[Federal Register Volume 82, Number 203 (Monday, October 23, 2017)]
[Proposed Rules]
[Pages 48948-48967]
From the Federal Register Online via the Government Publishing Office [www.gpo.gov]
[FR Doc No: 2017-22771]
[[Page 48948]]
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DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration
50 CFR Part 223
[Docket No. 160614518-7999-02]
RIN 0648-XE685
12-Month Finding and Proposed Rule To List the Chambered Nautilus
as Threatened 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 chambered nautilus (Nautilus pompilius) as a threatened species or
an endangered species under the Endangered Species Act (ESA). We have
completed a comprehensive status review of the species in response to
this petition. Based on the best scientific and commercial information
available, including the status review report (Miller 2017), and after
taking into account efforts being made to protect the species, we have
determined that the chambered nautilus is likely to become an
endangered species within the foreseeable future throughout its range.
Therefore, we propose to list the chambered nautilus as a threatened
species under the ESA. Any protective regulations determined to be
necessary and advisable for the conservation of the proposed threatened
chambered nautilus under ESA section 4(d) will be proposed in a
separate 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; however, we have
determined that critical habitat is not determinable at this time. We
solicit information to inform our final listing determination, the
development of potential protective regulations, and potential
designation of critical habitat in the event the proposed threatened
listing for the chambered nautilus is finalized.
DATES: Comments on the proposed rule to list the chambered nautilus
must be received by December 22, 2017. Public hearing requests must be
made by December 7, 2017.
ADDRESSES: You may submit comments on this document, identified by
NOAA-NMFS-2016-0098, 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-2016-0098. 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).
The petition, status review report, Federal Register notices, and
the list of references can be accessed electronically online at: http://www.fisheries.noaa.gov/pr/species/invertebrates/chambered-nautilus.html.
FOR FURTHER INFORMATION CONTACT: Maggie Miller, NMFS, Office of
Protected Resources, (301) 427-8403.
SUPPLEMENTARY INFORMATION:
Background
On May 31, 2016, we received a petition from the Center for
Biological Diversity to list the chambered nautilus (N. pompilius) as a
threatened species or an endangered species under the ESA. On August
26, 2016, we published a positive 90-day finding (81 FR 58895)
announcing that the petition presented substantial scientific or
commercial information indicating that the petitioned action may be
warranted for the chambered nautilus. We also announced the initiation
of a status review of the species, as required by section 4(b)(3)(a) of
the ESA, and requested information to inform the agency's decision on
whether this species warrants listing as endangered or threatened under
the ESA.
Listing Species Under the Endangered Species Act
We are responsible for determining whether the chambered nautilus
is 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 subspecies
and, for any vertebrate species, any distinct population segment (DPS)
that interbreeds when mature (16 U.S.C. 1532(16)). Because the
chambered nautilus is an invertebrate, the ESA does not permit us to
consider listing individual populations as DPSs.
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 (that is, at a later time). The key
statutory difference between a threatened and endangered species is the
timing of when a species is or is likely to become in danger of
extinction, either presently (endangered) or in the foreseeable future
(threatened).
When we consider whether a species qualifies as threatened under
the ESA, we must consider the meaning of the term ``foreseeable
future.'' It is appropriate to interpret ``foreseeable future'' as the
horizon over which predictions about the conservation status of the
species can be reasonably relied upon. What constitutes the foreseeable
future for a particular species depends on species-specific factors
such as the life history of the species, habitat characteristics,
availability of data, particular threats, ability to predict threats,
and the reliability to forecast the effects of these threats and future
events on the status of the species under consideration. Because a
species may be susceptible to a variety of threats for which different
data are available, or which operate across different time scales, the
foreseeable future is not necessarily reducible to a particular number
of years.
The statute 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
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any 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; the inadequacy of existing regulatory mechanisms;
or other natural or manmade factors affecting its continued existence.
16 U.S.C. 1533(a)(1). We are also required to make listing
determinations based solely on the best scientific and commercial data
available, after conducting a review of the species' status and after
taking into account efforts, if any, being made by any state or foreign
nation (or subdivision thereof) to protect the species. 16 U.S.C.
1533(b)(1)(A).
Status Review
A NMFS biologist in the Office of Protected Resources conducted the
status review for the chambered nautilus (Miller 2017). The status
review is a compilation of the best available scientific and commercial
information on the species' biology, ecology, life history, threats,
and status from information contained in the petition, our files, a
comprehensive literature search, and consultation with nautilus
experts. We also considered information submitted by the public in
response to our petition finding. In assessing the extinction risk of
the chambered nautilus, 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 is well accepted and 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 http://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 nautilus 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 chambered nautilus. Much of the information discussed below on the
species' biology, distribution, abundance, threats, and extinction risk
is presented in 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 at 50 CFR part 424. 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 chambered nautilus. Further details can be found in
Miller (2017).
Description, Life History, and Ecology of the Petitioned Species
Species Taxonomy and Description
Nautilus taxonomy is controversial. Based on the Integrated
Taxonomic Information System (ITIS), which has a disclaimer that states
it ``is based on the latest scientific consensus available . . . [but]
is not a legal authority for statutory or regulatory purposes,'' two
genera are presently recognized within the family of Nautilidae:
Allonautilus and Nautilus. The genus Allonautilus has two recognized
species: A. perforatus and A. scrobiculatus. The genus Nautilus has
five recognized species: N. belauensis (Saunders 1981), N. macromphalus
(Sowerby 1849), N. pompilius (Linnaeus 1758), N. repertus (Iredale
1944), and N. stenomphalus (Sowerby 1849). However, a review and
analysis of recent genetic and morphological data suggests that perhaps
only two of these five species are valid: N. pompilius and N.
macromphalus, with the other three species more appropriately placed
within N. pompilius (Vandepas et al. 2016; Ward et al. 2016). Saunders
et al. (2017) suggested that consensus may be trending towards treating
N. pompilius as a ``superspecies'' taxonomically, with N. stenomphalus,
N. belauensis, and N. repertus as subspecies.
However, because the taxonomy of the Nautilus genus is not fully
resolved, with ongoing debate as to the number of species that exist,
we follow the latest scientific consensus of the taxonomy of the
Nautilus genus as acknowledged by the ITIS, with N. pompilius
identified as one of five recognized species.
The chambered nautilus is an externally-shelled cephalopod with a
distinctive coiled calcium-carbonate shell that is divided into
chambers. The shell can range in color from white to orange, and even
purple, with unique color patterns (Barord 2015). Its distinctive
coiled shell is what makes the chambered nautilus a highly sought after
commodity in international trade (Convention on International Trade in
Endangered Species of Wild Fauna and Flora (CITES) 2016). The body of
the chambered nautilus is housed in the largest chamber within the
shell, and when the animal is attacked, it can seal itself into this
chamber, closing the opening with a large, fleshy hood (Jereb 2005).
The chambered nautilus also has up to 90 tentacles, without suckers,
which they use to dig in substrate and scavenge for food (Barord 2015)
and to grab on to reef surfaces for rest (CITES 2016).
Range, Distribution and Habitat Use
The chambered nautilus is found in tropical, coastal reef, deep-
water habitats of the Indo-Pacific. Its known range includes waters off
American Samoa, Australia, Fiji, India, Indonesia, Malaysia, Papua New
Guinea, Philippines, Solomon Islands, and Vanuatu, and it may also
potentially occur in waters off China, Myanmar, Western Samoa,
Thailand, and Vietnam (CITES 2016). Additionally, Saunders et al.
(2017) notes that traps set at Nautilus depths in Yap (Caroline
Islands), Pohnpei and Majuro (Marshall Islands), Kosrae (Gilbert
Islands), Western Samoa, and Tonga failed to catch any chambered
nautiluses, providing ``highly suggestive'' evidence that the
geographic range of N. pompilius may not extend out to these sites.
Within its range, the chambered nautilus has a patchy distribution
and is unpredictable in its area of occupancy. Based on multiple
research studies, the
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presence of suitable habitat on coral reefs does not necessarily
indicate the likelihood of chambered nautilus occurrence (CITES 2016).
Additionally, the chambered nautilus is limited in its horizontal and
vertical distribution throughout its range due to physiological
constraints. Physiologically, the chambered nautilus cannot tolerate
temperatures above approximately 25[deg]C or depths exceeding around
750-800 meters (m) (Ward et al. 1980; Carlson 2010). At depths greater
than 800 m, the hydrostatic pressure will cause the shell of the
nautilus to implode, thereby killing the animal (Ward et al. 1980).
Based on these physiological constraints, the chambered nautilus is
considered to be an extreme habitat specialist, found in association
with steep-sloped forereefs with sandy, silty, or muddy-bottomed
substrates. Within these habitats, the species ranges from around 100 m
depths (which may vary depending on the water temperature) to around
500 m depths (CITES 2016). The chambered nautilus does not swim in the
open water column (likely due to its vulnerability to predation), but
rather remains near the reef slopes and bottom substrate, and thus can
be best characterized as a nektobenthic or epibenthic species (Barord
(Barord et al. 2014; CITES 2016).
Nautilus pompilius can travel distances of up to 6 kilometers (km)
in a day facilitated by currents (Dunstan et al. 2011c). However, at
the depths where these animals are generally active (>200 m), currents
are weak and movements are primarily accomplished through self-
propulsion, with observed N. pompilius distances of up to 3.2 km per
day and maximum speeds of up to 1.18 km/hour for short periods of time
(less than 6 hours) (Dunstan et al. 2011a).
Despite the apparent temperature and depth constraints of the
species, larger-scale migrations, although rare, have occurred. For
example, an N. pompilius specimen was captured off southern Japan in
the 1970s and assumed to have drifted 2,000 km in the Kuroshio Current
from the Philippines (Saunders 2010). Saunders (2010) notes that these
movements across large stretches of either shallow, warm water (< 100
meters (m), > 25[deg] C) or deep water (> 800m) would likely be
accomplished only by drifting or rafting (i.e., moving passively with
ocean currents) through midwater or surface waters. However, the author
notes that these movement events must have occurred ``with sufficient
frequency'' to account for the species' distribution across the Indo-
Pacific (Saunders 2010).
Diet and Feeding
Chambered nautiluses are described as deep-sea scavenging
generalists and opportunistic predators. As previously mentioned, the
chambered nautilus uses its 90 retractable tentacles to dig in the
substrate and feed on a variety of organisms, including fish,
crustaceans, echinoids, nematodes, cephalopods, other marine
invertebrates, and detrital matter (Saunders and Ward 2010; Barord
2015). The chambered nautilus also has an acute sense of olfaction and
can easily smell odors (such as prey) in turbulent waters from
significant distances (of up to 10 m) (Basil et al. 2000).
Growth and Reproduction
The general life history characteristics of the chambered nautilus
are that of a rare, long-lived, late-maturing, and slow-growing marine
invertebrate species, with likely low reproductive output.
Circumferential growth rate for the chambered nautilus is estimated to
range from 0.053 mm/day to 0.23 mm/day and slows as the animal
approaches maturity (Dunstan et al. 2010; Dunstan et al. 2011b).
However, average size at maturity of N. pompilius appears to vary among
regions, with smaller shell diameters noted around the Philippines,
Fiji, and eastern Australia and larger diameters off Indonesia (see
Table 1 in Miller 2017). Additionally, the species exhibits sexual
dimorphism, with males consistently growing to larger sizes than
females (Saunders and Ward 2010).
Chambered nautilus longevity is at least 20 years, with age to
maturity between 10 and 17 years (Dunstan et al. 2011b; Ward et al.
2016). Very little is known regarding nautilus reproduction in the
wild. Observations of captive animals suggest that nautiluses reproduce
sexually and have multiple reproductive cycles over the course of their
lifetime. Based on data from captive N. belauensis and N. macromphalus
individuals, female nautiluses may lay up to 10 to 20 eggs per year,
which hatch after a lengthy embryonic period of around 10 to 12 months
(Uchiyama and Tanabe 1999; Barord and Basil 2014; Carlson 2014). There
is no larval phase, with juveniles hatching at sizes of 22 to 23
millimeters (mm) in diameter, and potentially migrating to deeper and
cooler waters (Barord and Basil 2014); however, live hatchlings have
rarely been observed in the wild.
Population Demographics and Structure
Isolated Populations
Most of the recent genetic data suggest that N. pompilius may
actually be comprised of unrecognized sibling species that are
genetically distinct and geographically isolated (CITES 2016). For
example, in a recent examination of the genetic structure between an N.
pompilius population off Western Australia and one off the Philippines,
Williams et al. (2015) concluded that very little gene flow exists
between these two populations. The authors note that the absence of
migration between the Philippines and Western Australia indicates that
recolonization would not be possible if the Philippines population were
to be extirpated (Williams et al. 2015).
