[Federal Register Volume 82, Number 8 (Thursday, January 12, 2017)]
[Proposed Rules]
[Pages 3694-3715]
From the Federal Register Online via the Government Publishing Office [www.gpo.gov]
[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,
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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