated, small populations and extremely low 
productivity, these threats are likely placing these populations on a 
trajectory toward a higher risk of extinction.
    The second question that needs to be addressed in the SPR analysis 
is whether these portions can be considered ``significant.'' Without 
these portions, would the species be in danger of extinction, or likely 
to become so in the foreseeable future, throughout all of its range? We 
find that this is unlikely to be the case. Even if these populations 
were gone, the species would still exist as small, isolated populations 
throughout the Indo-Pacific. There is no evidence of source-sink 
dynamics between these portions and other areas, which could affect the 
survival of the species. In fact, the only indication of a potential 
source-sink dynamic was hypothesized for the M. alfredi population off 
Yaeyama, Japan, which Kashiwagi (2014) found is presently increasing, 
indicating no risk of loss to this population. In fact, many of the M. 
alfredi populations outside of the portions identified above, while 
small in size, are presently thought to be stable or increasing. 
Additionally, these populations, such as the largest identified M. 
alfredi population, off the Maldives, benefit from national protections 
that prohibit the fishing, landing, or selling of the species. Because 
these populations occur nearshore, and the species exhibits high 
residency rates and site-fidelity behavior, these protections will be 
adequate to prevent overutilization of the species through the 
foreseeable future. As such, even without the portions identified 
above, the species will unlikely be in danger of extinction throughout 
all of its range now or in the foreseeable future.
    Thus, under the SPR policy, we could not identify any portions of 
the species' range that meet both criteria (i.e., the portion is 
biologically significant and the species may be in danger of extinction 
in that portion, or likely to become so within the foreseeable future). 
Therefore, we find that our conclusion about the species' overall risk 
of extinction does not change and conclude that M. alfredi is likely to 
be at a low risk of extinction throughout its range.

Protective Efforts

    There are many conservation efforts presently ongoing to collect 
research on manta ray life history, ecology, and biology, and to raise 
awareness of threats to manta rays (see Miller and Klimovich (2016) for 
detailed discussion). The available research and citizen science data 
that have resulted from these conservation efforts have already been 
considered in the above analysis, and future research activities will 
continue to provide valuable information on these manta ray species. 
Additionally, the efforts by these organizations to educate the public, 
such as through awareness campaigns, could eventually lead to decreases 
in the demand for manta ray products. For example, Lawson et al. 
(2016), citing unpublished data, noted an 18-month awareness-raising 
campaign conducted in 2015 in Guangzhou, China, that seemed to indicate 
a level of success in decreasing consumer demand for gill rakers, 
which, in turn, decreased the interest of traders to carry gill plates 
in the future. While more monitoring of trade and consumer behavior is 
required to evaluate the success of these efforts, it may indicate that 
awareness-raising campaigns could be successful tools for influencing 
customer behavior. With demand reduction viewed as a potential avenue 
to indirectly reduce fishing pressure on manta rays, these campaigns 
may ultimately help decrease the main threat to the species (Lawson et 
al. 2016).
    Awareness campaigns are also being used to educate the public on 
appropriate tourist behavior during manta ray dives, which can help 
decrease potential negative impacts of tourism activities on manta 
rays. As mentioned previously, best practice codes of conduct have been 
developed by a number of organizations and are increasingly being used 
by dive operators at a number of popular manta ray diving sites, 
including Kona, Hawaii, Western Australia, Mozambique, Bora Bora, and 
the Maldives, to promote the safe viewing of manta rays.
    While we find that these efforts will help increase the scientific 
knowledge and promote public awareness about manta rays, with the 
potential (but not certainty) to decrease the impacts of specific 
threats in the future, we do not find that these efforts have 
significantly altered the extinction risk for the giant manta ray to 
where it would not be at risk of extinction in the foreseeable future. 
However, we seek additional information on these and other conservation 
efforts in our public comment process (see below).

