[Federal Register Volume 79, Number 241 (Tuesday, December 16, 2014)]
[Proposed Rules]
[Pages 74954-74984]
From the Federal Register Online via the Government Publishing Office [www.gpo.gov]
[FR Doc No: 2014-29203]
[[Page 74953]]
Vol. 79
Tuesday,
No. 241
December 16, 2014
Part IV
Department of Commerce
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National Oceanic and Atmospheric Administration
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50 CFR Parts 223 and 224
Endangered and Threatened Wildlife and Plants; 12-Month Finding for the
Eastern Taiwan Strait Indo-Pacific Humpback Dolphin, Dusky Sea Snake,
Banggai Cardinalfish, Harrisson's Dogfish, and Three Corals Under the
Endangered Species Act; Proposed Rule
Federal Register / Vol. 79 , No. 241 / Tuesday, December 16, 2014 /
Proposed Rules
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DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration
50 CFR Parts 223 and 224
[Docket No. 140707555-4999-01]
RIN 0648-XD370
Endangered and Threatened Wildlife and Plants; 12-Month Finding
for the Eastern Taiwan Strait Indo-Pacific Humpback Dolphin, Dusky Sea
Snake, Banggai Cardinalfish, Harrisson's Dogfish, and Three Corals
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, have completed comprehensive status reviews under
the Endangered Species Act (ESA) for seven foreign marine species in
response to a petition to list those species. These seven species are
the Eastern Taiwan Strait population of Indo-Pacific humpback dolphin
(Sousa chinensis), dusky sea snake (Aipysurus fuscus), Banggai
cardinalfish (Pterapogon kauderni), Harrisson's dogfish (Centrophorus
harrissoni), and the corals Cantharellus noumeae, Siderastrea glynni,
and Tubastraea floreana. We have determined that the Eastern Taiwan
Strait Indo-Pacific humpback dolphin is not a distinct population
segment and therefore does not warrant listing. We have determined
that, based on the best scientific and commercial data available, and
after taking into account efforts being made to protect the species,
Pterapogon kauderni, and Centrophorus harrissoni meet the definition of
a threatened species; and Aipysurus fuscus, Cantharellus noumeae,
Siderastrea glynni, and Tubastraea floreana meet the definition of an
endangered species. Therefore, we propose to list these six species
under the ESA. We are not proposing to designate critical habitat for
any of the species proposed for listing, because the geographical areas
occupied by these species are entirely outside U.S. jurisdiction, and
we have not identified any unoccupied areas that are currently
essential to the conservation of any of these species. We are
soliciting comments on our proposals to list the six species. We are
also proposing related administrative changes to our lists of
threatened and endangered species.
DATES: Comments on our proposed rule to list eight species must be
received by February 17, 2015. Public hearing requests must be made by
January 30, 2015.
ADDRESSES: You may submit comments on this document, identified by
NOAA-NMFS-2014-0083, by any 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-2014-0083. Click the ``Comment Now'' icon,
complete the required fields, and enter or attach your comments.
Mail: Submit written comments to, Lisa Manning, NMFS
Office of Protected Resources (F/PR3), 1315 East West Highway, Silver
Spring, MD 20910, USA.
Instructions: You must submit comments by one of the above methods
to ensure that we receive, document, and consider them. 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. All
comments received are a part of the public record and will generally be
posted for public viewing on http://www.regulations.gov without change.
All personal identifying information (e.g., name, address, etc.),
confidential business information, or otherwise sensitive information
submitted voluntarily by the sender will be publicly accessible. We
will accept anonymous comments (enter ``N/A'' in the required fields if
you wish to remain anonymous). Attachments to electronic comments will
be accepted in Microsoft Word, Excel, or Adobe PDF file formats only.
You can obtain the petition, status review reports, the proposed
rule, and the list of references electronically on our NMFS Web site at
http://www.nmfs.noaa.gov/pr/species/petition81.htm.
FOR FURTHER INFORMATION CONTACT: Lisa Manning, NMFS, Office of
Protected Resources (OPR), (301) 427-8403.
SUPPLEMENTARY INFORMATION:
Background
On July 15, 2013, we received a petition from WildEarth Guardians
to list 81 marine species as threatened or endangered under the
Endangered Species Act (ESA). This petition included species from many
different taxonomic groups, and we prepared our 90-day findings in
batches by taxonomic group. We found that the petitioned actions may be
warranted for 27 of the 81 species and announced the initiation of
status reviews for each of the 27 species (78 FR 63941, October 25,
2013; 78 FR 66675, November 6, 2013; 78 FR 69376, November 19, 2013; 79
FR 9880, February 21, 2014; and 79 FR 10104, February 24, 2014). This
document addresses the findings for 7 of those 27 species: the Eastern
Taiwan Strait population of Indo-Pacific humpback dolphin (Sousa
chinensis), dusky sea snake (Aipysurus fuscus), Banggai cardinalfish
(Pterapogon kauderni), Harrisson's dogfish (Centrophorus harrissoni),
and the corals Cantharellus noumeae, Siderastrea glynni, and Tubastraea
floreana. The remaining 20 species will be addressed in subsequent
findings.
We are responsible for determining whether species are threatened
or endangered under the ESA (16 U.S.C. 1531 et seq.). To make this
determination, we consider first whether a group of organisms
constitutes a ``species'' under the ESA, then whether the status of the
species qualifies it for listing as either threatened or endangered.
Section 3 of the ESA defines a ``species'' to include ``any subspecies
of fish or wildlife or plants, and any distinct population segment of
any species of vertebrate fish or wildlife which interbreeds when
mature.'' On February 7, 1996, NMFS and the U.S. Fish and Wildlife
Service (USFWS; together, the Services) adopted a policy describing
what constitutes a distinct population segment (DPS) of a taxonomic
species (the DPS Policy; 61 FR 4722). The DPS Policy identified two
elements that must be considered when identifying a DPS: (1) The
discreteness of the population segment in relation to the remainder of
the species (or subspecies) to which it belongs; and (2) the
significance of the population segment to the remainder of the species
(or subspecies) to which it belongs. As stated in the DPS Policy,
Congress expressed its expectation that the Services would exercise
authority with regard to DPSs sparingly and only when the biological
evidence indicates such action is warranted.
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.'' We interpret an
``endangered species'' to be one that is presently in danger of
extinction. A ``threatened species,'' on the other hand, is not
presently in danger of extinction, but is likely to become so in the
foreseeable future (that
[[Page 74955]]
is, at a later time). In other words, the primary statutory difference
between a threatened and endangered species is the timing of when a
species may be in danger of extinction, either presently (endangered)
or in the foreseeable future (threatened).
When we consider whether species might qualify 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. The foreseeable future considers
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. Discussions of the considerations for each relevant species
are in the species-specific sections below.
Section 4(a)(1) of the ESA requires us to determine whether any
species is endangered or threatened due to any one or a combination of
the following five threat 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. 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 being made by any state or foreign nation
to protect the species.
In making a listing determination, we first determine whether a
petitioned species meets the ESA definition of a ``species.'' Next,
using the best available information gathered during the status review
for the species, we complete a status and extinction risk assessment.
In assessing extinction risk, we consider the demographic viability
factors developed by McElhany et al. (2000) and the risk matrix
approach developed by Wainwright and Kope (1999) to organize and
summarize extinction risk considerations. The approach of considering
demographic risk factors to help frame the consideration of extinction
risk has been used in many of our status reviews, including for Pacific
salmonids, Pacific hake, walleye pollock, Pacific cod, Puget Sound
rockfishes, Pacific herring, scalloped hammerhead sharks, and black
abalone (see http://www.nmfs.noaa.gov/pr/species/ for links to these
reviews). In this approach, the collective condition of individual
populations is considered at the species level according to four
demographic viability factors: Abundance, growth rate/productivity,
spatial structure/connectivity, and diversity. These viability factors
reflect concepts that are well-founded in conservation biology and that
individually and collectively provide strong indicators of extinction
risk.
We then assess efforts being made to protect the species, to
determine if these conservation efforts are adequate to mitigate the
existing threats. Section 4(b)(1)(A) of the ESA requires the Secretary,
when making a listing determination for a species, to take into
consideration those efforts, if any, being made by any State or foreign
nation to protect the species. We also evaluate conservation efforts
that have not yet been fully implemented or shown to be effective using
the criteria outlined in the joint NMFS/USFWS Policy for Evaluating
Conservation Efforts (PECE; 68 FR 15100, March 28, 2003), to determine
their certainty of implementation and effectiveness. The PECE is
designed to ensure consistent and adequate evaluation of whether any
conservation efforts that have been recently adopted or implemented,
but not yet demonstrated to be effective, will result in recovering the
species to the point at which listing is not warranted or contribute to
forming the basis for listing a species as threatened rather than
endangered. The two basic criteria established by the PECE are: (1) The
certainty that the conservation efforts will be implemented; and (2)
the certainty that the efforts will be effective. We consider these
criteria in each species-specific section, as applicable, below.
Finally, we re-assess the extinction risk of the species in light of
the existing conservation efforts.
Status Reviews
Status reviews for the petitioned species addressed in this finding
were conducted by NMFS OPR staff. Separate status reviews were done for
the Eastern Taiwan Strait Indo-Pacific humpback dolphin (Whittaker,
2014), dusky sea snake (Manning, 2014), Banggai cardinalfish (Conant,
2014), Harrison's dogfish (Miller, 2014), and the three corals
(Meadows, 2014). In order to complete the status reviews, we compiled
information on the species' biology, ecology, life history, threats,
and conservation status from information contained in the petition, our
files, a comprehensive literature search, and consultation with
experts. We also considered information submitted by the public in
response to our petition findings. Draft status review reports were
also submitted to independent peer reviewers; comments and information
received from peer reviewers were addressed and incorporated as
appropriate before finalizing the draft reports.
Each status review report provides a thorough discussion of
demographic risks and threats to the particular species. We considered
all identified threats, both individually and cumulatively, to
determine whether the species responds in a way that causes actual
impacts at the species level. The collective condition of individual
populations was also considered at the species level, according to the
four demographic viability factors discussed above.
The status review reports are available on our Web site (see
ADDRESSES section). Below we summarize information from those reports
and the status of each species.
Eastern Taiwan Strait Population of the Indo-Pacific Humpback Dolphin
The following section describes our analysis of the status of the
Eastern Taiwan Strait (ETS) population of the Indo-Pacific Humpback
dolphin, Sousa chinensis.
Species Description
The Indo-Pacific humpback dolphin, Sousa chinensis (Osbeck, 1765),
within the genus Sousa, family Delphinidae, and order Cetacea, is
broadly distributed. The taxonomy of the genus is unresolved and has
historically been based on morphology, but genetic analyses have
recently been used. Current taxonomic hypotheses identify Sousa
chinensis as one of two (Jefferson et al., 2001), three (Rice, 1998),
or four (Mendez et al., 2013) species within the genus. Each species is
associated with a unique geographic range, though the species' defined
ranges vary depending on how many species are recognized. Rice (1998)
recognizes Sousa teuzii in the eastern Atlantic, Sousa plumbea in the
western Indo-Pacific, and Sousa chinensis in the eastern Indo-Pacific.
Mendez et al. (2013) recently identified an as-yet unnamed potential
new species in waters off of northern Australia. Currently, the
International Union for Conservation of Nature (IUCN) and International
Whaling Commission (IWC) Scientific Committee
[[Page 74956]]
recognize only two species, Sousa chinensis in the Indo-Pacific, and
Sousa teuzii in the eastern Atlantic. Here, we follow a similar two-
species taxonomy in our consideration of the genus and identification
of the species Sousa chinensis. Under that taxonomy, Sousa chinensis'
range includes nearshore tropical and subtropical habitats in southern
Africa, the Indian Ocean, North Australia, southern mainland China,
Hong Kong, and Taiwan (Jefferson et al., 2001; Mendez et al., 2013). We
chose to follow a two-species taxonomy as it provides the clearest
genetic, morphological, and geographic delineation of the species and
is well supported by the current data available. While growing genetic
and phylogeographic evidence suggests that Sousa chinensis is
associated with further genetic subdivisions, more data are needed to
clarify the taxonomy and delineate the geographic boundaries and ranges
of these additional genetic units (Cockroft et al., 1997; Jefferson et
al., 2004b; Fr[egrave]re et al., 2008; Fr[egrave]re et al., 2011; Lin
et al., 2012; Mendez et al., 2013).
The Indo-Pacific humpback dolphin is easy to distinguish from other
dolphin species in its range, as it is characterized by a robust body,
a long, distinct beak, a short dorsal fin atop a wide dorsal hump, and
round-tipped, broad flippers and flukes (Jefferson et al., 2001). The
Indo-Pacific humpback dolphin is medium-sized, up to 2.8 m in length,
weighing 250-280 kg (Ross et al., 1994). Morphological plasticity
exists among populations of the species and is correlated with their
geographic distributions (Ross et al., 1994). For example, the Eastern
Taiwan Strait population, which occurs at the eastern portion of the
species' range, has a short dorsal fin with a wide base; the base of
the fin measures 5-10 percent of the body length and slopes gradually
into the surface of the body. This differs from individuals in the
western portion of the range, which have a larger hump that comprises
about 30 percent of body width, and forms the base of an even smaller
dorsal fin (Ross et al., 1994). Males and females from the Pearl River
Estuary population, and in other populations of Southeast Asia, do not
exhibit sexual dimorphism in size, growth patterns, or morphology
(Jefferson et al., 2001; Jefferson et al., 2012). In contrast,
individuals from South Africa exhibit sexual dimorphism in terms of
size and dorsal hump morphology (Ross et al., 1994; Karczmarski et al.,
1997).
The species occurs in a range of nearshore habitats, including
estuaries, mangroves, seagrass meadows, coastal lagoons, and sandy
beaches (Ross et al., 1994). In Thailand, Malaysia, and Indonesia,
nearshore ecosystems are associated with tropical seagrass, coral, and
mangrove lagoons (Beasley et al., 1997; Smith et al., 2003;
Adulyanukosol et al., 2006; Jaroensutasinee et al., 2011; Cherdsukai et
al., 2013). In India, the species is associated with nearshore habitat
consisting of mangroves, corals, and tidal mudflat, heavily influenced
by monsoons that regulate the influx of freshwater to the system
(Sutaria et al., 2004). The coast of mainland China is thought to host
at least eight populations of the species, primarily occurring in
estuarine systems at the mouths of large rivers (Jefferson et al.,
2001; Jefferson et al., 2004a). Two coastal Chinese populations, in
close proximity to the population in the Eastern Taiwan Strait, are
relatively well-studied. These are the Pearl River Estuary/Hong Kong
population and the Jiulong River Estuary/Xaimen population, both of
which depend upon ecosystem productivity associated with the nutrient
output supplied by large rivers (Chen et al., 2008; Chen et al., 2010).
The Eastern Taiwan Strait population of Sousa chinensis (henceforth
referred to as the ETS humpback dolphin), for which we were petitioned,
was first described in 2002 during an exploratory survey of coastal
waters off of western Taiwan (Wang et al., 2004). Prior to these
coastal surveys, there are few records mentioning the species in this
region, save two strandings, a few photographs, and anecdotal reports
(Wang, 2004), so their history in the region is unclear. Since the
first survey in 2002, researchers have confirmed their year-round
presence in the Eastern Taiwan Strait (Wang et al., 2011), inhabiting
estuarine and coastal waters of central-western Taiwan.
The ETS humpback dolphin habitat is most similar to that of the
populations located off the coast of mainland China. Individuals of the
ETS humpback dolphin population are thought to be restricted to water
less than 30 meters deep, and most observed sightings have occurred in
estuarine habitat with significant freshwater input (Wang et al.,
2007b). Across the ETS humpback dolphin habitat, bottom substrate
consists of soft-sloping muddy sediment with elevated nutrient inputs,
primarily influenced by river deposition (Sheehy, 2010). These nutrient
inputs support high primary production, which fuels upper trophic
levels, contributing to the dolphin's source of food (Jefferson, 2000).
The Indo-Pacific humpback dolphin is considered a generalist and
opportunistic piscivore (Barros et al., 2004). As is common to the
species as a whole, the ETS population uses echolocation and passive
listening to find its prey. While little is known about the specific
diet and feeding of the ETS population, diet can be inferred from that
of other humpback dolphin populations (Barros et al., 2004; Chen et
al., 2009). In Chinese waters off Hong Kong, the species consumes both
bottom-dwelling and pelagic fish species, including croakers
(Sciaenidae), mullets (Mugilidae), threadfins (Polynemidae), and
herring (Clupeidae) (Barros et al., 2004). Part of the feeding strategy
for this population may be to induce shoaling of fish by physically
corralling them, allowing individuals to forage and feed successfully,
even within murky nearshore waters (Sheehy, 2009). In general, the prey
species of the humpback dolphin include small fish which are generally
not commercially valuable to local fisheries (Barros et al., 2004;
Sheehy, 2009).
Little is known about the life history and reproduction of ETS
humpback dolphin. In some cases, comparison of the ETS population with
other populations may be appropriate, but one needs to be cautious
about making these comparisons, as environmental factors such as food
availability and habitat status may affect important rates of
reproduction and generation time in different populations. A recent
analysis of life history patterns for individuals in the Pearl River
Estuary (PRE) population is the best proxy for the ETS population. Like
the ETS population, the PRE population inhabits estuarine and
freshwater-influenced environments in similar proximity to
anthropogenic activity (Jefferson et al., 2012). Maximum longevity for
the PRE population is estimated to be greater than 38 years (Jefferson
et al., 2012). Evidence from multi-year photo-analysis of the ETS
population demonstrated that adult survivorship is high, 0.985,
suggesting that this population also has a relatively long lifespan
(Wang et al., 2012). In general, it is inferred that the population has
long calving intervals, between 3 and 5 years (Jefferson et al., 2012).
Gestation lasts 10-12 months (Jefferson et al., 2012). Weaning may take
up to 2 years, and strong female-calf association may last 3-4 years
(Karczmarski et al., 1997; Karczmarski, 1999). Peak calving activity
most likely occurs in the warmer months, but exact peak of calving time
may vary geographically (Jefferson et al., 2012). Age at sexual
maturity is late, estimated at between 12 and 14 years (Jefferson et
al., 2012).
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DPS Analysis
The following section provides our analysis, based on the best
available science and the DPS Policy, to determine whether the ETS
humpback dolphin population qualifies as a DPS of the taxon.
Discreteness
The Services' joint DPS Policy states that a population segment of
a vertebrate species may be considered discrete if it satisfies either
one of the following conditions: (1) It is markedly separated from
other populations of the same taxon as a consequence of physical,
physiological, ecological, or behavioral factors (quantitative measures
of genetic or morphological discontinuity may provide evidence of this
separation); or (2) it is delimited by international governmental
boundaries within which differences in control of exploitation,
management of habitat, conservation status, or regulatory mechanisms
exist that are significant in light of section 4(a)(1)(D) of the ESA
(61 FR 4722; February 7, 1996).
Individuals from the ETS population exhibit pigmentation that
differs significantly from nearby populations along the mainland coast
of China, and evidence suggests that pigmentation varies geographically
across the species' range (Jefferson et al., 2001; Jefferson et al.,
2004a; Wang et al., 2008). Across the species, pigmentation changes as
individuals mature. When young, dolphins appear dark grey with no or
few light-colored spots; as they age, they transform to mostly white
(appearing pinkish), as dark spots decrease with age. In particular,
the developmental transformation of pigment differs significantly
between ETS and nearby Chinese humpback dolphin populations;
specifically, the spotting intensity (density of spots) on the dorsal
fin of the ETS population is significantly greater than that of four
mainland Chinese populations, including the other nearby populations in
the Pearl River Estuary and Jiulong River estuaries (Wang et al.,
2008). Significantly greater spotting intensity on the dorsal fin of
the ETS population is consistent, regardless of age (Wang et al.,
2008). Further, the ETS humpback dolphin never loses the dark dorsal
fin spots completely, as has been observed in older individuals of
other humpback dolphin populations (Wang et al., 2008). In contrast,
dorsal fins of Chinese populations are strikingly devoid of spots,
compared to their bodies, throughout most of their lives, except when
they are very young or very old (Wang et al., 2008). These differences
in pigmentation can be used to reliably differentiate between the ETS
humpback dolphin and nearby Chinese populations (Wang et al., 2008).
Thus, we consider these significant differences in pigmentation of the
ETS humpback dolphin as evidence of its discreteness.
Several researchers have suggested that the ETS population of the
humpback dolphin is physically and geographically isolated from other
populations, based on the fact that individuals have not been observed
crossing or to have crossed the Strait of Taiwan, despite repeated
surveys of Chinese and Taiwanese populations using photo-identification
techniques (Wang et al., 2004; Wang et al., 2007b; Chen et al., 2010;
Wang et al., 2011; Wang et al., 2012). For instance, a detailed
analysis of more than 450 individually-recognizable dolphins catalogued
for Taiwanese and Chinese populations revealed no matches among them
(Wang et al., 2008). Movement of Sousa chinensis is thought to be
limited to shallow water and nearshore habitat (Karczmarski et al.,
1997; Hung et al., 2004). Water depth and fast-moving currents within
the Eastern Taiwan Strait are thought to isolate the ETS population
from Chinese populations, despite their relatively close geographic
proximity (Wang et al., 2004; Wang et al., 2008; Wang et al., 2011; Wee
et al., 2011; Wang et al., 2012). In fact, the ETS population has never
been observed in waters greater than 30 meters depth (Wang et al.,
2007b). Evidence suggests that the ETS population of the humpback
dolphin has a narrow home range, and does not migrate seasonally or mix
with Chinese populations (Wang et al., 2011). The population has been
shown to inhabit the shallow, narrow habitat on the western coast of
Taiwan throughout the year, and exhibits strong site fidelity (Wang et
al., 2011).
The evidence for geographic isolation is based on limited survey
data collected since 2002, which focused only on nearshore waters at
certain times of year and did not survey the Strait waters between
mainland China and Western Taiwan (Wang et al., 2004; Wang et al.,
2011; Wang et al., 2012). Thus, the possibility for Indo-Pacific
humpback dolphin migration or emigration across the Strait cannot be
eliminated entirely. However, the best available scientific information
indicates that the species is found primarily in shallow nearshore
habitat, and the ETS population has never been observed in waters
greater than 30 meters, and thus migration or emigration across the
deeper Strait is thought to occur rarely, if ever.
The best available data suggest that the ETS humpback dolphin
population is discrete from all other populations of the species based
on its morphological differences. Although limited, the best available
data also suggest that the ETS humpback dolphin population is
geographically isolated from other populations. The morphological
differences and geographic isolation set this population apart from
other populations of the Indo-Pacific humpback dolphin, and thus, we
conclude that the ETS humpback dolphin population meets the
discreteness criterion of the DPS Policy.
Significance
When the discreteness criterion is met for a potential DPS, as it
is for the ETS humpback dolphin population, the second element that
must be considered under the DPS Policy is the significance of the DPS
to the taxon as a whole. Significance is evaluated in terms of the
importance of the population segment to the taxon to which it belongs,
in this case the species Sousa chinensis. Some of the considerations
that can be used under the DPS Policy to determine a discrete
population segment's significance to the taxon as a whole include: (1)
Persistence of the population segment in an unusual or unique
ecological setting; (2) evidence that loss of the population segment
would result in a significant gap in the range of the taxon; and (3)
evidence that the population segment differs markedly from other
populations of the species in its genetic characteristics.
The ETS humpback dolphin population occurs in an ecological setting
similar to populations occurring along the coast of mainland China, and
many features of its habitat and ecology are similar to those of
populations throughout the range of the species, as discussed above.
