[Federal Register Volume 80, Number 163 (Monday, August 24, 2015)]
[Notices]
[Pages 51235-51247]
From the Federal Register Online via the Government Publishing Office [www.gpo.gov]
[FR Doc No: 2015-20754]
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DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration
[Docket No. 130718637-5699-02]
RIN 0648-XC775
Endangered and Threatened Wildlife and Plants; Notice of 12-Month
Finding on a Petition To List the Orange Clownfish as Threatened or
Endangered Under the Endangered Species Act
AGENCY: National Marine Fisheries Service (NMFS), National Oceanic and
Atmospheric Administration (NOAA), Commerce.
ACTION: Notice of 12-month finding and availability of a status review
report.
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SUMMARY: We, NMFS, announce a 12-month finding and listing
determination on a petition to list the orange clownfish (Amphiprion
percula) as threatened or endangered under the Endangered Species Act
(ESA). We have completed a comprehensive status review under the ESA
for the orange clownfish and we determined that, based on the best
scientific and commercial data available, the orange clownfish does not
warrant listing under the ESA. We conclude that the orange clownfish is
not currently in danger of extinction throughout all or a significant
portion of its range and is not likely to become so within the
foreseeable future.
DATES: The finding announced in this notice was made on August 24,
2015.
ADDRESSES: You can obtain the petition, status review report, 12-month
finding, and the list of references electronically on our NMFS Web site
at: http://www.fpir.noaa.gov/PRD/prd_reef_fish.html.
FOR FURTHER INFORMATION CONTACT: Krista Graham, NMFS, Pacific Islands
Regional Office, (808) 725-5152; or Kimberly Maison, NMFS, Pacific
Islands Regional Office, (808) 725-5143; or Chelsey Young, NMFS, Office
of Protected Resources, (301) 427-8491.
SUPPLEMENTARY INFORMATION:
Background
On September 14, 2012, we received a petition from the Center for
Biological Diversity (Center for Biological Diversity, 2012) to list
eight species of pomacentrid reef fish as threatened or endangered
under the ESA and to designate critical habitat for these species
concurrent with the listing. The species are the orange clownfish
(Amphiprion percula) and seven other damselfishes: The yellowtail
damselfish (Microspathodon chrysurus), Hawaiian dascyllus (Dascyllus
albisella), blue-eyed damselfish (Plectroglyphidodon johnstonianus),
black-axil chromis (Chromis atripectoralis), blue-green damselfish
(Chromis viridis), reticulated damselfish (Dascyllus reticulatus), and
blackbar devil or Dick's damselfish (Plectroglyphidodon dickii). Given
the geographic ranges of these species, we divided our initial response
to the petition between our Pacific Islands Regional Office (PIRO) and
Southeast Regional Office (SERO). PIRO led the response for the seven
Indo-Pacific species. On September 3, 2014, PIRO published a positive
90-day finding (79 FR 52276) for the orange clownfish announcing that
the petition presented substantial scientific or commercial information
indicating the petitioned action of listing the orange clownfish may be
warranted and explained the basis for that finding. We also announced a
negative 90-day finding for the six Indo-Pacific damselfishes: The
Hawaiian dascyllus, blue-eyed damselfish, black-axil chromis, blue-
green damselfish, reticulated damselfish, and blackbar devil or Dick's
damselfish. SERO led the response to the petition to list the
yellowtail damselfish and, on February 18, 2015, announced a negative
90-day finding for that species (80 FR 8619).
In our positive 90-day finding for the orange clownfish, we also
announced the initiation of a status review of the species, as required
by section 4(b)(3)(A) of the ESA, and requested information to inform
the agency's decision on whether the species warranted listing as
endangered or threatened under the ESA.
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 first consider 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 ``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 identifies 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. Based on the scientific information available, we
determined that the orange clownfish (Amphiprion percula) is a
``species'' under the ESA. There is nothing in the scientific
literature indicating that this species should be further divided into
subspecies or DPSs.
Section 3 of the ESA defines an endangered species as ``any species
which is in danger of extinction throughout all or a significant
portion of its range'' and a threatened species as one ``which is
likely to become an endangered species within the foreseeable future
throughout all or a significant portion of its range.'' 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 at risk of extinction, but is likely to become so in the
foreseeable future. In other words, the primary statutory difference
between an endangered and threatened 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 a 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
[[Page 51236]]
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. In determining an appropriate ``foreseeable future''
timeframe for the orange clownfish, we considered the generation length
of the species and the estimated life span of the species. Generation
length, which reflects turnover of breeding individuals and accounts
for non-breeding older individuals, is greater than first age of
breeding but lower than the oldest breeding individual (IUCN 2015)
(i.e., the age at which half of total reproductive output is achieved
by an individual). For the orange clownfish, we estimated this to range
between 6 and 15 years. We concluded that two to three generation
lengths of the species comports with the estimated lifespan of
approximately 30 years for the orange clownfish (Buston and Garcia,
2007). Therefore, we conservatively define the foreseeable future for
the orange clownfish as approximately 30 years from the present.