On a smaller geographic/population scale, Sinclair et al. (2007)
analyzed DNA sequence information from N. pompilius collected from the
Coral Sea and the outer edges of the Great Barrier Reef in northern
Queensland (``Northern GBR'') and found population-specific genetic
differentiation. Through use of Random Amplification of Polymorphic DNA
(RAPD) analysis and partial sequencing of the CoxI gene region, the
authors determined that there is genetic divergence between the
geographic lineages of ``Northern GBR'' and ``Coral Sea,'' indicating
distinct groups of populations and pointing to the potential for
larger-scale geographic divergence of the species. In a follow-up
study, Sinclair et al. (2011) found an even greater degree of genetic
variation between populations on the east coast of Australia (using the
``Northern GBR'' and ``Coral Sea'' populations) and the west coast of
Australia (Scott Reef), with phylogenetic analyses suggesting three
genetically divergent populations.
In addition to genetics, other studies have looked at morphological
differences to examine isolation between N. pompilius populations. For
example, based on biometric analysis of N. pompilius from the
Philippines and Fiji, Tanabe and Tsukahara (2010) concluded that the
populations are morphologically differentiated, finding statistically
significant differences in weight, size at maturity, and slopes of
allometric relationships of morphological characters between the two
populations.
While it is thought that deep water largely serves as a barrier to
movement of N. pompilius, explaining the isolation of the above
populations, results from Swan and Saunders (2010) suggest it is more
likely a combination of both depth and geographic distance. In their
study, Swan and Saunders (2010) examined the correlation between
morphological differences and distances between populations in Papua
New Guinea, including some that were separated by deep water (> 1000
m). Their findings
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showed that adaptive equilibrium had not yet been attained, indicating
that the populations are not completely genetically isolated (Swan and
Saunders 2010). As such, the authors surmised that there is at least
some degree of contact and gene flow between the Papua New Guinea
populations, through potentially rafting or midwater movements, with
the amount inversely related to the geographic distance between the
populations (Swan and Saunders 2010).
Given the above information, it is reasonable to assume that
populations separated by large geographic distances and deep water are
genetically differentiated, with very little to no gene flow.
Diversity
In terms of genetic diversity, Williams et al. (2015) estimated
large ancestral and current effective population sizes for the
Philippines (current median size = 3,190,920) and Ashmore Reef (Western
Australia) (current median size = 2,562,800) populations, indicating a
low likelihood of the fixation of alleles and no evidence of
significant genetic drift impacts in either population. Additionally,
the authors found no significant difference in the allelic richness
between the sampled locations in the Philippines and Western Australia.
In other words, the data tend to suggest that the species may have high
genetic diversity. However, Williams et al. (2015) caution that due to
the low fecundity and long generation time of the species, genetic
responses to current exploitation rates (such as decreases in genetic
diversity) may not yet be detectable. In fact, using CoxI sequences
from N. pompilius across its range and Tajima's D test to examine
departures from population equilibrium, Vandepas et al. (2016) found
significant negative Tajima's D values for the populations in Western
Australia, New Caledonia and Papua New Guinea. These results indicate
an excess of rare alleles or high-frequency polymorphisms within the
populations, suggesting they may be currently recovering from possible
bottleneck events. While not statistically significant, the Tajima's D
values for the rest of the sampled populations, with the exception of
Palau and Eastern Australia (i.e., Fiji, Indonesia, Vanuatu,
Philippines and American Samoa), were also negative, suggesting that
the species potentially has low genetic diversity across its range.
Overall, given the available and somewhat conflicting information,
the level of genetic diversity needed to maintain the survival of the
species and the current level of genetic diversity across the entire
range of the species remains highly uncertain. Further morphological
and genetic tests examining differences within and among populations
are needed.
Sex-Ratios and Population Structure
Regarding population structure, the available information indicates
chambered nautilus populations are comprised mainly of male and mature
individuals. Based on trapping data, including mark-recapture studies,
male N. pompilius appear to dominate the chambered nautilus catch, with
proportions of 75 to 80 percent (CITES 2016). In addition, a large
proportion of those captured (around 75 percent) are mature, with
juvenile N. pompilius individuals rarely caught (CITES 2016). Saunders
et al. (2017) state that the male-female sex ratio and composition of
mature individuals in nautilus populations provides clues to the
current stability of the population. In the authors' study, they
compared 16 nautilus populations from ``unfished'' areas (in Papua New
Guinea, Australia, Indonesia, Fiji, Palau, American Samoa, New
Caledonia, and Vanuatu) to two populations in the Philippines that have
been subject to decades of uncontrolled exploitation and provided an
estimate of quantitative measures to illustrate demographic
disturbance, or ``disequilibrium,'' in a nautilus population.
Specifically, Saunders et al. (2017) found that the mean percentage of
mature animals in the unfished nautilus populations (n = 16) was 73.9
percent (standard deviation (SD): 21.8, standard error (SE): 5.1) and
the mean percentage of males was 75.0 percent (SD: 16.4, SE: 4.1). The
authors suggested that these proportions could be used as a baseline
for determining whether a population (of n > 100 individuals) is at
equilibrium (Saunders et al. 2017). In contrast, the intensely fished
Philippine population from Ta[ntilde]on Straits (n = 353 individuals)
had a male proportion of only 28 percent and mature individuals
comprised only 26.6 percent of the population, which the authors
suggest are levels that signal pending collapse of the local fishery
(Saunders et al. 2017). Ultimately, the authors indicate that the
ratios obtained by examining the sex and maturity composition of a
nautilus population could be used as a basis for determining whether
management and conservation measures are appropriate. However, a caveat
to this method is that it is unclear if the male-biased sex ratio
reflects the natural equilibrium for chambered nautilus populations.
Because these population studies tend to use baited traps to capture
chambered nautiluses, there may be an aspect of sampling bias in terms
of the size and sex of individuals attracted to the traps. For example,
laboratory studies by Basil (2014) suggest that female N. pompilius may
repel each other. Potentially, this female avoidance of one another may
explain why fewer females are found in the baited-trap field studies.
In fact, in a study of N. pompilius drift shells that were collected
between 1984 and 1987 in Papua New Guinea (n = 1,329), 54 percent were
male, suggesting a much different sex ratio than those determined from
baited studies (Saunders et al. 1991). Given the conflicting
information, further research on sex ratios in the wild, as well as a
better understanding of the population structure of the species, is
needed before definitive conclusions can be drawn on this particular
point.
Population Abundance and Trends
The global abundance of N. pompilius is unknown, with no available
historical baseline population data. In fact, the first study to
estimate baseline population size and density for the species in a
given area was only recently conducted by Dunstan et al. (2011a). This
study examined the N. pompilius population at Osprey Reef, an isolated
coral seamount off Australia's northeastern coast with no history of
nautilus exploitation. Based on data collected from 2000 to 2006, the
authors estimated that the population at Osprey Reef consisted of
between 844 and 4,467 individuals, with a density estimate of 14.6 to
77.4 individuals per square kilometer (km\2\) (Dunstan et al. 2011a).
Subsequent research, conducted by Barord et al. (2014), provided
abundance estimates of nautiluses (species not identified) from four
locations in the Indo-Pacific: The Panglao region of the Bohol Sea,
Philippines, with 0.03 individuals per km\2\, Taena Bank near Pago Pago
Harbor, American Samoa, with 0.16 individuals per km\2\, the Beqa
Passage in Viti Levu, Fiji, with 0.21 individuals per km\2\, and the
Great Barrier Reef along a transect from Cairns to Lizard Island,
Australia, with 0.34 individuals per km\2\ (see Table 2 in Miller
2017). With the exception of the Bohol Sea, these populations are
located in areas where fishing for nautiluses does not occur,
suggesting that nautiluses may be naturally rare, or that other unknown
factors, besides fishing, may be affecting their abundance. The authors
also indicate that the population estimates from this study may, in
fact, be overestimates as they used baited remote underwater video
systems to
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attract individuals to the observation area (Barord et al. 2014). In
either case, these very low population estimates suggest that chambered
nautiluses are especially vulnerable to exploitation, with limited
capacity to recover from depletion. This theory is further supported by
the comparison between the population density in the Panglao region of
the Bohol Sea, where nautilus fishing is occurring, and the unfished
sites in American Samoa, Fiji, and Australia, with the Bohol Sea
density less than 20 percent of the smallest unfished population
(Barord et al. 2014).
Recently, Williams et al. (2015) used genetic modelling to estimate
median population sizes for N. pompilius from locations in Australia
and the Philippines. Specifically, the authors examined genetic markers
and used Bayesian clustering methods to estimate a median population
size for the Australian Ashmore Reef population (which the authors note
may possibly contain the entire Australian northwest shelf nautilus
population) at 2,562,800 individuals (Williams et al. 2015). Using the
same methods, Williams et al. (2015) estimated a median size for the
Palawan region, Philippines, population at 3,190,920 individuals. The
authors recognize that the use of different methods to generate
population density estimates (such as those used by Barord et al.
(2014)) will produce ``predictably dissimilar abundance data''
(Williams et al. 2015). Additionally, as mentioned previously, the
authors suggest that the large estimates from the genetic methods (with
no evidence of population reduction) may indicate that the genetic
response to exploitation (e.g., a decrease in allelic richness) has not
had enough time to become detectable yet, unlike the trapping data from
the above studies (Williams et al. 2015).
Overall, abundance information is extremely spotty and limited to
only a select number of locations (see Table 3 in Miller 2017). Based
on data from the 1980s, collected from sites off American Samoa, Fiji,
Papua New Guinea, and Vanuatu, the average number of N. pompilius
individuals caught per trap ranged from 1 to 30, depending on the site
(see Table 3 in Miller 2017). From 1998 to 2008, an average of 5.7 to
7.9 N. pompilius individuals were caught per trap off Osprey Reef in
Australia (Dunstan et al. 2011a). However, it is difficult to make
comparisons between these locations using the available abundance and
catch-per-unit-effort (CPUE) information (e.g., number of individuals
caught per trap) because the methods of collecting the data vary
greatly by study. For example, most studies examining abundance of
nautiluses are based on trapping data where multiple traps can be set
and left over multiple nights, or one trap can be set for one night,
and the particulars of the trapping methods are generally not available
from the anecdotal or study descriptions. As such, the available
reported data are hard to standardize across studies. It should also be
noted that the majority of the data are over two decades old, with no
available recent trapping estimates. Furthermore, although not yet
confirmed by research, many nautilus experts hypothesize that chambered
nautiluses likely occur in locations where they are not currently
observed (NMFS 2014), suggesting abundance may be underestimated.
However, these experts agree that current abundance estimates cannot be
extrapolated across the species' range without considering suitable
habitat and likelihood of nautilus presence (NMFS 2014), which has yet
to be done.
Regarding current trends in abundance, N. pompilius populations are
generally considered stable in areas where fisheries are absent (e.g.,
Australia) and declining in areas where fisheries exist for the
species; however, recent CPUE data from Fiji indicate a decline despite
no active fishery (FAO 2016). In the unfished Australian Osprey Reef
population discussed above, Dunstan et al. (2010) used mark-recapture
methods to examine the trend in CPUE of individuals over a 12-year
period. Analysis of the CPUE data showed a slight increase of 28
percent from 1997 to 2008, and while this increase was not
statistically significant, the results indicate a stable N. pompilius
population in this unexploited area (Dunstan et al. 2010).
In locations where fisheries have operated or currently operate,
anecdotal declines and observed decreases in catches of nautilus
species are reported (see Table 4 in Miller 2017). Citing multiple
personal communications, the CITES (2016) proposal (to include all
species of nautiluses in Appendix II of CITES) noted declines of N.
pompilius in Indian waters, where commercial harvest occurred in the
past for several decades, and in Indonesian waters, where harvest is
suspected to be increasing. In fact, traders in Indonesia have observed
a significant decrease (with estimates up to 97 percent) in the number
of nautiluses collected over the past 10 years, which may be an
indication of a declining and depleted population (Freitas and
Krishnasamy 2016). In the Philippines, Dunstan et al. (2010) estimated
that the CPUE of Nautilus from four main nautilus fishing locations in
the Palawan region has decreased by an estimated average of 80 percent
in less than 30 years. Anecdotal reports from fishermen that once
fished for N. pompilius in the Sulu Sea note that the species is near
commercial extinction, forcing fishermen to move to new areas in the
South China Sea (Freitas and Krishnasamy 2016). Furthermore, in Tawi
Tawi, Cayangacillo, and Ta[ntilde]on Strait/Cebu, Philippines,
fisheries that once existed for chambered nautiluses have since been
discontinued because of the rarity of the species, with Alcala and Russ
(2002) noting the likely extirpation of N. pompilius from Ta[ntilde]on
Strait in the late 1980s. The fact that the species has not yet
recovered in the Ta[ntilde]on Strait, despite an absence of nautilus
fishing in over two decades, further supports the susceptibility of the
species to exploitation and its limited capability to repopulate an
area after depletion.