Determination

    Section 4(b)(1) of the ESA requires that NMFS make listing 
determinations based solely on the best scientific and commercial data 
available after conducting a review of the status of the species and 
taking into account those efforts, if any, being made by any state or 
foreign nation, or political subdivisions thereof, to protect and 
conserve the species. We have independently reviewed the best available 
scientific and commercial information including the petition, public 
comments submitted on the 90-day finding (81 FR 8874; February 23, 
2016), the status review report (Miller and Klimovich 2016), and other 
published and unpublished information, and have consulted with species 
experts and individuals familiar with manta rays. We considered each of 
the statutory factors to determine whether it presented an extinction 
risk to each species on its own, now or in the foreseeable future, and 
also considered the combination of those factors to determine whether 
they collectively contributed to the extinction risk of the species, 
now or in the foreseeable future.
    Based on our consideration of the best available scientific and 
commercial information, as summarized here and in Miller and Klimovich 
(2016), including our SPR and DPS analyses, we find that the giant 
manta ray (Manta birostris) is at a moderate risk of extinction within 
a significant portion of its range, with the species likely to become 
in danger of extinction within the foreseeable future throughout that 
portion. We did not find that the significant portion meets the 
criteria of a DPS. Therefore, we have determined that the giant manta 
ray meets the definition of a threatened species and, per the SPR 
policy, propose to list it is as such throughout its range under the 
ESA.
    Based on our consideration of the best available scientific and 
commercial information, as summarized here and in Miller and Klimovich 
(2016), we find that the reef manta ray (Manta alfredi) faces an 
overall low risk of extinction throughout its range. As previously 
explained, we could not identify any portion of the species' range that 
met both criteria of the SPR policy. Accordingly, the reef manta ray 
does not meet the definition of a threatened or endangered species, and 
thus, the reef manta ray does not warrant listing as threatened or 
endangered at this time. This is a final action on the aforementioned 
petition to list the reef

[[Page 3713]]

manta ray under the ESA, and, therefore, we do not solicit comments on 
it.

Effects of Listing

    Conservation measures provided for species listed as endangered or 
threatened under the ESA include recovery actions (16 U.S.C. 1533(f)); 
concurrent designation of critical habitat, if prudent and determinable 
(16 U.S.C. 1533(a)(3)(A)); Federal agency requirements to consult with 
NMFS under section 7 of the ESA to ensure their actions do not 
jeopardize the species or result in adverse modification or destruction 
of critical habitat should it be designated (16 U.S.C. 1536); and 
prohibitions on ``taking'' (16 U.S.C. 1538). Recognition of the 
species' plight through listing promotes conservation actions by 
Federal and state agencies, foreign entities, private groups, and 
individuals.

Identifying Section 7 Conference and Consultation Requirements

    Section 7(a)(2) (16 U.S.C. 1536(a)(2)) of the ESA and NMFS/USFWS 
regulations require Federal agencies to confer with us on actions 
likely to jeopardize the continued existence of species proposed for 
listing, or that result in the destruction or adverse modification of 
proposed critical habitat. If a proposed species is ultimately listed, 
Federal agencies must consult on any action they authorize, fund, or 
carry out if those actions may affect the listed species or its 
critical habitat and ensure that such actions do not jeopardize the 
species or result in adverse modification or destruction of critical 
habitat should it be designated. Examples of Federal actions that may 
affect the giant manta ray include, but are not limited to: Alternative 
energy projects, discharge of pollution from point sources, non-point 
source pollution, contaminated waste and plastic disposal, dredging, 
pile-driving, development of water quality standards, vessel traffic, 
military activities, and fisheries management practices.

Critical Habitat

    Critical habitat is defined in section 3 of the ESA (16 U.S.C. 
1532(3)) as: (1) The specific areas within the geographical area 
occupied by a species, at the time it is listed in accordance with the 
ESA, on which are found those physical or biological features (a) 
essential to the conservation of the species and (b) that may require 
special management considerations or protection; and (2) specific areas 
outside the geographical area occupied by a species at the time it is 
listed upon a determination that such areas are essential for the 
conservation of the species. ``Conservation'' means the use of all 
methods and procedures needed to bring the species to the point at 
which listing under the ESA is no longer necessary. Section 4(a)(3)(a) 
of the ESA (16 U.S.C. 1533(a)(3)(A)) requires that, to the extent 
prudent and determinable, critical habitat be designated concurrently 
with the listing of a species. Designations of critical habitat must be 
based on the best scientific data available and must take into 
consideration the economic, national security, and other relevant 
impacts of specifying any particular area as critical habitat. If we 
determine that it is prudent and determinable, we will publish a 
proposed designation of critical habitat for the giant manta ray in a 
separate rule. Public input on features and areas in U.S. waters that 
may meet the definition of critical habitat for the giant manta ray is 
invited.