On July 1, 2014, NMFS and USFWS published a policy to clarify the
interpretation of the phrase ``significant portion of its range'' (SPR)
in the ESA definitions of ``threatened'' and ``endangered'' (the SPR
Policy; 79 FR 37578). Under this policy, the phrase ``significant
portion of its range'' provides an independent basis for listing a
species under the ESA. In other words, a species would qualify for
listing if it is determined to be endangered or threatened throughout
all of its range or if it is determined to be endangered or threatened
throughout a significant portion of its range. The policy consists of
the following four components:
(1) If a species is found to be endangered or threatened in only an
SPR, the entire species is listed as endangered or threatened,
respectively, and the ESA's protections apply across the species'
entire range.
(2) A portion of the range of a species is ``significant'' if the
species is not endangered or threatened throughout its range, and its
contribution to the viability of the species is so important that,
without the members in that portion, the species would be in danger of
extinction or likely to become so in the foreseeable future, throughout
all of its range.
(3) The range of a species is considered to be the general
geographical area within which that species can be found at the time
USFWS or NMFS makes any particular status determination. This range
includes those areas used throughout all or part of the species' life
cycle, even if they are not used regularly (e.g., seasonal habitats).
Lost historical range is relevant to the analysis of the status of the
species, but it cannot constitute an SPR.
(4) If a species is not endangered or threatened throughout all of
its range but is endangered or threatened within an SPR, and the
population in that significant portion is a valid DPS, we will list the
DPS rather than the entire taxonomic species or subspecies.
We considered this policy in evaluating whether to list the orange
clownfish as endangered or threatened under the ESA.
Section 4(a)(1) of the ESA requires us to determine whether any
species is endangered or threatened due to any one 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 assessing extinction risk of this species, we considered 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 (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.
Scientific conclusions about the overall risk of extinction faced
by the orange clownfish under present conditions and in the foreseeable
future are based on our evaluation of the species' demographic risks
and section 4(a)(1) threat factors. Our assessment of overall
extinction risk considered the likelihood and contribution of each
particular factor, synergies among contributing factors, and the
cumulative effects of all demographic risks and threats to the species.
NMFS PIRO staff conducted the status review for the orange
clownfish. In order to complete the status review, we compiled
information on the species' biology, demography, 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. A draft status review
report was then submitted to three independent peer reviewers; comments
and information received from peer reviewers were addressed and
incorporated as appropriate before finalizing the draft report. The
orange clownfish status review report is available on our Web site (see
ADDRESSES section). Below we summarize information from this report and
the status of the species.
Status Review
Species Description
The orange clownfish, A. percula, is a member of the Family
Pomacentridae. Two genera within the Family contain 28 species of
clownfish (also known as anemonefish). The number of recognized
clownfish species has evolved over time due to inconsistent recognition
of natural hybrids and geographic color variants of previously
described species as separate species in the literature (Allen, 1991;
Fautin and Allen, 1992, 1997; Buston and Garcia, 2007; Ollerton et al.,
2007; Allen et al., 2008; Thornhill, 2012; Litsios et al., 2014; and
Tao et al., 2014). All clownfish have a mutualistic relationship with
sea anemones and this relationship has facilitated the adaptive
radiation and accelerated speciation of clownfish species (Litsios et
al., 2012).
Amphiprion percula is known by many common English names. These
names include orange clownfish, clown anemonefish, percula clownfish,
percula anemonefish, orange anemonefish, true percula clownfish,
blackfinned clownfish, eastern
[[Page 51237]]
clownfish, eastern clown anemonefish, and orange-clown anemonefish.
The orange clownfish is bright orange with three thick white
vertical bars. The anterior bar occurs just behind the eye, the middle
bar bisects the fish and has a forward-projecting bulge, and the
posterior bar occurs near the caudal fin. The white bars have a black
border that varies in width. Although this describes the type specimen,
some polymorphism, or occurrence of more than one form or morph, does
occur with diverse geographic regional and local color forms, mostly in
the form of variation in the width of the black margin along the white
bars (Timm et al., 2008; Militz, 2015). While there is no difference in
color pattern between sexes, dimorphic variation, or differentiation
between males and females of the same species, is present in size as
females are larger than males (Fautin and Allen, 1992, 1997; Florida
Museum of Natural History, 2005). Maximum length for this species is
approximately 80 millimeters (mm) (Fautin and Allen, 1992, 1997), but
individuals up to 110 mm in length have been reported (Florida Museum
of Natural History, 2005). Standard length is reported as 46 mm for
females and 36 mm for males (Florida Museum of Natural History, 2005).
However, size alone cannot be used to identify the sex of an individual
because individuals in different groups will vary in maximum and
minimum size. The total length of a fish has been correlated with the
diameter of its host anemone (Fautin, 1992), with larger anemones
hosting larger clownfish.
The orange clownfish very closely resembles the false percula
clownfish (A. ocellaris), and the two are considered sibling species.
There are several morphological differences that may allow an observer,
upon closer examination, to distinguish between the two species. While
the orange clownfish has 9-10 dorsal spines, the false percula
clownfish has 10-11 dorsal spines (Timm et al., 2008), and the anterior
part of the orange clownfish's dorsal fin is shorter than that of the
false percula clownfish. In addition, the orange clownfish has a thick
black margin around its white bars whereas the false percula clownfish
often has a thin or even non-existent black margin, though this is not
always the case. The orange clownfish has been described as more
brilliant in color, and its orange iris gives the appearance of very
small eyes while the iris of false percula clownfish is grayish-orange,
thus giving the appearance of slightly larger eyes (Florida Museum of
Natural History, 2005). Ecologically, both species prefer the same
primary host anemone species (Heteractis magnifica; Stichodactyla
gigantean; S. mertensii) (Fautin and Allen, 1992, 1997), though the
orange clownfish prefers shallower waters than those of false percula
clownfish (Timm et al., 2008).