Species Finding
Based on the best available scientific and commercial information
described above, we find that the latest scientific consensus is that
N. pompilius is considered a taxonomically-distinct species and,
therefore, meets the definition of ``species'' pursuant to section 3 of
the ESA. Below, we evaluate whether this species warrants listing as
endangered or threatened under the ESA throughout all or a significant
portion of its range.
Summary of Factors Affecting the Chambered Nautilus
As described previously, 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 the chambered nautilus. We considered the impact of all factors for
which information is available. For each relevant factor, we also
considered whether a particular impact is having a minor or significant
influence on the species' status. A ``significant'' contribution is
defined, for purposes of this evaluation, as increasing the risk to
such a degree that
[[Page 48953]]
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. Demographic
stochasticity refers to the variability of annual population change
arising from random events such as birth and death rates, sex ratios,
and dispersal at the individual level. Depensatory processes refers to
those density-dependent processes that result in increased mortality as
density decreases. For example, decreases in the breeding population
can lead to reduced production and survival of offspring. This section
briefly summarizes our findings and conclusions regarding threats to
the chambered nautilus and their impact on the overall extinction risk
of the species. More details can be found in the status review report
(Miller 2017).
The Present or Threatened Destruction, Modification, or Curtailment of
Its Habitat or Range
Chambered nautilus habitat, and in particular coral reefs, are
impacted by a number of human activities. These activities include the
harvest of coral reef species through use of destructive or unselective
fishing practices, coastal development and deep-sea mining that can
contribute to pollution and sedimentation of habitat, and changes in
water temperature and pH caused by climate change. Below we briefly
describe these various threats to the habitat of N. pompilius and
evaluate the likely impact on the status of the species. More details
can be found in the status review report (Miller 2017).
Harvest of Coral Reef Species and Destructive and Unselective Fishing
Practices
Many coral reef species are harvested for the aquarium trade and to
satisfy the high-end Asian food markets (CITES 2016). In addition to
directly contributing to the loss of biodiversity on the reefs, some of
the techniques used to obtain coral reef species for these industries
can cause significant destruction to coral reef communities. For
example, blast and poison fishing are two types of destructive and
unselective fishing practices that are used to harvest coral reef
species throughout much of the range of the chambered nautilus (WRI
2011). Figure 3 in Miller (2017) depicts the extent and severity of
observed blast or poison fishing areas, which are primarily
concentrated off the Philippines, Indonesia, and Malaysia.
Blast fishing is particularly destructive as it not only destroys
coral reefs but also indiscriminately kills their marine inhabitants. A
``typical'' blast will shatter corals and turn them into rubble within
a 1 to 1.5 m diameter of the blast site, and can kill marine organisms,
including invertebrates, within a 20 m radius (Pet-Soede and Erdmann
1998; Njoroge 2014). Although blast fishing is largely illegal, the use
of this destructive practice still continues in many areas. For
example, in a September 2016 article in the Jakarta Post, Amnifu (2016)
reports that blast fishing, a common occurrence in East Nusa Tenggara
waters, and particularly around Sumba Island, has recently expanded to
parts of the Sawu Sea National Park's conservation area.
Because blast fishing is generally conducted in shallow reef waters
(e.g., 5 to 10 m depths) (Fox and Caldwell 2006), N. pompilius is
unlikely to experience direct mortality from these destructive
practices given that they generally inhabit much deeper waters.
However, the indirect impact, such as changes in coral reef community
structure and loss of fish biomass (Raymundo et al. 2007), may decrease
the availability of food resources for the scavenging chambered
nautilus. Also, depending on the extent of the coral reef destruction,
N. pompilius, because of its physiological constraints, may be
incapable of finding and exploiting other suitable habitat with greater
prey resources. Additional research is needed as to the potential
effects of blast fishing on the deeper-water inhabitants of these
impacted coral reefs before definitive conclusions can be drawn
regarding this particular factor.
Another primarily illegal fishing practice that destroys coral
reefs is the use of cyanide, which is primarily deployed to stun and
capture live reef fish. When exposed to cyanide, coral respiration
rates decrease and can cease altogether, with corals observed expelling
their zooxanthellae, resulting in bleaching and mortality events (Rubec
1986; Jones 1997). The practice of using cyanide to harvest reef fish
dates back to the 1960s, where it was developed and commonly used in
the Philippines, before spreading to Indonesia (CITES 2016). Similar to
blast fishing, cyanide fishing is unlikely to result in direct
mortality of N. pompilius, given the species' preferred depth range;
however, changes in coral reef community structure and loss of fish
biomass (Raymundo et al. 2007) might decrease the availability of food
resources for the chambered nautilus. Additional research is needed
before definitive conclusions can be drawn as to the potential effects
of cyanide on the deeper-water reef habitats and inhabitants.
Overall, given the speculative effects of blast and cyanide fishing
on nautilus populations, and the patchy and largely unknown
distribution of the species and its habitat preferences, the best
available information does not indicate that habitat degradation from
the harvest of coral reef species and destructive and unselective
fishing practices are likely significant threats to the species.
Further research is needed before definitive conclusions can be drawn
regarding the extent of nautilus habitat degradation and the impacts on
the status of the species.
Pollution and Sedimentation
Evidence of the impacts of pollution and sedimentation on chambered
nautilus habitat and the effects to the species is speculative or
largely unavailable. For example, in their review of the nautilus CITES
(2016) proposal, the fifth Food and Agriculture Organization of the
United Nations expert advisory panel (FAO panel) hypothesized that an
observed 60 percent decline in a local N. pompilius population in Fiji
was potentially because of pollution of its habitat (FAO 2016). This
assumption was largely based on the fact that no known local
utilization of the species and no commercial fishery exists in this
area. Therefore, the FAO panel speculated that the decline was
attributed to local habitat degradation, as they noted the population
is in close proximity to a major port (Suva) and its potentially small
and fragmented characteristics made it especially vulnerable to habitat
destruction (FAO 2016).
Although deep sea mining may also contribute to the pollution of
chambered nautilus habitat, it appears that the extent of this
pollution, and its subsequent impacts on nautilus populations, may be
largely site-specific. For example, in a study comparing
bioaccumulation rates of trace elements between nautilus species
located in a heavily mined location (i.e., N. macromphalus in New
Caledonia) versus a location not subject to significant mining (i.e.,
N. pompilius in Vanuatu), Pernice et al. (2009) found no significant
difference between the species for trace elements of Ag, Co, Mn, Ni,
Pb, Se, V, and Zn. The authors concluded that the geographical origin
of the nautilus species was not a major contributor to interspecific
differences in trace element concentrations (Pernice et al. 2009).
Additionally, the authors noted that, based on the study results, the
heavy nickel mining conducted in
[[Page 48954]]
New Caledonia does not appear to be a significant source of
contamination in the oceanic habitat of the nautilus, suggesting that
the lagoons in New Caledonia likely trap the majority of the trace
elements from the intense mining activities (Pernice et al. 2009).
The biological impact of potential toxin and heavy metal
bioaccumulation in chambered nautilus populations is unknown. Many of
the studies that have evaluated metal concentrations in cephalopods
examined individuals outside of the range of the chambered nautilus,
with results that show that metal concentrations vary greatly depending
on geography (Rjeibi et al. 2014; Jereb et al. 2015). As such, to
evaluate the degree of the potential threat of bioaccumulation of
toxins in chambered nautilus, information on concentrations of these
metals from N. pompilius, or similar species that share the same life
history and inhabit the same depth and geographic range of N.
pompilius, is necessary. For example, the study by Pernice et al.
(2009), mentioned above, examined the bioaccumulation rates of trace
elements between two nautilus species in similar depths and geographic
ranges. However, the authors found no significant difference between
those nautiluses located in areas of intensive mining (and, therefore,
high heavy metal pollutants) compared to nautiluses in areas without
significant mining (Pernice et al. 2009). With the exception of this
one study, we found no other information on the bioaccumulation rates
of metals in the chambered nautilus, including the lethal concentration
limits of toxins or metals in N. pompilius or evidence to suggest that
current concentrations of environmental pollutants are causing
detrimental physiological effects to the point where the species may be
at increased risk of extinction. As such, the best available
information does not indicate that present bioaccumulation rates and
concentrations of environmental pollutants in N. pompilius or their
habitat are likely significant threats to the species.
Climate Change and Ocean Acidification
Given the narrow range of temperature tolerance of the chambered
nautilus, warming surface water temperatures due to climate change may
further restrict the distribution of the species, decreasing the amount
of suitable habitat (particularly in shallower depths) available for
the species. Perhaps more concerning may be the effects of ocean
acidification. In terms of ocean acidification, which will cause a
reduction of pH levels and concentration of carbonate ions in the
ocean, it is thought that shelled mollusks are likely at elevated risk
as they rely on the uptake of calcium and carbonate ions for shell
growth and calcification. However, based on available studies, the
effects of increased ocean acidification on juvenile and adult mollusk
physiology and shell growth are highly variable (Gazeau et al. 2013).
For example, after exposure to severe CO2 levels
(pCO2 = 33,000 [micro]atm) for 96 hours, the deep-sea clam,
Acesta excavata, exhibited an initial drop in oxygen consumption and
intracellular pH but recovered with both levels approaching control
levels by the end of the exposure duration (Hammer et al. 2011). No
mortality was observed over the course of the study, with the authors
concluding that this species may have a higher tolerance to elevated
CO2 levels compared to other deep-sea species (Hammer et al. 2011).
This is in contrast to intertidal and subtidal mollusk species, such as
Ruditapes decussatus, Mytilus galloprovincialis, and M. edulis, which
exhibited reduced standard metabolic rates and protein degradation when
exposed to decreases in pH levels (Gazeau et al. 2013).
Regarding the impact of ocean acidification on calcification rates,
which is important for the growth of chambered nautiluses, one relevant
study looked at cuttlebone development in the cephalopod Sepia
officinalis (Gutowska et al. 2010). Similar to nautiluses, cuttlefish
also have a chambered shell (cuttlebone) that is used for skeletal
support and for buoyancy regulation. Results from the study showed that
after exposure to 615 Pa CO2 for 6 weeks, there was a seven-
fold increase in cuttlebone mass (Gutowska et al. 2010). However, it
should be noted that unlike N. pompilius, Sepia officinalis is not a
deep-sea dwelling species but rather found in 100 m depths, and their
cuttlebone is internal (not an external shell).
While the above were only a few examples of the variable impacts of
ocean acidification on mollusk species, based on the available studies,
such as those described in Gazeau et al. (2013), it is clear that the
effects are largely species-dependent (with differences observed even
within species). To date, we are unaware of any studies that have been
conducted on N. pompilius and the potential effects of increased water
temperatures or acidity on the health of the species. Therefore, given
the species-specific sensitivities and responses to climate change
impacts, and with no available information on chambered nautiluses, we
cannot conclude that the impacts from climate change are currently or
will in the foreseeable future be significant threats to the existence
of the species in the future.
Overutilization for Commercial, Recreational, Scientific or Educational
Purposes
Based on the best available information, the primary threat to the
chambered nautilus is overutilization for commercial purposes--mainly,
harvest for the international nautilus shell trade. Chambered nautilus
shells, which have a distinctive coiled interior, are traded as
souvenirs to tourists and shell collectors and also used in jewelry and
home d[eacute]cor items (where either the whole shell is sold as a
decorative object or parts are used to create shell-inlay designs)
(CITES 2016). The trade in the species is largely driven by the
international demand for their shells and shell products since fishing
for nautiluses has been found to have no cultural or historical
relevance (Dunstan et al. 2010; De Angelis 2012; CITES 2016; Freitas
and Krishnasamy 2016). Nautilus meat is also not locally in demand (or
used for subsistence) but rather sold or consumed as a by-product of
fishing for the nautilus shells (De Angelis 2012; CITES 2016). While
all nautilus species are found in international trade, N. pompilius,
being the most widely distributed, is the species most commonly traded
(CITES 2016).