Protective Regulations Under Section 4(d) of the ESA

    We are proposing to list the giant manta ray (Manta birostris) as a 
threatened species. In the case of threatened species, ESA section 4(d) 
leaves it to the Secretary's discretion whether, and to what extent, to 
extend the section 9(a) ``take'' prohibitions to the species, and 
authorizes us to issue regulations necessary and advisable for the 
conservation of the species. Thus, we have flexibility under section 
4(d) to tailor protective regulations, taking into account the 
effectiveness of available conservation measures. The 4(d) protective 
regulations may prohibit, with respect to threatened species, some or 
all of the acts which section 9(a) of the ESA prohibits with respect to 
endangered species. We are not proposing such regulations at this time, 
but may consider potential protective regulations pursuant to section 
4(d) for the giant manta ray in a future rulemaking. In order to inform 
our consideration of appropriate protective regulations for the 
species, we seek information from the public on the threats to giant 
manta rays and possible measures for their conservation.

Role of Peer Review

    The intent of peer review is to ensure that listings are based on 
the best scientific and commercial data available. In December 2004, 
the Office of Management and Budget (OMB) issued a Final Information 
Quality Bulletin for Peer Review establishing minimum peer review 
standards, a transparent process for public disclosure of peer review 
planning, and opportunities for public participation. The OMB Bulletin, 
implemented under the Information Quality Act (Pub. L. 106-554), is 
intended to enhance the quality and credibility of the Federal 
government's scientific information, and applies to influential or 
highly influential scientific information disseminated on or after June 
16, 2005. To satisfy our requirements under the OMB Bulletin, we 
obtained independent peer review of the status review report. 
Independent specialists were selected from the academic and scientific 
community for this review. All peer reviewer comments were addressed 
prior to dissemination of the status review report and publication of 
this proposed rule.

Public Comments Solicited on Listing

    To ensure that the final action resulting from this proposal will 
be as accurate and effective as possible, we solicit comments and 
suggestions from the public, other governmental agencies, the 
scientific community, industry, environmental groups, and any other 
interested parties. Comments are encouraged on this proposal (See DATES 
and ADDRESSES). Specifically, we are interested in information 
regarding: (1) New or updated information regarding the range, 
distribution, and abundance of the giant manta ray; (2) new or updated 
information regarding the genetics and population structure of the 
giant manta ray; (3) habitat within the range of the giant manta ray 
that was present in the past but may have been lost over time; (4) new 
or updated biological or other relevant data concerning any threats to 
the giant manta ray (e.g., post-release mortality rates, landings of 
the species, illegal taking of the species); (5) current or planned 
activities within the range of the giant manta ray and their possible 
impact on the species; (6) recent observations or sampling of the giant 
manta ray; and (7) efforts being made to protect the giant manta ray.

Public Comments Solicited on Critical Habitat

    We request information describing the quality and extent of 
habitats for the giant manta ray, as well as information on areas that 
may qualify as critical habitat for the species in U.S. waters. 
Specific areas that include the physical and biological features 
essential to the conservation of the species, where such features may 
require special management considerations or protection, should be 
identified. Areas outside the occupied geographical area should also be 
identified, if such areas themselves are essential to the

[[Page 3714]]

conservation of the species. ESA implementing regulations at 50 CFR 
424.12(g) specify that critical habitat shall not be designated within 
foreign countries or in other areas outside of U.S. jurisdiction. 
Therefore, we request information only on potential areas of critical 
habitat within waters under U.S. jurisdiction.
    Section 4(b)(2) of the ESA requires the Secretary to consider the 
``economic impact, impact on national security, and any other relevant 
impact'' of designating a particular area as critical habitat. Section 
4(b)(2) also authorizes the Secretary to exclude from a critical 
habitat designation those particular areas where the Secretary finds 
that the benefits of exclusion outweigh the benefits of designation, 
unless excluding that area will result in extinction of the species. 
For features and areas potentially qualifying as critical habitat, we 
also request information describing: (1) Activities or other threats to 
the essential features or activities that could be affected by 
designating them as critical habitat; and (2) the positive and negative 
economic, national security and other relevant impacts, including 
benefits to the recovery of the species, likely to result if these 
areas are designated as critical habitat. We seek information regarding 
the conservation benefits of designating areas within waters under U.S. 
jurisdiction as critical habitat. In keeping with the guidance provided 
by OMB (2000; 2003), we seek information that would allow the 
monetization of these effects to the extent possible, as well as 
information on qualitative impacts to economic values.
    Data reviewed may include, but are not limited to: (1) Scientific 
or commercial publications; (2) administrative reports, maps or other 
graphic materials; (3) information received from experts; and (4) 
comments from interested parties. Comments and data particularly are 
sought concerning: (1) Maps and specific information describing the 
amount, distribution, and use type (e.g., foraging or migration) by the 
giant manta ray, as well as any additional information on occupied and 
unoccupied habitat areas; (2) the reasons why any habitat should or 
should not be determined to be critical habitat as provided by sections 
3(5)(A) and 4(b)(2) of the ESA; (3) information regarding the benefits 
of designating particular areas as critical habitat; (4) current or 
planned activities in the areas that might be proposed for designation 
and their possible impacts; (5) any foreseeable economic or other 
potential impacts resulting from designation, and in particular, any 
impacts on small entities; (6) whether specific unoccupied areas may be 
essential to provide additional habitat areas for the conservation of 
the species; and (7) potential peer reviewers for a proposed critical 
habitat designation, including persons with biological and economic 
expertise relevant to the species, region, and designation of critical 
habitat.