The orange clownfish and the false percula clownfish have an
allopatric distribution, meaning their distributions do not overlap.
The orange clownfish is found in the Indo-Pacific region of northern
Queensland (Australia) and Melanesia; the false percula is found in the
Andaman and Nicobar Islands in the Andaman Sea (east of India), Indo-
Malayan Archipelago, Philippines, northwestern Australia, and the coast
of Southeast Asia northwards to the Ryukyu Islands in the East China
Sea (Fautin and Allen, 1992, 1997; Timm et al., 2008). Genetically, the
two species appear to have diverged between 1.9 and 5 million years ago
(Nelson et al., 2000; Timm et al., 2008; Litsios et al., 2012).
In the aquarium trade, the false percula clownfish is the most
popular anemonefish and the orange clownfish is the second most popular
(Animal-World, 2015). The two species are often mistaken for one
another and misidentified in the aquarium trade. They are also often
reported as a species complex (i.e., reported as A. ocellaris/percula)
in trade documentation and scientific research due to the difficulty in
visually distinguishing between the two species.
Habitat
The orange clownfish is described as a habitat specialist due to
its symbiotic association primarily with three species of anemone:
Heteractis crispa, H. magnifica, and Stichodactyla gigantea (Fautin and
Allen, 1992, 1997; Elliott and Mariscal, 1997a; Ollerton et al., 2007),
although the species has also been reported as associating with the
anemones S. mertensii (Elliott and Mariscal, 2001) and S. haddoni
(Planes et al., 2009). The distribution of these suitable host anemone
species essentially dictates the distribution of the orange clownfish
within its habitat (Elliott and Mariscal, 2001). Anemone habitat for
the orange clownfish, and thus the range of the orange clownfish, is
spread throughout northern Queensland (Australia), the northern coast
of West Papua (Indonesia), northern Papua New Guinea (including New
Britain), the Solomon Islands, and Vanuatu (Rosenberg and Cruz, 1988;
Fautin and Allen, 1992, 1997; De Brauwer, 2014).
Anemones and their symbiotic anemonefish inhabit coral reefs and
nearby habitats such as lagoons and seagrass beds. Although Fautin and
Allen (1992, 1997) estimate that as many anemone hosts and symbiotic
fish live on sand flats or other substrate surrounding reefs as live on
the reef itself, the symbiotic pairs are thought of as reef dwellers
because most diving and observations occur on reefs. Both symbionts
reside in shallow coastal waters primarily in depths of 1-12 meters (m)
(though the anemones can be found in depths up to 50 m) and water
temperatures ranging from 25-28 [deg]C (77-82 [deg]F) (Fautin and
Allen, 1992, 1997; Randall et al. 1997).
Although anemonefishes have been the subject of considerable
scientific research, less is known about the population dynamics or
biology of the anemones that serve as their hosts. There are over 1,000
anemone species but only 10 of them are known to be associated with
anemonefish. Anemones are able to reproduce both sexually and
asexually, but it is unknown which form of reproduction is more common.
Anemones are likely slow growing and very long lived, living decades to
several centuries (Fautin, 1991; Fautin and Allen, 1992, 1997). To be a
viable host for anemonefish, an anemone must be of a sufficient size to
provide shelter and protection from predators.
Clownfishes, including the orange clownfish, are a unique group of
fishes that can live unharmed among the stinging tentacles of anemones.
A thick mucus layer cloaks the fish from detection and response by
anemone tentacles (Rosenberg and Cruz, 1988; Elliott and Mariscal,
1997a, 1997b). The symbiosis between the orange clownfish and its host
anemones serves as an effective anti-predation measure for both
symbionts. Predators of both anemones and anemonefish are deterred by
the anemone's stinging tentacles and by the presence of territorial
clownfish. In return, anemonefish swim through, and create fresh water
circulation for, the stationary anemone, allowing it to access more
oxygenated water, speed up its metabolism, and grow faster (Szczebak et
al., 2013). Anemonefish also fertilize host anemones with their
ammonia-rich waste (Roopin and Chadwick, 2009; Cleveland et al., 2011),
leading to increases in anemone growth and asexual reproduction
(Holbrook and Schmitt, 2005).
Typically only one species of anemonefish occupies a single anemone
at any given time due to niche differentiation, although this is not
always the case. The orange clownfish is a highly territorial species,
likely due to intense competition for limited resources, with niche
differentiation
[[Page 51238]]
caused by the distribution, abundance, and recruitment patterns of
competing species (Fautin and Allen, 1992, 1997; Elliott and Mariscal,
1997a, 2001; Randall et al., 1997). Once anemonefishes settle into a
host, they are unlikely to migrate between anemones (Mariscal, 1970;
Elliott et al., 1995).
Diet, Feeding, and Growth
Anemonefishes are omnivorous and feed on a variety of prey items
consisting of planktonic algae and zooplankton, such as copepods and
larval tunicates (Fautin and Allen, 1992, 1997). The orange clownfish
also feeds on prey remnants left over from its host anemone's feeding
activity as well as dead tentacles from its host (Fautin and Allen,
1992, 1997; Florida Museum of Natural History, 2005).