Although most of the trade in chambered nautiluses originates from
the range countries where fisheries exist or have existed for the
species, particularly the Philippines and Indonesia, commodities also
come from those areas with no known fisheries (such as Fiji and Solomon
Islands). Other countries of origin for N. pompilius products include
Australia, China, Chinese Taipei, India, Malaysia, New Caledonia, Papua
New Guinea, Vanuatu, and Vietnam (Freitas and Krishnasamy 2016). Known
consumer markets for chambered nautilus products include the Middle
East (United Arab Emirates, Saudi Arabia), Australia, Singapore,
Malaysia, Indonesia, Philippines, Hong Kong, Russia, Korea, Japan,
China, Chinese Taipei and India, with major consumer markets noted in
the European Union (Italy, France, Portugal), the United Kingdom, and
the United States (Freitas and Krishnasamy 2016). In fact, between 2005
and 2014, the United States imported more than 900,000 chambered
nautilus products (CITES 2016). The vast majority of these U.S. imports
[[Page 48955]]
originated from the Philippines (85 percent of the traded commodities),
followed by Indonesia (12 percent), China (1.4 percent), and India (1.3
percent) (CITES 2016).
Because harvest of the chambered nautilus is primarily demand-
driven for the international shell trade, the intensive nautilus
fisheries that develop to meet this demand tend to follow a boom-bust
cycle that lasts around a decade or two before becoming commercially
nonviable (Dunstan et al. 2010; De Angelis 2012; CITES 2016). Fishing
for nautiluses is fairly inexpensive and not labor-intensive, requiring
a fish trap baited with locally-available meat (e.g., cow, duck, goat,
offal, chicken, pufferfish) (Freitas and Krishnasamy 2016). These traps
are usually set at 150 to 300 m depths and retrieved after a few hours
or left overnight (Freitas and Krishnasamy 2016). Given the fishing
gear requirements, and the fact that the chambered nautilus exists as
small, isolated populations, harvest of the species may continue for
years within a region, with the fisheries serially depleting each
population until the species is essentially extirpated from that region
(CITES 2016).
Commercial harvest of the species is presently occurring or has
occurred in the Philippines, Indonesia, India and Papua New Guinea, and
also potentially in China, Thailand and Vanuatu (CITES 2016). However,
based on the number of commodities entering the international trade, we
find that the best available information supports the conclusion that
the Philippines and Indonesia have the largest commercial fisheries for
chambered nautilus, with multiple harvesting sites throughout these
nations (CITES 2016). Although information on specific harvest levels
and the status of chambered nautilus populations within this portion of
its range is limited, the best available data, discussed below, provide
significant evidence of the negative impact of these fisheries and
resulting overutilization of the species.
Commercial Harvest
In the Philippines, the harvesting of chambered nautiluses appears
to have no cultural or historical relevance other than as a source of
local income for the shell trade, with meat either consumed by the
fishermen or sold in local markets (del Norte-Campos 2005; Dunstan et
al. 2010). Yet, anecdotal accounts of fishing for N. pompilius indicate
that trapping of the species has occurred as early as 1900 (Saunders et
al. 2017). Specifically, these accounts suggest trapping in 1900 and
1901 would yield anywhere from 4-5 nautiluses per trap to up to 20
animals (depending on the duration of the trap set) (Saunders et al.
2017). In 1971, Haven (1972, cited in Haven (1977)) found that
Ta[ntilde]on Strait, Philippines, was still an abundant source of N.
pompilius. From 1971 to 1972, around 3,200 individuals were captured
for study (Haven 1977). Prior to this time, N. pompilius was, for the
most part, caught as bycatch in fish traps by Filipino fishermen
(Saunders et al. 2017). However, Haven (1977) notes that it was during
this time when more fishermen began targeting Ta[ntilde]on Strait,
specifically for nautilus shells, with the numbers of fishermen
tripling during subsequent years. Trap yields in 1972 were similar to
those from the early 1900s, with fishermen reporting catches of zero to
19 nautiluses, with an average of 5 animals per trap (Saunders et al.
2017). However, by 1975, the impact of this substantial increase in
fishing pressure on the species was already evident (Haven 1977).
Fishermen in 1975 reported having to move operations to deeper water as
catches were now rare at shallower depths, and the number of
individuals per trap had also decreased (Haven 1977). Additionally,
although the number of fishermen had tripled in those 3 years, and
therefore fishing effort for the species intensified, the catch did not
see an associated increase, indicating a likely decrease in the
abundance of the species within the area (Haven 1977). By 1979, trap
yields had drastically fallen, to around 2 nautiluses per trap, and
only a few fishermen remained engaged in the fishery (Saunders et al.
2017). CITES (2016) reports that around 5,000 chambered nautiluses were
trapped per year in Ta[ntilde]on Strait in the early 1980s and, by
1987, the population was estimated to have declined by 97 percent from
1971 levels, with the species considered commercially extinct and
potentially extirpated from the area (Alcala and Russ 2002). Based on
2014 data from baited remote underwater video station footage in the
region, nautilus activity remains low, and the population density still
has yet to recover to pre-1970 levels (Saunders et al. 2017).
Similarly, other nautilus fishing sites that were established in
the late 1980s, including at Tawi Tawi (an island province in
southwestern Philippines), Cagayancillo (an island in the Palawan
province) and Cebu Strait (east of Ta[ntilde]on Strait), have also seen
harvest crash in recent decades (Dunstan et al. 2010). More recently,
in the Central Luzon region, Bulacan and Pampanga Provinces were
formerly collection and trade sites for nautilus species; however,
collectors and traders noted that the last shipments from these areas
were in 2003 and 2007, respectively, indicating they are likely no
longer viable harvesting sites (Freitas and Krishnasamy 2016).
The level of historical harvest (5,000 chambered nautilus
individuals/year) that appeared to lead to local extirpations in
Ta[ntilde]on Strait is being greatly exceeded in a number of other
areas throughout the chambered nautilus' range in the Philippines. In
Tibiao, Antique Province, in northwestern Panay Island, del Norte-
Campos (2005) estimated annual yield of the chambered nautilus at
around 12,200 individuals for the entire fishery (data from 2001 to
2002). In the Palawan nautilus fishery, 9,091 nautiluses were harvested
in 2013 and 37,341 in 2014 (personal communication cited in CITES
(2016)). This level of harvest is particularly concerning given the
significant declines already observed in these fisheries. In fact, in
four of the five main nautilus fishing areas in this province, Dunstan
et al. (2010) estimated a decline in CPUE of the species ranging from
70 percent to 90 percent (depending on the fishing site) over the
course of only 6 to 24 years. The one main fishing region in Palawan
that did not show a decline was the municipality of Balabac; however,
the authors note that this fishery is relatively new (active for less
than 8 years), with fewer fishermen, and, as such, may not yet have
reached the point where the population crashes or declines become
evident in catch rates (Dunstan et al. 2010). Given that the estimated
annual catches in the Balabac municipality ranged from 4,000 to 42,000
individuals in 2008 (Dunstan et al. 2010), this level of annual
harvest, based on the trends from the other Palawan fishing sites
(Dunstan et al. 2010), will likely lead to similar population declines
and potential extirpations of chambered nautiluses in the near future.
In addition to the declines in harvest and CPUE of the species from
observed fishing sites throughout the Philippines, the overutilization
of N. pompilius in this area is also evident in the available trade
data. In a personal communication cited in CITES (2016), it was stated
that over the past 5 years, shell traders in Palawan Province have seen
a decline in the number of shells being offered to them by local
harvesters. Similarly, harvesters and traders in the Visayan regions
have noted increasing difficulty in obtaining shells, with this trend
beginning in 2003 (CITES (2016) citing
[[Page 48956]]
Schroeder (2003)). Based on U.S. trade data from the last decade,
Philippine export and re-export of nautilus commodities to the United
States has decreased by 92 percent since 2005 (see Figure 4 in Miller
(2017)) (CITES 2016). Despite the extensive evidence of overutilization
of the species throughout the Philippines, including the serial
depletion and potential extirpation of local populations, harvest and
trade in N. pompilius continues, with the Philippines still the number
one supplier of nautilus commodities to the United States (based on
figures from 2014).
Off Indonesia, signs of decline and overutilization of chambered
nautilus populations are also apparent. In fact, based on the
increasing number of chambered nautilus commodities originating from
Indonesia, it is suggested that nautilus fishing has potentially
shifted to Indonesian waters because of depletion of the species in the
Philippines (CITES 2016). According to trade data reported in De
Angelis (2012), the Philippines accounted for 87 percent of the
nautilus commodities in U.S. trade from 2005 to 2010, whereas Indonesia
accounted for only 9 percent. However, with the significant decline of
nautilus exports coming out of the Philippines in recent years (2010 to
2014), Indonesia has become a larger component of the trade, accounting
for 42 percent of the nautilus commodities in 2014, while the
Philippines has seen a decrease in their proportion, down to 52 percent
(CITES 2016).
Similar to the trend observed in the Philippines, a pattern of
serial depletion of nautiluses because of harvesting is emerging in
Indonesia. Both fishermen and traders note a significant decline in the
numbers of chambered nautiluses over the last 10 years, despite a
prohibition on the harvest and trade of N. pompilius that has been in
place since 1999 (CITES 2016; Freitas and Krishnasamy 2016). For
example, fishermen in North Lombok note that they historically trapped
around 10 to 15 nautiluses in one night, but currently catch only 1 to
3 per night (Freitas and Krishnasamy 2016). Similarly, in Bali,
fishermen reported nightly catches of around 10 to 20 nautiluses until
2005, after which yields have been much less (Freitas and Krishnasamy
2016). While fishing for chambered nautiluses has essentially decreased
in western Indonesia (likely due to a depletion of the local
populations), the main trade centers for nautilus commodities are still
located here (i.e., Java, Bali, Sulawesi and Lombok). The sources of
nautilus shells for these centers now appear to originate from eastern
Indonesian waters (including northeastern Central Java, East Java, and
West Nusa Tengarra eastward) where it is thought that nautilus
populations may still be abundant enough to support economically viable
fisheries, and where enforcement of the current N. pompilius
prohibition appears weaker (Nijman et al. 2015; Freitas and Krishnasamy
2016). For example, data collected from two large open markets in
Indonesia (Pangandaran and Pasir Putih) indicate that chambered
nautiluses were still being offered for sale as of 2013. Over the
course of three different weekends, Nijman et al. (2015) observed 168
N. pompilius shells for sale from 50 different stalls in the markets
(average price was $17 USD/shell). In addition to catering to tourists,
a wholesaler with a shop in Pangandaran noted that he also exports
merchandise to Malaysia and Saudi Arabia on a bimonthly basis (Nijman
et al. 2015). In total, Nijman et al. (2015) found evidence of six
Indonesian wholesale companies that offered protected marine mollusks
(and mostly nautilus shells) for sale on their respective Web sites
(with two based in East Java, two in Bali, and one in Sulawesi). The
company in Sulawesi even had a minimum order for merchandise of 1
metric ton, and a company in Java noted that they could ship more than
one container per month, indicating access to a relatively large supply
of nautilus shells (Nijman et al. 2015).
The available U.S. trade data provide additional evidence of the
overutilization and potential serial depletion of populations within
Indonesia, although not yet as severe as what has been observed in the
Philippines. Overall, based on data from the last decade, Indonesian
export and re-export of nautilus commodities to the United States has
decreased by 23 percent since 2005 (see Figure 5 in Miller (2017))
(CITES 2016); however, large declines were seen between 2006 and 2009
before smaller increases in the following years. As noted above, these
trends likely reflect the depletion of nautilus populations in western
Indonesian waters and a subsequent shift of fishing effort to eastern
Indonesian waters in recent years to support the nautilus trade
industry.
In India, CITES (2016) states that the chambered nautilus has been
exploited for decades and is also caught as bycatch by deep sea
trawlers. A 2007 survey aimed at assessing the status of protected
species in the curio trade in Tamil Nadu confirmed the presence of N.
pompilius shells and found them highly valued in the retail domestic
markets (John et al. 2012). Out of 13 major coastal tourist curio
markets surveyed, N. pompilius shells were found in 20 percent of the
markets (n = 40 shops) (John et al. 2012). Based on estimated sales
from these markets, N. pompilius was the fourth highest valued species
(n = 25 total species), accounting for 7 percent of the annual profit
from the protected species curio trade (John et al. 2012). During the
survey, chambered nautilus shells sold, on average, for approximately
275 INR each (7 USD in 2007 dollars) (John et al. 2012).
Interviews with the curio traders indicate that the Gulf of Mannar
and Palk Bay, the island territories of Andaman and Lakshadweep, and
Kerala are the main collection areas for the protected species sold in
the curio trade (John et al. 2012). While the extent of harvest of N.
pompilius is unknown, the fact that the nautilus shells sold in markets
are nearly half the size of the reported common wild size (90 mm vs 170
mm) (John et al. 2012) suggests that this curio trade may be
contributing to overfishing of the population, causing a shift in the
local population structure. Compared to observed mature shell sizes
elsewhere throughout the range of N. pompilius (average mature shell
length range: 114 to 200 mm; see Table 1 in Miller (2017)), the Indian
market nautilus shells are likely entirely from immature individuals.