References

    A complete list of the references used in this proposed rule is 
available upon request (see ADDRESSES).

Classification

National Environmental Policy Act

    The 1982 amendments to the ESA, in section 4(b)(1)(A), restrict the 
information that may be considered when assessing species for listing. 
Based on this limitation of criteria for a listing decision and the 
opinion in Pacific Legal Foundation v. Andrus, 675 F. 2d 825 (6th Cir. 
1981), NMFS has concluded that ESA listing actions are not subject to 
the environmental assessment requirements of the National Environmental 
Policy Act (NEPA).

Executive Order 12866, Regulatory Flexibility Act, and Paperwork 
Reduction Act

    As noted in the Conference Report on the 1982 amendments to the 
ESA, economic impacts cannot be considered when assessing the status of 
a species. Therefore, the economic analysis requirements of the 
Regulatory Flexibility Act are not applicable to the listing process. 
In addition, this proposed rule is exempt from review under Executive 
Order 12866. This proposed rule does not contain a collection-of-
information requirement for the purposes of the Paperwork Reduction 
Act.

Executive Order 13132, Federalism

    In accordance with E.O. 13132, we determined that this proposed 
rule does not have significant Federalism effects and that a Federalism 
assessment is not required. In keeping with the intent of the 
Administration and Congress to provide continuing and meaningful 
dialogue on issues of mutual state and Federal interest, this proposed 
rule will be given to the relevant governmental agencies in the 
countries in which the species occurs, and they will be invited to 
comment. As we proceed, we intend to continue engaging in informal and 
formal contacts with the states, and other affected local, regional, or 
foreign entities, giving careful consideration to all written and oral 
comments received.

List of Subjects in 50 CFR Part 223

    Endangered and threatened species.

    Dated: January 5, 2017.
Samuel D. Rauch, III,
Deputy Assistant Administrator for Regulatory Programs, National Marine 
Fisheries Service.

    For the reasons set out in the preamble, 50 CFR part 223 is 
proposed to be amended as follows:

PART 223--THREATENED MARINE AND ANADROMOUS SPECIES

0
1. The authority citation for part 223 continues to read as follows:

    Authority: 16 U.S.C. 1531-1543; subpart B, Sec.  223.201-202 
also issued under 16 U.S.C. 1361 et seq.; 16 U.S.C. 5503(d) for 
Sec.  223.206(d)(9).

0
2. In Sec.  223.102, in the table in paragraph (e) add a new entry for 
``ray, giant manta'' in alphabetical order by common name under the 
``Fishes'' subheading to read as follows:


Sec.  223.102  Enumeration of threatened marine and anadromous species.

* * * * *
    (e) * * *

[[Page 3715]]



----------------------------------------------------------------------------------------------------------------
                              Species \1\
-----------------------------------------------------------------------  Citation(s) for   Critical
                                                Description  of listed       listing        habitat   ESA  rules
      Common name           Scientific name              entity         determination(s)
----------------------------------------------------------------------------------------------------------------
 
                                                  * * * * * * *
Fishes
 
                                                  * * * * * * *
Ray, giant manta......  Manta birostris.......  Entire species........  [Insert Federal   NA........  NA.
                                                                         Register page
                                                                         where the
                                                                         document
                                                                         begins],
                                                                         [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