An anemone will typically host a female and male breeding pair and
up to four other subordinate, non-breeding and non-related A. percula
males (Buston, 2003a; Buston and Garcia, 2007; Buston et al., 2007).
Individuals rarely stray beyond the periphery of their anemone's
tentacles to feed (Buston, 2003c). A size-based hierarchy develops
within each group; the female is the largest (rank 1), the dominant
male second largest (rank 2), and the non-breeding subordinate males
get progressively smaller as you descend the hierarchy (ranks 3-6)
(Allen, 1991). Subordinates tend to be 80 percent of the size of their
immediate dominant in the hierarchy (Buston, 2003b; Buston and Cant,
2006). Subordinates likely regulate their growth to avoid coming into
conflict with their immediate dominant, and thereby avoid eviction from
the social group (Buston, 2003b; Buston and Wong, 2014). When a fish is
removed from the hierarchical social group structure (due to mortality
or collection), all smaller members grow rapidly, filling in the size
gap, to the point that they are once again 80 percent the size of their
immediate dominant (Fautin and Allen, 1992, 1997; Buston, 2003b).
Reproduction and Development
Spawning for orange clownfish can occur year-round due to
perpetually warm waters within the species' range (Fautin and Allen,
1992, 1997). Spawning is also strongly correlated with the lunar cycle,
with most nesting occurring when the moon is full or nearly so (Fautin
and Allen, 1992, 1997).
Like all anemonefishes, all orange clownfish are born as males
(Fautin and Allen, 1992, 1997). Females develop through protandrous
hermaphroditism, or sex change from male to female. This occurs when
the female and largest member of the group dies (or is otherwise
removed) and the next largest male changes sex to become the dominant
breeding female. The second largest male subsequently becomes the
dominant male (Rosenberg and Cruz, 1988; Fautin and Allen 1992, 1997).
Only the dominant pair contributes to the reproductive output of a
group within an anemone. Non-breeders within the social group do not
have an effect on the reproductive success of mating pairs (Buston,
2004; Buston and Elith, 2011).
Adult male and female orange clownfish form strong monogamous pair-
bonds. Once eggs are laid, the male follows closely behind and
fertilizes them externally. Clutch sizes vary widely between 100 to
over 1000 eggs laid (Fautin and Allen, 1992, 1997; Dhaneesh et al.,
2009), with an average of 324 eggs 153 (mean
one standard deviation) recorded in Madang Lagoon, Papua New Guinea
(Buston and Elith, 2011), depending on fish size and previous
experience. Larger and more experienced mating pairs will produce more
eggs per clutch (Fautin and Allen, 1992, 1997; Buston and Elith, 2011;
Animal-World, 2015), and can produce up to three clutches per lunar
cycle (Gordon and Hecht, 2002; Buston and Elith, 2011).
After egg deposition and fertilization have finished, a 6-8 day
incubation period begins, with developmental rate varying with
temperature and oxygen content of the water (Dhaneesh et al., 2009).
Average hatch success recorded in Madang Lagoon, Papua New Guinea, was
estimated at 87 percent (Buston and Elith, 2011). Upon hatching, larvae
enter a pelagic phase and are likely engaged in active swimming and
orientation, and also transported by ocean currents (Fautin and Allen,
1992, 1997; Leis et al., 2011). The larval stage of the species ends
when the larval anemonefish settles into a host anemone approximately
8-12 days after hatching (Fautin and Allen, 1992, 1997; Almany et al.,
2007; Buston et al., 2007).
Anemonefish search for and settle into a suitable host anemone
using a variety of cues. Embryos and newly hatched juveniles may learn
cues from the host anemone where they hatched and respond to these
imprinted cues when searching for suitable settlement locations (Fautin
and Allen, 1992, 1997; Arvedlund et al., 2000; Dixson et al., 2014;
Miyagawa-Kohshima, 2014; Paris et al., 2013). Dixson et al. (2008,
2014) and Munday et al. (2009a) found that orange clownfish are
responsive to olfactory cues such as leaf litter and tropical trees, a
means of locating island reef habitats, when searching for a settlement
site. Innate recognition is also used and refers to the ability of
anemonefish to locate a suitable host without prior experience (Fautin
and Allen, 1992, 1997; Miyagawa-Kohshima, 2014). Studies indicate that
imprinting on anemone olfactory cues complements innate recognition,
leading to rigid species-specific host recognition (Miyagawa-Kohshima,
2014).
Fish acclimation to a host anemone lasts anywhere from a few
minutes to a few hours (Fautin and Allen, 1992, 1997; Arvedlund et al.,
2000) as a protective mucus coating develops on the anemonefish as a
result of interaction with the host anemone tentacles (Davenport and
Norris, 1958; Elliott and Mariscal, 1997a). Once acclimated, the mucus
protection may disappear upon extended separation between host and
fish. Continued contact with tentacles appears to reactivate the mucus
coat (Arvedlund et al., 2000). Coloration of anemonefish usually also
begins during this anemone acclimation process (Elliott and Mariscal,
2001). Upon settlement, the entire metamorphosis from larva to juvenile
takes about a day (Fautin and Allen, 1992, 1997).
Longevity and Resilience
Buston and Garcia (2007) studied a wild population of orange
clownfish in Papua New Guinea and their results suggest that females
can live up to 30 years in the wild. Although this life expectancy
estimate has not been empirically proven through otolith examination,
it is notably two times greater than the longevity estimated for any
other coral reef damselfish and six times greater than the longevity
expected for a fish that size (Buston and Garcia, 2007). Their results
are consistent with the idea that organisms subjected to low levels of
extrinsic mortality, like anemonefish, experience delayed senescence
and increased longevity (Buston and Garcia, 2007).