The removal of these nautilus individuals before they have time to
reproduce, particularly for this long-lived and low fecundity species,
could have devastating impacts on the viability of the local
populations. While the authors note that curio vendors may
strategically stock a larger number of undersized shells rather than
fewer larger shells to meet the demand of the tourists, given the
relative rarity of chambered nautilus shells in Indian waters (with
only 9 shells sold during the 2007 survey) and the fact that larger
shells generally obtain higher prices, we conclude it is at least
equally likely that curio vendors are stocking whatever is available.
Although trend data are not available, the popularity of the
species in the curio trade as well as information suggesting that the
marketed shells are significantly smaller than wild-caught and, hence,
likely belong to immature individuals, indicate that this level of
utilization may have already negatively impacted the local populations
within India. The continued and essentially unregulated fishing and
selling of N. pompilius within southern Indian waters will lead to
overutilization of the species in the future, as has been observed in
other
[[Page 48957]]
parts of its range, and potential extirpation of these small and
isolated populations.
In Papua New Guinea, most of the available information indicates
that trade of chambered nautilus shells is primarily supplied from
incidental collection of drift shells. CITES (2016) states that the
species may be caught as bycatch in some deep-sea fisheries and also
notes that new nautilus fishing sites may have recently become
established in 2008. The extent of harvest of the species in these
waters, however, is unknown.
Possible commercial harvest of the species has also been identified
in East Asia (China, Hong Kong, and Chinese Taipei), Thailand, Vanuatu,
and Vietnam. In East Asia, minimal numbers of nautilus shells are sold
in art markets, home d[eacute]cor shops, small stores, and airport gift
shops, with meat found in seafood markets (particularly in the south of
China on Hainan Island, the large coastal cities of Fujian and
Guangdong Provinces, and Chinese Taipei) (Freitas and Krishnasamy
2016). There is also evidence of a small trade in live specimens for
aquaria in Hong Kong; however, the origin of these live specimens is
unclear (Freitas and Krishnasamy 2016). While the CITES (2016) proposal
suggests that nautilus harvest may occur on Hainan Island, we are aware
of no information to confirm that a fishery exists.
In Thailand, nautilus experts note that targeted chambered nautilus
fisheries have occurred and are still operating (NMFS 2014), with past
observations of shells found in gift shops (CITES 2016); however, we
are aware of no published information on the current intensity or
duration of such harvest (or confirmation that the fishery is still
occurring). Nautilus experts also note that targeted chambered nautilus
fisheries have occurred and are occurring in Vanuatu (NMFS 2014), with
shells sold to tourists and collectors (Amos 2007). While we are aware
of no published information regarding the current intensity or duration
of such harvest (or confirmation that the fishery is still occurring),
available information suggests the fishery may have begun in the late
1980s. From March to June 1987, the Vanuatu Fisheries Department
conducted a deep sea fishing trial, aimed at testing commercial fishing
traps on the outer-reef slope of north Efate Island, Vanuatu (Blanc
1988). Results showed the successful capture of N. pompilius, with a
CPUE of around 2.6 nautilus per trap per day, taken at depths greater
than 300 m (Blanc 1988). In total, 94 traps were set and 114 N.
pompilius were captured (Blanc 1988). Those shells that were in good
condition (approximately two-thirds of the total) were sold locally for
around 300 to 500 VUV each ($2.89 to $4.81 U.S. dollars based on the
1987 conversion rate) (Blanc 1988). It was noted in the report that the
capture of nautiluses can be a good supplementary source of income
(Blanc 1988).
In Vietnam, some of the nautilus shells observed for sale may be
sourced from local harvest of the animal. For example, an interview
with a Vietnamese seller revealed that his nautilus shells come from
islands in Vietnam and that 1,000 shells a month are able to be
acquired (of 5 to 7 inches in size; 127 to 178 mm) (Freitas and
Krishnasamy 2016). However, the species was not identified, nor was it
clear whether the origin of the shells was from Vietnam (indicating
potential harvest) or if the islands simply serve as transit points for
the trade.
In our review of the available information, we also found no
evidence of known local utilization or commercial harvest of the
chambered nautilus in the following portions of the species' range:
American Samoa, Australia, Fiji, or the Solomon Islands. While products
that incorporate nautilus shells, such as jewelry and wood inlays, are
sold to tourists in these locations, the nautilus parts appear to be
obtained solely from the incidental collection of drift shells. In
these areas, where the species is not subject to commercial harvest,
populations appear stable (with the exception of Fiji; however, the
threat in this case was not identified as overutilization--see Present
or Threatened Destruction, Modification, or Curtailment of Habitat or
Range section). Given that the species exists as geographically
isolated populations, we conclude it is unlikely that these local,
unfished populations will see significant declines as a result of
overutilization in other portions of its range.
Overall, out of the 10 nations in which N. pompilius is known to
occur, potentially half historically or currently have targeted
nautilus fisheries. Given that this harvest is largely unregulated, and
has led to the serial depletion and extirpation of local N. pompilius
populations, with no evidence of a decline in fishing effort or demand
for the species, the best available information indicates that
overutilization of N. pompilius is the most significant threat to the
species throughout its range.
Trade
As mentioned previously, the commercial harvest of the chambered
nautilus is primarily demand-driven for the international shell trade.
The Philippines and Indonesia appear to supply the majority of the
nautilus products in the trade. In Indonesia, most of the networks that
aid in the illegal trade of marine mollusks originate in Java and Bali,
with the United States, China, and New Caledonia as main destinations
(Nijman et al. 2015). While the extent of export from the Philippines
and Indonesia is unknown, data collected from Indonesia over the past
10 years suggest the amounts are likely substantial. For example, based
on seizure data from 2005 to 2013, over 42,000 marine mollusk shells
protected under Indonesian law, including over 3,000 chambered
nautiluses, were confiscated by Indonesian authorities (Nijman et al.
2015). At least two-thirds of the shells were meant to enter the
international trade, with the largest volumes destined for China and
the United States (Nijman et al. 2015). Between 2007 and 2010, De
Angelis (2012), citing a personal communication, estimated that around
25,000 nautilus specimens were exported from Indonesia to China for the
Asian meat market.
In addition to the United States and China, other major consumer
destinations for nautilus commodities include Europe, the Middle East,
and Australia, with suspected markets in South Africa, South America
(Argentina), and Israel (Freitas and Krishnasamy 2016). Freitas and
Krishnasamy (2016) indicate that, in Europe, the trade and sale of
nautiluses occur at fairly low levels and mainly involve whole nautilus
shells. Their internet research and consultations indicate that the
majority of Web sites selling nautilus products are located in France,
Germany and the United Kingdom; however, details regarding the product,
including species and origin of the nautilus, are often not provided
(Freitas and Krishnasamy 2016). Based on interviews with trade experts
and online sellers, it appears that the Philippines is the main source
of nautilus shells for the European trade (Freitas and Krishnasamy
2016). Some German online sellers indicate that the wholesalers also
receive imports from Thailand (Freitas and Krishnasamy 2016).
In the United States, the most recent 5 years of available trade
data (2010 to 2014) reveal that around 6 percent of the imported
commodities were whole shells (n = 9,076) and less than 1
[[Page 48958]]
percent were live animals, with the remaining products primarily
comprised of jewelry, shell products, and trim pieces (CITES 2016).
Based on trade data from 2010-2013 and using rough approximations of
individual nautilus counts for different commodity labels, Freitas and
Krishnasamy (2016) estimated that between 20,000 and 100,000 nautilus
individuals comprised the commodities being imported into the United
States, representing between 6,000 and 33,000 individuals annually.
However, it is important to note that even these figures likely
underestimate the actual trade volumes in the United States, as
additional nautilus imports could have also been lumped under a more
general category, such as ``mollusks'' (De Angelis 2012). This is
likely true for other countries as well, because specific custom codes
are lacking for nautilus products (with nautilus commodities frequently
lumped as ``coral and similar materials'' and worked or unworked shell
products) (Freitas and Krishnasamy 2016). Therefore, estimating the
number of nautilus individuals traded annually around the globe remains
extremely challenging. Despite these unknowns, based on the available
trade data from the United States, and data garnered from seizures and
research, it is clear that nautilus commodities are in high demand and
nautilus products are globally traded likely in the hundreds of
thousands (De Angelis 2012). This market demand is a significant threat
driving the commercial harvest and overutilization of N. pompilius
throughout most of its range.
Disease or Predation
We are aware of no information to indicate that disease is a factor
that is significantly and negatively affecting the status of the
chambered nautilus. Diseases in nautiluses are not well known, nor is
there information to indicate that disease is contributing to
population declines of the species. However, shells of N. pompilius,
like other mollusks, are subject to marine fouling from a variety of
epizoans and may also be hosts to parasites. In an examination of 631
N. pompilius shells from the Philippines and Papua New Guinea, Landman
et al. (2010) found the incidence of encrustation by epizoans varied by
site. In the N. pompilius shells from the Philippines, 12 percent were
encrusted whereas 49 percent of the shells from the Papua New Guinea
sample showed signs of encrustation. However, the encrusted area only
averaged around 0.5 percent of the shell surface, with the maximum
encrustation at 2.2 percent (Landman et al. 2010). Additionally, the
authors note that the encrusted surface comprised less than 1 percent
of the total shell weight in air, which they deemed ``a negligible
factor in the overall buoyancy of the animal'' (Landman et al. 2010).
As such, it is likely that the species has some other defense against
epizoan settlement, with encrustation not a significant threat to the
survival of N. pompilius individuals.
Regarding parasites, Carlson (2010) notes that newly collected
nautilus individuals are usually heavily infested with the copepod
Anchicaligus nautili; however, no information on the effect of these
infestations on the nautilus animal is available. Therefore, based on
the available data, marine fouling and parasitism do not appear to be
significant threats to the species.
Chambered nautiluses may serve as prey to a number of teleost fish
(such as triggerfish), octopuses, and sharks; however, predation rates
appear to vary across the species' range (CITES 2016). For example,
octopod predation rates on live nautiluses have been estimated at 1.1
percent in the Philippines, 4.5 to 11 percent in Indonesia, 2 to 8
percent in Papua New Guinea, 5 percent in American Samoa, and 3.2
percent on Australia's Great Barrier Reef, indicating that predation by
octopuses likely occurs throughout the entire species' range (Saunders
et al. 1991).
Recently, Ward (2014) analyzed the prevalence of shell breaks in
nautiluses as an indicator of predation and found that those nautilus
populations subject to fishing had a statistically significant higher
number of major shell breaks compared to unfished populations.
Specifically, Ward (2014) found that over 80 percent of mature N.
pompilius shells had major shell breaks in the fished Bohol,
Philippines population (in 2012 and 2013) and calculated an over 40
percent rate in the fished New Caledonia N. macromphalus population in
1984. In contrast, only 30 percent of mature shells had major shell
breaks in the unfished nautilus populations on the Great Barrier Reef
(based on 2012 data) (Ward 2014). In the unfished Osprey Reef
population, this rate was around 20 percent (based on 2002 to 2006
data), and in Papua New Guinea and Vanuatu in the 1980s, this rate was
less than 20 percent (Ward 2014).
Predation is clearly evident in all sampled nautilus populations.
It appears that predation rates may be substantially higher in those
populations compromised from other threats (such as overutilization).
This, in turn, exacerbates the risk that predation poses to those
already vulnerable chambered nautilus populations, contributing
significantly to their likelihood of decline and to the species'
overall risk of extinction.
The Inadequacy of Existing Regulatory Mechanisms
Based on the available data, N. pompilius appears most at risk from
overutilization in those range states supplying the large majority of
nautilus shells for the international trade. Substantial commercial
harvest of the species in Indonesia, Philippines, and India has led to
observed declines in the local N. pompilius populations. As we discuss
below, although there are some national and international legal
protections, including a recent listing under CITES, poor enforcement
of these laws and continued illegal fishing demonstrate that the
existing regulatory mechanisms are inadequate to achieve their purpose
of protecting the chambered nautilus from harvest and trade. It is too
early to conclude that the CITES listing will be effective at
ameliorating the threat of overutilization.