Throughout its range, the Indo-Pacific humpback dolphin is consistently
associated with coastal river output and is found in shallow nearshore
waters (Jefferson et al., 2001). It displays no apparent preference for
clear or turbid waters (Karczmarski et al., 2000). The habitat and
ecosystem use of the species differ in some ways geographically, but
evidence suggests that the dolphin is an opportunistic piscivore, and
thus does not exhibit unique or restricted feeding ecology across its
range (Jefferson et al., 2001).
In Thailand, Malaysia, and Indonesia, the species occurs in
tropical seagrass, coral, and mangrove lagoons not present in ETS
humpback dolphin habitat (Beasley et al., 1997; Smith et al., 2003;
Adulyanukosol et al., 2006; Jaroensutasinee et al., 2011; Chersukjai
[[Page 74958]]
et al., 2013). In India, the species is associated with nearshore
habitat consisting of mangroves, corals, and tidal mudflat, heavily
influenced by monsoons that regulate the influx of freshwater to the
system (Sutaria et al., 2004). The ETS humpback dolphin habitat is most
similar to that of coastal Chinese populations, with more temperate
water, soft muddy substrate, and consistent input from river systems.
The ETS humpback dolphin habitat differs from the habitat occupied by
mainland Chinese populations in some ways, with nearby rivers generally
smaller than those in mainland China, and with warmer waters in the
winter due to the influence of the Kuroshio Current, which periodically
moves into the Strait of Taiwan (Chern et al., 1990; Jan et al., 2002;
Wang et al., 2008). However, feeding ecology, prey availability, and
prey preference are thought to be similar in mainland China and Taiwan
(Barros et al., 2004; Wang et al., 2007a), so these small differences
in habitat do not seem to have significant effects on the species'
ecology.
The presumed habitat of the ETS humpback dolphin is narrower in
offshore width than that of other studied populations of the taxon. For
instance, the ETS population is thought to inhabit a small area of
coastal shallow waters within 3 km from the shore (Wang et al., 2007b).
In contrast, Chinese populations inhabit a broader shallow area ranging
tens of kilometers offshore, where dolphins can range farther from the
coastline without moving into deeper water (Hung et al., 2004; Chen et
al., 2011). While the ETS population exhibits some behavioral
differences, such as increased cooperative calf-rearing and social
connectivity, as compared to Chinese populations (Dungan et al., 2011),
it is uncertain whether or not these differences are adaptive or
facultative, and simply based on the population's low abundance. Thus,
insufficient evidence exists to suggest significant differences in the
dolphin's ecology or adaptation have derived from the differences in
the physical parameters of its environment. Therefore, differences in
the habitat and ecological setting of the ETS humpback dolphin do not
set it apart from the rest of the taxon, and do not appear to relate to
significant selection pressures affecting the population's foraging,
behavior, or ecology.
There is no evidence to suggest that loss of the ETS humpback
dolphin population would result in a significant gap in the range of
the taxon. The ETS humpback dolphin population constitutes a small and
peripheral portion of the entire range of the species, and its loss
would not inhibit population movement or gene flow among other
populations of the species (Lin et al., 2012). The ETS humpback dolphin
is distributed throughout only 512 square kilometers of coastal waters
off Western Taiwan; this small range is not geographically significant
in comparison to the taxon's range throughout the coastal Indo-Pacific
and Indian Oceans.
There are no data to show that the genetic characteristics of the
ETS humpback dolphin population differ markedly from other populations
in a significant way. While pigmentation of the ETS population is
significantly different from other populations within the taxon (Wang
et al., 2008), whether the pattern is adaptive or has genetic
underpinnings is unknown. In other cetacean species, differences in
pigmentation have been hypothesized to relate to several adaptive
responses, allowing individuals to hide from predators, communicate
with conspecifics (promoting group cohesion), and disorient and corral
prey (Caro et al., 2011). However, the differences in ETS humpback
dolphin pigmentation may be a result of a genetic bottleneck from the
small size of this population (less than 100 individuals) and the
possibility that it represents a single social and/or family group.
Such small populations are more heavily influenced by genetic drift
than large populations (Frankham, 1996). Insufficient data exist to
determine whether significant differences in ETS humpback dolphin
pigmentation relate to the functional divergence of the population, or
are simply a product of genetic drift and a genetic bottleneck. The
best data available thus lead us to conclude that loss of the ETS
humpback dolphin population would not result in significant loss of
overall genetic or ecological diversity of the taxon as a whole.
DPS Conclusion and Proposed Determination
According to our analysis, the ETS humpback dolphin population is
considered discrete based on its unique pigmentation patterns, which
set it apart morphologically from the rest of the taxon, and evidence
for its geographic isolation. However, while discrete, the ETS humpback
dolphin population does not meet any criteria for significance to the
taxon as a whole. The ecological setting it occupies is similar to that
of the rest of the species, loss of the population would not constitute
a significant gap in the taxon's extensive range, and no genetic or
other data have demonstrated that the population makes a significant
contribution to the adaptive, ecological, or genetic diversity of the
taxon. As such, based on the best available data, we conclude that the
ETS humpback dolphin population is not a DPS and thus does not qualify
for listing under the ESA. This is a final action, and, therefore, we
do not solicit comments on it.
Dusky Sea Snake
The section below presents our analysis of the status of the dusky
sea snake, Aipysurus fuscus. Further details can be found in Manning
(2014).
Species Description
The dusky sea snake, Aipysurus fuscus, is a species within the
family Elapidae, which is a very diverse family of venomous snakes. The
genus Aipysurus contains seven species, six of which are restricted to
Australasian waters. The dusky sea snake is brown, blackish-brown, or
purplish-brown with wide ventral scales and diamond-shaped body scales
that are smooth and imbricate (i.e., overlapping). There are generally
19 scale rows around the neck, 19 around the mid-body, and 155 to 180
ventral scales (Rasmussen, 2000). The dusky sea snake is completely
aquatic and, like all sea snakes, has a paddle-like tail for swimming.
Its maximum total length is about 90 cm (Rasmussen, 2000). Growth rates
for the dusky sea snake have not been documented, but reported growth
rates for other sea snakes range from 0.07-1.0 mm per day and decline
with age (Heatwole, 1997). The maximum lifespan for dusky sea snakes
has been assumed to be about 10 years, and age at first maturity has
been assumed to be about 3-4 years (Lukoschek et al., 2010). Generation
length is thought to be approximately 5 years (Lukoschek et al., 2010).
Despite its aquatic existence, and like all reptiles, the dusky sea
snake lacks gills and must surface to breathe air. Dive durations vary
by species, but most sea snakes typically stay submerged for about 30
minutes, and some for up to 1.5-2.5 hours (Heatwole and Seymour, 1975).
Maximum dive depth for dusky sea snakes is unknown, but co-occurring
members of this genus are considered ``shallow'' and ``intermediate''
depth species that dive no deeper than 20 m or 50 m, respectively
(Heatwole and Seymour, 1975).
The dusky sea snake is viviparous, meaning embryos develop
internally and young undergo live birth. Because this species never
ventures on land, mating occurs at sea and young are born alive in the
water. Within the genus Aipysurus, the number of young per
[[Page 74959]]
brood is small, usually less than four, and young are relatively large
at birth (Cogger, 1975). Timing and seasonality of the dusky sea
snake's breeding cycles are unknown, and very little is known about the
juvenile life stage.
The dusky sea snake preys mainly on labrid (e.g., wrasses) and
gobiid (e.g., gobies) fishes, and to a lesser extent, fish eggs
(McCosker, 1975). Food competition among sympatric sea snakes is
thought to be minimal, based on examinations of diet composition for
sympatric sea snakes (McCosker, 1975; Voris and Voris, 1983). Feeding
behavior of dusky sea snakes has not been thoroughly investigated;
however, during surveys at Ashmore Reef, Australia, Guinea and Whiting
(2005) commonly saw dusky sea snakes over sand bottom habitat and
watched one snake actually force its head and about 15 percent of its
body into the sand. However, because it emerged without a prey item
(Guinea and Whiting, 2005), it is unclear whether this was foraging or
some other behavior. Like their terrestrial relatives, sea snakes
swallow their prey whole and therefore must have some strategy for
subduing them. McCosker (1975) hypothesized that the highly toxic venom
of sea snakes is probably more of a feeding adaptation than a defensive
one.
The dusky sea snake is a benthic, coral reef-associated species
endemic to several shallow emergent reefs of the Sahul Shelf off the
coast of Western Australia in the Timor Sea, between Timor and
Australia. These reefs are relatively isolated and lie at the edge of
the continental shelf over several hundred kilometers from the
mainland. The dusky sea snake has been reported to occur at Ashmore,
Scott, Seringapatam, and Hibernia Reefs and Cartier Island; however,
individual surveys have not consistently recorded dusky sea snakes at
all of these locations. For example, in transect surveys conducted by
Minton and Heatwole (1975) over several weeks during December 1972 and
January 1973 at Ashmore, Scott, and Hibernia Reefs and Cartier Island,
dusky sea snakes were recorded at Scott and Ashmore reefs only.
Extensive surveys conducted more recently at Ashmore Reef, where dusky
sea snakes were once relatively common, have located no specimens
(Guinea, 2013; Lukoschek et al., 2013). Lukoschek et al. (2010)
estimated that the area of occurrence of dusky sea snakes is probably
less than 500 km\2\.
During their surveys, Minton and Heatwole (1975) observed dusky sea
snakes in shallow water (<10 m) as well as in the 12 to 25 m depth-
zone. They were observed in areas of moderate to heavy coral growth,
but they were also observed to congregate in sandy-bottomed gullies and
channels (Minton and Heatwole, 1975). Home-range size and site fidelity
of individual dusky sea snakes has not been evaluated. However, a
short-term (6-9 days), telemetry study on the sympatric olive sea
snakes (A. laevis) and a long-term (8-year), mark-recapture study on
the turtle-headed sea snake (Emydocephalus annulatus) suggest that
home-ranges of sea snakes are small, movement of adults is very
limited, and longer-distance dispersal may be due mainly to passive
transport, such as by currents and storms (Burns and Heatwole, 1998;
Lukoschek and Shine 2012). While it is very plausible that adult A.
fuscus are similar to these other species, research to evaluate adult
and juvenile A. fuscus habitat use and movement is needed.
Sea snakes typically have patchy distributions and can be found in
very dense aggregations in certain locations within their ranges
(Heatwole, 1997). This patchiness complicates efforts to understand
habitat use patterns, as seemingly suitable habitat can remain
unoccupied. On a smaller spatial scale, distributions of sea snake
fauna on Australian reefs appear to be influenced by water depth,
substrate type, and feeding strategies (McCosker, 1975; Heatwole,
1975b). Other biotic factors, such as limited juvenile dispersal, may
also contribute to the observed patchy distributions (Lukoschek et al.,
2007a). Overall, however, causative factors for observed distributions
are not completely understood.
Population Abundance, Distribution, and Structure
There are no historical or current population estimates for the
dusky sea snake. However, multiple reefs have been surveyed repeatedly,
and although survey methodologies have varied, the data provide some
indication of population trends for some locations. For Ashmore Reef in
particular, the survey data provide a strong indication of severe
population decline and possible extirpation. Older surveys dating from
1972 to 2002 by various researchers indicate that the relative
abundance of A. fuscus was fairly consistent and represented about 10-
23 percent of the sea snakes observed (see Table 1, Manning, 2014). A
footnote in Smith (1926) also indicates that a sample of 27 dusky sea
snakes (out of an ~100-specimen sea snake collection) had recently been
collected for him at Ashmore Reef. The dusky sea snake, however, has
not been recorded in a single survey conducted at Ashmore Reef after
2005, despite considerable effort (Lukoschek et al., 2013; Table 1,
Manning, 2014). Based on reef area data reported in Skewes et al.
(1999), Ashmore Reef represents about 40 percent of the dusky sea
snake's historical reef habitat. Extirpation from this reef would
represent a substantial change in the species' distribution and
abundance.
A survey in 2005 at Hibernia Reef indicated a relatively low
abundance of A. fuscus, and the most recent surveys, conducted in 2012
and 2013, have failed to detect any dusky sea snakes despite extensive
survey effort (Guinea, 2005; Guinea, 2013). Dusky sea snakes were
observed in surveys conducted at Scott Reef in 1972/73, 2006, 2012 and
2013; however, their relative abundance varies across the surveys, and
no trends are detectable given the limited data (see Table 1, Manning,
2014). For example, Guinea (2012) visited Scott Reef in February, 2006,
and reported that dusky sea snakes, as the third-most abundant species,
made up 15 percent of the total sea snake sightings (Guinea, 2013).
Portions of Scott Reef were surveyed again in 2012 and 2013, and dusky
sea snakes made up only 3.2 percent and 7.4 percent of the total
sightings respectively for each year (Guinea, 2013). At Seringapatam
Reef and Cartier Island, A. fuscus is rare or potentially absent.
Overall, while these limited abundance data are very difficult to
interpret, they indicate that dusky sea snakes have not been present in
high numbers in any recent reef surveys (Table 1, Manning, 2014).
The dusky sea snake has a restricted range, and structure and
connectivity of populations is uncertain. Assuming that A. fuscus is
extirpated from Ashmore Reef, Sanders et al. (2014) recently estimated
that the dusky sea snake's range is now less than 262 sq km. Although
structure and connectivity of reef populations of A. fuscus have not
been studied directly, some information may be gleaned from several
studies on the olive sea snake, A. laevis, a sympatric congener that is
larger in size, more common, and more widely distributed than A.
fuscus, but is very closely related to A. fuscus (Sanders et al.,
2013b). As mentioned above, a short-term (6-9 days) tracking study on
A. laevis suggests that adults of this species have small home ranges
(1,500-1,800 sq m) and undergo limited active dispersal (Burns and
Heatwole, 1998). Results of that study are somewhat supported by
analyses by Lukoschek et al. (2007b) of mitochondrial DNA (mtDNA) from
354 olive sea snakes collected across its range, including some samples
from Hibernia, Scott, and
[[Page 74960]]
Ashmore reefs and Cartier Island. Based on their results, Lukoschek et
al. (2007b) concluded that gene flow among the reefs of the Timor Sea
is low, and that olive sea snakes at these reefs have been diverging
for some time. A subsequent analysis of microsatellite DNA from the
same specimens indicates that two of the most distant Timor reef
populations of A. laevis are significantly diverged (Lukoschek et al.,
2008). However, the degrees of divergence of other reef populations
were not statistically significant, and there was no clear isolation-
by-distance relationship (Lukoschek et al., 2008). Although not
conclusive, the available information for the olive sea snake and the
fact that dusky sea snakes also lack a dispersive larval phase, suggest
connectivity of A. fuscus may be limited among some reefs within the
region. Limited inter-population exchange would increase the extinction
risk and reduce the recovery potential for local populations that have
experienced severe declines or have been lost.
Summary of Factors Affecting the Dusky Sea Snake
Available information regarding current, historical, and potential
threats to the dusky sea snake was thoroughly reviewed (Manning, 2014).
Although causes for observed declines in dusky sea snake have not been
conclusively determined, we found that the species is being threatened
by hybridization. Other possible threats include vessels, pollution,
climate change, and inadequate regulatory mechanisms. We summarize
information regarding each of these threats below according to the
factors specified in section 4(a)(1) of the ESA. Available information
does not indicate that disease, predation, or overutilization
(including bycatch) are operative threats on this species; therefore,
we do not discuss those further here. See Manning (2014) for additional
discussion of all ESA Section 4(a)(1) threat categories.
The Present or Threatened Destruction, Modification, or Curtailment of
Its Habitat or Range
Aipysurus fuscus is dependent on coral reefs for prey and shelter,
and loss of live coral is a possible mechanism contributing to the
decline of A. fuscus at locations such as Ashmore Reef. Coral reefs of
the Sahul Shelf experienced widespread bleaching in response to El
Ni[ntilde]o events in 1998 and 2003. Ashmore Reef experienced bleaching
in 1998 and again, to an apparently greater extent, in 2003 (Lukoschek
et al., 2013). However, because there are no estimates of coral
coverage prior to 1998, the extent of coral loss following the 1998
event has not been quantified. Widespread mortality of corals was
documented in response to the 2003 bleaching event, and average live
coral coverage was reduced to 10 percent (Kospartov et al., 2006; as
cited in Lukoschek et al., 2013). Surveys conducted in 2005 and 2009
indicated that recovery of corals at Ashmore Reef was rapid but delayed
by about 7 years (Ceccarelli et al., 2011). Overall, there has been an
eight-fold increase in hard coral coverage from 1998 to 2009 (Hale and
Butcher, 2013), with all of the recorded recovery occurring after 2005.
Meanwhile, survey data suggest complete loss of dusky sea snakes at
Ashmore Reef after 2005. Existing survey data also show sharp declines
in total sea snake abundance and species diversity at Ashmore Reef
following both the 1998 and 2003 bleaching events (Lukoschek et al.,
2013). These patterns are consistent with a hypothesis that loss of
live corals affects reef-associated sea snakes.
The patterns at Ashmore Reef are contrasted, however, by those
observed at Scott Reef. Following the 1998 bleaching event, a greater
than 80 percent loss of hard and soft coral cover occurred, which
translated into a reduction of live coral coverage to a total of
roughly 10 percent (Smith et al., 2008). The 1998 El Ni[ntilde]o event
represents the most extreme temperature anomaly recorded for Scott
Reef, and involved a rapid rise in water temperatures that remained
above normal for two months (NOAA, 2013). Almost 6 years after the
bleaching event (in 2004), the hard corals had partially recovered to
40 percent of their pre-bleaching cover, the soft corals showed no sign
of recovery, and community composition of corals remained significantly
altered (Smith et al., 2008). Within 12 years after the event (by
2010), coral cover, recruitment, community composition, and generic
diversity were similar to pre-bleaching years (Gilmour et al., 2010).
Several lesser disturbances, including two cyclones and the 2003 El
Ni[ntilde]o event, occurred during this time period and may have slowed
the rate of recovery to some extent (Gilmour et al., 2013). Available
sea snake survey data, spanning 1972-2013, with surveys in 1972-73,
2006, 2012, and 2013, do not appear to indicate a major decline in
abundance of dusky sea snakes at Scott Reef, which were relatively
common during the surveys conducted by Guinea (2012) in 2006. However,
the temporal gaps in these survey data, especially from 1973 to 2006,
could conceal shorter-term patterns.
A comprehensive understanding of the relationship between live
coral cover and dusky sea snake abundance likely requires more detailed
information regarding coral species composition, habitat complexity,
and coral and prey fish resiliency relative to both the 1998 and 2003
bleaching events. Such an analysis might offer further insights into
the differing response patterns at the two reefs, and an indication of
whether sea snake abundance is driven by live coral coverage over
timescales relevant to these disturbances. At this time, however,
because a clear or consistent pattern does not emerge from the
available data regarding dusky sea snake abundances at Ashmore and
Scott reefs in relationship to these two bleaching events, we cannot
conclude that loss of live coral is contributing to the decline of the
dusky sea snake.
The reefs where dusky sea snakes are found lie more than several
hundred kilometers offshore and thus enjoy a considerable degree of
protection from human activities and land-based sources of pollution.
Despite this remoteness, the reefs may experience some degradation as a
result of vessel traffic. Anchor damage, pollution from contaminated
bilge water, and marine debris are among the potential issues
identified at Ashmore Reef, which experiences a relatively high level
of traffic from Indonesian fishers, yachts, merchant ships, and illegal
entry vessels (Whiting, 2000; Lukoschek et al., 2013). The mechanisms
for and extent to which these boat-based habitat threats are impacting
dusky or any other sea snake species of the Timor Sea reefs are
unknown.
The extensive oil and gas industry activity in this region may also
be a possible source of disturbance affecting dusky sea snakes and
their habitat. Exploration and extraction activities within the Ashmore
Platform began in 1968 (Geoscience Australia, 2012) and are expected to
continue for some time, given the significant resources within this
region. Ashmore Reef and Cartier Islands lie about 50-80 km west of the
main offshore wells in the Timor Sea, and the closest exploration wells
are 36 km away (Russell et al., 2004). However, Scott Reef lies
directly above a significant portion of the Torosa Reservoir, where
drilling for natural gas is expected to start by 2017. The development
of the natural gas facility in this area will mean increased vessel
traffic and potentially light, sound, and chemical pollution. The area
is also expected to experience minor subsidence or compaction as the
gas is removed (Woodside Energy LTD, 2013).
[[Page 74961]]
Whether, and the degree to which, any of these threats or a combination
of these threats will impact dusky sea snakes is not yet known.
Unfortunately, extremely limited information also exists regarding
the toxic effects of oil exposure on sea snakes. Oil spills, which
occur more frequently as a result of vessel or pipeline incidents
rather than exploration and drilling activities (www.amsa.gov.au), have
also not occurred very often in this region. Some information is
available from the August 2009 explosion of the West Atlas oil rig on
the Montara Well, which leaked oil and gas uncontrollably into the
Timor Sea for 74 days until the well was finally capped in November
2009. Considered one of the worst oil-related spills to have ever
occurred in Australia, the Montara leak was analogous in nature to the
Deepwater Horizon disaster of April 2010 in the Gulf of Mexico. In an
effort to rapidly assess impacts to multiple taxa, Watson et al. (2009)
conducted ship-based transect surveys in areas around the Atlas
drilling platform in September 2009. They did not observe or identify
any dusky sea snakes; however, they did observe ``lethargic sea snakes
lying in thick oil (i.e., not moving much when approached, unable to
dive)'' and collected a dead horned sea snake (Acalyptophis peronii)
from oil-affected waters for further analysis (Watson et al., 2009).
The necropsy report indicated that this snake was in good physical
condition, with no visible external or internal pathologies, and no oil
was detected in swab samples of the skin (Gagnon and Rawson, 2010).
Chemical analysis of tissues clearly indicated that exposure to crude
oil occurred through ingestion of prey and not through inhalation
(Gagnon and Rawson, 2010). Acalyptophis peronii is considered more of a
diet specialist than the dusky sea snake and primarily consumes
burrowing gobies (McCosker, 1975; Voris and Voris, 1983). Because they
saw no physical damage to the gut structure and no contamination of the
tissues, Gagnon and Rawson (2010) concluded it was unlikely that oil
ingestion was the primary cause of death. Tests for presence of
chemical dispersants used during the spill-response were not conducted.
A necropsy was also performed on a dead sea snake landed by a
commercial fisherman operating in the vicinity of the West Atlas spill
on September 14, 2009 (Gagnon, 2009). This specimen was identified as
Hydrophis elegans, which is a relatively widespread and abundant
species that preys on eels and other fishes (McCosker, 1975; Voris and
Voris, 1983). The necropsy indicated that the snake had fed recently
and that the stomach contents were contaminated with oil (Gagnon,
2009). Relatively high levels of polycyclic aromatic hydrocarbons were
also detected in the lungs, trachea, and muscle tissue (Gagnon, 2009).
Neither of two dispersant chemicals used to treat the spill were
detected in lung samples (Gagnon, 2009). The necropsy report concluded
that the likely cause of death for this specimen was exposure to
petroleum hydrocarbons (Gagnon, 2009).
In 2012 and 2013, Guinea (2013) conducted surveys to evaluate the
potential impacts of the Montara leak on species of marine reptiles.
Potentially impacted areas surveyed included Ashmore Reef, Cartier
Island, and Hibernia Reef; Scott and Seringapatam reefs were surveyed
as control reefs (Guinea, 2013). Ashmore Reef and Cartier Island are
167 km west-north-west and 108 km west from the Montara well,
respectively. Seringapatam and Scott reefs are several hundred km
south-east of the Montara well and far from modeled oil trajectories
(Guinea, 2013). The extensive survey efforts of Guinea (2013) did not
indicate any impact of the hydrocarbon release on marine reptiles (sea
turtles and sea snakes) of the potentially affected reefs. Of the reefs
surveyed, Hibernia Reef and Cartier Island had the highest sea snake
density; however, no sea snakes were observed at Ashmore Reef, where
sea snake abundance and diversity had already declined to very low
levels prior to the 2009 incident (Guinea, 2013). Overall, these data
suggest that while there are likely to be acute impacts to sea snakes
in response to major spills, it is unlikely that pollution stemming
from oil and gas industry activities has contributed to the observed
declines of the dusky sea snake.