Using a methodology designed to determine resilience to fishing
impacts, Fishbase.org rates the orange clownfish as highly resilient,
with an estimated minimum population doubling time of less than 15
months. Another analysis, using the Cheung et al. (2005) ``fuzzy
logic'' method for estimating fish vulnerability to fishing pressure,
assigned the species a low vulnerability score, with a level of 23 out
of 100 (Fishbase.org, 2015).
[[Page 51239]]
Population Distribution, Abundance, and Structure
Clownfish first appeared and diversified in the Indo-Australian
Archipelago (Litsios et al., 2014). As previously mentioned, the orange
clownfish is native to the Indo-Pacific region and range countries
include northern Queensland (Australia), northern coast of West Papua
(Indonesia), northern Papua New Guinea (including New Britain), the
Solomon Islands, and Vanuatu (Rosenberg and Cruz, 1988; Fautin and
Allen, 1992, 1997; De Brauwer, 2014).
The distribution of suitable host anemone species dictates the
distribution of orange clownfish within its habitat (Elliott and
Mariscal, 2001). The anemones Heteractis crispa, H. magnifica, and S.
gigantea range throughout and beyond the orange clownfish's geographic
extent. Stichodactyla haddoni occurs in Australia and Papua New Guinea,
but has not yet officially been recorded in Vanuatu or the Solomon
Islands, and S. mertensii officially has been recorded only from
Australia within the orange clownfish's range (Fautin and Allen, 1992,
1997; Fautin, 2013). However, two recent observations extended the
known distribution of S. haddoni, both northward and southward,
indicating they have the ability to expand in range and facilitate the
expanded occurrence of commensal species (Hobbs et al., 2014; Scott et
al., 2014). Anecdotally, there are photo images and video footage of S.
haddoni and S. mertensii in the Solomon Islands, Vanuatu, and Papua New
Guinea (e.g., Shutterstock, National Geographic, and Getty Images).
Species experts, however, have not officially confirmed these reports.
Although geographically widespread, anemone species differ in their
preferred habitat (e.g., reef zonation, substrate, depth (Fautin,
1981)). Hattori (2006) found that H. crispa individuals were larger
along reef edges and smaller in shallow inner reef flats. The larger
anemones on reef edges experienced higher growth, probably because
deeper (up to 4 m) reef edges provide more prey and lower levels of
physiological stress. The author speculates that habitat and depth
ideal for high anemone growth will vary by study site and occur at
depths where there is a balance between available sunlight to allow for
photosynthesis and low physiological stress, both of which are
dependent on site-specific environmental conditions.
It is difficult to generalize the likely distribution, abundance,
and trends of anemone hosts throughout A. percula's range; these
parameters are likely highly variable across the species' range. In an
assessment done throughout the Great Barrier Reef, Australia, anemones,
including those that host the orange clownfish, were quantified as
``common'' (Roelofs and Silcock, 2008). On the other hand, Jones et al.
(2008) and De Brauwer et al. (in prep) note that anemones occur in
relatively low densities throughout the Indo-Pacific. Because it is
difficult to generalize the likely distribution, abundance, and trends
of anemones, it is therefore difficult to generalize these same
parameters for A. percula in coral reef environments throughout its
range; it is likely to be variable and dependent on local environmental
conditions.
We found no information on historical abundance or recent
population trends for the orange clownfish throughout all or part of
its range. We also found no estimate of the current species abundance.
With no existing estimate of global abundance for the orange clownfish,
we estimated, based on the best available information, a total of 13-18
million individuals for the species throughout its range. This estimate
is derived from De Brauwer (2014) who determined an average density for
the orange clownfish within its range from 658 surveys across 205 sites
throughout the species' range (northern Papua New Guinea, Solomon
Islands, Vanuatu, and northern Australia). He calculated the global
estimated mean density at 0.09 fish per 250 m\2\, or 360 fish per
km\2\. In order to extrapolate this average density to estimate
abundance, we used two different estimates of coral reef area within
the species' range. De Brauwer (2014) estimated 36,000 km\2\ of coral
reef area within the species' range based on Fautin and Allen (1992,
1997) and Spalding et al. (2001). We also used newer coral reef mapping
data from Burke et al. (2011) resulting in an estimate of approximately
50,000 km\2\ of coral reef area within the orange clownfish's range. We
used both values to determine a range of estimated abundance (13-18
million) to reflect uncertainty. It is important to note that this may
be an underestimate because it is based on coral reef area, which
likely does not account for most of the non-reef area where the species
occurs throughout its range.
As for spatial structure and connectivity, based on the best
available information, we conclude that the species is likely to have
highly variable small-scale connectivity among and between meta-
populations, but unknown large-scale genetic structure across its
entire range. In the absence of a broad-scale phylogeographic study for
A. percula, we are left with small-scale meta-population connectivity
studies as the best available information. Results from studies in
Kimbe Bay, Papua New Guinea, an area known for its high diversity of
anemones and anemonefish, indicate that A. percula larvae have the
ability to disperse at least up to 35 km away from natal areas (Planes
et al., 2009). In addition, there is evidence that rates of self-
recruitment are likely to be linked with not only pelagic larval
duration, but also geographical isolation (Jones et al., 2009; Pinsky
et al., 2012). Because of the size and distribution of A. percula's
range, there are likely areas of higher and lower connectivity
throughout, linked with the variability in geographic isolation across
locations, creating significant spatial structure. This is, however,
speculative because no large-scale connectivity study has been
conducted for this species.