In Indonesia, N. pompilius was provided full protection in the
nation's waters in 1999 (Government Regulation 7/1999). While the
species was first added to Indonesia's protected species list in 1987
(SK MenHut No 12 Kptd/II/1987), the implementing legislation in 1999
made it illegal to harvest, transport, kill, or trade live or dead
specimens of N. pompilius (CITES 2016). Despite this prohibition, the
commercial harvest and trade in the species continues (see
Overutilization for commercial, recreational, scientific, or
educational purposes). For example, in a survey of 343 shops within 6
Provinces in Indonesia, Freitas and Krishnasamy (2016) found that 10
percent were selling nautilus products, with the majority located in
East Java. Interviews with local suppliers of nautilus shells revealed
that many are aware of the prohibition and therefore have found ways to
conduct business covertly, such as selling more products online and
purposely mislabeling N. pompilius shells as A. perforatus (which are
not protected) (Freitas and Krishnasamy 2016). Nijman et al. (2015)
observed the sale of chambered nautilus shells in two of Indonesia's
largest open markets (Pangandaran and Pasir Putih, both on Java) and
remarked that the shells were prominently displayed. In interviews with
the traders, none mentioned the protected status of the species (Nijman
et al. 2015). Additionally, nautilus shells and products (such as
furniture) are often on display by government officials and offered for
sale in airports (Freitas and
[[Page 48959]]
Krishnasamy 2016), indicating that enforcement of the Indonesian
regulation protecting the species is very weak. Therefore, given the
apparent disregard of the prohibition, with substantial evidence of
illegal harvest and trade in the species, and issues with enforcement,
we conclude that existing regulatory mechanisms are inadequate to
protect the species from further declines in Indonesia from
overutilization.
In the Philippines, shelled mollusks are protected from collection
without a permit under Fisheries Administrative Order no. 168; however,
it is unclear how this is implemented or enforced for particular
species (CITES 2016). In Palawan Province, a permit is also required to
harvest or trade the chambered nautilus, as it is listed as
``Vulnerable'' under Palawan Council for Sustainable Development
Resolution No. 15-521 (CITES 2016). Freitas and Krishnasamy (2016)
report that some municipalities in Cebu Province and the Panay Islands
have local ordinances that prohibit the harvest of N. pompilius;
however, even in these Provinces, there is evidence of harvest and
trade in the species. For example, in a survey of 66 shops in Cebu, the
Western Visayas region, and Palawan, 83 percent of the shops sold
nautilus products. For the most part, the harvest and trade of nautilus
is largely allowed and essentially unregulated throughout the
Philippines (Freitas and Krishnasamy 2016). Given the significant
declines in the N. pompilius populations throughout this portion of the
species' range, existing regulations to protect N. pompilius from
overutilization throughout the Philippines are clearly inadequate.
In India, N. pompilius has been protected from harvest and trade
since 2000 when it was listed under Schedule I of the Indian Wildlife
(Protection) Act of 1972 (John et al. 2012). However, as noted in the
Overutilization for commercial, recreational, scientific, or
educational purposes section, N. pompilius shells were being collected
in Indian waters and sold in major coastal tourist curio markets as
recently as 2007. Interviews with retail vendors (n = 180) indicated
that a large majority were aware of the Indian Wildlife Protection Act
and legal ramifications of selling protected species yet continued to
sell large quantities of protected marine mollusks and corals in the
curio shops (John et al. 2012). Because there is no official licensing
system for these shops, the annual quantities sold remain largely
unrecorded and unknown (John et al. 2012). The high demand for nautilus
shells and profits from this illegal curio trade, coupled with the lack
of enforcement of existing laws, indicates that overutilization of N.
pompilius will continue to threaten populations within Indian waters.
In China, N. pompilius is listed as a ``Class I'' species under the
national Law of the People's Republic of China on the Protection of
Wildlife, which means that harvest is allowed (under Article 16) but
only with special permission (i.e., for purposes of scientific
research, ranching, breeding, exhibition, or ``other''). Unfortunately,
enforcement of this law has proven difficult, as many nautilus products
for sale have unknown origin or claim origin from the Philippines
(Freitas and Krishnasamy 2016). While the extent of harvest in East
Asia remains unclear based on the available data, the fact that trade
is allowed, and the difficulties associated with enforcement and
identifying N. pompilius products and origin in the trade, indicate
that existing regulatory measures are likely inadequate to prevent the
harvest of the species within Chinese waters.
In areas where trade of N. pompilius is prohibited, available data
suggest smugglers are using other locations as transit points for the
trafficking and trade of the species to circumvent prohibitions and
evade customs (Freitas and Krishnasamy 2016). For example, New
Caledonia, where only N. macromphalus is protected, has become a stop-
over destination for smuggling nautilus shells to Europe (CITES 2016;
Freitas and Krishnasamy 2016). In 2008, officials confiscated at least
213 N. pompilius shells that were being smuggled into New Caledonia
from Bali, Indonesia (Freitas and Krishnasamy 2016). At this time, the
extent of the illegal trade, including transit points for smugglers,
remains largely unknown; however, the impact of this illegal trade on
the species only contributes further to its overutilization.
Overall, given the ongoing demand for chambered nautilus products,
the apparent disregard of current prohibition regulations by collectors
and traders, lack of enforcement, and the observed declining trends in
N. pompilius populations and crashing of associated fisheries, the best
available information strongly suggests that existing regulatory
mechanisms are inadequate to control the harvest and overutilization of
N. pompilius throughout most of its range, significantly contributing
to the species' risk of extinction.
Recognizing that the international trade is the clear driving force
of the intense exploitation of nautiluses, in October 2016, the member
nations to CITES agreed to add all nautilus species to Appendix II of
CITES (effective January 2017). This listing means increased protection
for N. pompilius and the other nautilus species, but still allows legal
and sustainable trade. Export of nautilus products now requires CITES
permits or re-export certificates that ensure the products were legally
acquired and that the Scientific Authority of the State of export has
advised that such export will not be detrimental to the survival of
that species in the wild (i.e., a ``non-detriment finding''). Given
that the international trade is the main driver of the threat to the
species (i.e., overutilization), the CITES listing should provide N.
pompilius with some safeguards against future depletion of populations
and potential extinction of the species. However, given the limited
information on the present abundance of the species throughout its
range, it may prove difficult for State Authorities to determine what
level of trade is sustainable. As the FAO panel notes, based on
previous cases for species listed under Appendix II with similar
circumstances where the State Authorities' abilities to make non-
detriment findings are limited due to an absence of information, the
following outcomes are likely to occur: (1) International trade in
products from that country ceases; (2) international trade continues
but without proper CITES documentation (``illegal trade''); and/or (3)
international trade continues with inadequate non-detriment findings
(FAO 2016). Because this listing only recently went into effect
(January 2017), it is too soon to know which outcome(s) will dominate
in the various nautilus-exporting countries. There is thus not yet a
body of information on which to evaluate the adequacy of the CITES
listing to reduce the threat of overutilization.
Other Natural or Man-Made Factors Affecting Its Continued Existence
Ecotourism
While the status review (Miller 2017) discusses ecotourism
operations as a possible threat to nautilus species, the examples of
these activities come entirely from Palau, where N. pompilius does not
occur. These ecotourism activities tend to involve bringing nautiluses
to the surface for photographic opportunities with customers and
subsequently releasing them into shallow waters (CITES 2016). In the
daytime, nautiluses are especially vulnerable to predation in shallow
waters, and observations of triggerfish feeding on nautiluses as they
are
[[Page 48960]]
released suggest that consistent release of these animals in a certain
location may create feeding stations for nautilus predators (Carlson
2015). Additionally, nautiluses may suffer negative physiological
effects if released into shallow water, including overheating and the
development of air bubbles that can inhibit quick escape movements
(CITES 2016). We acknowledge the potential risks that these ecotourism
operations may pose to nautilus species; however, at this time, there
is no substantial evidence to indicate that there are dive tour
operators within the N. pompilius range who practice this same behavior
(i.e., taking photographs and releasing the species in shallow waters).
As such, the best available information does not indicate that
ecotourism is presently a significant threat to the species.
Natural Behavior
Because of their keen sense of smell (Basil et al. 2000), chambered
nautiluses are easily attracted to baited traps. Additionally, field
studies indicate that nautiluses may also habituate to baited sites.
For example, in a tag and release study conducted in Palau, the
proportion of previously tagged animals over the trapping period
increased in the baited traps, reaching around 58 percent in the last
trap deployed (Saunders et al. in press). Given this behavior, nautilus
populations, including N. pompilius, are likely highly susceptible to
being caught by fisheries. For isolated and small populations, this
could result in rapid depletions of these populations in a short amount
of time, potentially just months (Saunders et al. in press). However,
Saunders et al. (in press) note that this vulnerability to depletion
from overfishing is likely lower in those populations where barriers to
movement do not exist, such as Papua New Guinea and Indonesia. These
sites both have large swaths of habitat (thousands of km) within the
optimal nautilus depth range that are parallel to coastal areas and
could serve as natural refugia but also allow for the restocking of
depleted populations (Saunders et al. in press). Therefore, the best
available information suggests that these aspects of the species'
natural behavior (i.e., attraction and habituation to baited trap
sites) are likely significant threats to those N. pompilius populations
that are already subject to other threats (e.g., overutilization) or
demographic risks (e.g., spatially isolated, small 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.'' We define ``foreseeable future'' generally as the time frame
over which identified threats can be reliably predicted to impact the
biological status of the species. As mentioned previously, because a
species may be susceptible to a variety of threats for which different
data are available, or which operate across different time scales, the
foreseeable future is not necessarily reducible to a particular number
of years.
For the assessment of extinction risk for the chambered nautilus,
the ``foreseeable future'' was considered to extend out several decades
(> 40 years). Given the species' life history traits, with longevity
estimated to be at least 20 years, maturity ranges from 10 to 17 years,
with very low fecundity (potentially 10-20 eggs per year with a 1-year
incubation period), 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 the species could be realized in the form of
noticeable population declines within this time frame, as demonstrated
in the available survey and fisheries data (see Table 4 in Miller
2017). As the main potential operative threat to the species is
overutilization, this time frame would allow for reliable predictions
regarding the impact of current levels of fishery-related mortality on
the biological status of the species. Additionally, this time frame
allows for consideration of the previously discussed impacts on
chambered nautilus habitat from climate change and the potential
effects on the status of this 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 impacts of external threats that may affect the
species' status. To this end, a demographic analysis was conducted for
the chambered nautilus. A demographic risk analysis is essentially 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
data available for the chambered nautilus, such as abundance, growth
rate/productivity, spatial structure and connectivity, and diversity,
to determine the potential risks these demographic factors pose to the
species. The information from this demographic risk analysis was
considered alongside the information previously presented on threats to
the 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 N. pompilius.
Because the available data are insufficient to conduct a reliable
quantitative population viability assessment (because there is, for
example, sporadic abundance data, and uncertain demographic
characteristics), the qualitative reference levels of ``low risk,''
``moderate risk'' and ``high risk'' were used to describe the overall
assessment of extinction risk in the Status Review. A species at a
``low risk'' of extinction was defined as one that is not at a moderate
or high level of extinction risk. A species may be at low risk of
extinction if it is not facing threats that result in declining trends
in abundance, productivity, spatial structure, or diversity. A species
at low risk of extinction is likely to show stable or increasing trends
in abundance and productivity with connected, diverse populations. A
species is at a ``moderate risk'' of extinction when it is on a
trajectory that puts it at a high level of extinction risk in the
foreseeable future. A species may be at moderate risk of extinction
because of projected threats or declining trends in abundance,
productivity, spatial structure, or diversity. A species with a high
risk of extinction is at or near a level of abundance, productivity,
spatial structure, and/or diversity that places its continued
persistence in question. The demographics of a species at such a high
level of risk may be highly uncertain and strongly influenced by
stochastic or depensatory processes. Similarly, a species may be at
high risk of extinction if it faces clear and present threats (e.g.,
confinement to a small geographic area; imminent destruction,
modification, or curtailment of its habitat; or disease epidemic) that
are likely to create imminent and substantial demographic risks.
Although the conclusions in the status review report do not
constitute findings as to whether the species should be listed under
the ESA (because that determination must be made by the
[[Page 48961]]
agency after considering all relevant information and after evaluating
ongoing conservation efforts of any state, foreign nation, or political
subdivision thereof. 16 U.S.C. 1533(b)(1)(A)), a finding of ``moderate
risk'' generally indicates that a species may qualify for listing as a
``threatened species'' and a finding of ``high risk'' generally
indicates that a species may be an ``endangered species.''
Demographic Risk Analysis
Abundance
The global abundance of the chambered nautilus is unknown, with no
available historical baseline population data. The species likely
exists as small, isolated populations distributed throughout its range.