Overall, based on the existing information, we conclude that there
is a low likelihood that these habitat-related threats have contributed
to the observed decline of the dusky sea snake. At this time, there is
insufficient information to indicate whether and how the dusky sea
snake will be affected by these habitat issues in the future. We do
expect that each of the various habitat-related issues summarized above
will continue well into the future, and some may worsen. Given that El
Ni[ntilde]o and its associated warming of equatorial Pacific Ocean
waters is a natural and reoccurring climate phenomenon, coral bleaching
in response to sufficiently strong El Ni[ntilde]o events will continue.
Furthermore, because climate warming as a consequence of carbon dioxide
emissions is expected to continue (IPCC, 2013), and elevated sea
surface temperatures are expected to rise at an accelerated rate (Lough
et al., 2012), loss of corals through bleaching events is expected to
increase. The expansion of Australia's oil and gas exploration and
extraction in the Timor Sea may also result in an increased risk of oil
spills and additional habitat threats for dusky sea snakes.
Inadequacy of Existing Regulatory Mechanisms
The dusky sea snake and its habitat receive a significant degree of
regulatory protections. The largest potential gap in existing
regulatory mechanism may be for threats related to climate change. Oil
spills, while rare and unpredictable, and other oil and gas industry
activities may also pose threats to the species as a consequence of
inadequate management and regulation. We summarize the available
information regarding related regulatory protections below; a more in-
depth discussion is available in Manning (2014).
Along with all of Australia's other hydrophiine sea snakes, dusky
sea snakes are listed under the Commonwealth Environment Protection and
Biodiversity Conservation Act 1999 (EPBC Act). The EPBC Act provides a
legal framework to protect and manage Australia's nationally and
internationally important flora, fauna, ecological communities, and
heritage places that are of national environmental significance. Under
the EPBC Act, no one may ``kill, injure, take, trade, keep or move a
member of a native species'' within any reserve without a permit
(Commonwealth of Australia, 2000). The EPBC Act requires that surveys
be conducted for listed marine species. The EPBC Act also provides that
the Australian Government Minister for the Environment may make or
adopt a recovery plan for a listed species, to set out the research and
management actions needed to stop the decline of the species and
support its recovery. There are no recovery plans in place for any sea
snake species, however (www.environment.gov.au/topics/biodiversity/
threatened-species-ecological-communities/recovery-plans). Thus, while
the dusky snake receives substantial protection under the EPBC Act,
without a recovery plan, that protection may not be enough to help
stabilize and recover the species.
Two of the five main reefs within the dusky sea snake's historical
range, Ashmore Reef and Cartier Island, are protected reserves. Ashmore
Reef National Nature Reserve was established
[[Page 74962]]
in 1983, under the National Parks and Wildlife Conservation Act 1975 (a
predecessor to the EPBC Act), and later listed as a Ramsar Site in
2000, under the Ramsar Convention, which is an intergovernmental treaty
on sustainable use of wetlands. In Australia, Ramsar Sites receive
protection under the EPBC Act: Any action that will have or is likely
to have a significant impact on a Ramsar Site requires an environmental
assessment and approval. The EPBC Act also sets forth national
standards for managing, planning, monitoring, involving the community
in, and conducting environmental assessments of Ramsar Sites to insure
consistent compliance with the Ramsar Convention. Cartier Island, a
former British Air Force bombing range, was designated as a Marine
Reserve in 2000. These two reserves cover a combined area of 750 km\2\
and are both assigned to IUCN category Ia--strict nature reserve. IUCN
category Ia areas are protected to preserve biodiversity and maintain
the areas for the benefit of scientific research. Human access to such
areas is tightly controlled and limited. A small section of Ashmore
Reserve is managed as IUCN category II--national park. Such areas are
managed to protect ecosystems and biodiversity, and while still
restricted, human visitation is not as limited as for category Ia
areas. No fishing or harvest of any biota is allowed within the
reserves, with the limited exception of finfish fishing within the
category II area of Ashmore Reef, and then only as long as the fish are
used for relatively immediate consumption. Given the lack of clearly
identified habitat-related or human-disturbance-related threats to the
dusky sea snake, there is no indication that these reserves and area
protections are inadequate such that they have contributed to the
observed decline of the species.
According to the Australia Department of Sustainability,
Environment, Water, Population, and Communities (DSEWPC) 2012 Report
Card for marine reptiles listed under the EPBC Act, pollution from
offshore oil rigs and operations is a potential concern for sea snakes
(DSEWPC, 2012). This report also states that Australia has a strong
system for regulating the oil and gas industry and that this system was
strengthened further in the wake of the Montara oil spill. Details on
how any particular processes or regulations were strengthened are not
provided in this report and could not be found. Although oil spills
pose a potential threat to the health and status of the dusky sea
snake, oil spills are relatively rare, and there is insufficient
information to indicate that the existing regulatory mechanisms are
inadequate or that they have contributed to the decline of this
species.
Potential threats to dusky sea snakes stemming from anthropogenic
climate change include elevated sea surface temperature, ocean
acidification, and increased coral bleaching events (see below).
Impacts of climate change on the marine environment are already being
observed in Australia and elsewhere (Melillo et al., 2014; Poloczanska
et al., 2012), and the most recent United Nations Intergovernmental
Panel on Climate Change (IPCC) assessment provides a high degree of
certainty that human sources of greenhouse gases are contributing to
global climate change (IPCC, 2013). Ocean temperatures around Australia
have increased by 0.68 [deg]C since 1910-1929 (Poloczanska et al.,
2012), and carbon dioxide inputs have lowered ocean pH by 0.1 units
since 1750 (Howard et al., 2009). Australia and other countries have
responded to climate change through various international and national
mechanisms. Australia signed on to the Kyoto Protocol in 2007 and has
active domestic and international programs to lower greenhouse gas
emissions (www.climatechange.gov.au/). However, in Australia, there
appear to be no specific actions to address potential climate change
effects on marine reptiles beyond monitoring (Fuentes et al., 2012).
Because climate change related threats have not been clearly or
mechanistically linked to decline of dusky sea snakes, the adequacy of
existing or developing measures to control climate change threats is
not possible to fully assess, nor are sufficient data available to
determine what regulatory measures would be needed to adequately
protect this species from climate change. While it is not possible to
conclude that the current efforts have been inadequate, such that they
have contributed to the decline of this species, we consider it likely
that dusky sea snakes will be negatively impacted by climate change,
given the predictions of widespread and potentially permanent damage to
coral reefs in Australia (IPCC, 2013).
Overall, we do not find there is substantial evidence indicating
that A. fuscus is currently threatened by the lack of adequate
regulatory mechanisms. Beyond the direct protection the species
receives through its listing under the EPBC Act, the dusky sea snake
receives additional direct and indirect protection within the Ashmore
Reef and Cartier Island Marine Reserves. Given the predictions of
worsening damage to coral reefs in Australia in response to climate
change (IPCC, 2013), the largest potential future gap in the existing
regulatory mechanisms appears to be related to climate change.
Other Natural or Manmade Factors Affecting Their Continued Existence
Elevated sea surface temperature as a consequence of climate change
has been proposed as a possible threat to sea snakes, and we have
addressed habitat-related effects above. The IUCN Red List assessment
for A. fuscus, suggests that climate-induced increases in water
temperature may actually exceed the upper lethal limit for A. fuscus,
and thereby pose a threat to the species (Lukoschek et al., 2010).
These authors assumed an upper lethal limit of 36 [deg]C, based on data
for the pelagic sea snake, Pelamis platurus. Experiments to measure the
thermal tolerances of A. fuscus have not been conducted.
Sea snakes, like all reptiles, are ectotherms, and thus to a great
extent are physiologically affected by temperature. On a large
geographic scale, the distribution of sea snakes is considered to be
dictated by ocean temperatures: Sea snakes generally do not occur in
waters below about 18 [deg]C (Davenport, 2011). Most sea snakes can
tolerate temperatures up to a mean of about 39-40 [deg]C, but
tolerances may vary with the size of the snake and the rate of
temperature change (Heatwole et al., 2012). Also, although sea snakes
are able to dive to avoid extreme temperatures of surface waters, they
have limited capacity to acclimate and cannot thermoregulate (Heatwole
et al., 2012).
Sea surface temperatures vary seasonally within the Timor Sea. The
highest recorded oceanic water temperature in the Ashmore region is 31
[deg]C, and the highest recorded lagoon water temperature is 35.4
[deg]C (Commonwealth of Australia, 2002). These temperatures are below
the assumed upper lethal temperature limit for dusky sea snakes; but
Australia's average ocean temperatures have increased by over half a
degree since 1910-1929, and the rate of warming has accelerated since
the mid-20th century (Poloczanska et al., 2012). Given the thermal
tolerances of other sea snakes and the ocean temperatures currently
experienced by A. fuscus at present, it is very unlikely that elevated
ocean temperature has been a source of mortality. However, it is
plausible that a continuation of the observed rate of ocean warming
would, in the distant future, result in negative physiological
consequences for A. fuscus.
[[Page 74963]]
Hybridization and introgression have recently been identified by
Sanders et al. (2014) as a threat to the continued existence of A.
fuscus. Hybridization, or the production of viable offspring through
the crossing of genetically distinct taxa or groups, occurs in the wild
for about 10 percent of animal species (Mallet, 2005). Hybridization
can lead to introgression, or the integration of foreign genetic
material into a genome. The conservation concern in this particular
case is that reproductive barriers between the olive sea snake, A.
laevis, and the dusky sea snake, A. fuscus, appear to be breaking down,
potentially allowing A. fuscus to undergo reverse speciation.
The dusky sea snake co-occurs with the closely-related olive sea
snake throughout its range, and the two species are thought to have
shared a common ancestor approximately 500,000 years ago (Sanders et
al., 2013b). The olive sea snake is a relatively abundant and much more
widely distributed species compared to the dusky sea snake. Although
similar in appearance, the two species can be distinguished based on
body scale rows, body size, and color pattern. Sanders et al. (2014)
analyzed 11 microsatellite markers for A. fuscus and A. laevis across
four reefs (Ashmore, Hibernia, Scott, and Seringapatam) to assess
inter-specific gene flow and introgression. Results of their genetic
analyses indicate significant and asymmetric gene flow, with higher
rates of introgression from A. laevis into the smaller A. fuscus
population (Sanders et al., 2014). A high frequency of hybrids was also
found at each of the four reefs included in the study area. Forty-three
percent of the snakes sampled (n=7) at Ashmore, 55 percent of the
snakes sampled (n= 42) at Scott Reef, and 42 percent of the snakes
sampled (n=12) at Seringapatam Reef were identified as hybrids (Sanders
et al., 2014). At Hibernia Reef, 95 percent of the snakes sampled
(n=19) were hybrids (Sanders et al., 2014). Phenotypically, the
majority of hybrids resembled the olive sea snake (Sanders et al.,
2014). Whether the observed hybridization is a purely natural process
or has human causes is not yet known. Regardless, the high rates of
hybridization of A. fuscus with another species across its range may
lead to the eventual disappearance of this taxonomic species and is a
threat to its survival.
Extinction Risk
Although accurate and precise data for many demographic
characteristics of dusky sea snakes are lacking, the best available
data provide multiple lines of evidence indicating that this species
currently faces a high risk of extinction. The probable extirpation of
the dusky sea snake from Ashmore Reef, which constitutes about 40
percent of the historical reef habitat, represents a contraction of an
already limited range for this species. Loss of dusky sea snakes from
Ashmore Reef and low relative abundances at all other reefs, coupled
with high rates of hybridization throughout the range and a presumed
low rate of dispersal, suggest that the species is declining and
unlikely to recover without intervention. The interaction of the
threats of low and declining abundance, limited dispersal, and high
rates of hybridization all suggest a high risk of extinction in the
near term.
Protective Efforts
As mentioned previously, all of Australia's hydrophiine sea snakes
are listed and protected under the EPBC Act, making it illegal to kill,
injure, take, trade, or move dusky sea snakes in Commonwealth waters
without a permit (DSEWPC, 2012a). The EPBC Act also requires that
surveys be conducted for listed marine species.
Sea snakes are also identified as a ``conservation value'' in
Australia's North-west Marine Bioregional Plan (DSEWPC, 2012b). Marine
bioregional plans are meant to improve the way decisions are made under
the EPBC Act, particularly with respect to balancing protection of
marine biodiversity with the sustainable use of natural resources. The
North-west Plan identifies activities that may affect sea snakes and
thus require prior approval. National heritage places are also listed
and protected under the EPBC Act. Ashmore, Scott, and Seringapatam
reefs are all listed on Australia's Commonwealth Heritage List, and
under the EPBC Act, approval must be obtained before any action takes
place that could have a significant impact on the national heritage
values of these areas.
Also mentioned previously were the various habitat protections
currently in place that directly and indirectly protect the coral reefs
within the dusky sea snake's range. For example, the Ashmore
Commonwealth Marine Reserve, which includes 583 km\2\ of sandy islands,
coral reefs, and surrounding waters up to 50 m deep (Commonwealth of
Australia, 2002), is almost completely closed to the general public.
Permits may be issued to authorize visits for tourism or recreation.
There are 1-2 visits per year by commercial tourism vessels to view
wildlife, and about 15-20 recreational yachts that visit each year
(Hale and Butcher, 2013). Indonesians have fished this site for
centuries and subsistence fishing is allowed in only the IUCN category
II portion of the reserve (Hale and Butcher, 2013). No commercial
fishing is allowed in any part of the Reserve. The relatively pristine
state of the site makes it attractive for the long-term monitoring and
other scientific projects that are conducted there (Hale and Butcher,
2013). Starting in the late 1980's, Environment Australia (EA)
contracted a private vessel and crew to undertake on-site management at
the Reserve; however, as of 2000, Australian Customs Service took over
this responsibility (Whiting, 2000). Enforcement of protections at the
Reserve depends largely on the presence of Customs officials, which is
not quite continuous (Lukoschek et al., 2013; Whiting, 2000).
The Cartier Island Commonwealth Marine Reserve, designated in 2000
under the EPBC Act, is completely closed to the public. No commercial
or recreational fishing is allowed. General access and several specific
activities, such as scientific research, photography and tourism, may
be allowed with prior approval from the Director of National Parks
issued under the EPBC Act (see http://www.environment.gov.au/topics/marine/marine-reserves/north-west/cartier-activities).
Since the early 18th century, Indonesian fishers have visited and
fished reefs within the Timor Sea, mainly in search of trepang,
trochus, turtle, shark fin, and reef fishes (Commonwealth of Australia,
2002). In 1974, a Memorandum of Understanding (MOU) was established
between Australia and Indonesia that set out arrangements by which
traditional fishers may access resources in Australia's territorial
sea. Because of its shape, the area covered by this MOU is often
referred to as the MOU Box. The MOU Box, which covers an area of about
50,000 km\2\, includes the five main reefs where the dusky sea snake
occurs (Skewes et al., 1999). The marine resources within this area are
managed by the Australian Government, and traditional fishing by
Indonesian fishers is allowed. However, as discussed above, certain
restrictions apply within the Marine Reserves. Traditional Indonesian
fishers may access parts of the Ashmore Reserve for shelter and
freshwater and to visit grave sites, but, as mentioned previously,
fishing is prohibited in both the Cartier Island and Ashmore Marine
Reserves, with the limited exception for fishing for immediate
consumption within the category II area of the Ashmore Reserve. There
is no evidence that sea snakes
[[Page 74964]]
have been targeted by Indonesian fishers (Hale and Butcher, 201;
Lukoschek et al., 2013).
Because sea snakes are listed under the EPBC Act, all Australian
fisheries are required to demonstrate that direct and indirect
interactions with sea snakes are sustainable (Zhou et al., 2012).
Commercial trawls take over a dozen species of sea snakes (Heatwole
1997; Wassenberg et al., 2001; Zhou et al., 2012), and in the absence
of bycatch reduction devices (BRDs), an estimated 48.5 percent of all
incidentally captured sea snakes will die (Wassenberg et al., 2001).
BRDs are required in the prawn trawl fishery to minimize bycatch
mortality and help conserve protected species. The only trawl fishery
that operates within the range of the dusky sea snake is the North West
Slope Trawl Fishery (NWSTF). The Australian Fisheries Management
Authority (AFMA) reports that the NWSTF, which targets three scampi
species (lobsters), is a low effort fishery with a very low level of
bycatch and no documented interactions with threatened, endangered, or
protected species (AFMA, 2012). The NWSTF is also a deep-water fishery,
and thus unlikely to encounter the reef-associated dusky sea snake (Fry
et al., 2001; Lukoschek et al., 2007a; Lukoschek et al., 2013). As
discussed here and in further detail in the status review report
(Manning, 2014), there is no indication that direct harvest or
incidental capture poses a threat to the dusky sea snake.
Sea snake products have been traded internationally since the 1930s
(Marsh et al., 1994), but no sea snake species is currently listed
under the Convention on International Trade in Endangered Species of
Wild Fauna and Flora (CITES). Australia's Wildlife Protection Act 1982
restricts the export of sea snake products out of Australia (Marsh et
al., 1994). There are no data to suggest that the dusky sea snake is
threatened by past, present, or future trade.
Despite their apparent substantiveness, these existing and ongoing
conservation efforts seem unlikely to prevent further decline of the
dusky sea snake, because they have failed to prevent the decline of the
species to date. For example, decades of protections at Ashmore Reef,
while maintaining this as a relatively pristine reef (Hale and Butcher,
2013), have not prevented the severe decline and likely extirpation of
dusky sea snakes there. Furthermore, the threat posed by hybridization
is beyond the scope of existing protections. We are thus not able to
conclude that the existing protective efforts alter the extinction risk
for the dusky sea snake. We are not aware of any additional, planned or
not-yet-implemented conservation measures that would protect this
species; thus, we did not conduct an analysis under the PECE. We seek
additional information on other conservation efforts in our public
comment process (see below).
Proposed Determination
Based on our consideration of the best available data, as
summarized here and in Manning (2014), and protective efforts being
made to protect the species, we conclude that the dusky sea snake, A.
fuscus, is currently at high risk of extinction throughout its range.
We therefore propose to list it as endangered under the ESA.
Banggai Cardinalfish
The following section describes our analysis of the status of the
Banggai cardinalfish, Pterapogon kauderni. More details can be found in
Conant (2014).
Species Description
The Banggai cardinalfish is a species within the family Apogonidae
and genus Pterapogon. It was discovered in 1920 by Walter Kaudern and
described by Koumans (1933). The genus Pterapogon contains one other
species, P. mirifica, from northwestern Australia (Allen and Donaldson,
2007).
The Banggai cardinalfish is a relatively small marine fish. Adults
generally do not exceed 55 to 57 mm standard length (Vagelli, 2011).
The species is distinguished from all other apogonids by its tasseled
first dorsal fin, elongated anal and second dorsal fin rays, and deeply
forked caudal fin (Allen, 2000). It is brilliantly colored, with
contrasting black and light bars with whitish spots over a silvery
body.
The Banggai cardinalfish has an exceptionally restricted natural
range (approximately 5,500 km\2\) within the Banggai Archipelago,
Indonesia. Populations have been introduced in areas of Indonesia
outside of the Banggai Archipelago, including Luwuk Harbor (Bernardi
and Vagelli, 2004), Palu Bay (Moore and Ndobe, 2007), Lembeh Strait
(Erdmann and Vagelli, 2001), Tumbak (Ndobe and Moore, 2005), Kendari
Bay (Moore et al., 2011), and north Bali (Lilley, 2008). These
introductions are a result of discards from the ornamental live reef
aquarium trade and introductions by dive-resort operators to support
the tourist industry (Vagelli, 2011). The introduced populations are an
artifact of the commercial ornamental live reef trade and are not part
of any conservation program to benefit the native populations. Because
we interpret the ESA as conserving species and the ecosystems upon
which these species depend, we consider the natural range to be
biologically and ecologically important to the species' viability to
persist in the face of threats. Distances between non-introduced
populations range from less than 1 km (Vagelli, 2011) up to 153 km
(Vagelli et al., 2009). Distribution of populations is discontinuous,
with deep water, strong currents, or coast exposed to severe weather
serving as effective ecological barriers to migration (Bernardi and
Vagelli, 2004; Ndobe et al., 2012; Ndobe and Moore, 2013). The Banggai
cardinalfish exhibits the highest known degree of genetic structure of
any marine fish (Bernardi and Vagelli, 2004; Hoffman et al., 2005;
Vagelli et al., 2009). Populations occurring on the same reef,
separated by only a few kilometers, are genetically isolated from one
another (Bernardi and Vagelli, 2004; Hoffman et al., 2005; Vagelli et
al., 2009).
The Banggai cardinalfish is generally found in calm waters of
sheltered bays or on the leeward side of islands (Allen and Donaldson,
2007). It inhabits a variety of shallow (from about 0.5 to 6 m)
habitats including coral reefs, seagrass beds, and less commonly, open
areas of low branching coral and rubble. To avoid predators, it
associates with microhabitats such as sea urchins and anemones
(Vagelli, 2011). Banggai cardinalfish are found in waters ranging from
26-31 [deg]C, but averaging 28 [deg]C (Ndobe et al., 2013).
The Banggai cardinalfish, like many apogonids, exhibits reversed
sex roles, where males provide parental care and brood eggs in their
mouths. It lacks a planktonic larval stage and extends the brooding of
larvae for about 7 days after hatching, which results in the release of
fully formed juveniles. Spawning occurs year round but peaks around
September through October, which is a period of fewer storms in the
region (Ndobe et al., 2013). The Banggai cardinalfish has the lowest
fecundity reported for any apogonid (Vagelli, 2011). Generation length
(the age at which half of total reproductive output is achieved by an
individual) is estimated to be 1.5 years (Vagelli, New Jersey Academy
for Aquatic Sciences (NJAAS), personal communication cited in Allen and
Donaldson (2007)) to 2 years (Ndobe et al., 2013). Its lifespan in the
wild has been estimated at approximately 2.5-3 years (Vagelli, 2011),
with a maximum lifespan up to 3-5 years (Ndobe et al., 2013). Based on
a conservative estimate, a male could incubate/brood approximately 400
to 640 offspring over his lifespan (Vagelli, personal communication,
2014), of which less
[[Page 74965]]
than 5 percent may survive to adulthood (Vagelli 2007 as cited in CITES
(2007)). High mortality occurs during the first days after release from
the brood pouch due to predation, including parental and non-parental
cannibalism (Vagelli, 1999).
Banggai cardinalfish form stable groups. Natural group size is
difficult to know because group size decreases with fishing pressure,
and most populations are not pristine. However, one bay (oyster pearl
farm) in private ownership in the Banggai Islands had, until 2006,
never been fished, and group size averaged about 13 fish, but varied
from 2-33 fish per group (Lunn and Moreau, 2002). At the same site in
2004, group size varied from 1 to over 200 fish per group (Moore,
unpublished data, 2014). Group size is typically less than 25
individuals, although smaller groups are common and vary by age class
and habitat type (Vagelli, 2011).