Summary of Factors Affecting the Orange Clownfish
Available information regarding current, historical, and potential
future threats to the orange clownfish was thoroughly reviewed in the
status review report for the species (Maison and Graham, 2015). We
summarize information regarding the 12 identified threats below
according to the five factors specified in section 4(a)(1) of the ESA.
See Maison and Graham (2015) for additional discussion of all ESA
section 4(a)(1) threat categories.
Present or Threatened Destruction, Modification, or Curtailment of Its
Habitat or Range
Among the habitat threats affecting the orange clownfish, we
analyzed anemone bleaching, anemone collection, and sedimentation and
nutrient enrichment effects. We found the threats of anemone bleaching
and anemone collection each to have a low likelihood of contributing
significantly to extinction risk for the species now or in the
foreseeable future. We found the threat of sedimentation and nutrient
enrichment to have a low-to-medium likelihood, meaning it is possible
but not necessarily probable, that this threat contributes or will
contribute significantly to extinction risk for the species.
Evidence, while limited, indicates that thermally-induced bleaching
can have negative effects on orange clownfish host anemones, which may
lead to localized effects of unknown magnitude on the fish itself.
Evidence thus far indicates high variability in the response of both
anemones and anemonefish to localized bleaching events. Susceptibility
to thermal stress
[[Page 51240]]
varies between different species of the same taxon and is often
variable within individual species; as a result of habitat
heterogeneity across a species' range, individuals of the same species
may develop in very different environmental conditions. Hobbs et al.
(2013) compiled datasets that were collected between 2005 and 2012
across 276 sites at 19 locations in the Pacific Ocean, Indian Ocean,
and Red Sea to examine taxonomic, spatial, and temporal patterns of
anemone bleaching. Their results confirm that bleaching has been
observed in 7 of the 10 anemone species that host anemonefish
(including 4 of the 5 orange clownfish host species), with anecdotal
reports of bleaching in the remaining 3 host anemone species. In
addition, they report anemone bleaching at 10 of 19 survey locations
that are geographically widespread. Importantly, the authors report
considerable spatial and inter-specific variation in bleaching
susceptibility across multiple major bleaching events (Hobbs et al.,
2013). Over the entire timeframe and across all study areas, 3.5
percent of all anemones observed were bleached, although during major
bleaching events, the percentage at a given study area ranged from 19-
100 percent. At sites within the same study area, bleaching ranged
between as much as 0 and 94 percent during a single bleaching event. To
further highlight the variability and uncertainty associated with
anemone bleaching susceptibility, Hobbs et al. (2013) report opposite
patterns of susceptibility for the same two species at the same site
during two different bleaching events. Additionally, the study reports
decreased bleaching with increased depth in most of the major bleaching
events, indicating that depth, in some cases as shallow as 7 m, offers
a refuge from bleaching (Hobbs et al., 2013). Some anemone species have
even been reported from mesophotic depths, including one A. percula
host species (H. crispa) (Bridge et al., 2012). These depths likely
serve as refugia from thermal stress. Although the capacity for
acclimation or adaptation in anemones is unknown, evidence from one
site indicated that prior bleaching history might influence subsequent
likelihood of an anemone bleaching, as previously bleached individuals
were less likely to bleach a second time (Hobbs et al., 2013). It is
also of note that, similar to corals, bleaching does not automatically
lead to mortality for anemones. Hobbs et al. (2013) report variable
consequences as a result of bleaching between and among species and
locations in their assessment of bleaching for all anemone species that
host anemonefish (including those that host orange clownfish); some
species decreased in abundance and/or size after bleaching events,
while others showed no effect and recovered fully.
When considering the effect of anemone bleaching into the
foreseeable future, we evaluated the best available information on
future projections of warming-induced bleaching events, but also
considered the existing information on the effects of previous
bleaching events on anemones. Evidence suggests that bleaching events
will continue to occur and become more severe and more frequent over
the next few decades (van Hooidonk, 2013). However, newer multivariate
modeling approaches indicate that traditional temperature threshold
models may not give an accurate picture of the likely outcomes of
climate change for coral reefs, and effects and responses will be
highly nuanced and heterogeneous across space and time (McClanahan et
al., 2015). Although observed anemone bleaching has thus far been
highly variable during localized events, the overall effect of
bleaching events on anemones globally (i.e., overall proportion of
observed anemones that have shown ill effects) has been of low
magnitude at sites across their ranges, as only 3.5 percent of the
nearly 14,000 observed anemones were recorded as bleached across 19
study sites and multiple major bleaching events (Hobbs et al., 2013).
In summary, there are a number of factors that, in combination,
indicate that the orange clownfish is likely resilient to bleaching
effects that may affect their hosts both now and in the foreseeable
future. These factors include the low overall effect of anemone
bleaching thus far; the high amount of variability in anemone
susceptibility; the existence of depth refugia for anemones; the
evidence of potential acclimation in some species; and the fact that
the orange clownfish has been observed in the wild to associate with at
least five different species of anemone, all of which have shown
different levels of susceptibility to bleaching in different locations
and over time. As such, we conclude that the threat of habitat loss due
to anemone bleaching has a low likelihood of contributing significantly
to extinction risk for the orange clownfish now or in the foreseeable
future.