However, abundance estimates of these fragmented populations are
largely unavailable, as the species is difficult to survey. Currently,
population size has been estimated for N. pompilius off Osprey Reef in
Australia using baited trap techniques (n = 844 to 4,467 individuals)
and for the Palawan region, Philippines and Western Australia
populations using genetic markers (median population size for Western
Australia = 2.6 million individuals; for Philippines = 3.2 million
individuals). Population density estimates (individuals/km\2\) are also
available from Osprey Reef (13.6 to 77.4), the Great Barrier Reef
(0.34), American Samoa (0.16), Fiji (0.21) and the Panglao region,
Philippines (0.03). While there may be some sampling bias in the baited
trap technique, we find that the population size and density estimates
from these studies provide a useful representation of the current
abundance of the species because they rely on the best available field
data.
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. Additionally, when populations are very small,
chance demographic events can have a large impact on the population.
However, the threshold for depensation in the chambered nautilus is
unknown.
Populations of N. pompilius are assumed to be naturally small, and,
when not faced with outside threats, appear stable (e.g., Osprey Reef
population increased by 28 percent over the course of a decade).
However, those populations in areas where nautilus fishing occurs have
experienced significant declines in less than a generation time for the
species, indicating a greater risk of extirpation because of
depensatory processes. Saunders et al. (in press) suggest that trapping
data that result in < 1 to 2 nautiluses per trap likely reflect a
minimally viable population level. In other words, further removal of
individuals from those populations would likely result in population
crashes and potential extirpation. Based on the available abundance
trend data (see Table 4 in Miller (2017)), many of the populations
surveyed in Indonesia and the Philippines currently reflect this
minimally viable level, indicating that abundance of these particular
populations may be close to levels that place them at immediate risk of
inbreeding depression and demographic stochasticity, particularly given
their reproductive isolation. Extirpations of these populations would
increase the risk of extinction for the entire species to some degree.
While overall abundance is highly uncertain, the evidence indicates
that the species exists as small and isolated populations throughout
its range, making them inherently vulnerable to exploitation and
depletion. Data suggest that many of these populations are in decline
and may be extirpated in the next several decades. Taken together, this
information indicates that N. pompilius is not currently at risk of
extinction throughout its range but will likely be at risk of
extinction from environmental variation or human-caused threats
throughout its range within the foreseeable future.
Growth Rate/Productivity
The current net productivity of N. pompilius is unknown because of
the imprecision or lack of available abundance estimates or indices.
Fecundity, however, is assumed to be low (but note that no egg-laying
has been observed in the wild). Based on estimates from other captive
Nautilus species (i.e., N. macromphalus and N. belauensis), the
chambered nautilus may lay up to 10 to 20 eggs per year, with a long
incubation period (10 to 12 months). Given that the chambered nautilus
is a slow-growing and late-maturing species (with maturity estimated
between 10 and 17 years, and longevity at least 20 years), it likely
has very low productivity and, thus, is extremely susceptible to
decreases in its abundance.
In terms of demographic traits, Saunders et al. (in press) suggest
that a nautilus population at equilibrium would have a higher
percentage of male (75 percent) and mature (74 percent) animals. Ratios
that are significantly lower than these estimates suggest the
population is in ``disequilibrium'' and likely portend declines in per
capita growth rate. Saunders et al. (in press) further provides
evidence that fished nautilus populations tend to show significant
demographic differences in relative age class (i.e., predominance of
immature individuals) and sex ratios (i.e,, no longer male-biased)
compared to unfished populations. Under the current assumption that
males are the critical sex for population growth, the significant
change in the population demographics for these fished populations may
portend further declines and potential extirpations of these
populations, inherently increasing the risk of extinction for the
entire species in the foreseeable future. However, with the exception
of the Osprey Reef (Australia), Lizard Island (Great Barrier Reef;
Australia), and Sumbawa Island (Indonesia) populations, which showed
male percentages of 82 to 91 percent and mature percentages of 58 to 91
percent based on data from the past decade (Saunders et al. in press),
we have no available recent data to assess the demographic traits of
current N. pompilius populations throughout the species' range.
Spatial Structure/Connectivity
Chambered nautilus populations are extreme habitat specialists. The
species is closely associated with steeply-sloped forereefs and muddy
bottoms and is found in depths typically between 200 m and 500 m. Both
temperature and depth are barriers to movement for N. pompilius, which
cannot physiologically withstand temperatures above around 25 [deg]C or
depths greater than 800 m. Chambered nautiluses are bottom-dwelling
scavengers and do not swim in the open water column. While larger-scale
migrations have occurred (across shallow, warm waters and/or depths >
1000 m), these events are believed to be extremely rare, with gene flow
thought to be inversely related to the geographic distance between
populations (Swan and Saunders 2010). As such, current chambered
nautilus populations, particularly those separated by large geographic
distances, are believed to be largely isolated, with a limited ability
to find or exploit available resources in the case of habitat
destruction. Collectively, this information suggests that gene flow is
likely limited among populations of N. pompilius, with available data
specifically indicating the isolation between populations in Fiji and
Western Australia and those in the Philippines.
Regarding destruction of habitat patches, while anthropogenic
threats, such as climate change and destructive
[[Page 48962]]
fishing practices, have been identified as potential sources that could
contribute to habitat modification for the chambered nautilus, there is
no evidence that habitat patches used by N. pompilius are being
destroyed faster than they are naturally created such that the species
is at an increased risk of extinction. Additionally, there is no
information to indicate that N. pompilius is composed of conspicuous
source[hyphen]sink populations where loss of one critical population or
subpopulation would pose a risk of extinction to the entire species.
Diversity
As noted above, N. pompilius appears to exist as isolated
populations with low rates of dispersal and little gene flow among
populations, particularly those that are separated by large geographic
distances and deep ocean expanses. Given the physiological constraints
and limited mobility of the species, coupled with the selective
targeting of mature males in the fisheries, connectivity among breeding
populations may be disrupted. Additionally, while it is unknown whether
genetic variability within the species is sufficient to permit
adaptation to environmental changes, the best available information
suggests that genetic variability has likely been reduced due to
bottleneck events and genetic drift in the small and isolated N.
pompilius populations throughout its range. Because higher levels of
genetic diversity increase the likelihood of a species' persistence,
the current, presumably reduced level among chambered nautiluses
appears to pose a risk to the species.
Threats Assessment
As discussed above, the most significant and certain threat to the
chambered nautilus is overutilization through commercial harvest to
meet the demand for the international nautilus shell trade. Out of the
10 nations where N. pompilius is known to occur, potentially half have
targeted nautilus fisheries either historically or currently. These
waters comprise roughly three-quarters of the species' known range,
with only the most eastern portion (e.g., eastern Australia, American
Samoa, Fiji) afforded protection from harvest. Fishing for nautiluses
is fairly inexpensive and easy, and the attraction of N. pompilius to
baited traps further increases the likely success of these fisheries
(compounding the severity of this threat on the species). The estimated
level of harvest from many of these nautilus fisheries in the
Philippines (where harvest data are available) has historically led to
extirpations of local N. pompilius populations. Given the evidence of
declines (of 70 to 94 percent) in the CPUE from these Philippine
nautilus fisheries, and the fact that fished populations tend to
experience higher predation rates (another compounding factor that
further increases the negative impact of fishing on the species), these
populations are likely on the same trend toward local extinction.
Serial depletion of populations based on anecdotal trapping reports is
also evident throughout nautilus fishing sites in Indonesia, with
reported declines of 70 to 97 percent. In India, the predominance of
immature shells for sale in the curio markets suggests potential
overfishing of these local populations as well. Commercial harvest of
the species is also thought to occur in Papua New Guinea, East Asia,
Thailand, Vanuatu, and Vietnam. Efforts to address overutilization of
the species through regulatory measures appear inadequate, with
evidence of targeted fishing of and trade in the species, particularly
in Indonesia, Philippines, and China, despite prohibitions.
As fishing for the species has no cultural or historical relevance,
trade appears to be the sole driving force behind the commercial
harvest and subsequent decline in N. pompilius populations, with
significant consumer markets in the United States, China, Europe
(Italy, France, Portugal, United Kingdom), the Middle East, and
Australia. If international trade were to be successfully managed to
ensure sustainable harvest of N. pompilius, then the serial decline of
local populations could be halted and partially depleted populations
could have time to recover. The CITES Appendix II listing aims to
achieve these conservation outcomes; however, given that the listing
only recently went into effect (i.e, January 2017), it is too soon to
evaluate the ability and capacity of the affected countries (who are
parties to CITES) to implement the required measures and ensure the
sustainability of their trade. Of concern is the illegal selling and
trade of the species that already exists despite domestic prohibitions.
Therefore, it is unclear whether and how the new CITES requirements
will be adequately implemented and enforced in those countries that are
presently unable to prevent the overutilization of the species despite
prohibitions (e.g., Indonesia, Philippines, China). We note that the
United States appears to be a significant importer of nautilus products
and, therefore, this CITES listing could potentially cut-off a large
market (and associated demand) for the species if adequate non-
detriment findings are not issued by the exporting countries. However,
the evidence of illegal trade routes (see Figure 7 in Miller (2017))
and difficulty with tracking the amount and origin of nautilus products
suggests that it may take some time before the extent of the ``ins and
outs'' of the nautilus trade are fully understood. Therefore, we find
that the adequacy of the CITES Appendix II listing in reducing the
threat of overutilization (through ensuring sustainable trade) is
highly uncertain at this time.
Additional threats to N. pompilius that were identified as
potentially contributing to long-term risk of the species include
unselective and destructive fishing techniques (e.g., blast fishing and
cyanide poisoning) and ocean warming and acidification as a result of
climate change effects; however, because of the significant data gaps
(such as the effects on nautilus habitat and the species' physiological
responses), the impact of these threats on the status of the species is
highly uncertain.
Overall Extinction Risk Summary
Given the species' low reproductive output and overall productivity
and existence as small and isolated populations, it is inherently
vulnerable to threats that would deplete its abundance, with a very low
likelihood of recovery or repopulation. While there is considerable
uncertainty regarding the species' overall current abundance, the best
available information indicates that N. pompilius has experienced
population declines of significant magnitude, including evidence of
extirpations, throughout most of its range, primarily because of
fisheries-related mortality (i.e., overutilization). While stable
populations of the species likely exist in those waters not subject to
nautilus fishing (e.g., Osprey Reef, Australia and American Samoa),
only a few populations have actually been found and studied. These
populations appear small (particularly when compared to trade figures)
and genetically and geographically isolated, and, therefore, if subject
to environmental variation or anthropogenic perturbations in the
foreseeable future (such as through illegal fishing or climate change),
will likely be unable to recover.
Currently, the best available information, though not free from
uncertainties, does not indicate that the species is currently at risk
of extinction throughout its range. The species is still traded in
considerable amounts (upwards of thousands to hundreds of
[[Page 48963]]
thousands annually), with evidence of new sites being established for
nautilus fishing (e.g., in Indonesia, Philippines, Papua New Guinea),
and areas of stable, unfished populations (e.g., eastern Australia,
American Samoa). Although this continued trading presents a moderate
threat as has been discussed, current overall abundance throughout its
range is not so low that the species' viability is presently at risk.
However, the continued harvesting of the species for the international
nautilus shell trade and the subsequent serial depletion of populations
throughout its range are placing the species on a trajectory to be in
danger of extinction within the foreseeable future, likely within the
next couple of decades. The species' current demographic risks,
including small and isolated populations, low productivity, habitat
specificity, and physiological limitations that restrict large-scale
migrations, mean that as populations are depleted and extirpated,
recovery of those populations and/or repopulation is unlikely. Many of
the observed populations of the species are already on this path, with
data indicating significant declines in abundance and even local
extinctions. Further exacerbating these declines is the evidence of
increased predation on fished nautilus populations and the disruption
of population demographics (through the attraction of predominantly
males and mature individuals to baited traps). As the unsustainable
harvesting of nautiluses continues, with fisheries that follow a boom-
bust cycle, and fishing efforts that serially exploit populations and
then move on to new sites as the populations become depleted
(particularly evident in the Philippines and Indonesia), this trend is
unlikely to reverse in the foreseeable future. In fact, despite current
domestic prohibitions on the harvest and trade of the species
throughout most of the species' range (and particularly in the large
exporting range states), these regulatory measures are ineffective
because they are largely ignored or circumvented through illegal trade
networks. Further, although the species was recently listed on CITES
Appendix II, there is as of yet no basis to conclude whether that
listing will be effective at decreasing the threat of overutilization
to the species through the foreseeable future.