The first scientific surveys of Banggai cardinalfish estimated
population abundance and density between 1.7 million, with a mean
density of 0.03 fishes per m\2\, based on a census at three sites in
2001 (Vagelli, 2002; Vagelli and Erdmann, 2002), and 2.4 million, with
a mean density of 0.07 fishes per m\2\, based on an expanded census of
34 sites conducted in 2004 (CITES, 2007). In 2007, population the
density estimate of the expanded survey sites indicated a mean density
of 0.08 fishes per m\2\ (Vagelli, 2008); however, overall population
abundance was not reported for the 2007 survey. By 2011-2012, Ndobe et
al. (in press) estimated the population abundance at 1.5-1.7 million,
with a mean observed density of 0.05 fishes per m\2\, reportedly for
the 24 of the 34 sites that were surveyed in 2004 and 2007. The 2011-
2012 estimates does not include locations in Toado where the habitat
was limited and density was very high (Ndobe et al., in press); thus,
the population abundance estimate likely is biased low. However, 7 of
the major sites first surveyed in 2004 have declined in abundance and
mean density (Ndobe et al., in press), indicating the population has
likely decreased from the 2.4 million estimated in 2004. Although the
mean observed density estimate of 0.03 fishes per m\2\ found in the
2001 survey (Vagelli, 2002; Vagelli and Erdmann, 2002) is less than the
2011-2012 survey, the 2001 survey was based on only three sites, while
the 2011-2012 survey was based on 24 sites of the 34 sites. Ndobe (et
al., in press) selected the expanded survey sites from 2004 and 2007
for their 2011-2012 survey based on the author's previous work on
habitat conditions and to better compare trends, over time, in density
and abundance. Ndobe (et al., in press) stated that their 2011-2012
estimate of 1.5-1.7 million represented 62-71 percent of the abundance
estimate of 2.4 million from the 2004 survey. A total abundance
estimate was not provided for the 2007 survey, however mean observed
density decreased approximately 38 percent between 2007 (0.08 fishes
per m\2\) and 2011-2012 (0.05 fishes per m\2\).
Historical data on abundance are lacking, as surveys were done
after harvest began in the early to mid-1990s. The private oyster pearl
farm mentioned above is thought to represent a proxy for historical
abundance by several researchers, though others disagree that the site
is representative of historical abundance. The private oyster farm
exists within a privately owned bay in Banggai Island, and fishing has
been prohibited there since trade began, although illegal poaching in
the bay was reported in 2006 (Talbot et al., 2013). The habitat in the
bay may be similar to other sites that support the Banggai
cardinalfish; thus, several researchers claim this population can be
used as a proxy for a baseline of population abundance (Allen and
Donaldson, 2007; Vagelli, 2008). In 2001, densities of fish in the
private oyster pearl farm averaged 0.63 0.39 fishes per
m\2\ (1 standard deviation, SD) (range: 0.28 to 1.22 fishes per m\2\)
(Lunn and Moreau 2002) and 0.58 fishes per m\2\ in 2004 (Vagelli 2005).
When these densities are compared to the densities found in the 2001
and 2004 survey data discussed above, they indicate that the Banggai
cardinalfish abundance has declined up to 90% from historical levels
(Allen and Donaldson, 2007; Vagelli, 2008). However, several
researchers (Moore, Sekolah Tinggi Perikanan dan Kelautan (STPL),
personal communication 2014; Ndobe, Tadulako University, personal
communication 2014) caution against the use of this bay as a baseline
for population trends. Banggai cardinalfish population distribution is
inherently patchy, and density is highly variable between and within
sites of the Banggai Archipelago, including this bay (Moore,
unpublished data, 2004). The researchers also question whether the
habitat in the bay is comparable to other sites. The bay has been
protected from degradation because it is privately owned and contains
significant amounts of sheltered habitat and good quality microhabitat/
habitat, with limited suitable habitat for predators of the
cardinalfish, such as groupers and other larger reef fish. We
acknowledge the debate regarding the use of the data from the private
oyster farm as a baseline for historical abundance. However, even
without that data, it is clear that population abundance estimates at
sites throughout the Banggai Archipelago declined significantly between
2004 and 2011-2012.
Declines and extirpations of local populations have been observed
across years, likely due to directed harvest and, more recently,
habitat destruction. In the 2001 survey, Bakakan Island had about 6,000
fish, but by the 2004 census, only 17 fish remained (Vagelli, 2008). In
the 2007 survey, 350 individuals were found at Bakakan Island, but this
was still well below the 6,000 fish found in the 2001 survey (Vagelli,
2008). In 2014, Moore (personal communication) reported that local
fishers characterize the cardinalfish population on Bakakan Island as
small and declining. Between the 2001 and 2004 surveys, the population
density at Masoni Island doubled from 0.03 to 0.06 fish per m\2\ (an
increase of approximately 150 fish in 3 years) (Vagelli, 2005). This
increase is thought to have occurred in response to a collecting ban
that the local people imposed in early 2003. However, in the 2007
survey, the population was found to have declined to 0.008 fish per
m\2\, with 38 fish recorded over the entire census site (the largest
group consisted of 2 individuals). An extensive search around the
entire island identified only 150 fish (Vagelli, 2008). A population in
southeast Peleng Island had 159 and 207 fish in 2002 and 2004,
respectively (Vagelli, 2005). However, by 2007, it had been practically
extirpated, with only 27 fish found (Vagelli, 2008). Overharvest of
microhabitat, such as Diadema sea urchins and sea anemones, and coral
mining have resulted in local population depletions on an island off
Liang, which was surveyed in 2004, and was extirpated by 2012 (Ndobe et
al., 2013). Extirpation of local populations has been documented in
areas with increased harvest of microhabitat, combined with fishing
pressure on Banggai cardinalfish. Interviews with locals and visits to
several sites in 2011 and 2012 indicate populations are declining in
the Banggai Archipelago (Ndobe et al., 2013).
Summary of Factors Affecting the Banggai Cardinalfish
Next we consider whether any one or a combination of the five
threat factors specified in section 4(a)(1) of the ESA are contributing
to the extinction risk of the Banggai cardinalfish. We discuss each of
the five factors below, as all factors pose some degree of extinction
risk. More details are available in Conant (2014).
[[Page 74966]]
Present or Threatened Destruction, Modification, or Curtailment of
Habitat or Range
The illegal use of fish bombs (typically made with fertilizer and
phosphorus) and cyanide to catch fish has resulted in significant loss
of coral reef habitat within the Banggai cardinalfish range (Allen and
Werner, 2002). Damage to coral reefs due to fish bombs is prevalent,
even in protected areas (Talbot et al., 2013). Cyanide is used to catch
fish for the live reef fish trade, and the practice kills corals (e.g.,
see Jones and Steven, 1997; Mous et al., 2000). Boats have degraded the
coral reefs in the area, and clear-cutting of wooded slopes and
mangroves has occurred, increasing sedimentation, which degrades coral
reef habitat (Lilley, 2008). Other upland activities, such as
agriculture and human population growth, have increased the amount of
waste and nitrates in the marine environment, promoting algal blooms
(Lilley, 2008), which may destroy coral reefs by outcompeting them for
vital resources such as light and oxygen (reviewed by Fabricius, 2005).
Significant plastic, styrofoam, and other human-made debris occurs in
the area (Lilley, 2008). This information indicates destruction of
habitat is occurring within the Banggai cardinalfish's range. Although
quantitative data on impacts to cardinalfish populations are lacking,
considerable qualitative information exists indicating that where
habitat has been degraded (e.g., Tanjung Nggasuang and Toropot surveyed
in 2004 and 2012, and Mbuang-Mbuang, on Bokan Island, surveyed in
2012), large and thriving Banggai cardinalfish populations spread over
large areas can be reduced to isolated remnants crowded into small
remaining patches of habitat with some protective microhabitat (Ndobe,
personal communication, 2014).
Coral reef conditions in the Central Sulawesi Province, including
the Banggai Archipelago, were examined from 2001 through 2007 in seven
Districts in the region (Moore and Ndobe, 2008). Average condition of
the reefs was poor, and major impacts included coral mining,
sedimentation, fishing, and predation (Moore and Ndobe, 2008).
Population explosions of the crown-of-thorns starfish (Acanthaster
planci), a coral predator, have been observed in the area, indicating
an ecological imbalance, likely due to overharvest of natural predators
and changes in hydrology and water quality (Moore et al., 2012).
Surveys conducted at five sites around Banggai Island from 2004 through
2011 showed coral reef cover declined by more than half, from 25
percent to 11 percent (Moore et al., 2011; 2012). Major causes of the
coral reef decline around Banggai Island were attributed to destructive
fishing methods and general fishing pressure, coastal development, and
the replacement of traditional homes with concrete and breeze-block
dwellings, which increases the demand for mined coral and sand. Loss of
coral reef cover may increase mortality of Banggai cardinalfish
recruits due to cannibalism (Moore, personal communication, 2014; Ndobe
et al., in press).
Climate change may also impact Banggai cardinalfish habitat as a
result of coral bleaching. Coral bleaching events due to warming
temperatures are anticipated to increase by 2040 in areas of the Indian
Ocean, including waters of Indonesia (van Hooidonk et al., 2013). Coral
bleaching due to elevated water temperatures has not been observed
around Banggai Island up through December 2011; however, extensive
bleaching was observed in nearby Tomini Bay in 2010 (Moore et al.,
2011; 2012). The Banggai cardinalfish is restricted to shallow waters
with ambient temperatures ranging from 28 to 31 [deg]C. Thus, warming
temperatures may render habitat unsuitable, but specific data on
impacts to the Banggai cardinalfish are lacking.
Sea urchins and anemones are experiencing intensive and increasing
harvest pressure, which negatively impacts the Banggai cardinalfish
(Moore et al., 2012; Ndobe et al., 2012). Sea anemones were once
abundant but were drastically reduced from Tinakin Laut, Banggai
Island, which resulted in a collapse of the Banggai cardinalfish
population in the area (Moore et al., 2012). Heavy harvest of sea
anemones at Mamboro, Palu Bay, resulted in a drastic reduction of new
recruits and juvenile Banggai cardinalfish (observed since 2006) in
2008 (Moore et al., 2011). Moore et al. (2011; 2012) report that
intensive harvesting of shallow water invertebrates, including sea
anemones and sea urchins, is increasing and is linked to socio-economic
trends associated with consumption by local seaweed farmers and use as
feed for carnivorous fish destined for the ornamental live reef trade.
In addition, a disease of unknown origin may be damaging hard
corals in habitat occupied by the Banggai cardinalfish. The disease
affects the top sections of long-branched Acropora species as well as
species of Porites, both of which are important microhabitat for the
Banggai cardinalfish (Vagelli, 2011). Data are lacking on the extent of
impact the disease poses to Banggai cardinalfish habitat.
Overutilization for Commercial, Recreational, Scientific, or
Educational Purposes
The Banggai cardinalfish is traded internationally as a live marine
ornamental reef fish. It has been collected in the Banggai Islands,
Indonesia, since 1995 (Marini and Vagelli, 2007). The United States,
Europe, and Asia are the major importers of the Banggai cardinalfish
for the aquarium trade (CITES, 2007). The Banggai cardinalfish is the
tenth most common ornamental fish imported into the United States
(Rhyne et al., 2012). Banggai cardinalfish exports for the ornamental
live reef fish trade may be decreasing, although systematic data are
lacking. In 2001, up to 118,000 Banggai cardinalfish were sold to trade
centers each month, with a total estimate of 700,000-1.4 million fish
traded (Lunn and Moreau, 2002, 2004). From 2004 through 2006, around
600,000-700,000 fish were traded yearly (Moore et al., 2011). In 2008
and 2009, 236,373 and 330,416 fish, respectively, were traded at Bone
Bone, Toropot, and Bone Baru trade centers (Moore et al., 2011, 2012).
However, these numbers do not include trading data from Bone Bone in
2008 and other active centers (e.g., Panapat for 2008 and 2009). These
collections centers each reported about 15,000 fish per month in 2007
(Vagelli, 2008; 2011). Vagelli (personal communication, 2014) estimates
that 1,000,000 Banggai cardinalfish are currently captured each year
for the ornamental live reef trade.
The ornamental live reef fish trade has resulted in decreases in
cardinalfish population density and extirpation of local populations.
By 2000 (after less than a decade of trade), negative impacts on the
Banggai cardinalfish from the trade were observed. The trade results in
high mortality of cardinalfish collected. Based on interviews with
collectors, Lilley (2008) estimated that only one out of every four to
five fish collected makes it to the buyer for export due to high
mortality and discard practices. Density and group size of cardinalfish
and sea urchins are negatively impacted by the trade (Kolm and
Berglund, 2003). Ndobe and Moore (2009) also found that populations
were exploited, but observed high population density in areas where
collection had been ongoing for some years with rotation between sites,
indicating some harvest sustainability. Unfortunately, habitat
destruction and collection and destruction of microhabitat (unrelated
to the Banggai cardinalfish fishery) have
[[Page 74967]]
now greatly reduced cardinalfish populations at sites which had
previously sustained periodic collection for more than a decade (Moore,
personal communication, 2014). Decreases in population density are also
evidenced by significant declines in the catch per unit effort
(Vagelli, personal communication, 2014). In Bone Baru, from 1993-2000,
fishers were catching an average of 1,000-10,000 fish per day, but by
2003 they only averaged 100-1,000 per day, with most catching between
200-300 fish (EC-Prep Project, 2005). Prior to 2003, collectors from
Bone Baru typically required one day to capture approximately 2,000
specimens. In 2007, they reported requiring one week to capture the
same number (Vagelli, 2011). Vagelli (2011) reports similar declines
for Banggai Island, where between 2000 and 2004, the reported mean
catch declined from about 1,000 fish/hour to 25-330 fish/hour.
Information suggests the number of active participants in the trade
may have dropped. In 2001, there were 12 villages that collected the
Banggai cardinalfish, but only 3 were active in 2011 (Moore et al.,
2011, 2012), and at least 5 villages were active in 2014 (Moore,
personal communication, 2014). Reported as number of collectors, the
data indicate a decline in participation as well, from about 130 in
2001 (Lunn and Moreau, 2004) to about 80 in 2007 (Vagelli, 2011) and
2012 (Vagelli, personal communication, 2014).
In 2012, a large-scale aquaculture facility based in Thailand began
to breed Banggai cardinalfish in captivity for export, which may
alleviate some of the pressure to collect fish from wild populations
(Talbot et al., 2013; Rhyne, Roger Williams University, unpublished
data 2014). In 2013, approximately 120,000 Banggai cardinalfish were
imported into the United States from the Thailand facility. The volume
represents a significant portion of overall United States imports of
the cardinalfish and may even exceed the number of wild fish currently
imported (Rhyne, unpublished data, 2014). Efforts to captive-breed the
species in the United States are also ongoing, which may alleviate
dependence on wild-caught cardinalfish. In the United States, the
Florida Department of Agriculture and Consumer Services has certified
eight aquaculture facilities that are beginning to culture and market
farm-raised Banggai cardinalfish (Knickerbocker, Florida Department of
Agriculture and Consumer Services, personal communication 2014). In-
situ breeding by the fishing communities in the endemic area may also
alleviate pressure on the natural population, but the concept requires
further research before it can be implemented at a local community
level (Ndobe, personal communication, 2014).
Disease or Predation
Predation and cannibalism are high among new recruits (Moore et
al., 2012). However, specific data are lacking on whether predation
pressure is increasing or impacting the Banggai cardinalfish population
growth beyond natural levels.
A virus known as the Banggai cardinalfish iridovirus (genus
Megalocytivirus) is linked to high mortality of wild-caught fish
imported for the ornamental live reef fish trade (Vagelli, 2008; Weber
et al., 2009). The virus causes necrosis of spleen and renal tissue,
which appears as darkened tissue. Other symptoms are lethargy and lack
of appetite. Surveys of wild populations have not reported symptoms of
the disease. Necropsies of over 100 fish collected in the wild and at
holding facilities showed no indication of the virus (Talbot et al.,
2013). Thus, the virus is likely transmitted from other specimens at
containment centers, or is carried by the Banggai cardinalfish and is
only expressed as a result of stress incurred during the long transport
process (Weber et al., 2009; Talbot et al., 2013) and may not be a
concern for wild fish.
Inadequacy of Existing Regulatory Mechanisms
Current Indonesian legislation requires that all trade in Banggai
cardinalfish go through quarantine procedures before crossing internal
administrative borders or prior to export (Moore et al., 2011).
Compliance historically has been low, but is improving (Moore, personal
communication, 2014; Moore et al., 2011). However, reported collection
through the Fish Quarantine Data system, which records fish that go
through quarantine procedures, was well below the total reported
collection from Bone Baru, Toropot, and Bone Bone for 2008 and 2009.
Bone Baru, Toropot, and Bone Bone reported collection of 236,373 fish
in 2008 and 330,416 fish in 2009. Whereas in 2008 and 2009, the Fish
Quarantine Data reported collection of 83,200 and 215,950 fish,
respectively (Moore et al., 2011). Enforcement of the Fish Quarantine
procedures is weak, and illegal, unregulated, and unreported capture
and trade are still a major problem, especially in remote areas (Ndobe,
personal communication, 2014).
Legislation is needed to establish fishing quotas and size limits;
however, no legally binding regulations have been passed or implemented
(Moore et al., 2011). Indonesia prohibits the use of chemicals or
explosives to catch fish (Fisheries Law No. 31/2004, Article 8(1)).
However, the practice continues (Vagelli, 2011), and damage to coral
reefs due to fish bombs is prevalent, even in protected areas (Talbot
et al., 2013).
In 2011, Indonesia had proposed to list the Banggai cardinalfish
for restricted protected status under domestic law. But the proposal
stalled when the Indonesian Institute for Science argued that the
introduced populations meant the species was no longer endemic, and
thus did not meet the criteria for protected status (Moore, personal
communication, 2014; Ndobe, personal communication, 2014). In 2007, the
Banggai cardinalfish was proposed for listing under CITES Appendix II.
However, the proposal failed. The species is listed in Annex D of the
European Wildlife Trade Regulations, which only requires monitoring of
European Union import levels through import notifications.
Based on the weaknesses discussed above, regulatory mechanisms on
the commercial harvest industry do not appear adequate to ensure the
population will be sustainable.
Other Natural or Manmade Factors Affecting Continued Existence
Global averaged combined land and ocean surface temperatures show a
warming of 0.85 [deg]C over the period 1880 to 2012 (IPCC, 2013). As
discussed earlier (see Present or Threatened Destruction, Modification,
or Curtailment of Habitat or Range), warming temperatures may destroy
or modify habitat, but data are lacking on specific direct impacts to
the Banggai cardinalfish.
The Banggai Archipelago sits at the junction of three tectonic
plates (Eurasian, Indian-Australian, and Pacific-Philippine Sea) and is
vulnerable to earthquakes. An earthquake measuring 7.6 on the Richter
scale occurred in 2000 and destroyed coral reefs in the region
(Vagelli, 2011). Frequent earthquakes within the Banggai Archipelago
may have impacted localized Banggai cardinalfish populations (CITES,
2007), but specific data are lacking.
Extinction Risk
The life history characteristics (i.e., low fecundity, high degree
of parental care and energetic investment in offspring, high new
recruit mortality, no
[[Page 74968]]
planktonic dispersal, high site fidelity) of the Banggai cardinalfish
render it less resilient and more vulnerable to stochastic events than
marine species that are able to disperse over large areas and
recolonize sites that have been lost due to these events. Because the
Banggai cardinalfish also has an exceptionally restricted natural range
(approximately 5,500 km\2\), these demographic traits become more
important in terms of the extent to which the threats appreciably
reduce the fitness of the species. The Banggai cardinalfish lacks
dispersal ability and exhibits high site fidelity, and new recruits
stay within parental habitat. Thus, recolonization is unlikely once a
local population is extirpated. Local populations off Liang and Peleng
Island are reported extirpated, and interviews with local fishermen
indicate extirpation of small local populations throughout the Banggai
Archipelago. The Banggai cardinalfish also exhibits high genetic
population substructuring; thus, extirpation of local populations from
overharvest and/or loss of habitat can result in loss of genetic
diversity and further fragmentation of spatial distribution. In
considering the demographic risks to the species, its growth rate/
productivity, spatial structure/connectivity, and diversity are
assigned to the high risk of extinction category. However, the overall
population abundance (estimated at 1.5 to 1.7 million) is assigned to
the moderate risk of extinction category, because the abundance may
allow some resilience against stochastic events.
In considering the threats, we rely on the best available data to
assess how the threats are currently impacting or likely to impact the
species in the foreseeable future. The best available data indicate
that several threats to the Banggai cardinalfish will continue and
increase, with the species responding negatively, but other threats
will decrease, with the species responding favorably. Habitat
degradation has occurred and is anticipated to continue and increase in
the foreseeable future. Although Indonesia prohibits the use of
chemicals or explosives to catch fish, historically, compliance has
been low, and data indicate compliance is not improving. Data also
indicate that by 2007, harvest of microhabitat (sea urchins and sea
anemones) had negatively impacted cardinalfish populations, and the
harvest had increased by 2011. Moore et al. (2011, 2012) concluded that
it would be difficult to establish and enforce local regulations for
controlling the overharvest of microhabitat. Thus, it is reasonable to
expect that microhabitat harvest will continue and increase in the
foreseeable future, which negatively impacts the Banggai cardinalfish
and its ability to avoid predators. Overutilization from direct harvest
for the ornamental live reef fish trade has significantly impacted the
Banggai cardinalfish and remains a concern. Trade continues resulting
in high mortality, and in areas of heavy overexploitation, populations
have been extirpated. However, an increase in compliance with the Fish
Quarantine regulations and improved trade practices have occurred in
recent years, and we anticipate compliance and trade practices will
likely continue to improve in the future, which may mitigate impacts
through sustainable trade. Participation in collection of Banggai
cardinalfish for the live ornamental reef trade has dropped in recent
years. Captive-bred facilities have recently started in the United
States and Thailand and are anticipated to decrease the threat of
directed harvest of the wild populations in the future. Predation of
new recruits is high. Mortality from disease in wild-caught fish
imported for the ornamental live reef fish trade and disease affecting
the Banggai cardinalfish habitat are both plausible threats. However,
data are lacking on how these threats impact the population and what,
if any, impacts will occur and at what rate in the future. Climate
change within the Banggai cardinalfish range will continue to affect
coral reefs in the future, and it is reasonable to expect that future
earthquakes that may destroy or modify habitat within the species'
range will occur at the current rate.
The Banggai cardinalfish is exposed, and negatively responds to
some degree, to the five threat factors discussed above. Although
quantitative analyses are lacking, it is reasonable to expect that when
these exposures are combined, synergistic effects may occur. For
example, the ornamental live reef fish trade likely causes the
expression of the iridovirus in the Banggai cardinalfish, which results
in increased mortality. The indiscriminate harvest of sea anemones and
sea urchins and destruction of coral reefs eliminates important
cardinalfish shelter and substrate and increases the likelihood of
predation. Interactions among these threats may lead to a higher
extinction risk than predicted based on any individual threat.
In sum, based on the life history characteristics of the Banggai
cardinalfish, which indicate high vulnerability to demographic risks
(due to trends in population growth/productivity, spatial structure and
connectivity, and diversity), coupled with ongoing and projected
threats to habitat and microhabitat, commercial use, inadequate
regulatory mechanisms, disease and predation, and additional natural or
manmade factors, we conclude that demographic risks and the combination
of threats to the species may contribute to the overall vulnerability
and resiliency of the Banggai cardinalfish. The Banggai cardinalfish
has experienced a decline in abundance as evidenced by the decrease in
mean density at survey sites between 2004 and 2012. Moreover, at least
some researchers believe that the population may have experienced a
dramatic decline from historical abundance due to overharvest based on
comparisons between populations in a private bay and other populations.
Most of the species' demographic characteristics put it at a high risk
of extinction. However, the threat of overharvest has been and will
likely continue to be reduced in the future. Further, the overall
population abundance (1.5 to 1.7 million) may allow some resilience
against stochastic events; thus, placing the Banggai cardinalfish at an
overall moderate risk of extinction.