                                                    3694                   Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules

                                                       (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.
                                                    linked to patient information and be                    accredit qualified suppliers that
                                                                                                                                                                   [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
                                                                                                            must be one of the following:                          DEPARTMENT OF COMMERCE
                                                    fabricating, to identify any parts that
                                                    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: Proposed rule; 12-month
                                                    equipment, and computers commonly                       qualified suppliers as defined in
                                                    used in the fabrication of particular                                                                          petition finding; request for comments.
                                                                                                            § 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 ray (Manta birostris) and
                                                                                                            *       *    *     *     *
                                                    or direct formed), as applicable: These                                                                        reef manta ray (Manta alfredi) as
                                                                                                            ■ 4. Section § 424.535 is amended as
                                                    tools and equipment would include, but                                                                         threatened or endangered under the
                                                    are not limited to the following                        follows:
                                                                                                                                                                   Endangered Species Act (ESA). We have
                                                       (A) Computers with appropriate                       ■ a. Revising the section heading.
                                                                                                                                                                   completed a comprehensive status
                                                    graphics/modeling capacity and                          ■ b. In paragraph (a)(2) introductory text
                                                                                                                                                                   review of both species in response to
                                                    technology.                                             by removing the phrase ‘‘the provider or
                                                                                                                                                                   this petition. Based on the best scientific
                                                       (B) Band saw.                                        supplier is—’’ and adding in its place
                                                                                                                                                                   and commercial information available,
                                                       (C) Disc sander.                                     ‘‘the provider or supplier is any of the
                                                                                                                                                                   including the status review report
                                                       (D) Sanding paper.                                   following:’’.
                                                                                                                                                                   (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.                                                                                          Therefore, we propose to list the giant
                                                                                                            § 424.535 Revocation of enrollment and
                                                       (M) Ovens capable of heating plastics                                                                       manta ray as a threatened species under
                                                                                                            billing privileges in the Medicare program.
                                                    for molding.                                                                                                   the ESA. Any protective regulations
                                                       (N) Computer controlled milling                        (a) * * *
                                                                                                                                                                   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
mstockstill on DSK3G9T082PROD with PROPOSALS




                                                    *      *     *     *    *                               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


                                               VerDate Sep<11>2014   17:58 Jan 11, 2017   Jkt 241001   PO 00000   Frm 00018   Fmt 4702   Sfmt 4702   E:\FR\FM\12JAP1.SGM   12JAP1


                                                                           Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules                                               3695

                                                    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
                                                    DATES: Comments on the proposed rule
                                                                                                            scientific or commercial information                   future (threatened).
                                                                                                            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                                                                               of extinction risk can be based on either
                                                                                                            Caribbean manta ray is not a
                                                    February 27, 2017.                                                                                             assessment of the range wide status of
                                                                                                            taxonomically valid species or
                                                    ADDRESSES: You may submit comments                                                                             the species, or the status of the species
                                                                                                            subspecies for listing, and explained the
                                                    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
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                                                    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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                                                    3696                   Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules

                                                    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,
                                                                                                            review report, its cited references, and               there is some evidence that the
                                                    Status Review                                                                                                  pigmentation pattern of M. birostris may
                                                                                                            peer review comments, and believe the
                                                       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,                                                                     slits and the abdominal area below the
                                                                                                            month finding determination and
                                                    information was compiled on each                                                                               gill-slits (Kitchen-Wheeler 2013).
                                                                                                            proposed rule, we have independently
                                                    species’ biology, ecology, life history,
                                                                                                            applied the statutory provisions of the                Range, Distribution and Habitat Use
                                                    threats, and status from information
                                                                                                            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
                                                                                                            ADDRESSES section) and the peer review
                                                    finding. In assessing the extinction risk                                                                      sometimes overlap; however, at a finer
                                                    of both species, we considered the                      report is available at http://                         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
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                                                    links to these reviews). In this approach,              planktivorous rays, considered part of                 productivity and predictable prey
                                                    the collective condition of individual                  the Mobulidae 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 Mobula 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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                                                                           Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules                                            3697

                                                    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-
                                                    within the Northern Hemisphere, the                                                                            example, along the east coast of
                                                                                                            line distance of 1,500 km, further
                                                    species has been documented as far                                                                             Australia, mark-recapture methods and
                                                                                                            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 Hawaii, 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 zooplankton, 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                     Mozambique (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
                                                    exceeding 1,000 m (A. Marshall et al.                                                                          Education and Research Inc. 2005).
                                                                                                            concentrated survey effort in order to
                                                    unpubl. data 2011 cited in Marshall et                                                                         Mantas appear to be primarily nocturnal
                                                                                                            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,
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                                                    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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                                                    3698                   Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules

                                                    Growth and Reproduction                                 turning abruptly (Deakos et al. 2011).                 Indonesia, Ningaloo Reef, Hawaii, Fiji,
                                                       Manta rays are viviparous (i.e., give                Sexual dimorphism is present in manta                  New Caledonia, 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).
                                                                                                            2010; Marshall and Bennett 2010b).                        The population structure for the
                                                    anywhere from 1 to 5 years (see Table
                                                                                                            Additionally, males have never been                    wider-ranging M. birostris is less clear.
                                                    3 in Miller and Klimovich (2016)).
                                                                                                            observed to compete with each other                    While Clark (2010), using photo-
                                                    Generally, not much is known about
                                                                                                            directly for the attention of the female,              identification survey data collected
                                                    manta ray growth and development.
                                                                                                            so these mating chains may function as                 between 1992 and 2007 along the Kona,
                                                    Free swimming wild mantas have been
                                                                                                            a kind of endurance rivalry (Andersson                 Hawaii, coast, found low site-fidelity for
                                                    observed as small as 1.02 m DW and
                                                                                                            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                                                                            island-associated, Stewart et al. (2016a)
                                                                                                            a mating advantage, but this kind of
                                                    and 3 in Miller and Klimovich (2016));                                                                         provided recent evidence to show that
                                                                                                            endurance trial usually selects for the
                                                    however, the lack of observations of                                                                           the giant manta rays off Pacific Mexico
                                                                                                            success of larger males (Andersson and
                                                    small manta rays throughout the                                                                                may exist as isolated subpopulations,
                                                                                                            Iwasa 1996; Deakos 2012).
                                                    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 Yucatán
                                                    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              Yucatán 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 Yucatán
                                                    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 Yucatán
                                                    3.37 DW for female M. alfredi and 2.80                  Population Structure
                                                                                                                                                                   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
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                                                       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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                                                                           Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules                                            3699

                                                    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 Animals
                                                    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
                                                    populations that are currently stable,                                                                         Klimovich (2016)), despite observational
                                                                                                            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
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                                                    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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                                                    3700                   Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules

                                                    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.
                                                    of M. alfredi from 2009 to 2012 and                     The Present or Threatened Destruction,
                                                                                                                                                                   2015), potentially polluting the habitat
                                                    found an annual increase in abundance                   Modification, or Curtailment of Its
                                                                                                                                                                   used by the nearby Maldives aggregation
                                                    for both sexes, but cautioned that the                  Habitat or Range
                                                                                                                                                                   of manta rays. While the ingestion of
                                                    modeled increase could be an artifact of                                                                       plastics is likely to negatively impact
                                                                                                               Due to their association with
                                                    improvements in photo-identification                                                                           the health of the species, the levels of
                                                                                                            nearshore habitats, manta rays are at
                                                    by observers over the study period.                                                                            microplastics in manta ray feeding
                                                                                                            elevated risk for exposure to a variety of
                                                    Within Ningaloo Marine Park, the status                                                                        grounds and frequency of ingestion are
                                                                                                            contaminants and pollutants, including
                                                    of reef manta rays was assessed as                                                                             presently being studied to evaluate the
                                                                                                            brevotoxins, heavy metals,
                                                    ‘‘Good’’ in 2013, but with low                                                                                 impact on these species (Germanov
                                                                                                            polychlorinated biphenyls, and plastics.
                                                    confidence in the ratings (Marine Parks                                                                        2015b; Germanov 2015a).
                                                                                                            Many pollutants in the environment
                                                    & Reserves Authority 2013). Overall,
                                                                                                            have the ability to bioaccumulate in fish                 Because manta rays are migratory and
                                                    however, the reef manta ray population
                                                    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
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                                                    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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                                                                           Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules                                            3701

                                                    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
                                                                                                            species where available) are evaluated                 appear to be the trend throughout
                                                    Overutilization for Commercial,
                                                                                                            for both fisheries that target mantas and              Indonesia at the common mobulid
                                                    Recreational, Scientific or Educational
                                                                                                            those that catch mantas as bycatch.                    landing sites. For example, Lewis et al.
                                                    Purposes
                                                                                                                                                                   (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
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                                                    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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                                                    3702                   Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules

                                                    (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                 Micronesia, 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
                                                    the gill plate trade). Dharmadi et al.                                                                         Ghana, there is no available data on the
                                                                                                            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).                                            with manta rays consumed locally. In
                                                    (Marshall and Conradie 2014). The high
                                                    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,
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                                                    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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                                                                           Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules                                             3703