Given the best available information, we find that N. pompilius is
at a moderate risk of extinction throughout its range. Although the
species is not currently at risk of extinction throughout its range, it
will likely become so within the foreseeable future. Without adequate
measures controlling the overutilization of the species, N. pompilius
is on a trajectory where its overall abundance will likely see
significant declines within the foreseeable future eventually reaching
the point where the species' continued persistence will be in jeopardy.
We therefore propose to list the species as a ``threatened species.''
Protective Efforts
Having found that the chambered nautilus is likely to become in
danger of extinction throughout its range within the foreseeable
future, we next considered protective efforts as required under Section
4(b)(1)(A) of the ESA. The focus of this evaluation is to determine
whether these efforts are effective in ameliorating the threats we have
identified to the species and thus potentially avert the need for
listing.
As we already considered the effectiveness of existing regulatory
protective efforts, discussed above in connection with the evaluation
of the adequacy of existing regulatory mechanisms, we consider other,
less formal conservation efforts in this section. We identified a non-
profit Web site devoted to raising the awareness of threats to the
chambered nautilus (e.g., http://savethenautilus.com/about-us/),
including raising funds to support research on the species.
Additionally, we note that chambered nautiluses are found in a number
of aquariums worldwide where additional research is being conducted on
the reproductive activity of the species. However, survival of the
species in captivity is relatively low compared to its natural
longevity. Based on a 2014 survey of 102 U.S. aquariums with nautilus
species (with 52 responses), Carlson (2014) reported that survival
rates for captive N. pompilius of more than 5 years was only 20
percent. The rates of survival for less than 5 years were as follows: 0
to 1 year = 33.3 percent, 1-2 years 6.7 percent; 2 to 3 years = 20.0
percent, 3 to 5 years = 20.0 percent. While some of these aquariums
have successfully bred nautilus species (e.g., Waikiki Aquarium (U.S.),
Birch Aquarium at Scripps (U.S.), Toba Aquarium (Japan), Farglory Ocean
Park (Chinese Taipei) (Tai-lang 2012; Blazenhoff 2013; Carlson 2014)),
based on the results from these efforts, it is unlikely that
aquaculture or artificial propagation programs could substantially
improve the conservation status of the species. On average, survival
rate after hatching is less than 1 in 1,000 (Tai-lang 2012) and, to
date, none of the captive-bred nautiluses have obtained sexual maturity
(NMFS 2014). The process is also costly and time-consuming (given the
year-long incubation period of eggs). Therefore, captive breeding would
not be a feasible alternative to help satisfy the trade industry or
restore wild populations (NMFS 2014). Additionally, it should be noted
that the shells of nautiluses in captivity tend to be smaller and
irregular, with black lines that mar the outside of the shells (Moini
et al. 2014). Therefore, those shells would likely not be acceptable as
suitable alternatives to wild-caught shells in the trade, given the
preference for large, unblemished nautilus shells in the market.
While we find that these protective efforts will help increase the
scientific knowledge about N. pompilius and potentially promote public
awareness regarding declines in the species, none has significantly
altered the extinction risk for the chambered nautilus to the point
where it would not be in danger 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)(A) 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 58895; August 26,
2016), the status review report (Miller 2017), and other published and
unpublished information, and have consulted with species experts and
individuals familiar with the chambered nautilus.
As summarized above and in Miller (2017), we assessed the ESA
section 4(a)(1) factors both individually and collectively and conclude
that the species faces ongoing threats from overutilization and that
existing regulatory mechanisms are inadequate to ameliorate that
threat. Evidence of the continued substantial trade in the species,
establishment of new N. pompilius fishing sites, and areas of unfished
populations indicate that the species has not yet declined to abundance
levels that would trigger the onset of depensatory processes. However,
the species' demographic risks (including small and isolated
[[Page 48964]]
populations, with substantial reductions of 70 to 97 percent and
extirpations of local chambered nautilus populations from waters
comprising roughly three-quarters of the species' known range, low
productivity, habitat specificity, and physiological limitations that
restrict large-scale migration), coupled with the ongoing serial
exploitation of N. pompilius to supply the international trade, and
evidence of illegal harvest, trade, and poorly enforced domestic
regulatory measures, significantly increase the species' vulnerability
to depletion and subsequent extinction from environmental variation or
anthropogenic perturbations, placing it on a trajectory indicating that
it will likely be in danger of extinction within the foreseeable future
throughout its range.
We found no evidence of protective efforts for the conservation of
the chambered nautilus that would eliminate or adequately reduce
threats to the species to the point where it would no longer be in
danger of extinction in the foreseeable future. Therefore, we conclude
that the chambered nautilus is not currently in danger of extinction,
but likely to become so in the foreseeable future throughout its range
from threats of overutilization and the inadequacy of existing
regulatory mechanisms. As such, we have determined that the chambered
nautilus meets the definition of a threatened species and propose to
list it is as such throughout its range under the ESA.
Because we find that the chambered nautilus is likely to become an
endangered species within the foreseeable future throughout its range,
we find it unnecessary to consider whether the species might be in
danger of extinction in a significant portion of its range. We believe
Congress intended that, where the best available information allows the
Services to determine a status for the species rangewide, such listing
determination should be given conclusive weight. A rangewide
determination of status more accurately reflects the species' degree of
imperilment, and assigning such status to the species (rather than
potentially assigning a different status based on a review of only a
portion of the range) best implements the statutory distinction between
threatened and endangered species. Maintaining this fundamental
distinction is important for ensuring that conservation resources are
allocated toward species according to their actual level of risk. We
also note that Congress placed the ``all'' language before the
``significant portion of its range'' phrase in the definitions of
``endangered species'' and ``threatened species.'' This suggests that
Congress intended that an analysis based on consideration of the entire
range should receive primary focus, and thus that the agencies should
do a ``significant portion of its range'' analysis as an alternative to
a rangewide analysis only if necessary. Under this reading, we should
first consider whether listing is appropriate based on a rangewide
analysis and proceed to conduct a ``significant portion of its range''
analysis if (and only if) a species does not qualify for listing as
either endangered or threatened according to the ``all'' language. We
note that this interpretation is also consistent with the 2014 Final
Policy on Interpretation of the Phrase ``Significant Portion of its
Range'' (79 FR 37578 (July 1, 2014)). That policy is the subject of
pending litigation, including litigation against the United States Fish
and Wildlife Service in the United States District Court for the
District of Arizona, which ordered the policy vacated and is currently
considering a motion for reconsideration. See Center for Biological
Diversity v. Jewell, No. CV-14-02506-TUC-RM, 2017 WL 2438327 (D. Ariz.
March 29, 2017). Our approach in this proposed rule, explained above,
has been reached and applied independently of the Final Policy.
Effects of Listing
Measures provided for species of fish or wildlife listed as
endangered or threatened under the ESA include development of recovery
plans (16 U.S.C. 1533(f)); designation of critical habitat, to the
maximum extent prudent and determinable (16 U.S.C. 1533(a)(3)(A)); the
requirement that Federal agencies consult with NMFS under section 7 of
the ESA to ensure their actions are not likely to jeopardize the
species or result in adverse modification or destruction of critical
habitat should it be designated (16 U.S.C. 1536(a)(2)). Certain
prohibitions, including prohibitions against ``taking'' and import,
also apply with respect to endangered species under Section 9 (16
U.S.C. 1538); at the discretion of the Secretary, some or all of these
prohibitions may be applied with respect to threatened species under
the authority of Section 4(d) (16 U.S.C. 1533(d)). Recognition of the
species' plight through listing also promotes voluntary conservation
actions by Federal and state agencies, foreign entities, private
groups, and individuals.
Identifying Section 7 Conference and Consultation Requirements
Section 7(a)(4) (16 U.S.C. 1536(a)(4)) 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 under Section 7(a)(2) (16 U.S.C.
1536(a)(2)) 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 are not likely to jeopardize the species or
result in destruction or adverse modification of critical habitat
should it be designated. At this time, based on the currently available
information, we determine that examples of Federal actions that may
affect the chambered nautilus include, but are not limited to:
alternative energy projects, discharge of pollution from point and non-
point sources, deep-sea mining, contaminated waste and plastic
disposal, dredging, pile-driving, development of water quality
standards, military activities, and fisheries management practices.
Critical Habitat
Critical habitat is defined in section 3 of the ESA (16 U.S.C.
1532(5)) 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. 16 U.S.C. 1532(3).
Section 4(a)(3)(A) of the ESA (16 U.S.C. 1533(a)(3)(A)) requires that,
to the maximum 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. At this time, we find that critical habitat for the chambered
nautilus is not determinable because
[[Page 48965]]
data sufficient to perform the required analyses are lacking.
Therefore, public input on features and areas in U.S. waters that may
meet the definition of critical habitat for the chambered nautilus is
invited. If we determine that designation of critical habitat is
prudent and determinable, we will publish a proposed designation of
critical habitat for the chambered nautilus in a separate rule. Such
designation must be limited to areas under United States jurisdiction.
50 CFR 424.12(g).
Protective Regulations Under Section 4(d) of the ESA
We are proposing to list the chambered nautilus as a threatened
species. In the case of threatened species, ESA section 4(d) gives the
Secretary discretion to determine whether, and to what extent, to
extend the prohibitions of Section 9 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 chambered nautilus 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 the chambered
nautilus 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 (Public Law 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 all aspects of this
proposal (See DATES and ADDRESSES).We are particularly interested in:
(1) New or updated information regarding the range, distribution, and
abundance of the chambered nautilus; (2) new or updated information
regarding the genetics and population structure of the chambered
nautilus; (3) habitat within the range of the chambered nautilus 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
chambered nautilus (e.g., landings of the species, illegal taking of
the species); (5) information on the commercial trade of the chambered
nautilus; (6) recent observations or sampling of the chambered
nautilus; (7) current or planned activities within the range of the
chambered nautilus and their possible impact on the species; and (8)
efforts being made to protect the chambered nautilus.
Public Comments Solicited on Critical Habitat
As noted above, we have determined that critical habitat is not
currently determinable for the chambered nautilus. To facilitate our
ongoing review, we request information describing the quality and
extent of habitat for the chambered nautilus, as well as information on
areas that may qualify as critical habitat for the species in waters
under U.S. jurisdiction. We note that based on the best available
scientific information regarding the range of the chambered nautilus,
waters of American Samoa may contain the only potential habitat for the
species that is currently under U.S. jurisdiction. We request that
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, be identified.
Areas outside the occupied geographical area should also be identified,
if such areas themselves are essential to the conservation of the
species and under U.S. jurisdiction. 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. 16
U.S.C. 1533(b)(2). Section 4(b)(2) also authorizes the Secretary to
exclude from a critical habitat designation any particular area 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. To facilitate our consideration under
Section 4(b)(2), we also request for any area that may potentially
qualify as critical habitat information describing: (1) Activities or
other threats to the essential features of occupied habitat or
activities that could be affected by designating a particular area 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 particular 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. See 50 CFR 424.12(g). In keeping with the guidance
provided by OMB (2000; 2003), we seek information that would allow the
quantification 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) by the chambered nautilus, as well as any additional
information on occupied and unoccupied habitat areas; (2) the reasons
why any specific area of 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
[[Page 48966]]
areas as critical habitat; (4) current or planned activities in the
areas that might qualify 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 for the conservation
of the species; and (7) individuals who could serve as peer reviewers
in connection with 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 within the docket folder under ``Supporting Documents''
(www.regulations.gov/#!docketDetail;D=NOAA-NMFS-2016-0098) and 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, 657 F. 2d 829 (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: October 16, 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, paragraph (e), add a new table subheading for
``Molluscs'' before the ``Corals'' subheading and adding a new entry
for ``nautilus, chambered'' under the ``Molluscs'' table subheading to
read as follows:
Sec. 223.102 Enumeration of threatened marine and anadromous species.
* * * * *
(e) * * *
----------------------------------------------------------------------------------------------------------------
Species \1\
--------------------------------------------------------------- Citation(s) for Critical
Description of listing habitat ESA rules
Common name Scientific name listed entity determination(s)
----------------------------------------------------------------------------------------------------------------
* * * * * * *
----------------------------------------------------------------------------------------------------------------
Molluscs
----------------------------------------------------------------------------------------------------------------
Nautilus, chambered......... Nautilus Entire species. [Insert Federal NA NA
pompilius. Register
citation and
date when
published as a
final rule].
----------------------------------------------------------------------------------------------------------------
Corals
----------------------------------------------------------------------------------------------------------------
* * * * * * *
----------------------------------------------------------------------------------------------------------------
\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).
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[FR Doc. 2017-22771 Filed 10-20-17; 8:45 am]
BILLING CODE 3510-22-P