Protective Efforts
The Banggai cardinalfish is listed as `endangered' by the World
Conservation Union (IUCN; Allen and Donaldson, 2007). Although listing
under the IUCN provides no direct conservation benefit, it raises
awareness of the species. In addition, the Banggai cardinalfish was one
of the first entrants into the Frozen Ark Project, which is a program
to save the genetic material of imperiled species (Williams, 2004;
Clarke, 2009).
In 2007, Indonesia developed a national multi-stakeholder Banggai
cardinalfish action plan (BCF-AP), which focused on conservation,
trade, and management issues (Ndobe and Moore, 2009). As part of the
BCF-AP, annual stakeholder meetings are held to share data, review
progress, and set goals (Moore et al., 2011). The BCF-AP called for
biophysical and socio-economic monitoring of trade, population status,
and habitat, and several organizations have begun to report on these
activities. However, there is no integrated or comprehensive monitoring
system, and long-term data sets are lacking (Moore et al., 2011).
Several aspects of the BCF-AP appear to have improved the
sustainability of the Banggai cardinalfish trade. Fishermen groups have
gained legal status (allowing them access to various benefits such as
funding or loan support), which has led to socialization of sustainable
harvest in Bone Baru. The
[[Page 74969]]
legally-established fishermen's group Kelompok BCFLestari, in Bone
Baru, implemented collection practices designed to prevent capture of
brooding males (Moore et al., 2011). Workshops have been held on
improving capture methods and post-harvest care, and several community
members have become active in conservation efforts. However, the BCF-AP
officially ended in 2012 and so did the funding. Some of the
stakeholders are still active and are likely to continue to be so,
despite lack of government support (Moore, personal communication,
2014).
As discussed earlier, compliance with the Fish Quarantine
regulations has increased, which is largely due to the development and
implementation of the BCF-AP (Moore et al., 2011). In 2004, one Banggai
cardinalfish trader followed Fish Quarantine procedures. By 2008, there
was a marked increase in legal trade, but unreported fishing still
occurs (Moore et al., 2011). With the lapse of the BCF-AP, legislation
is needed to support and restart the goals described in the BCF-AP, and
although efforts have been ongoing to establish fishing quotas and size
limits, no legally binding regulations have been passed or implemented
(Moore et al., 2011).
In 2007, the Banggai Cardinal Fish Centre (BCFC) was established in
the Banggai Laut District to serve as a central point for sharing
information and managing the species over a wider community area
(Lilley, 2008; Moore et al., 2011). As of 2011, the BCFC had no
electricity, no operational budget, and was operated on a voluntary
basis (Moore et al., 2011). Further inhibiting the continued operation
of the BCFC is that in 2013, the region was split into two Districts by
constitutional law (UU No. 5/2013). The BCFC will need to be officially
approved under the new District to maintain its legal status (Ndobe,
personal communication, 2014).
A marine protected area (MPA) consisting of 10 islands was declared
by Indonesia in 2007, with conservation of the Banggai cardinalfish as
the primary goal of the Banggai and Togong Lantang Islands (Ndobe et
al., 2012). However, Banggai cardinalfish populations are not found at
Togong Lantang Island, while for three other islands within the
proposed MPA with known populations, Banggai cardinalfish conservation
is not included as a conservation goal in the designation (Ndobe et
al., 2012). In addition, based on genetic analysis, only 2 of 17 known
populations occur within the MPA, which led Ndobe et al. (2012) to
conclude the MPA design was ill-suited for conserving the Banggai
cardinalfish. It is uncertain whether the MPA will be changed in the
foreseeable future to better suit the species.
Although no longer active, the Marine Aquarium Council (MAC), an
international non-governmental organization, developed a certification
system to improve the management of the marine aquarium trade. MAC
developed best practices for collectors and exporters, including those
in Indonesia. Best practices include improvement of product quality,
reduction in mortality rates, safer practices for collectors, and
fairer prices paid to collectors. By applying the MAC standards,
traders could be certified as meeting these international standards
(Lilley, 2008). Building on the MAC efforts, the Yayasan Alam Indonesia
Lestari (LINI) has worked in the Banggai Islands to promote a
sustainable fishery for the Banggai cardinalfish and to protect habitat
(Talbot et al., 2013). LINI focuses on surveys, capacity building, and
training of local suppliers and reef restoration (Lilley, 2008). LINI's
training and education efforts may raise awareness of needed
conservation efforts to benefit the Banggai cardinalfish. For example,
more benign collection methods have been implemented at Bone Baru, the
species has been adopted as a mascot, and local citizens craft and
market items related to the fish. LINI is also trying to set up a
mechanism for hobbyists to buy only from distributors who use best
practices and are sustainable (Talbot et al., 2013). However, continued
funding for the program is a concern (Moore, personal communication,
2014).
In addition to the protective efforts described above, Indonesia
has committed to develop a comprehensive management plan for the
Banggai cardinalfish under the auspices of Indonesia's national plan of
action under the Coral Triangle Initiative on Coral Reefs, Fisheries,
and Food Security (CTI-CFF). The CTI-CFF specifies a goal to use an
ecosystems-based approach to managing fisheries (EAFM), including a
more sustainable trade in live reef fishes. In 2013, World Wide Fund
for Nature (WWF), in partnership with STPL, implemented a pilot project
in Central Sulawesi Province under the ecosystems-based approach and
chose the Banggai cardinalfish as one of five fisheries case studies in
Banggai Laut District. The goal is to draft local regulations for an
EAFM for two Districts--Banggai Laut District (which encompasses the
majority of the endemic Banggai cardinalfish populations) and Banggai
Kepulauan District (which includes the Peleng Island Banggai
cardinalfish populations). The STPL EAFM Learning Centre team will be
implementing this component through January 2015. These efforts are
likely to introduce local measures to sustain the Banggai cardinalfish
trade (Moore, personal communication, 2014; Ndobe, personal
communication, 2014).
Under the PECE, conservation efforts not yet implemented or not yet
shown to be effective must have certainty of implementation and
effectiveness before being considered as factors decreasing extinction
risk. The effort described above does not satisfy the PECE criteria of
having a certainty of implementation and effectiveness. Although a
pilot project in Central Sulawesi Province under the ecosystems-based
approach is underway with the Banggai cardinalfish as one of five
fisheries case studies, we lack information on how this effort will
yield measures that will be funded, regulated, or regularly practiced
to sustain the Banggai cardinalfish trade in the future; thus, this
effort cannot be considered to alter the risk of extinction of the
Banggai cardinalfish. We seek additional information on other
conservation efforts in our public comment process (see below).
Proposed Determination
Based on the best available scientific and commercial information
discussed above, we find that the Banggai cardinalfish is at a moderate
risk of extinction, but the nature of the threats and demographic risks
identified do not suggest the species is presently in danger of
extinction, and therefore, it does not meet the definition of an
endangered species. We do find, however, that both the species' risk of
extinction and the best available information on the extent of and
trends in the major threats affecting this species (habitat destruction
and overutilization) make it likely this species will become an
endangered species within the foreseeable future throughout its range.
We therefore propose to list it as threatened under the ESA.
Harrisson's Dogfish
The following section describes our analysis of the status of the
gulper shark, Harrisson's dogfish (Centrophorus harrissoni). More
details can be found in Miller (2014).
Species Description
Centrophorus harrissoni, or Harrisson's dogfish, is a shark
belonging to the family Centrophoridae (order Squaliformes). The
Centrophoridae contain two genera: Deania (long-snouted or bird-beak
dogfishes) and
[[Page 74970]]
Centrophorus, usually referred to as gulper sharks. ``Gulper shark'' is
also the common name for the largest species, C. granulosus (White et
al., 2013).
Harrisson's dogfish is endemic to subtropical and temperate waters
off eastern Australia and neighboring seamounts. Specimens identified
as C. harrissoni have also been collected along the Three Kings,
Kermadec, and Norfolk Ridges north of New Zealand, and it has also
possibly been identified off New Caledonia (Duffy, 2007). It is a
demersal species, primarily found along the upper- to mid-continental
and insular slopes off eastern Australia, from north of Evans Head in
northern New South Wales (NSW) to Cape Hauy on the island of Tasmania,
and on the Tasmantid Seamount Chain off NSW and southern Queensland
(hereafter referred to as its ``core range''). It occurs in depths of
180 to 1000 m, with a principal depth range of 200 to 900 m (White et
al., 2008; Last and Stevens, 2009; Williams et al., 2013a). However,
specimens have been collected in deeper waters from the seamounts and
ridges north of New Zealand and off southeastern Australia and in
shallower depths off eastern Bass Strait (Daley et al., 2002; Graham
and Daley, 2011; Williams et al., 2013a). Gulper sharks, including
Harrisson's dogfish, are thought to conduct diel vertical feeding
migrations, whereby the sharks ascend the continental slope near dusk
to around 200 m depths to feed and then descend before dawn (Williams
et al., 2013a), which helps to explain the large depth distribution for
the species. Small bathypelagic bony fishes (particularly myctophids,
lantern fishes), cephalopods, and crustaceans have been found in the
stomachs of C. harrissoni (Daley et al., 2002).
Research studies indicate that C. harrissoni may also exhibit
spatial sexual segregation (Graham and Daley, 2011), based on the
evidence that males tend to dominate the sex ratios on survey grounds
and assumption that females must be more abundant elsewhere to
compensate for the uneven sex ratios. Specifically, sex ratios varied
from 1.5:1 to 4.9:1 along the east coast of Australia, illustrating the
predominance of males (Graham and Daley, 2011). Two notable sites,
however, did show females outnumbering males and were located off
northern NSW, from Newcastle to Danger Point, and off Taupo Seamount
(Graham and Daley, 2011), providing some support for spatial sexual
segregation. Interestingly, Graham and Daley (2011) found no evidence
of sexual or age segregation by depth, with males dominating throughout
all depth zones sampled (with the exception of the two sites noted
above) and juveniles evenly interspersed with adults across all depths.
In terms of mating and reproductive behavior, which could provide
some insight into potential spatial structuring, very little
information is available. It is known that Harrisson's dogfish is
viviparous (i.e., gives birth to live young), with a yolk-sac placenta.
Females have litters of one or (more commonly) two pups, with size at
birth around 35-40 cm TL (Graham and Daley, 2011). Although the
gestation period is unknown, a 2 to 3 year period has been estimated
for other Centrophorus species, with continuous breeding from maturity
to maximum age (Kyne and Simpfendorfer, 2007; Graham and Daley, 2011).
Female C. harrissoni mature at sizes around 98 cm TL and reach maximum
sizes of 112-114 cm TL, while males mature around 75-85 cm TL and reach
maximum sizes of 95-99 cm TL (Graham and Daley, 2011). Female age at
maturity is estimated between 23 and 36 years of age (Daley et al.,
2002; Wilson et al., 2009; Last and Stevens, 2009; Graham and Daley,
2011). Longevity is estimated at over 46 years of age (Wilson et al.,
2009). Current breeding sites for Harrisson's dogfish are thought to
include waters off eastern Australia, from Port Stephens to 31 Canyon,
areas off North Flinders and Cape Barren in southeastern Australia, and
waters around Taupo Seamount (Williams et al., 2012). These are areas
where mature males, mature females, and juveniles have been recorded,
and thus are likely to be areas that support viable populations where
mating and pupping occur (Williams et al., 2012). However, more
extensive sampling, as well critical information regarding the aspects
of the Harrisson's dogfish breeding cycle (including necessary sex
ratios for successful reproduction, preferred mating and breeding
grounds, and mating and breeding behaviors), is needed to identify and
fully comprehend the spatial dynamics of Harrisson's dogfish.
For management purposes, Harrisson's dogfish in Australia have been
separated into two stocks that are considered to be ``distinct''
populations: A ``continental slope'' stock that occurs continuously
along the Australian eastern continental margin, and a ``seamount
stock'' that occurs on the Tasmantid Seamount Chain off NSW and
southern Queensland, including the Fraser, Recorder, Queensland,
Britannia, Derwent Hunter, Barcoo, and Taupo Seamounts. However, to
date, no genetic studies have been conducted to confirm that these two
populations are genetically distinct, and tagging studies are limited,
with insufficient recapture rates to make any determination regarding
the connectivity of the populations. In addition, there are a number of
other uncertainties associated with the assumption of two separate
Harrisson's dogfish stocks, including necessary sex ratios and other
successful reproduction requirements, which are further discussed in
Miller (2014). Due to these uncertainties, we do not find conclusive
evidence of separate populations of Harrisson's dogfish. Therefore, we
consider the available information for these two stocks, including
estimates of depletion rates and protection benefits of management
measures, together when we determine the status of the entire species
throughout its range.
Because species-specific historical and current abundance estimates
are not available, Williams et al. (2013a) used a variety of methods
and analyses to estimate the pre-fishery (pre-1980s) and current
abundance (in biomass units) at fishery stock and sub-regional scales
(detailed information on the data sources and methods can be found in
Williams et al. (2013a)). Results from the various analyses revealed
that Harrisson's dogfish is currently estimated to be at 21 percent of
its pre-fishery population size throughout its core range (with a lower
estimate of 11 percent and upper estimate of 31 percent). The authors
note that this overall estimate of decline is strongly influenced by
the small declines estimated on seamounts (Williams et al. 2013a). The
continental margin population is estimated to be at 11 percent of its
pre-fishery population size (range of 4 to 20 percent; with the
estimate influenced by uncertainty surrounding the level of cumulative
fishing effort off the northern NSW slope). The seamount population is
estimated to be at 75 percent of its pre-fishery population size (range
50 percent to 100 percent).
Summary of Factors Affecting Harrisson's Dogfish
Available information regarding current, historical, and potential
threats to Harrisson's dogfish were thoroughly reviewed (Miller, 2014).
We find that the main threat to the species is overutilization for
commercial purposes, with the species' natural biological vulnerability
to overexploitation exacerbating the severity of the threat, and hence
also identified as a secondary threat contributing to the species' risk
of extinction. We summarize information regarding these threats and
their
[[Page 74971]]
interactions below, according to the factors specified in section
4(a)(1) of the ESA. Available information does not indicate that
habitat destruction, modification, or curtailment, disease, or
predation are operative threats on this species; therefore, we do not
discuss those further here. Because new regulatory measures were just
recently implemented, the adequacy and effectiveness of existing
regulatory measures is discussed in the ``Protective Efforts'' section
below. See Miller (2014) for full discussion of all threat categories.
Overutilization for Commercial, Recreational, Scientific, or
Educational Purposes
Historically, Harrisson's dogfish and other gulper sharks were
taken in both Australian Commonwealth-managed commercial trawl
fisheries (those that are managed by the Australian Federal Government,
in coordination with Australian State fisheries agencies, through the
Australian Fisheries Management Authority (AFMA) (Kyne and
Simpfendorfer, 2007)) and State-managed commercial trawl fisheries
operating on the upper slope off eastern Australia, within the core
range of Harrisson's dogfish. Unfortunately, little information is
available on the specific catch of these deep-water sharks, primarily
due to the historical inaccuracy of data reporting and species
identification issues. These Commonwealth and State-managed commercial
trawl fisheries developed off NSW in the 1970s and off Victoria and
Tasmania in the 1980s. By the early 1980s, more than 100 trawlers were
operating off NSW, with around 60 percent regularly fishing on the
upper slope. In fact, between 1977 and 1988, catches from these upper-
slope trawl operations comprised more than half of the total trawl
landings in NSW (Graham et al., 2001). Large numbers of C. harrissoni
were likely caught and discarded off NSW during this time, due to the
absence of a market for deepwater shark carcasses (a result of mercury
content regulations and preference for more marketable bony fishes)
(Daley et al., 2002; Graham and Daley, 2011). Similarly, trawlers
operating on the upper-slope off eastern Victoria reported minimal
catches of Centrophorus dogfishes, but also likely discarded
substantial numbers due to Victorian State restrictions on mercury
content in shark flesh (Daley et al., 2002). Graham and Daley (2011)
estimate that landings of Centorphorus spp. were around several hundred
tonnes per year during the 1980s and early 1990s.
Daley et al. (2002) note that in the early 1990s significant
quantities of Centrophorus spp. were also caught off eastern Victoria
by fishermen using droplines targeting blue-eye trevalla (Centrolophus
antarctica) and ling (Genypterus blacodes). In addition, some Southern
and Eastern Scalefish and Shark Fishery (SESSF) operators off Victoria
used deep-set gillnets to target Centrophorus species for their livers
in the 1990s (Daley et al., 2002). Squalene oil, which is extracted
from the liver of deep-sea sharks, is used in a number of cosmetics and
health products, and the livers of Centrophorus species have the
highest squalene oil content (67-89 percent) of any deep-sea shark.
Fishermen would keep the livers of the Centrophorus spp. and discard
the carcasses due to their mercury content. However, by the time the
mercury restrictions were eased in 1995 (allowing for carcasses to also
be sold), very few Centrophorus species were being caught off eastern
Victoria, with targeting of these sharks having essentially ceased
(Daley et al., 2002). Since 2002, total catch of gulper sharks by
Commonwealth licensed vessels has been less than 15 t per year
(Woodhams et al., 2013).
In 2001, Graham et al. (2001) quantified the effects of the
historical trawling on the abundance of gulper sharks off NSW using
data from fishery-independent surveys conducted along the upper slope
before and after the expansion of the commercial trawl-fishery (Andrews
et al., 1997). The initial pre-fishery survey was carried out during
1976 and 1977. There were three trawling survey grounds: (1) Sydney-
Newcastle, (2) Ulladulla-Batemans Bay, and (3) Eden-Gabo Island and
eight depth zones (covering depths of 200-650 m). The two northern
grounds (Sydney and Ulladulla) were surveyed twice in 1976 and twice in
1977; the southern (Eden) ground was surveyed three times in 1977.
These surveys were repeated in 1996-1997, (with two surveys conducted
off Sydney and Ulladulla and three off Eden) using the same vessel and
trawl gear and similar sampling protocols, to examine the changes in
relative abundances of the main species (number and kg per trawling
hour) after 20 years of trawling (see Andrew et al., 1997; Graham et
al., 2001). Results from these surveys show that Harrisson's dogfish
were present and, at one time, were caught across all of the survey
grounds and depth zones. In 1976, catches of Harrisson's dogfish were
combined with southern dogfish (C. zeehaani) in the initial two surveys
off Sydney and one off Ulladulla. When these species were separated in
the later 1976 surveys, and in 1977, southern dogfish comprised around
75 percent and Harrisson's dogfish comprised 25 percent of the combined
catch. In 1976-77, Harrisson's and southern dogfishes combined
represented around 9 percent, 18 percent, and 32 percent of the total
fish catches off Sydney, Ulladulla, and Eden, respectively. The overall
mean catch rate (for all grounds and depths) was 126 kg/hour. This is
in stark contrast to the 0.4 kg/h catch rate in 1996-1997, when only 14
southern and 8 Harrisson's dogfishes were caught, comprising 0.18
percent of the total fish catch weight (Graham et al., 2001). For the
1976-77 surveys where the two species were separated, the mean catch
rate of Harrisson's dogfish was 28.8 kg/hr caught over the course of
173 tows. In 1996-97, the mean catch rate of Harrisson's dogfish was
0.1 kg/hr over the course of 165 tows (Graham et al., 1997; 2001).
These decreases in survey catch rates provide compelling evidence of
declines of over 99.7 percent in relative abundance of C. harrissoni on
the upper-slope of NSW, a core part of their range, after 20 years of
trawling activity (Graham et al., 2001).
In Australia, the commercial trawl fisheries are still active, as
are demersal line fisheries, which also incidentally catch Harrisson's
dogfish. In terms of Commonwealth-managed fisheries, Harrisson's
dogfish are primarily caught as bycatch by the SESSF, which operates
over an extensive area of the Australian Fishing Zone (AFZ) around
eastern, southern, and southwestern Australia. The distribution of
recent (2006-2010) commercial fishing effort in the SESSF shows that
there is still substantial fishing effort on Commonwealth upper-slope
grounds using demersal gears, specifically trawl and auto-longline
operations (see Miller (2014) for more details). According to Graham
(2013), around 30 trawlers and 3 auto-longliners in the SESSF still
operate along the upper-slopes. Since auto-longline vessels, which
deploy up to 15,000 hooks per vessel per day, can operate on the steep
and rough ground that would potentially be a refuge for C. harrissoni
from trawling (R. Daley, Commonwealth Scientific and Industrial
Research Organization (CSIRO), personal communication, 2014), the
combined operation of both the trawl and auto-longline fisheries within
the range of Harrisson's dogfish significantly increases the likelihood
of incidental catch of the species. Catch rates of Harrisson's dogfish
in the SESSF have been minimal in recent years, likely due to their low
abundance
[[Page 74972]]
on the continental margin; however, the combined operation of these
demersal gears on the upper-slope grounds may further decrease
abundance of the remaining population. For the 2012-2013 season,
reported gulper shark (C. harrissoni, C. moluccensis, C. zeehaani)
landings (in trunk weight) were 0.9 t with discards of 1.2 t (Woodhams
et al., 2013). This is a decrease from the previous year, which
reported landings of 3.8 t. Given the evidence of substantial depletion
of both Harrisson's and southern dogfishes in Australian waters over
the years, high risk of overfishing in the SESSF, with no current
indication of recovery (based on 2012-2013 season data), the Australian
Government Department of Agriculture classified the above three gulper
sharks as ``overfished'' in 2012, with the current level of fishing
mortality noted as ``uncertain'' (Woodhams et al., 2013). In fact,
upper-slope gulper sharks have been classified as overfished since they
were first included in Australia's Fishery Status Reports in 2005
(Woodhams et al., 2011). In February 2013, a zero retention limit was
implemented for Harrisson's dogfish (Woodhams et al., 2013), along with
other management measures detailed in AFMA's Upper-Slope Dogfish
Management Strategy (AFMA, 2012) and evaluated in the ``Protective
Efforts'' section below.
In terms of state-managed fisheries, the range of Harrisson's
dogfish extends within NSW, Victoria, and Tasmania jurisdictions. In
both Victorian and Tasmanian fisheries, catch records of Harrisson's
dogfish are rare and interactions with these fisheries are considered
to be unlikely, based on their respective fishing operations
(Threatened Species Scientific Committee (TSSC), 2013). In NSW
commercial fisheries, Harrisson's dogfish may be caught by the Ocean
Trap and Line Fishery and the Ocean Trawl Fishery. According to Graham
(2013), there are up to five trawlers in the Ocean Trawl Fishery that
fish seasonally between Newcastle and Sydney and may incidentally catch
Harrisson's dogfish, and only minimal line fishing effort on the upper-
slope (K. Graham, Australian Museum, personal communication, 2014). In
2013, a zero retention limit was implemented for Harrisson's dogfish
(unless for scientific purposes as agreed by Fisheries NSW) (NSW DPI,
2013).
Because of their low productivity, sustainable harvest rates of
gulper sharks are estimated to be less than five percent of their
virgin biomass, and maybe even as low as one percent (reflecting the
proportion of total population that can be caught and still maintain
sustainability of the population; Forrest and Walters, 2009). However,
these harvest levels can only be sustained by a population in a
significantly less depleted state (Woodhams et al., 2011). In the case
of Harrison's dogfish, Woodhams et al. (2013) notes that even low
levels of mortality can pose a risk because of its significantly
depleted state. Although total fishing mortality on gulper sharks is
unknown, the level of catch and observed discards in recent years was
deemed likely to result in further population declines (Woodhams et al.
2011; 2012; 2013). In the 2012-13 fishing season, discards actually
outnumbered landings (1.2 t compared to 0.9 t; Woodhams et al., 2013).
Thus, even with the prohibition on retention of the species, there is
still a potential for discards based on the significant overlap of
current fishing effort within the core range of the species (Woodhams
et al., 2013). This is a concern because Harrisson's dogfish suffers
from high at-vessel mortality in trawl gear and potentially high at-
vessel mortality in auto-longline gear (Williams et al., 2013a).