With regard to anemone collection, there is little information
available on this threat to the orange clownfish globally. Thus far,
there has been limited successful aquaculture of anemones for aquaria.
Moe (2003) reports the results from a survey of hobbyists, scientists,
and commercial breeders indicating several species have been
successfully propagated (typically via asexual reproduction), but
anemones typically thwart both scientific and hobbyist attempts at
captive culture, especially on a large scale. This is primarily due to
their slow growth and infrequent reproduction. While asexual
propagation has been successful in some cases, no study has yet
addressed the optimization of this practice (e.g., determining the
minimum size at which an anemone can be successfully propagated, the
best attachment technique, etc.) (Olivotto et al. 2011). As such, the
vast majority of anemone specimens in the trade are currently from wild
collection. In the Queensland marine aquarium fishery, Roelofs and
Silcock (2008) found that all anemone species had low vulnerability due
to collection. While there was no information on anemone collection
available from the Solomon Islands, Vanuatu, or Papua New Guinea
(likely because these countries tend to focus on exporting fish vs.
invertebrates), our assessment reveals that collection and export of
aquarium reef species, including anemones, in these three countries is
relatively small-scale at just a few sites scattered throughout large
archipelagos. The industry appears limited by freight costs and other
financial burdens (Kinch, 2008). As such, it seems unlikely that
collection would expand to other areas within the species' range. There
is no information to indicate that demand for wild harvested anemones
will increase over the next few decades within the range of the orange
clownfish. Several studies have provided valuable biological data on
the reproductive biology (Scott and Harrison 2007a, 2009), embryonic
and larval development (Scott and Harrison 2007b), and settlement and
juvenile grow-out (Scott and Harrison 2008). Although speculative,
scientists and hobbyists are likely to use this information to continue
to engage in attempts to propagate anemones in captivity, which may
lead to lower demand for wild capture if successful. While little
information is available on the threat of anemone collection to A.
percula globally, the aquarium trade collection information from
countries within the species' range indicates that fisheries in general
are relatively small scale, and tend to focus on fish rather than
invertebrates for export. Because there is some uncertainty and a lack
of specific information associated with this threat to the orange
clownfish, we conclude that the threat of habitat loss from anemone
collection poses a low (instead of very low) likelihood of
[[Page 51241]]
contributing significantly to the extinction risk for the orange
clownfish, both now and in the foreseeable future.
Regarding the threat of sedimentation and nutrient enrichment to A.
percula's habitat, organisms in coral reef ecosystems, including
clownfish, are likely to experience continuing effects from
anthropogenic sources of this threat at some level as economies
continue to grow. Indeed, exposure of host anemones is likely to be
variable across the range of A. percula, with effects being more acute
in areas of high coastal development. There is very little information
available regarding the susceptibility and exposure of anemones to
sedimentation and nutrients. In the absence of this information, we
consider it reasonable to assume that the susceptibility of corals as a
direct result of their association with symbiotic algae (described
above) is an indicator of the potential susceptibility of anemones,
since they share a similar association with microscopic algal symbionts
and because anemones are in the same phylum (Cnidaria) as corals and
thus are biologically related. While information for anemones is
sparse, we know that some coral species can tolerate complete burial in
sediment for several days; however, those that are unsuccessful at
removing sediment may be smothered, resulting in mortality (Nugues and
Roberts, 2003). Sediment can also induce sub-lethal effects in corals,
such as reductions in tissue thickness, polyp swelling, zooxanthellae
loss, and excess mucus production (Rogers, 1990). In addition,
suspended sediment can reduce the amount of light in the water column,
making less energy available for photosynthesis (of symbiotic
zooxanthellae) and growth. Again for corals, sedimentation and nutrient
enrichment can have interactive effects with other stressors including
disease and climate factors such as bleaching susceptibility and
reduced calcification (Ateweberhan et al., 2013; Suggett et al., 2013).
In addition to the potential effects from sedimentation and
nutrient enrichment to host anemones, there could be potential effects
to A. percula. Wenger et al. (2014) found in a controlled experiment
that suspended sediment increased pelagic larval duration for A.
percula. A longer pelagic larval duration may reduce the number of
larvae that make it to the settlement stage because of the high rate of
mortality in the pelagic larval phase. Conversely, in this study longer
pelagic larval durations led to larvae that were larger with better
body condition, traits that may confer advantages during the first few
days of settlement when mortality is still high for those that do
recruit to settlement habitat. As such, the overall effect of increased
sedimentation at the population level is hard to predict.
Land-based sources of pollution are of primary concern for
nearshore marine habitats in areas where human populations live in
coastal areas and engage in any or all of the following: Intensive
farming and aquaculture, urbanization and industrialization, greater
shipping traffic and fishing effort, and deforestation and nearshore
development, all of which are growing in Southeast Asia (Todd et al.,
2010; Schneider et al., 2015) and the Indo-Pacific (Edinger et al.,
1998; Edinger et al., 2000). The range of A. percula is largely outside
of areas that are experiencing the most rapid growth and
industrialization, such as Indonesia and the Philippines. Throughout
the range of A. percula, there are thousands of islands, many of which
are uninhabited or have small, sparse human populations leading
traditional lifestyles. These remote locations are unlikely to suffer
from much exposure to increased sedimentation or nutrients. However,
there is evidence that some of these remote and otherwise pristine
areas in countries like Papua New Guinea and the Solomon Islands are
targeted for intense or illegal logging and mining operations which may
be causing degradation of the nearshore environment, even in remote and
uninhabited areas (Seed, 1986; Kabutaulaka, 2005).