                                                    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 (Amandè 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
                                                    observed a seasonally-active mobulid                                                                           this translates to a minimum of around
                                                                                                            Ocean. However, information is severely
                                                    fishery located near La Paz, Baja                                                                              400 giant manta rays caught annually in
                                                                                                            lacking on both population sizes and
                                                    California Sur. Mobulids were fished in                                                                        recent years by Sri Lankan fishing fleets.
                                                                                                            distribution of the giant manta ray as
                                                    the Gulf of California using both gillnets                                                                     Given that fishermen have already noted
                                                                                                            well as current catch and fishing effort
                                                    and harpoons, with their meat either                                                                           a decrease in catches of manta rays over
                                                                                                            on the species throughout this portion
                                                    fileted for human consumption or used                                                                          the past 5 years, it is likely that the
                                                                                                            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; Amandè 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.
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                                                    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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                                                    3704                   Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules

                                                    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 cleaner fish 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
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                                                    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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                                                                           Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules                                             3705

                                                    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 animal, 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
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                                                    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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                                                    3706                   Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules

                                                    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.
                                                                                                               In Indonesia, while the majority of                 water tourists, based on studies of
                                                    aggregation site), researchers have
                                                                                                            landings data is reported as M. birostris,             interaction effects conducted by the
                                                    observed large numbers of manta rays
                                                                                                            anecdotal reports from fishermen note                  organization from 2005–2013 (available
                                                    with life-threatening injuries as a result
                                                                                                            that M. alfredi used to be caught as                   here: http://www.mantatrust.org/
                                                    of incidental capture in illegal wahoo
                                                                                                            bycatch in drift gillnets. Evidence of                 awareness/resources/). The Hawaii
                                                    (Acanthocybium solandri) trawl and
                                                                                                            declines and extirpations of local reef                Association for Marine Education and
                                                    drift gillnet fisheries operating within
                                                    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
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                                                    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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                                                                           Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules                                            3707

                                                    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
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                                                    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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                                                    3708                   Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules

                                                    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                       sufficient gene flow among populations.
                                                    Demographic Risk Analysis
                                                                                                            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                  conspicuous source-sink populations or
                                                    Abundance
                                                                                                            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                                                                              wide-ranging inhabitants of offshore,
                                                    individuals to over 600, estimates of                   Growth Rate/Productivity
                                                                                                                                                                   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
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                                                    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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                                                                           Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules                                             3709

                                                    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
                                                    example, Kashiwagi (2014) recently                                                                             threat to the giant manta ray is
                                                                                                               The reef manta ray is commonly seen
                                                    estimated the effective population size                                                                        overutilization for commercial
                                                                                                            inshore near coral and rocky reefs. The                purposes. Giant manta rays are both
                                                    of the M. alfredi population off the
                                                                                                            species is associated with warmer                      targeted and caught as bycatch in a
                                                    Yaeyama Islands to be Ne = 89,
                                                                                                            waters (≤21 °C) and productive                         number of global fisheries throughout
                                                    indicating that the population is not
                                                    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).
                                                    genetic variants, or fixation of                                                                               Additionally, given the migratory and
                                                                                                            Collectively, this information suggests
                                                    deleterious mutations.                                                                                         pelagic behavior, national protections
                                                                                                            that gene flow is likely limited among                 for the species are less likely to
                                                       Overall, based on the information
                                                                                                            populations of M. alfredi, particularly                adequately protect the species from
                                                    above, the estimates of small and
                                                    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
                                                                                                            loss may pose a risk of extinction.                    enter into high seas. While the species
                                                    Growth Rate/Productivity
                                                                                                                                                                   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                                                                       history functions as a result of increased
                                                                                                            providing the species with resilience to
                                                    to 1 off Australia, Hawaii, and Japan                                                                          tourism; however, due to the significant
                                                                                                            these effects. For example, in response
                                                    (Deakos et al. 2011; Couturier et al.                                                                          data gaps, the likelihood and impact of
                                                                                                            to changing ecological conditions, like
                                                    2014; Kashiwagi 2014). In Mozambique,                                                                          these threats on the status of the species
                                                    rates were lower, between 0.6–0.7;                      the biannual reversal of monsoon
                                                                                                                                                                   is highly uncertain.
                                                    however shark attacks are also more                     currents, reef manta rays will migrate to
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                                                    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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                                                    3710                   Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules

                                                    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
                                                    populations of M. alfredi throughout the                                                                       throughout the Indo-Pacific and eastern
                                                                                                            Overall Risk Summary                                   Pacific portion of its range. Estimated
                                                    western and central Pacific are currently
                                                    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
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                                                    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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                                                                           Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules                                             3711

                                                    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                    Yucatán 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 Yucatán                  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 Yucatán 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
                                                    a species is determined to be threatened                                                                       SPR Analysis
                                                                                                            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
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                                                    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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                                                    3712                   Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules

                                                    species throughout these other areas has                Protective Efforts                                     conservation efforts in our public
                                                    not been quantified. But while the rate                                                                        comment process (see below).
                                                    of decline is unknown, fishing pressure                    There are many conservation efforts
                                                                                                            presently ongoing to collect research on               Determination
                                                    on the species continues in these
                                                                                                            manta ray life history, ecology, and                      Section 4(b)(1) of the ESA requires
                                                    portions of range and, combined with
                                                                                                            biology, and to raise awareness of                     that NMFS make listing determinations
                                                    the species’ demographic risks of
                                                                                                            threats to manta rays (see Miller and                  based solely on the best scientific and
                                                    isolated, small populations 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
                                                                                                            rakers, which, in turn, decreased the                  whether it presented an extinction risk
                                                    which could affect the survival of the
                                                                                                            interest of traders to carry gill plates in            to each species on its own, now or in
                                                    species. In fact, the only indication of a
                                                                                                            the future. While more monitoring of                   the foreseeable future, and also
                                                    potential source-sink dynamic was                                                                              considered the combination of those
                                                                                                            trade and consumer behavior is required
                                                    hypothesized for the M. alfredi                                                                                factors to determine whether they
                                                                                                            to evaluate the success of these efforts,
                                                    population off Yaeyama, Japan, which                                                                           collectively contributed to the
                                                                                                            it may indicate that awareness-raising
                                                    Kashiwagi (2014) found is presently                                                                            extinction risk of the species, now or in
                                                                                                            campaigns could be successful tools for
                                                    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                  a significant portion of its range, with
                                                    Maldives, benefit from national
                                                                                                            used to educate the public on                          the species likely to become in danger
                                                    protections that prohibit the fishing,
                                                                                                            appropriate tourist behavior during                    of extinction within the foreseeable
                                                    landing, or selling of the species.
                                                                                                            manta ray dives, which can help                        future throughout that portion. We did
                                                    Because these populations occur
                                                                                                            decrease potential negative impacts of                 not find that the significant portion
                                                    nearshore, and the species exhibits high
                                                                                                            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
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                                                    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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                                                                           Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules                                           3713

                                                    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
                                                    through listing promotes conservation                                                                          Public Comments Solicited on Listing
                                                                                                            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
                                                                                                            giant manta ray is invited.                            solicit comments and suggestions from
                                                    Identifying Section 7 Conference and
                                                                                                                                                                   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                                                                                                 We request information describing the
                                                                                                            threats to giant manta rays and possible
                                                       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
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                                                    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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                                                    3714                   Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules

                                                    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
                                                    critical habitat, we also request                                                                              entities, giving careful consideration to
                                                                                                            References                                             all written and oral comments received.
                                                    information describing: (1) Activities or
                                                    other threats to the essential features or                A complete list of the references used
                                                                                                                                                                   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).
                                                    administrative reports, maps or other                   Reduction Act
                                                                                                                                                                   ■ 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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                                                                           Federal Register / Vol. 82, No. 8 / Thursday, January 12, 2017 / Proposed Rules                                                     3715

                                                                               Species 1
                                                                                                                                                                                             Critical          ESA
                                                                                                       Description                           Citation(s) for listing determination(s)        habitat           rules
                                                      Common name            Scientific name            of listed
                                                                                                         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 Speciesincludes 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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Document Created: 2017-03-21 14:41:06
Document Modified: 2017-03-21 14:41:06
CategoryRegulatory Information
CollectionFederal Register
sudoc ClassAE 2.7:
GS 4.107:
AE 2.106:
PublisherOffice of the Federal Register, National Archives and Records Administration
SectionProposed Rules
ActionProposed rule; 12-month petition finding; request for comments.
DatesComments on the proposed rule to list the giant manta ray must be received by March 13, 2017. Public hearing requests must be made by February 27, 2017.
ContactMaggie Miller, NMFS, Office of Protected Resources, (301) 427-8403.
FR Citation82 FR 3694 
RIN Number0648-XE39

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