Therefore, the continued fishing effort on the upper-slope and
potential for incidental capture of Harrisson's dogfish in the trawl
and line fisheries described above, which will likely result in
mortality of the species, is considered a threat that is currently
contributing to the overutilization of the species and its risk of
extinction.
In the areas off New Zealand where C. harrissoni have been observed
(Three Kings Ridge, Norfolk Ridge, and Kermadec Ridge), there is
limited fishing effort (Graham, 2013). The fishing activities include
trawling on the West Norfolk Ridge, drop-lining for large bony fishes
on the Three Kings Rise, West Norfolk Ridge, and Wanganella Bank, and
minimal longlining and close to no trawling on the Kermadec Ridge. No
bycatch of gulper sharks has been reported from these fishing
activities (based on a personal communication from C. Duffy in Graham
(2013)). Given the uncertainty surrounding the C. harrissoni abundance
in this area, it is currently unknown if these fishing activities are
impacting Harrisson's dogfish populations or significantly contributing
to its extinction risk (Graham, 2013).
Other Natural or Manmade Factors Affecting the Continued Existence of
Harrisson's Dogfish
Many sharks are biologically vulnerable to overexploitation due to
their life history parameters. Species with slow population growth
rates, late age at maturity, long gestation times, low fecundity, and
higher longevity are especially sensitive to elevated fishing mortality
(Musick, 1999; Garc[iacute]a et al., 2008; Hutchings et al., 2012).
These life history traits increase the species' susceptibility to
depletion by decreasing the species' ability to rapidly recover from
exploitation. Harrisson's dogfish exhibits these same life history
traits, with late maturity, long gestation times, small litter sizes,
and high longevity. These life history traits have exacerbated the
overall impact of the historical overutilization of the species on its
extinction risk, leading to the substantial decline in Harrisson's
dogfish abundance, and will continue to place the species at increased
risk of demographic stochasticity.
Extinction Risk
It is clear that the species faces current demographic risks that
greatly increase its susceptibility to extinction. Due to the
significant decline, the species is no longer found in approximately 19
percent of its Australian range and, furthermore, throughout the rest
of its core range, is estimated to be at 21 percent of its total virgin
population size (with separate estimates of 11 percent for the
continental margin population and 75 percent for the seamount
population) (Williams et al., 2013a). Although the population on the
seamounts may be less depleted, it also likely comprises a
significantly smaller portion of the entire Harrisson's dogfish
population, based on the amount of available habitat and corresponding
carrying capacity. In fact, the continental margin habitat, where the
population is estimated to be at only 11 percent of its total virgin
population size, represents 86 percent of Harrisson's dogfish's
estimated extent of occurrence and 84 percent of its estimated area of
occupancy (TSSC, 2013), indicating significant depletion throughout
most of the species' range. In addition, the existing Harrisson's
dogfish populations along the continental margin and off the seamounts
in Australia and New Zealand are small and fragmented, with only three
identified remnant populations that are thought to be viable (due to
presence of mature males, females, and/or juveniles within the same
area). Two of these populations are located off the continental margin
and the third is off Taupo Seamount. It is unclear the extent to which
these populations can help recover Harrisson's dogfish, as breeding
behavior, stock structure, inter-
[[Page 74973]]
population exchange, and general movement of individuals is currently
unknown. Due to their size and isolation, these populations may be at
an increased risk of random genetic drift and could experience the
fixing of recessive detrimental alleles that could further contribute
to the species' extinction risk (Musick, 2011). In addition, the patchy
distribution of these populations throughout the species' entire range
increases susceptibility to local extirpations from environmental and
anthropogenic perturbations or catastrophic events. Given the apparent
spatial structuring of the species and dominance of males in the sex
ratios at many locations, a further reduction in the numbers of females
at any given site may decrease reproductive success and prevent
population replacement. The species has extremely low fecundity (2-3
year gestation period resulting in 1 to 2 pups), slow growth rates, and
late maturity, all of which contribute to a long population doubling
time. In a severely depleted state, these traits may contribute to
increasing the species' extinction risk, especially if the species is
still subject to threats that further reduce its abundance. Thus,
although the species' biological characteristics have allowed it to
successfully thrive in the past, under the current conditions of
severely fragmented populations and low abundance throughout its range,
questionable population viability, and risk of incidental mortality
from fisheries, the species' natural life history traits are presently
threatening its continued existence. Specific information is lacking on
interactions among threats.
Without considering the effectiveness of the recently implemented
management measures in reducing the threat of overutilization and
improving the status of Harrisson's dogfish in Australian waters
(discussed in the ``Protective Efforts'' section below), Miller (2014)
concluded that Harrisson's dogfish is presently at a high risk of
extinction due to threats of overutilization exacerbated by its natural
biological vulnerability to depletion, the interaction of which has
resulted in significant demographic risks to the species. We agree with
this analysis and find that the species is presently in danger of
extinction throughout its range. Below we evaluate formalized
conservation efforts that have yet to be implemented or to show
effectiveness to determine whether these efforts contribute to making
listing the species as endangered unnecessary. We evaluate these
conservation efforts using the criteria outlined in PECE.
Protective Efforts
The EPBC Act, the Australian Government's central piece of
environmental legislation, applies to any group or individual whose
actions may have a significant impact on a ``matter of national
environmental significance.'' Any proposed action that meets this
standard must then be assessed to determine its environmental impact.
Species listed as ``vulnerable,'' ``endangered,'' and ``critically
endangered'' under the EPBC Act are considered to be matters of
national environmental significance and receive these provisions.
In 2009, Harrisson's dogfish was nominated for listing under the
EPBC Act. Its status was reviewed by the Threatened Species Scientific
Committee (TSSC), a committee established under the EPBC Act to advise
the Australian Minister for the Environment on the amendment and
updating of lists of threatened species, threatened ecological
communities, and key threatening processes, and with the making or
adoption of recovery plans and threat abatement plans. In 2013, the
TSSC concluded that Harrisson's dogfish was eligible for listing as
endangered under the EPBC Act because the species had suffered a severe
reduction in numbers, with a suspected population decline of between 74
and 82 percent (TSSC, 2013). However, the TSSC concluded that the
species was also eligible for listing as a conservation dependent
species under the EPBC Act because it is the ``focus of a plan of
management [the Strategy] that provides for managed actions necessary
to stop the decline of, and support the recovery of, the species so
that its chances of long term survival in nature are maximized'' (TSSC,
2013). In May 2013, based on the TSSC recommendation, the Minister of
the Environment officially listed Harrisson's dogfish as a conservation
dependent species under the EPBC Act. This listing means that the
species is not considered a matter of national environmental
significance in the context of the EPBC Act, and, as such, Harrisson's
dogfish are exempt from the EPBC Act protective provisions.
In 2012, AFMA published the Upper-Slope Dogfish Management Strategy
(the ``Strategy''; see AFMA, 2012) to satisfy the aforementioned
management requirements for a conservation dependent listing of
Harrisson's Dogfish and Southern Dogfish under Australia's EPBC Act.
The Strategy, which we evaluate below according to the guidelines in
the PECE (68 FR 15100; March 28, 2003), includes regulatory management
measures designed to rebuild the Harrisson's dogfish population above a
limit reference point of 25 percent of its unfished biomass
(B25). Setting a recovery time frame was deemed not feasible
until further research on the species is completed; however, an interim
time frame to reach this reference point was estimated based solely on
the biological characteristics of the species (three generation times)
and equal to 85.5 years (SWG, 2012).
The outcomes and the effectiveness of the Strategy are expected to
be measured on a biennial basis, as detailed in AFMA's ``Upper-Slope
Dogfish Research and Monitoring Workplan.'' The workplan for the period
of 2014-2016 (Workplan 1) focuses on the development of a cost-
effective method for measuring baseline relative abundance of gulper
sharks and recovery over time (AFMA, 2014). This output will be
assessed as part of the Research and Monitoring Workplan 2014-16 review
(proposed time frame of July 2014-Dec 2016). Once the methodology has
been developed, the next output (Workplan 2) is expected to produce
baseline relative abundance estimates for Southern and Harrisson's
dogfish (proposed time frame for output: Jan 2017-Dec 2019). Subsequent
workplans will provide estimates of rebuilding over time and will be
periodically assessed to ensure that the actions within the workplans
are achieving the desired outputs. Hence, it appears it will be a
number of years before the effectiveness of the Strategy will be able
to be quantified. As outlined in the PECE, we must evaluate these
conservation efforts that have not yet demonstrated effectiveness at
the time of listing to determine whether these efforts are likely to be
effective at reducing or eliminating threats and improving the status
of Harrisson's dogfish. Below are the regulatory measures from the
Strategy that have already been implemented by AFMA for the
conservation of the species (under the legal authority of section 41A
of the Australian Fisheries Management Act 1991 and implemented under
``SESSF Fishery Closures Direction No. 1 2013;'' satisfying the first
criteria of the PECE) and our subsequent evaluation of their likely
effectiveness at improving the status of Harrisson's dogfish (the
second criteria of the PECE). The figures and tables referenced below
can be found in the PECE supplement (Miller, 2014b).
Prohibition on the Commercial Retention of Gulper Sharks
The Strategy implements a complete prohibition on the commercial
retention
[[Page 74974]]
of all gulper sharks. However, even before the prohibition, reported
catch rates of Harrisson's dogfish in the SESSF have been minimal in
recent years, likely due to the low abundance of the species on the
continental margin where the fisheries operate. Harrisson's dogfish are
not a targeted species, but rather taken as incidental catch. Although
this prohibition will decrease the numbers of sharks being landed, it
is worth noting that discards have outnumbered landings in recent years
and at a rate that was deemed likely to result in further declines of
the species (Woodhams et al., 2011). Additionally, in the latest
Fishery Status Report for Commonwealth-managed fish stocks, it states:
``[t]here is potential for unreported or underestimated discards (based
on the large degree of overlap of current fishing effort with the core
range of the species [Harrisson's dogfish]), and low levels of
mortality can pose a risk for such depleted populations'' (Woodhams et
al., 2013). Based on the above discarding trends, the fact that it is
the Commonwealth Trawl Sector of the SESSF which is the main fishery
operating within the species' core continental margin range, and the
evidence that Harrisson's dogfish are not expected to survive after
incidental capture in trawl gear (Rowling et al., 2010), the new
retention prohibition may only have a minor impact on decreasing
current fisheries-related mortality.
Network of Spatial/Area Closures
Prior to the Strategy, a number of closures were implemented across
the SESSF operational area (AFMA, 2012); however, there were concerns
that these closures were too small in relation to the historical
distribution of the species to prevent further declines or recover the
species (Musick, 2011; Woodhams et al., 2011). Musick (2011) estimated
that the closures protected Harrisson's dogfish from all forms of
industrial fishing in only 9.8 percent of its habitat. In response to
these concerns, AFMA evaluated options for closures in the Strategy and
created a new network of spatial/area closures in 2013, taking into
account the species' distribution and habitat potential, which would
protect the species from various forms of fishing and prevent further
declines.
Regulations that are the most effective in protecting the species
from threats of overutilization (i.e., incidental catch) are those that
prohibit all types of fishing methods. An analysis of already
implemented conservation efforts from the Strategy estimates that 26.3
percent of the core Harrisson's dogfish seamount habitat (weighted by
carrying capacity--the habitat area's ability to support dogfish
populations) and 5.5 percent of the continental margin habitat are
closed to all types of fishing (see Table 1; Figures 1 and 4 in Miller,
2014b). In terms of the areas that support Harrisson's dogfish
populations, this coverage translates to protection for 26.3 percent of
the current biomass of the seamount population (provided by the new
Derwent Hunter closure) and 19.1 percent of the biomass of the
continental margin population. Contributing to the protection of the
continental margin population are the Strategy's extension of the
Flinders Research Zone closure and revision to the Harrisson's Gulper
closure that prohibits fishing in the depth range of Harrisson's
dogfish. The fact that these closures encompass areas critical to
population viability further increases the effectiveness of this
regulation in improving the status of the species. For example, the
Extended Flinders Research Zone (see Figures 2a and 2b in PECE
supplement) protects the only known potentially reproducing population
of Harrisson's dogfish found south of Sydney. Specifically, this
closure protects the mature male population found around Babel Island,
the mature female population found around Cape Barren, and the likely
migration route between these two populations that is thought to
support mating activities (Middle Ground). Prior to this closure, only
the Babel and Cape Barren grounds were protected, leaving the closely
adjacent Trawl Corridor and Middle Ground open to fishing activities
(and the potential for incidental catch). Now, this closure has been
extended and prohibits all fishing methods from 200 to 1000 m deep,
covering the entire depth range of Harrisson's dogfish.
If we also consider closures that prohibit all high-risk fishing
methods (permitting only power hand-line), the protection coverage
increases to 24 percent of Harrisson's dogfish's entire core habitat
(see Table 1; Figures 1-4 in Miller, 2014b). The effectiveness of these
regulations in improving the status of Harrisson's dogfish partly
depends on the handling of the species in fishing gear and subsequent
post-release mortality rates of the shark. In other words, these
regulations are only likely to be effective in decreasing threats if
they reduce incidental catch altogether or reduce mortality rates of
Harrisson's dogfish when incidentally caught. As these closures
prohibit all fishing with the exception of power-handline methods, we
need to consider the selectivity and post-release mortality of power-
handline methods on Harrisson's dogfish in order to evaluate the
effectiveness of these closures. Based on findings from Graham (2011)
and Williams et al. (2013b), there is a high selectivity rate for
target species (and consequently low bycatch) when using the power
handline technique. For example, in one of the experiments designed to
replicate normal power-handline fishing operations for harvesting blue-
eye trevalla (the target species for power-handline fishing), results
showed that Harrisson's dogfish could be successfully avoided. Out of a
total of 1,435 individual line drops, 25,509 hooks, and over 10 fishing
trips, no Harrisson's dogfish were taken as bycatch. This is in
contrast to the 6,819 blue-eye trevalla that were caught using the
power-handline method (Williams et al., 2013b). Likely contributing to
this high degree of selectivity using the power handline method and
avoidance of Harrisson's dogfish is the fact that fishing for blue-eye
trevalla is normally conducted during daylight hours, in depths of 280-
550 m. Based on Harrisson's dogfish's diel-migration patterns, the
species is normally found in depths greater than 550 m during daylight
hours, deeper than the normal power handline operating depths.
Insight into post-release mortality was also provided from the
Williams et al. (2013b) study, as exploratory fishing for Harrisson's
dogfish was conducted to determine the occurrence of the species on the
seamounts. A total of 105 Harrisson's dogfish were captured during this
exploratory component of the survey and Williams et al. (2013b)
observed that many of these sharks, when brought to the surface, were
in good physical condition. All but one shark were released back into
the water alive and actively swam away. Williams et al. (2013b)
attribute this potentially low post-release mortality to the short soak
times associated with power-handline fishing. In addition, this type of
fishing method consists of a high degree of spatial targeting and small
gear size, which also likely contribute to a high survival rate of
Harrisson's dogfish when caught on lines (Williams et al., 2013b).
Based on these findings, we consider closures that prohibit all high-
risk fishing methods (permitting only power hand-line), as effectively
decreasing the threat of overutilization (i.e., mortality from
incidental catch) of Harrisson's dogfish (see Table 1; Figures 1-4 in
Miller, 2014b). The coverage of these closures, when broken out by
continental margin and seamount proportions and weighted by carrying
capacity, translates to protection for
[[Page 74975]]
Harrisson's dogfish over 18.4 percent of its core continental margin
habitat and 77.6 percent of its seamount habitat (see Table 1 in
Miller, 2014b). Contributing to the protection of the continental
margin population is the Strategy's extension of the Endeavour closure,
and for the seamount population, the newly created Queensland and
Britannia seamount closures.
If we look at the closures that prohibit trawling operations next,
it is estimated that 29.5 percent of the species' core habitat range is
protected from trawling activities (see Table 1 in Miller, 2014b). With
these regulations, almost all of the Harrisson's dogfish's core
seamount habitat would be protected. As Harrisson's dogfish are not
expected to survive when caught in trawl gear, these closures are
likely to be effective in decreasing mortality rates from incidental
catch in trawls. In fact, there is already evidence of rebuilding in
areas that were extensively trawled but have seen significantly less
activity recently. Graham and Daley (2011) note the presence of a high
numbers of juveniles (<80 cm TL, including neonates) that were caught
during a 2009 long-line survey at sites off Port Stephens NSW. This
area had been extensively trawled during the first 20 years of the
upper-slope fishery, but over the last 10 years has seen significantly
less trawling activity (Graham et al., 2001; Graham and Daley, 2011).
The authors of the study attribute the increase in juvenile sightings
as potentially a re-establishment of the population in this area.
NSW closures and regulations may also offer additional protection
to the species (TSSC, 2013). Specifically, the NSW ``North of Sydney
closure'' (see Figure 3 in Miller, 2014b) prohibits all fishing methods
except for power-handline, but allows trawling in depths over 650 m
(which overlaps with the Harrisson's dogfish depth range). The NSW
trawl restriction areas 4 and 6 (see Figure 5 in Miller, 2014b) also
provide some protection by prohibiting trawling, but are open to line
methods. Overall, these additional regulations protect 2.4 percent of
the core habitat (and 3 percent of the core continental margin
habitat), mainly from trawling, except at the shallowest depths (TSSC,
2013).
Many uncertainties surround these estimates. We currently do not
know the locations of important foraging grounds or nursery areas that
are critical for population viability. In addition, we have no
information regarding the movement of Harrisson's dogfish in and out of
these protective closures, or the connectivity between the seamounts
and continental margin populations. However, preliminary tagging
studies of a closely related species, C. zeehaani, inside a fishery
closure off southern Australia suggest that the home ranges of deep-
water dogfish sharks may be small, with evidence of resident female
populations that can be effectively protected by fishery closures
(Daley et al., 2014). Furthermore, as new information becomes available
that improves the understanding of Harrisson's dogfish biology and
stock structure, the management arrangements in the Strategy can be
adapted as necessary to ensure the effectiveness of the Strategy over
time.
Compliance and Enforcement
In addition to the actual spatial extent of the closure network,
the certainty of effectiveness of these regulatory measures in
decreasing threats to the species also depends on the compliance and
enforcement of these closures. For the Commonwealth fisheries, AFMA has
created a compliance team to assist with issues such as quota evasion
and balancing, Vessel Monitoring System (VMS) requirements, and
compliance with fisheries closures and interactions with protected
species. In terms of VMS requirements (a key monitoring provision in
the Strategy), compliance rates have significantly increased over the
years, thanks to outreach material to vessel operators. Compliance
rates for the requirement for vessels to have an operational VMS
averaged around 97 percent for the 2012-2013 year (AFMA, 2013a).
Another key to the successful and effective conservation of the
Harrisson's dogfish population so that it may rebuild in the future is
compliance with fishing prohibitions inside closures. In 2010-2011,
AFMA identified the activity of fishing boats entering and/or fishing
inside closures as an occasional but significant risk. To combat this,
they developed a ``show cause'' program whereby breaches inside
closures were identified from VMS, and the operators of these vessels
were sent a letter asking them to explain or ``show cause'' for their
activity. Within a year of running the program, the incidence of
fishing or navigating inside fishery closures had decreased from an
average of 11 breaches per month to less than 2 breaches per month
(AFMA, 2013b).
Conclusion
After consideration of the evaluation criteria for certainty of
effectiveness under the PECE, we find that these existing regulatory
measures are likely to be effective in improving the present status of
the species. The network of implemented closures addresses the threat
of overutilization by prohibiting high-risk fishing methods, which
decreases fishery-related mortality from bycatch. Based on a prior
review by Musick (2011), it was recommended that closures include at
least 20 to 35 percent of important Harrisson's dogfish habitat in
order to prevent further decline of the species and potentially support
recovery. Overall, the closures evaluated above appear to provide the
species with effective protection from high-risk fishing methods over
24 percent of its core habitat range (see Table 1 in Miller, 2014b).
Specifically, the core habitat of the much-less-depleted seamount
population is significantly protected from high-risk fishing methods
and almost entirely protected (98.2 percent) from trawling activities
(see Table 1 in Miller, 2014b). In fact, 77.6 percent of the seamount
population biomass is protected from all high-risk fishing methods by
the new closures created by the Strategy. These conservation efforts
are likely to effectively improve and protect the status of this
population so that it is no longer presently in danger of extinction.
In terms of the continental margin population, the new network of
spatial closures provides protection from high-risk fishing methods
over 18.4 percent of the core margin habitat. The closures protect 32.4
percent of the current biomass, including the only known viable
population found south of Sydney, from all fishing activities, which
will be critical for improving the status of the population (see Table
1; Figure 1 in Miller, 2014b). Although incidental fishing mortality
may occur outside of these closures, based on the best available
information, we consider the current network of closures effective in
adequately decreasing the present threat of overutilization throughout
the species' range to the point where the species is not currently in
danger of extinction.
As mentioned previously, these conservation efforts have been
designed with the explicit objective to stop the decline of Harrisson's
dogfish and rebuild the population above 25 percent of its unfished
biomass. AFMA's ``Upper-Slope Dogfish Research and Monitoring
Workplan'' details the provisions for monitoring and reporting progress
on the objective and effectiveness (based on evaluation of quantifiable
parameters and using principles of adaptive management) of the
implemented conservation efforts. Specifically, the outcomes and the
effectiveness of the Strategy are expected to be measured on a biennial
basis. However, as noted below,
[[Page 74976]]
certainty that the above conservation efforts will remain in place
after 5 years cannot be predicted at this time. As it stands, the
Strategy, and conservation efforts therein, are only a force under
Australian law if AFMA continues to implement the closures under
section 41A of the Fisheries Management Act 1991. These closures are
implemented under ``Directions'' (for example, the current fishery
closures to protect Harrisson's dogfish have been implemented under
``SESSF Fishery Closures Direction No. 1 2013''). These legal
instruments are only in effect for 5 years, after which AFMA may choose
to extend the closures by creating a new Direction. If AFMA does not
take action after 5 years, these closures will expire.
Although the Upper-Slope Dogfish Research and Monitoring Workplan
details AFMA's commitment to stop the decline of Harrisson's dogfish
and work to rebuild the population, the protection of the species is
not required under the EPBC Act since the species was listed as
conservation dependent instead of endangered. In addition, in the case
where any part of this Strategy ceases to exist or changes, the species
would not automatically be listed as endangered under the EPBC Act.
Rather, the TSSC would be convened and asked to evaluate how the
changes impact the status of the species and provide recommendations on
listing eligibility to the Minister for the Environment, with the
ultimate decision on whether to list the species in a given category
made by the Minister.
While we conclude that the present conservation efforts are
currently effective in preventing the extinction of the species, we
have no certainty that they will remain in place after 5 years. Taking
into account the present state and life history of the species, we do
not consider 5 years to be sufficient time for the status of the
species to improve to where it is no longer in danger of extinction
without the continued implementation of these efforts. In other words,
the removal of these conservation efforts after 5 years will once again
subject the species to the threats described previously, and based on
the information from the extinction risk analysis (e.g., substantial
depletion, fragmented populations, extremely low productivity,
sensitivity to low levels of mortality), we find that the species will
likely become in danger of extinction at that time.
In conclusion, after consideration of the evaluation criteria under
the PECE, we are sufficiently certain that the implemented conservation
efforts will effectively decrease the threat of overutilization by
fisheries in the near term to the point where the species is no longer
presently in danger of extinction. However, given that the
implementation of these conservation efforts is only certain for 5
years, a time frame that is insufficient to increase the species'
chances of survival when faced again with prior threats, we conclude
that the species will likely be in danger of extinction in the
foreseeable future. We specifically seek additional information from
the public comment process on these conservation efforts and their
certainty of implementation and effectiveness (see below).
