12-Month Finding and Proposed Rule To List the Chambered Nautilus as Threatened Under the Endangered Species Act, 48948-48967 [2017-22771]

Agencies

• DEPARTMENT OF COMMERCE
• National Oceanic and Atmospheric Administration

[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]



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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: https://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 https://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 https://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., https://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

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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).


[[Page 48967]]

[FR Doc. 2017-22771 Filed 10-20-17; 8:45 am]
 BILLING CODE 3510-22-P