Proposed Determination
We assessed the ESA section 4(a)(1) factors and conclude that the
species faces ongoing threats from overutilization, with the species'
natural biological vulnerability to overexploitation exacerbating the
severity of the threats. The species faces demographic risks, such as
small and fragmented populations with low productivity, which make it
likely to be influenced by stochastic or depensatory processes
throughout its range and place the species in danger of extinction from
the aforementioned threats. We deem ongoing conservation efforts as
currently effective in decreasing the main threat of overutilization to
the point where the species is no longer presently in danger of
extinction. However, the time frame over which these conservation
efforts will certainly be in place is insufficient to increase the
species' chances of survival or prevent its extinction through the
foreseeable future. Therefore, based on the best available scientific
and commercial information as presented in the status report and this
finding, we find that C. harrissoni is not currently in danger of
extinction throughout its range, but is likely to become so in the
foreseeable future. We propose to list Harrisson's dogfish as a
threatened species under the ESA.
Corals
The three coral species considered herein are all marine
invertebrates in the phylum Cnidaria. The phylum is called Cnidaria
because member species use cnidae (capsules containing stinging
nematocysts) for prey capture and defense. All are tropical, shallow
water, scleractinian (``stony'') corals that secrete a calcium
carbonate skeleton. Two of the three have the typical stony coral
symbiosis with zooxanthellae (photosynthetic) algae that reside in
gastrodermal cells of the coral tissue. All are non-reef building
corals that live in small colonies or as solitary individuals. The
following section describes our analysis of the status of the three
species. Information on many of the species is sparse, so we cannot
provide complete descriptions of their natural history. More details
can be found in Meadows (2014).
Species Description of Cantharellus noumeae
Cantharellus noumeae is a fungiid or mushroom coral that was the
first described species of its genus, in 1984 (Hoeksema and Best,
1984). It received its own new genus name because, unlike most other
fungiid corals, it is stalked and not free-living as an adult. Other
species in the genus have since been discovered and named, so the genus
is no longer monotypic. Polyps are relatively small for a fungiid
coral, ranging from 25 to 65 mm in diameter (Hoeksema and Best, 1984).
The polyps are cup-shaped when fully developed and have wavy margins
(AIMS, 2013a). The primary septa are thin. The species may be solitary
or colonial; colonies consist of a few contorted polyps. Their typical
color is mottled brown.
Cantharellus noumeae was thought to occur only in a restricted area
of less than 225 km \2\ on reefs in sheltered bays in New Caledonia, on
the southern tip of the main island of Grand Terre (Hoeksema et al.,
2008). Recent research by the French Institut de Recherche pour le
D[eacute]veloppement (IRD) has found that the species also occurs on
fringing reefs farther up the southeast coast at Noumea and at Balabaio
in the northeastern part of New Caledonia (www.lagplon.ird.nc; Antoine
Gilbert, Ginger Soproner, personal communication, 2013). It is found in
waters 10 to 35 m deep, close to soft sediment habitats that are in
sheltered bays and lagoons (Hoeksema and Best, 1984). There are records
of it in western, northern, and eastern parts of the island of New
Guinea that includes Papua New Guinea and West Papua, Indonesia, with
details likely to be published soon on a new Web site (http://coralsoftheworld.com; Charlie Veron, personal communication). There are
also reports of it from Papua New Guinea in the International Union for
Conservation of Nature (IUCN) assessment, but the assessment questions
the validity of this record (Hoeksema et al., 2008). The IUCN
assessment and the researcher whose published record is in question
(Doug Fenner) suggest further confirmation is necessary (Hoeksema et
al., 2008; Fenner, personal communication). Fossil records from over 5
million years ago indicate that this species was at one time found as
far west as East Kalimantan, on the island of Borneo,
[[Page 74977]]
Indonesia (Hoeksema, 1989; Hoeksema, 1993).
Scleractinian corals have diverse reproductive strategies,
including both asexual and sexual modes of reproduction (see Brainard
et al., 2011). Individual reproductive modes for these three species
have not been studied. Cantharellus noumeae may be a sequential sex-
changing species like other members of its family. Because of their
relationship with symbiotic zooxanthellae, C. noumeae needs to live in
shallow water to be exposed to light the symbiotic algae use to
photsynthetically fix carbon.
There is no quantitative species-specific population or trend
information available for C. noumeae (Hoeksema et al., 2008; Gilbert,
personal communication). The current and continuing presence of the
species in New Caledonia was confirmed by Bert Hoeksema (personal
communication) in 2012 and in one murky location in Prony Bay on the
southern tip of Grand Terre in 2013 (Andrew Bruckner, personal
communication). In addition, Antoine Gilbert (personal communication)
notes that from surveys he has done over the past 4 years, the species
is ``uncommon and usually found in fringing reefs where sedimentation
is quite intense.'' He also noted that the species is ``usually found
in low density, [but] it was observed in relative[ly] high density on
the slope of artificial shores (embankment) in the biggest (commercial
and industrial) harbour of New Caledonia: la Grande Rade.'' We found no
information on abundance or trends on New Guinea. Its presence at one
site in Milne Bay (Fenner, 2003) is uncertain; Charlie Veron may
publish information from New Guinea on his Web site soon (see above).
Species Description of Siderastrea glynni
Siderastrea glynni was described in 1994 (Budd and Guzm[aacute]n,
1994). It occurs in non-reef-forming spherical colonies that are 70 to
100 mm in diameter (AIMS, 2013b). They have polygonal corallites that
are 2.5 to 3.5 mm in diameter (Budd and Guzm[aacute]n, 1994). The
species is a light reddish-brown in color and occurs on coarse sand-
rubble substrates. Recent genetic work by Forsman et al. (2005) has
shown that S. glynni is genetically very similar to the Caribbean
species S. siderea, though there are differences between the species.
Their study could not differentiate between two possible explanations
of the species' evolution: (1) that S. siderea and S. glynni are the
same species and that S. glynni may have recently passed through or
been carried across the Panama Canal to the Pacific Ocean side; or (2)
the alternate possibility that S. glynni evolved from S. siderea,
likely about 2 to 2.3 million years ago during a period of high sea
level, when the Isthmus of Panama may have been breached, allowing
inter-basin transfer of the species' ancestors. Because the available
information to reclassify the species is inconclusive, we determine
that S. glynni is a valid and unique species.
The range of S. glynni is a small area of the Pacific Ocean near
the small island of Uraba in Panama Bay, a few kilometers from the
opening of the Panama Canal (Guzm[aacute]n and Edgar, 2008). Identified
colonies of S. glynni were reported to be unattached and occur ``along
the upper sand-coral rubble reef slope at a depth of 7 to 8.5 meters''
(Budd and Guzm[aacute]n, 1994). All the islands around the site, as
well as another set of islands to the south, were searched several
times without finding any additional colonies (Fenner, 2001).
The reproductive mode for this species has also not been studied.
Because of their relationship with symbiotic zooxanthellae, S. glynni
need to live in shallow water to be exposed to light the symbiotic
algae use to photsynthetically fix carbon.
Only five colonies of S. glynni have ever been found. All were
found by Budd and Guzm[aacute]n (1994) when they discovered the species
in 1992. All five colonies occurred within a small area of less than 10
m \2\, with each colony within 1 m of another (Budd and Guzm[aacute]n,
1994). Each colony was no more than 20 cm \2\ in size. One colony was
sacrificed in order to provide material for the species' description.
During the 1997-98 El Ni[ntilde]o event, the four surviving colonies
started to deteriorate, displaying signs of bleaching and tissue loss.
Due to their unhealthy state, the four colonies were moved to
Smithsonian Tropical Research Institute (STRI) aquaria in Panama City,
Panama, where they remain to this day (Guzm[aacute]n and Edgar, 2008;
Hector Guzm[aacute]n, STRI, personal communication, 2013). According to
Guzm[aacute]n (personal communication, 2013) the colonies were
fragmented to increase the number of specimens, but their growth rate
has been very slow, and some fragments did not survive. From the
original colonies, only one survives, with less than 4 cm\2\ of living
tissue. Nine of the fragmented colonies also survive in the lab and all
are less than 9 cm \2\ in area (Guzm[aacute]n, personal communication,
2013). No known colonies exist in the wild; however, there is a
possibility that it still exists elsewhere in the wild and is yet
undiscovered (Guzm[aacute]n and Edgar, 2008). There are no plans to re-
introduce the species, as existing colonies are too small to survive,
though three of the fragments are being considered for
cryopreservation, which would further reduce the population size
(Guzm[aacute]n, personal communication, 2013).
Species Description of Tubastraea floreana
Tubastraea floreana was first described by Wells (1982). It is an
azooxanthellate species, which means it lacks the symbiotic
photosynthetic zooxanthellae that most scleractinians have. It has a
bright pink color while alive, but turns deep red-black when dead out
of water. Corallites in the species are closely spaced (Cairns, 1991)
and about 4-6 mm in size (Wells, 1983).
Tubastraea floreana is endemic to a few sites on a number of
islands in the Galapagos Islands chain. It is mostly found in cryptic
habitats, including on the ceilings of caves, and on ledges and rock
overhangs (Hickman et al., 2007). It has been reported to occur at
depths of 2 to 46 m (Hickman et al., 2007).
The reproductive mode of this species has not been studied, but
other Tubastraea species reproduce asexually. Other Tubastraea species
are invasive and productive (Riul et al., 2013), so T. floreana is also
likely to be moderately productive.
According to Hickman et al. (2007), prior to the 1982-83 El
Ni[ntilde]o Southern Oscillation (ENSO) this species was known from six
sites on four islands in the Galapagos. Since the 1982-83 ENSO,
specimens have only been observed at two sites. At one of these two
sites, the species has not been seen since 2001, leaving only a single
confirmed site with living specimens (Hickman et al., 2007). Recent
reports indicate the species is still present in at least one site
(Stuart Banks, Charles Darwin Foundation, personal communication,
2013). We know of no other published information on distribution or
abundance for this species.
Summary of Factors Affecting the Three Species of Coral
Next we consider whether any one or a combination of the threat
factors specified in section 4(a)(1) of the ESA are contributing to the
extinction risk of these three corals. Available information does not
indicate that overutilization is an operative threat for these species;
therefore, we do not discuss this factor further here. We discuss each
of the remaining four factors and their
[[Page 74978]]
interaction in turn below, with species-specific information following
a general discussion relevant to all of the species. A full review of
all of the ESA section 4(a)(1) threat factors can be found in Meadows
(2014b) and our final rule listing 20 corals (20-coral listing rule)
under the ESA (79 FR 53851; September 10, 2014), which provides a
general global summary of threats facing corals. Our 20-coral listing
rule identified ocean warming, ocean acidification, sea-level rise,
disease, sedimentation, nutrient enrichment, and fishing as the major
global threats to coral reefs. The information about these threats and
the species' responses to these threats is described in the 20-coral
listing rule and incorporated herein by reference. Species-specific
information regarding applicability of these threats to the three
species considered here is discussed below, where available. The extent
to which the risks discussed in the 20-coral listing rule are similar
to the risks to these three corals is discussed for each species.
The Present or Threatened Destruction, Modification, or Curtailment of
Its Habitat or Range
Habitat modification from climate change is a potential threat to
all three species of corals (79 FR 53851; September 10, 2014). Coral
bleaching occurs when the photosynthetic zooxanthellae symbionts of
corals are damaged by light at higher than normal temperatures. The
resulting damage leads to the expulsion of these important organisms
from the coral host, depriving the host of the nutrients and energy
provided by the zooxanthellae. While corals can survive mild to
moderate bleaching, repeated, severe, or prolonged bleaching can lead
to colony mortality. Bleaching events have been increasing both in
intensity and geographic extent due to worldwide anthropogenic climate
change (Hoegh-Guldberg, 2006; Eakin et al., 2009). Certain genera and
growth forms, particularly branched species, are more sensitive to
bleaching than others (Wooldridge, 2013). Many corals are
physiologically optimized to their local long-term seasonal variations
in temperatures and an increase of only 1-2 [deg]C above the normal
local seasonal maximum can induce bleaching (Brainard et al., 2011;
Logan et al., 2013). The United States NOAA Coral Reef Watch satellite
bleaching database shows that the range of all three species occurs in
areas that frequently have bleaching alerts, with alerts being more
frequent and severe in the ranges of S. glynni and T. floreana, than in
the range of C. noumeae.
Ocean acidification threatens to slow or halt coral growth and reef
building entirely if the pH of the ocean becomes too low for corals to
form their calcite skeletons, but tolerance appears to vary by species
for those that have been studied (see Brainard et al., 2011). In
addition, bioerosion of reefs is likely to accelerate as coral
skeletons become more fragile as a result of the effects of
acidification, but effects are highly species-specific. Since the
petitioned species are not reef-building, this effect is likely to be
less significant.
Sea-level is also likely to rise as a result of climate change, but
effects on corals are highly uncertain, owing to uncertainty in both
the likely rate and extent of sea-level rise as well as the ability of
corals generally (or the petitioned species specifically) to keep pace
with the rise in sea level (Brainard et al., 2011; 79 FR 53851;
September 10, 2014).
While climate change effects are likely to be serious for many
corals, Brainard et al. (2011) and our final rule listing 20 corals
under the ESA (79 FR 53851; September 10, 2014) show that adaptation
and acclimatization of corals to increased ocean temperatures are
possible, that there is intra-genus and inter-species variation in
susceptibility to bleaching, ocean acidification, and sedimentation,
that at least some species have already expanded their range in
response to climate change, and that not all species are seriously
affected by ocean acidification. In addition, a more recent paper by
Logan et al. (2013) examined the potential for coral adaptation and
acclimatization to climate change and found that these processes can
reduce the frequency of mass bleaching events in the future. Their
modeling results suggest some adaptation or acclimatization may even
have already occurred. A study by Wooldridge (2014) provides support
that a suite of morphological and physiological traits relate to
bleaching vulnerability. These include symbionts' type, metabolic rate,
colony tissue thickness, skeletal growth form, mucus production rates,
fluorescent pigment concentrations, and heterotrophic feeding capacity.
According to Wooldridge (2014), these traits tend to correlate with the
ends of the dichotomy of branching and plate corals with thin tissue
layers versus massive and encrusting corals with thick tissue layers.
The species under consideration here are not necessarily the most
vulnerable, based on those traits (see below). Therefore, while climate
change is generally considered a potential threat to these candidate
corals, the likelihood and magnitude of threats from climate change are
largely species-specific and must be examined on that basis to fully
assess extinction risk (79 FR 53851; September 10, 2014).
In addition to the general global threats identified in our status
review of 82 corals and final rule listing 20 corals under the ESA
(Brainard et al., 2011; 79 FR 53851; September 10, 2014), there are
some species-specific threats for which we have detailed information at
the scale of these species' ranges that are discussed below.
Cantharellus noumeae
Cantharellus noumeae is exposed to deforestation, urbanization, and
mining activity that causes sedimentation and water pollution
throughout its range in New Caledonia (Hoeksema et al., 2008; David et
al., 2010; McKenna et al., 2011). The mining activity is a result of
nickel and smaller amounts of other metal mining (cobalt and chromium
especially) on land throughout the main island of Grand Terre (McKenna
et al., 2011; Hoeksema, personal communication). Grand Terre holds 25
percent of the world's known nickel deposits (McKenna et al., 2011).
Nickel mining started there in the 1870s. Currently, most mining is
done by open-cast strip mining, which has caused deforestation and
increased erosion and runoff of sediments leading to varying degrees of
sedimentation and light attenuation throughout the lagoon of Grand
Terre, including in areas in and adjacent to the species' range
(Ouillon et al., 2010). Labrosse et al. (2000) estimate that 300
million m \3\ of soil has been displaced since the beginning of mining
activities. Mines are located across the country, including the large
new Goro complex, which includes mines, processing facilities, and a
port. The complex began production in late 2010 and is very near the
most abundant population of C. noumeae. The Goro complex has already
had three incidents affecting the environment, involving spills or
releases of sulfuric acid solutions used in the processing of the
nickel ore (Sulfuric Acid on the Web, 2013). Runoff of heavy metals
from the mining operations has greatly increased concentrations of
those metals in the marine environment (Fichez et al., 2010). Nickel
has been shown to affect fertilization success of four reef coral
species in the families Acroporidae and Faviidae (Reichelt-Brushett and
Harrison, 2005) and to affect settlement and cause mortality of larvae
in the coral Pocillopora damicornis (Goh, 1991). Gilbert (personal
communication, 2013) reports that the species is common in areas of
high sedimentation and in the largest harbor, so it may be
[[Page 74979]]
tolerant to environmental stressors like sedimentation. The species may
have the ability to actively remove sediments, as has been shown in
some other fungiid corals (Bongaerts et al., 2012), but this is
uncertain. Mitigation measures for mining operations are required by
legislation and include reef monitoring requirements (UNESCO, 2011;
Gilbert, personal communication, 2013), but this monitoring is not at
the species level (Gilbert, personal communication, 2013). It is
unclear how effective the mitigation methods are, as sedimentation and
pollution remain concerns (David et al., 2010).
Despite the frequency of bleaching alerts, heat-related bleaching
is apparently not a significant current threat in the range of C.
noumeae in New Caledonia, as water temperatures there are relatively
low (Hoeksema, Naturalis Biodiversity Center, personal communication,
2013) and the ReefBase coral bleaching database only reports events
with low bleaching severity as the worst past events to ever occur
there. We have found no species-specific information on the
susceptibility of this species to bleaching or ocean acidification;
however, its growth form suggests it is not among the most susceptible
species (Wooldridge, 2014).
Anthropogenic eutrophication occurs in the range of the species
near the capital of Noumea and is attributed mostly to inadequately
treated sewage (Fichez et al., 2010), although 19 aquaculture farms on
the west coast and island-wide agriculture may also play roles (David
et al., 2010). Storm events and flooding have also recently occurred in
the range of the species (EMR, 2013), and there is concern that climate
change may make such events more frequent in New Caledonia (Gilbert,
personal communication, 2013).
The biggest threats to New Guinea's coral reef resources include
sedimentation and pollution from inland sources (e.g., forest
clearance, sewage, and erosion), climate change, and dynamite fishing
(Burke et al., 2011; PNG, 2009; PNG, 2012). There is little specific
data on these threats in New Guinea in the above references.
Siderastrea glynni
Should S. glynni ever be restored to the wild, it faces
considerable habitat degradation threats from coastal development, oil
production, sedimentation, eutrophication and other pollution, and
increased transportation activities in the Panama City area, the Gulf
of Panama, and the enlarged Panama Canal, which is due to open in 2016
(Mate, 2003; Guzm[aacute]n and Edgar, 2008). Almost continuous dredging
and release of oil-based compounds (bunker oil, diesel, gasoline, etc.)
that are spilled from nearby port facilities and commercial vessels
anchored near the species' natural range are other reasons why it was
decided to transfer and then keep in captivity the remaining known
colonies (Guzman, personal communication, 2013). ``During the 1997-98
ENSO event, the four known colonies of S. glynni began to deteriorate,
displaying bleaching and tissue loss'' (Guzm[aacute]n and Edgar, 2008).
This suggests this species is vulnerable to increased ocean
temperatures, though there is no specific research on this point. As
discussed above, the area of the species' range is subject to a high
frequency of bleaching warnings. We have found no species-specific
information on the susceptibility of this species to ocean
acidification.
Tubastraea floreana
For T. floreana, there is a lack of information on thermal
tolerances, but ``the dramatic reduction in its distribution
immediately after the 1982-83 [ENSO] event suggests that this mortality
resulted from the event'' (Hickman et al., 2007). This is true despite
the fact that this species is azooxanthellate, suggesting that other
mechanisms besides loss of calorie subsidy from symbionts are involved.
Edgar et al. (2010) document a series of drastic ecosystem changes in
the Galapagos following the 1982-83 ENSO event, including dramatic
declines in dissolved nutrients and phytoplankton productivity, leading
to declines across the food chain and resulting in heavily grazed reefs
with crustose coralline algae (``urchin barrens'') replacing former
macroalgal and coral habitats. A total of 95-99 percent of reef coral
cover was lost from the Galapagos between 1983 and 1985 (Edgar et al.,
2010). All known coral reefs based on calcareous frameworks died and
subsequently disintegrated to rubble and sand (Glynn, 1994). These
changes led to large decreases in biodiversity. The urchin Eucidaris
galapagensis now appears to be present in sufficient numbers to prevent
re-establishment of coral and macroalgal habitat, thereby facilitating
a regime shift in local benthic habitats (Edgar et al., 2010).
Moreover, the Galapagos Islands sit near the center of the most intense
El Ni[ntilde]o events in the region (Glynn and Ault, 2000) and are
regularly included in bleaching threat warnings issued by NOAA (see
above). Therefore, future ENSO events and inhibition of recruitment are
likely to remain threats to T. floreana. We have found no species-
specific information on the susceptibility of this species to ocean
acidification.
Disease and Predation
Coral disease has been linked to the effects of climate change (see
Brainard et al., 2011), especially indirectly as a synergistic effect,
as climate change and other threats potentially increase stress on
corals, making them more susceptible to disease. Coral diseases also
appear to be increasing worldwide (Roessig et al., 2004). Nevertheless,
susceptibility of coral species to disease is highly species-specific
and no generalizations can be made. We found no species-specific
information on disease in C. noumeae or T. floreana. Black-band, dark
spot, and white plague diseases in the Caribbean occur in S. siderea,
which is closely related to S. glynni (Sekar et al., 2008; Brandt and
McManus, 2009; Cardenas et al., 2012), suggesting S. glynni may be
susceptible to similar coral diseases, but we have no solid
information.
With respect to predation, we found no information on predation
threats to S. glynni or T. floreana. For C. noumeae, one potential
predation threat is Acanthaster planci (crown-of-thorns starfish).
Acanthaster planci does not appear to be a major cause of coral
mortality in New Caledonia (Adjeroud, 2012), but several remote reefs
surveyed during the Global Reef Expedition in November 2013 on the
outer-slope of Guilbert's atolls showed evidence of past outbreaks
(LOF, 2013).
Inadequacy of Existing Regulatory Mechanisms
The petitioners discussed regulation of trade in corals under CITES
as a threat to these species. All of the species considered in this
petition were listed in Appendix II of CITES in 1989, when all
scleractinian corals were listed. While only some scleractinians were
in trade at the time, the 1989 listing rationale for including all
scleractinians in Appendix II was because of identification
difficulties where non-traded species resemble species in trade.
According to Article II of CITES, species listed on Appendix II are
those that are ``not necessarily now threatened with extinction but may
become so unless trade in specimens of such species is subject to
strict regulation in order to avoid utilization incompatible with their
survival.'' Based on the CITES definitions and standards for listing
species on Appendix II, the species' listing on Appendix II is not
itself an inherent indication that these species may now warrant
threatened or endangered status under the ESA. The
[[Page 74980]]
significance of any threat from international trade would depend on the
amount of international trade relative to the population size of the
species, as well as any other factors related to the trade, such as
habitat damage caused in the collecting process, or synergistic effects
of other threats. We have no information any of these three species is
traded internationally.
Because each of the species considered herein exists in small
ranges that do not overlap with each other, and they are not otherwise
managed or regulated under any other common international regimes,
additional discussion of this factor is left for the species-specific
entries for this section, below.
Cantharellus noumeae
Since the Organic Law (No. 99-209) on March 19, 1999, New Caledonia
has been recognized as an ``Overseas Country'' of France. This status
gives New Caledonia extensive autonomy with respect to France. In
particular, the national laws in force within France are no longer
applicable to New Caledonia, and New Caledonia now manages the ocean
resources of its Exclusive Economic Zone. The territorial sea and the
maritime public domain (coastal terrestrial and nearshore aquatic zone
originating under French colonial law) depend on management from New
Caledonia's three provinces (David et al., 2010). In the two provinces
where C. noumeae occurs, collection of live corals (and other marine
resources) is restricted to scientists and licensed fishers who can
only collect for a domestic market.
The range of C. noumeae is included in the United Nations
Education, Scientific and Cultural Organization (UNESCO) World Heritage
Site designation for the ``Lagoons of New Caledonia'' site,
specifically within the South Grand Lagoon area. The World Heritage
Site implementation is supported by specific legislation on fisheries,
land and water use planning, urban development, and mining (Morris and
Mackay, 2008). A wide monitoring program of the heritage site all
around New Caledonia was created (Andr[eacute]fou[euml]t 2008), but
this suffers from a lack of sampling at a species level (Gilbert,
personal communication, 2013). In 2011, the World Heritage Committee of
UNESCO (the organizing body for World Heritage Sites) issued Decision
35Com 7B.22, which expressed concern regarding permits granted to the
mining company GEOVIC to explore for cobalt in mineral sands in areas
adjacent to the site and near the range of C. noumeae. The committee
requested that New Caledonia submit Environmental Impact Assessments
for the proposed exploration and possible exploitation of cobalt sands
to the World Heritage Centre. We have no evidence this has occurred.
The New Caledonian Mining Code prescribes mitigation measures to
mitigate the impacts of mining activities (see above), and abandoned
mines are being restored using indigenous plant species (UNESCO, 2011).
In Papua New Guinea, there is a variety of legislation to protect
biodiversity and habitat, including a mandate to ensure marine resource
sustainability, and a plan of action directed at coral reef
conservation (PNG, 2009). However, as noted above, threats remain.
Resources and capacity may not be adequate to ensure full
implementation of the laws and plan (PNG, 2009; PNG, 2012).
Overall, we do not believe that the threat to C. noumeae from
habitat modification, destruction, and pollution is adequately
addressed or mitigated by existing regulatory mechanisms.
Siderastrea glynni
A national law in Panama prohibits coral extraction or mining
(Guzm[aacute]n, 2003), but enforcement is weak and the law may not
fully protect rare species (Guzm[aacute]n, personal communication,
2013). The range of S. glynni is adjacent to the Bay of Panama, which
is designated an internationally important wetland under the Ramsar
Convention and contains extensive mangrove beds that are critical
nursery grounds for many marine species. The Bay is a protected
Wildlife Refuge under Panamanian law. However, developers seek to open
the area for tourism, and Panamanian authorities have requested a
reduction of the Ramsar area of the bay (AIDA, 2013). We were not able
to find any other species-specific information on this threat. Based on
the available information, it is not clear that existing regulatory
mechanisms would be adequate to protect S. glynni, should it be
reintroduced into the wild or found in additional locations.
Tubastraea floreana
The Gal[aacute]pagos Marine Reserve was established in 1986 and
expanded to its current size around all the islands in 1998. The
reserve has a zoning plan with both limited and multiple use zones.
Rules prohibit removing or disturbing any plant, animal, or remains of
such, or other natural objects. Tubastraea floreana also occurs inside
the Galapagos Island World Heritage Site (expanded to include Galapagos
Marine Reserve areas in 2001) and the Gal[aacute]pagos Island Man and
Biosphere Reserve (1984), both designations of UNESCO. The area was
also designated a Gal[aacute]pagos Archipelago Particularly Sensitive
Area in 2005. This is a designation by the International Maritime
Organization (IMO) that recognizes the area as having ecological,
socio-economic, or scientific attributes that make the area vulnerable
to damage by international shipping activities. Based on this
designation, the IMO instituted special navigation rules in the area.
In addition, Ecuador's ``Ley de Gestion Ambiental'' (Law of
Environmental Management) establishes principles and directives for
environmental management, land-use planning, zoning, sustainable use,
and natural heritage conservation. Ecuador's fisheries law states that
no harm may be caused to areas that are declared protected, with corals
included under those protections (MCA Toolkit, 2013). While the above
laws and protected area designations provide a great deal of protection
for resources in the area in principal, in practice, illegal activities
and incomplete and difficult enforcement, as discussed in the status
review report (Meadows, 2014), could threaten T. floreana. Moreover,
the threats from climate change and ENSO events are outside the scope
of these protections.
Other Natural or Manmade Factors Affecting Their Continued Existence
The range of C. noumeae in New Caledonia is exposed to eight
tropical storms per year on average (David et al., 2010). Specific
effects of storms on this species are not documented, but the
petitioner submitted an undated Web page that claims Cyclone Erica
destroyed between 10 and 80 percent of live coral in New Caledonia in
2003 (EDGE, Undated; Guillemot et al., 2010). We were not able to find
any other species-specific information available regarding this threat
category for C. noumeae. Based on this information, we consider
tropical storms an additional potential natural threat to the species,
for which we seek additional information (see below).
For S. glynni and T. floreana, both species have such a small
number of colonies, they are susceptible to all of the problems of
species with low genetic diversity and population size, including
inbreeding depression, population bottlenecks, Allee effects, and
density-independent mortality, among others.
Extinction Risk
The extinction risk analyses of Meadows (2014) found all three
species to be at either a moderately high or high
[[Page 74981]]
risk of extinction. The extinction risk for C. noumeae was found to be
moderately high, based on the species' small, restricted range, likely
low growth rate and genetic diversity, and potential threats from
development, water pollution, possibly sedimentation at some level, and
potential illegal activities, mitigated by consideration of potential
resilience to sedimentation threats and uncertainty regarding
sensitivity to heavy metals. Based on the current information, this is
the case whether or not the species' range includes New Guinea. The
extinction risk for S. glynni was found to be high, due to the lack of
known populations in the wild, a small captive population in a single
location, likely low growth rates and genetic diversity, and potential
increased threats from El Ni[ntilde]o, climate change, disease, and
other development and habitat degradation, should the species be
reintroduced to Panama. The extinction risk for T. floreana was found
to be high, based on its small, restricted range, documented declines,
likely low levels of genetic diversity, and threats from El
Ni[ntilde]o, climate change, development, and illegal activities,
mitigated by potential for moderate productivity.
After reviewing the best available scientific data and the
extinction risk evaluations of the three species of coral, we concur
with Meadows (2014) and conclude that the risk of extinction for all
three species is currently high.
Protective Efforts
We evaluated conservation efforts we are aware of to protect and
recover coral that are either underway but not yet shown to be
effective, or are only planned. We were not able to find any
information on conservation efforts specific to C. noumeae or T.
floreana, or their habitat, that are not yet implemented or shown to be
effective and that would potentially alter the extinction risk for the
species. For S. glynni, we are aware that Dr. Hector Guzm[aacute]n, who
maintains the only surviving colonies of this species in captivity at
the STRI laboratories, is planning to cryopreserve some specimens to
provide an additional means to recover the species and preserve its
genetic information. The certainty that this effort will be implemented
is unclear. Further, the effectiveness of a cryopreservation effort for
species recovery is largely unknown, and thus it is impossible to
determine whether this effort will be effective in conserving or
improving the status of this species. We are thus not able to conclude
that any current conservation efforts would alter the extinction risk
for any of these three species. We seek additional information on other
conservation efforts in our public comment process (see below).
Proposed Determination
Based on the best available scientific and commercial information
as presented in the status report and this finding, we find that all
three species of coral are in danger of extinction throughout all of
their ranges. We assessed the ESA section 4(a)(1) factors and conclude
that Cantharellus noumeae, Siderastrea glynni, and Tubastraea floreana
all face ongoing threats from habitat alteration, small ranges and/or
population sizes, and the inadequacy of existing regulatory mechanisms
throughout their ranges. C. noumeae also faces risks from pollution and
S. glynni may be at risk from disease. We therefore propose to list all
three species as endangered.
Effects of Listing
Conservation measures provided for species listed as endangered or
threatened under the ESA include recovery actions (16 U.S.C. 1533(f));
concurrent designation of critical habitat, if prudent and determinable
(16 U.S.C. 1533(a)(3)(A)); Federal agency requirements to consult with
NMFS under section 7 of the ESA to ensure their actions do not
jeopardize the species or result in adverse modification or destruction
of critical habitat should it be designated (16 U.S.C. 1536); and
prohibitions on taking (16 U.S.C. 1538). Recognition of the species'
plight through listing promotes conservation actions by Federal and
state agencies, foreign entities, private groups, and individuals. The
main effects of the proposed endangered listings are prohibitions on
take, including export and import.
Identifying Section 7 Conference and Consultation Requirements
Section 7(a)(2) (16 U.S.C. 1536(a)(2)) of the ESA and NMFS/USFWS
regulations require Federal agencies to consult with us to ensure that
activities they authorize, fund, or carry out are not likely to
jeopardize the continued existence of listed species or destroy or
adversely modify critical habitat. Section 7(a)(4) (16 U.S.C.
1536(a)(4)) of the ESA and NMFS/USFWS regulations also 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 of
those species. It is unlikely that the listing of these species under
the ESA will increase the number of section 7 consultations, because
these species occur outside of the United States and are unlikely to be
affected by Federal actions.
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. Section 4(a)(3)(A)
of the ESA (16 U.S.C. 1533(a)(3)(A)) requires that, to the extent
prudent and determinable, critical habitat be designated concurrently
with the listing of a species. However, critical habitat shall not be
designated in foreign countries or other areas outside U.S.
jurisdiction (50 CFR 424.12 (h)).
The best available scientific and commercial data as discussed
above identify the geographical areas occupied by Aipysurus fuscus,
Cantharellus noumeae, Centrophorus harrissoni, Pterapogon kauderni,
Siderastrea glynni, and Tubastraea floreana as being entirely outside
U.S. jurisdiction, so we cannot designate critical habitat for these
species.
We can designate critical habitat in areas in the United States
currently unoccupied by the species, if the area(s) are determined by
the Secretary to be essential for the conservation of the species.
Regulations at 50 CFR 424.12(e) specify that we shall designate as
critical habitat areas outside the geographical range presently
occupied by the species only when the designation limited to its
present range would be inadequate to ensure the conservation of the
species. The best available scientific and commercial information on
these species does not indicate that U.S. waters provide any specific
essential biological function for any of the species proposed for
listing. Based on the best available information, we have not
identified unoccupied area(s) in U.S. water that are currently
essential to the conservation of any of the corals proposed for
listing. Therefore, based on the available
[[Page 74982]]
information, we do not intend to designate critical habitat for
Aipysurus fuscus, Cantharellus noumeae, Centrophorus harrissoni,
Pterapogon kauderni, Siderastrea glynni, and Tubastraea floreana.
Identification of Those Activities That Would Constitute a Violation of
Section 9 of the ESA
On July 1, 1994, NMFS and FWS published a policy (59 FR 34272) that
requires us to identify, to the maximum extent practicable at the time
a species is listed, those activities that would or would not
constitute a violation of section 9 of the ESA.
Because we are proposing to list all three corals and the dusky sea
snake as endangered, all of the prohibitions of section 9(a)(1) of the
ESA will apply to these species. These include prohibitions against the
import, export, use in foreign commerce, or ``take'' of the species.
These prohibitions apply to all persons subject to the jurisdiction of
the United States, including in the United States, its territorial sea,
or on the high seas. Take is defined as ``to harass, harm, pursue,
hunt, shoot, wound, kill, trap, capture, or collect, or to attempt to
engage in any such conduct.'' The intent of this policy is to increase
public awareness of the effects of this listing on proposed and ongoing
activities within the species' range. Activities that we believe could
result in a violation of section 9 prohibitions for these species
include, but are not limited to, the following:
(1) Possessing, delivering, transporting, or shipping any
individual or part (dead or alive) taken in violation of section
9(a)(1);
(2) Delivering, receiving, carrying, transporting, or shipping in
interstate or foreign commerce any individual or part, in the course of
a commercial activity;
(3) Selling or offering for sale in interstate commerce any part,
except antique articles at least 100 years old;
(4) Importing or exporting;
(5) Releasing captive animals into the wild without a permit issued
under section 10(a)(1)(A). Although animals held non-commercially in
captivity at the time of listing are exempt from the prohibitions of
import and export, the individual animals are considered listed and
afforded most of the protections of the ESA, including most
importantly, the prohibition against injuring or killing. Release of a
captive animal has the potential to injure or kill the animal. Of an
even greater conservation concern, the release of a captive animal has
the potential to affect wild populations through introduction of
diseases or inappropriate genetic mixing;
(6) Harming captive animals by, among other things, injuring or
killing a captive animal, through experimental or potentially injurious
care or conducting research or sexual breeding activities on captive
animals, outside the bounds of normal animal husbandry practices.
Captive sexual breeding of corals is considered potentially injurious.
Furthermore, the production of coral progeny has conservation
implications (both positive and negative) for wild populations.
Experimental or potentially injurious care or procedures and research
or sexual breeding activities of corals or dusky sea snakes may,
depending on the circumstances, be authorized under an ESA 10(a)(1)(A)
permit for scientific research or the enhancement of the propagation or
survival of the species.
Identification of Those Activities That Would Not Constitute a
Violation of Section 9 of the ESA
We will identify, to the extent known at the time of the final
rule, specific activities that will not be considered likely to result
in a violation of section 9 of the ESA. Although not binding, we are
considering the following actions, depending on the circumstances, as
not being prohibited by ESA section 9:
(1) Take authorized by, and carried out in accordance with the
terms and conditions of, an ESA section 10(a)(1)(A) permit issued by
NMFS for purposes of scientific research or the enhancement of the
propagation or survival of the species;
(2) Continued possession of parts that were in possession at the
time of listing. Such parts may be non-commercially exported or
imported; however the importer or exporter must be able to provide
evidence to show that the parts meet the criteria of ESA section
9(b)(1) (i.e., held in a controlled environment at the time of listing,
in a non-commercial activity);
(3) Continued possession of live corals or sea snakes that were in
captivity or in a controlled environment (e.g., in aquaria) at the time
of this listing, so long as the prohibitions under ESA section 9(a)(1)
are not violated. Facilities must provide evidence that the animals
were in captivity or in a controlled environment prior to listing. We
suggest such facilities submit information to us on the animals in
their possession (e.g., size, age, description of animals, and the
source and date of acquisition) to establish their claim of possession
(see For Further Information Contact);
(4) Provision of care for live corals or sea snakes that were in
captivity at the time of listing. These individuals are still protected
under the ESA and may not be killed or injured, or otherwise harmed,
and, therefore, must receive proper care. Normal care of captive
animals necessarily entails handling or other manipulation of the
animals, and we do not consider such activities to constitute take or
harassment of the animals so long as adequate care, including
veterinary care, when such practices, procedures, or provisions are not
likely to result in injury, is provided; and
(5) Any interstate and foreign commerce trade of animals already in
captivity. Section 11(f) of the ESA gives NMFS authority to promulgate
regulations that may be appropriate to enforce the ESA. NMFS may
promulgate future regulations to regulate trade or holding of these
species (if any), if necessary. NMFS will provide the public with the
opportunity to comment on future proposed regulations.
Protective Regulations Under Section 4(d) of the ESA
We are proposing to list Pterapogon kauderni, and Centrophorus
harrissoni as threatened species. In the case of threatened species,
ESA section 4(d) leaves it to the Secretary's discretion whether, and
to what extent, to extend the section 9(a) ``take'' prohibitions to the
species, and authorizes us to issue regulations necessary and advisable
for the conservation of the species. Thus, we have flexibility under
section 4(d) to tailor protective regulations, taking into account the
effectiveness of available conservation measures. The 4(d) protective
regulations may prohibit, with respect to threatened species, some or
all of the acts which section 9(a) of the ESA prohibits with respect to
endangered species. These 9(a) prohibitions apply to all individuals,
organizations, and agencies subject to U.S. jurisdiction. We will
consider potential protective regulations pursuant to section 4(d) for
the proposed threatened species. For example, we may consider future
regulations on trade of wild-caught Banggai cardinalfish (see number 7
below). We seek public comment on potential 4(d) protective regulations
(see below).
Public Comments Solicited
To ensure that any final action resulting from this proposed rule
to list six species will be as accurate and effective as possible, we
are soliciting comments and information from the public, other
concerned governmental
[[Page 74983]]
agencies, the scientific community, industry, and any other interested
parties on information in the status review and proposed rule. Comments
are encouraged on these proposals (See DATES and ADDRESSES). We must
base our final determination on the best available scientific and
commercial information when making listing determinations. We cannot,
for example, consider the economic effects of a listing determination.
Final promulgation of any regulation(s) on these species' listing
proposals will take into consideration the comments and any additional
information we receive, and such communications may lead to a final
regulation that differs from this proposal or result in a withdrawal of
this listing proposal. We particularly seek:
(1) Information concerning the threats to any of the six species
proposed for listing;
(2) Taxonomic information on any of these species;
(3) Biological information (life history, genetics, population
connectivity, etc.) on any of these species;
(4) Efforts being made to protect any of these species throughout
their current ranges;
(5) Information on the commercial trade of any of these species;
(6) Historical and current distribution and abundance and trends
for any of these species; and
(7) Information relevant to potential ESA section 4(d) protective
regulations for any of the proposed threatened species, especially the
application, if any, of the ESA section 9 prohibitions on import, take,
possession, receipt, and sale of the Banggai cardinalfish which is
currently in international trade.
We request that all information be accompanied by: (1) Supporting
documentation, such as maps, bibliographic references, or reprints of
pertinent publications; and (2) the submitter's name, address, and any
association, institution, or business that the person represents.
Role of Peer Review
In December 2004, the Office of Management and Budget (OMB) issued
a Final Information Quality Bulletin for Peer Review establishing a
minimum peer review standard. Similarly, a joint NMFS/FWS policy (59 FR
34270; July 1, 1994) requires us to solicit independent expert review
from qualified specialists, concurrent with the public comment period.
The intent of the peer review policy is to ensure that listings are
based on the best scientific and commercial data available. We
solicited peer review comments on each of the status review reports,
including from: four scientists with expertise on sea snakes or the
dusky sea snake specifically, five familiar with the Banggai
cardinalfish, five familiar with Harrisson's dogfish, and ten
scientists familiar with corals. For these species, we received
comments from the scientists, and their comments are incorporated into
the draft status review reports for each species and this 12-month
finding.
Proposed Revisions to the NMFS Lists
We propose to revise and add table subheadings to accommodate the
proposed listings in our lists of threatened and endangered species at
50 CFR 223.102 and 50 CFR 224.101, respectively. We propose to revise
the subheading of ``Sea Turtles'' in both tables by changing the
subheading to ``Reptiles.'' This new subheading will encompass all
currently listed sea turtles as well as other marine reptiles like the
dusky sea snake. In addition, we propose to add the subheading
``Corals'' to our table at 50 CFR 224.101. This subheading has already
been added to our table at 50 CFR 223.102 in a previous rulemaking (79
FR 20802; April 14, 2014). These revisions and additions are not
substantive changes, but having these headings will help the public
identify and locate species of interest in a more efficient manner.
References
A complete list of the references used in this proposed rule is
available upon request (see ADDRESSES).
Classification
National Environmental Policy Act
The 1982 amendments to the ESA, in section 4(b)(1)(A), restrict the
information that may be considered when assessing species for listing.
Based on this limitation of criteria for a listing decision and the
opinion in Pacific Legal Foundation v. Andrus, 675 F. 2d 825 (6th Cir.
1981), NMFS has concluded that ESA listing actions are not subject to
the environmental assessment requirements of the National Environmental
Policy Act (NEPA) (See NOAA Administrative Order 216-6).
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. We will confer with the U.S. Department of State to ensure
appropriate notice is given to foreign nations within the range of all
three species. As the process continues, we intend to continue engaging
in informal and formal contacts with the U.S. State Department, giving
careful consideration to all written and oral comments received.
List of Subjects in 50 CFR Parts 223 and 224
Administrative practice and procedure, Endangered and threatened
species, Exports, Imports, Reporting and record keeping requirements,
Transportation.
Dated: December 8, 2014.
Samuel D. Rauch, III.
Deputy Assistant Administrator for Regulatory Programs, National Marine
Fisheries Service.
For the reasons set out in the preamble, 50 CFR parts 223 and 224
are 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, amend the table in paragraph (e) by:
0
A. Revising the table subheading of ``Sea Turtles \2\'' to ``Reptiles
\2\''; and
0
B. Adding new entries for two species in alphabetical order under the
``Fishes'' table subheading to read as follows:
Sec. 223.102 Enumeration of threatened marine and anadromous species.
* * * * *
[[Page 74984]]
(e) The threatened species under the jurisdiction of the Secretary
of Commerce are:
----------------------------------------------------------------------------------------------------------------
Species \1\
-------------------------------------------------------------------- Citation(s) for Critical
Description of listing habitat ESA rules
Common name Scientific name listed entity determination(s)
----------------------------------------------------------------------------------------------------------------
* * * * * * *
Reptiles \2\
* * * * * * *
Fishes
Cardinalfish, Banggai......... Pterapogon Entire species.. Insert Federal NA NA
kauderni. Register
citation and
date when
published as a
final rule].
* * * * * * *
Shark, Harrisson's dogfish.... Centrophorus Entire species.. Insert Federal NA NA
harrissoni. Register
citation and
date when
published as a
final rule].
----------------------------------------------------------------------------------------------------------------
\1\ Species includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement,
see 61 FR 4722, February 7, 1996), and evolutionarily significant units (ESUs) (for a policy statement, see 56
FR 58612, November 20, 1991).
\2\ Jurisdiction for sea turtles by the Department of Commerce, National Oceanic and Atmospheric Administration,
National Marine Fisheries Service, is limited to turtles while in the water.
PART 224--ENDANGERED MARINE AND ANADROMOUS SPECIES
0
3. The authority citation for part 224 continues to read as follows:
Authority: 16 U.S.C. 1531-1543 and 16 U.S.C. 1361 et seq.
0
4. In Sec. 224.101, paragraph (h), amend the table by:
0
A. Revising the table subheading of ``Sea Turtles \2\'' to ``Reptiles
\2\'';
0
B. Adding an entry for the dusky sea snake in alphabetical order under
the new ``Reptiles \2\'' table subheading;
0
C. Adding a ``Corals'' table subheading to follow the ``Molluscs''
table subheading; and
0
D. Adding entries for three species of coral in alphabetical order by
scientific name under the ``Corals'' table subheading to read as
follows:
Sec. 224.101 Enumeration of endangered marine and anadromous species.
* * * * *
(h) The endangered species under the jurisdiction of the Secretary
of Commerce are:
----------------------------------------------------------------------------------------------------------------
Species \1\
-------------------------------------------------------------------- Citation(s) for Critical
Description of listing habitat ESA rules
Common name Scientific name listed entity determination(s)
----------------------------------------------------------------------------------------------------------------
* * * * * * *
Reptiles \2\
Sea snake, dusky.............. Aipysurus fuscus. Entire species.. Insert Federal NA NA
Register
citation and
date when
published as a
final rule].
* * * * * * *
Molluscs
* * * * * * *
Corals
Coral, [no common name]....... Cantharellus Entire species.. Insert Federal NA NA
noumeae. Register
citation and
date when
published as a
final rule].
Coral, [no common name]....... Siderastrea Entire species.. Insert Federal NA NA
glynni. Register
citation and
date when
published as a
final rule].
Coral, [no common name]....... Tubastraea Entire species.. Insert Federal NA NA
floreana. Register
citation and
date when
published as a
final rule].
----------------------------------------------------------------------------------------------------------------
\1\ Species includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement,
see 61 FR 4722, February 7, 1996), and evolutionarily significant units (ESUs) (for a policy statement, see 56
FR 58612, November 20, 1991).
\2\ Jurisdiction for sea turtles by the Department of Commerce, National Oceanic and Atmospheric Administration,
National Marine Fisheries Service, is limited to turtles while in the water.
* * * * *
[FR Doc. 2014-29203 Filed 12-15-14; 8:45 am]
BILLING CODE 3510-22-P