Efforts to specifically examine the direct and indirect effects of
nutrients and sedimentation to the orange clownfish and its habitat
throughout its range are lacking. Land-based sources of pollution on
reefs act at primarily local and sometimes regional levels, with direct
linkages to human population and land-use within adjacent areas. Orange
clownfish occur mostly in shallow reef areas and rarely migrate between
anemone habitats as adults; these are traits that may make this species
more susceptible to land-based sources of pollution in populated areas
than other, more migratory or deeper-ranging reef fish. To account for
the uncertainty associated with the magnitude of this threat, and
consider the species' traits that may increase its susceptibility and
exposure, we conservatively conclude that there is a low-to-medium
likelihood that the threat of sedimentation and nutrient enrichment is
currently or will significantly contribute to extinction risk for the
orange clownfish. Spanning the low and medium categories indicates that
the threat is likely to affect the species negatively and may have
visible consequences at the species level either now and/or in the
future, but we do not have enough confidence in the available
information to determine the negative effect is of a sufficient
magnitude to significantly increase extinction risk.
Overutilization for Commercial, Recreational, Scientific or Educational
Purposes
For the ESA factor of overutilization for commercial, recreational,
scientific or educational purposes, we analyzed the threat of
collection for the aquarium trade. We conclude that this threat has a
low likelihood of having a significant effect on the species' risk of
extinction now or in the foreseeable future.
It is estimated that 1.5-2 million people worldwide keep marine
aquaria, including 600,000 households in the United States (U.S.) alone
(Wabnitz et al., 2003). Estimates place the value of the marine
aquarium trade at approximately U.S. $200-330 million per year (Wabnitz
et al., 2003). The largest importers of coral reef fish, corals, and
invertebrates for display in aquaria are the U.S., followed by the
European Union, Japan, and China. The U.S. accounted for an average of
61 percent of global imports of marine aquarium species from 2000-2010
(Wood et al., 2012). A tremendous diversity and volume of species are
involved in the marine aquarium trade (Rhyne et al., 2012). It is
estimated that every year, approximately 14-30 million fish, 1.5
million live stony corals, and 9-10 million other invertebrates are
removed from coral reef ecosystems across the world (Wood, 2001a,b;
Wabnitz et al., 2003; Tsounis et al., 2010) although Rhyne et al.
(2012) assert that the volume of marine fish has been overestimated.
These include the trade in at least 1,802 species of fish, more than
140 species of corals, and more than 500 species of non-coral
invertebrates (Wabnitz et al., 2003; Rhyne et al., 2012). Clownfish,
specifically A. ocellaris and A. percula, are among the top five most
imported and exported species of marine aquarium fish in the aquarium
trade (Wabnitz et al., 2003; Rhyne et al., 2012).
Rhyne et al. (2012) reported a total of 400,000 individuals of the
species complex A. ocellaris/percula were imported into the U.S. in
2005. Of note is that data for the two species were combined and
reported for the species complex in this report due to common
misidentification leading to the inability to separate them out in the
import
[[Page 51242]]
records. More recently, the author provided NMFS with updated estimates
based on newer data from 2008-2011, which indicate the number of A.
percula alone imported into the U.S. was less than 50,000 per year
(Szczebak and Rhyne, unpublished). Notably, this estimate does not
distinguish between wild-caught and captively-propagated individuals
from foreign sources. The Philippines and Indonesia account for 80
percent of A. percula imports into the United States according to the
new species-specific information from Szczebak and Rhyne (unpublished
data); however, these countries are outside the geographic range of A.
percula, indicating that 80 percent or more of the imported individuals
were likely propagated in captivity and not collected from the wild, or
misidentified. Similarly, according to Tissot et al. (2010), the U.S.
imports 50-70 percent of aquarium reef fish in the global trade. If we
extrapolate the U.S. import estimate to infer global wild harvest for
the aquarium trade, the number of globally traded wild A. percula in
2011 was likely closer to approximately 70,000-100,000 individuals,
with as much as 80 percent potentially originating from aquaculture
operations and not actually harvested from the wild (or misidentified
if U.S. imports are considered representative of the global trade). If
we conservatively assume that 100,000 orange clownfish are harvested
from the wild annually (likely a vast over-estimate), this represents
0.0076 percent of our conservatively estimated wild global population
size of 13-18 million individual A. percula.
Orange clownfish are currently collected at varying levels in three
out of the four countries in which the species occurs. Papua New Guinea
had a fishery for this species, but does not currently export for the
aquarium trade. There is a small local aquarium industry, but
collection for this purpose is likely minimal (Colette Wabnitz, pers.
comm. 2015). Collection from the wild appears relatively limited in
Vanuatu, the Solomon Islands, and Australia, according to U.S. import
information. While A. percula are targeted in these aquarium fisheries,
they are not the most sought after species in most cases.
Additionally, anemonefish were among the first coral reef fish
raised in captivity throughout their entire life cycle and now
represent one of the most well-known and well-developed captive
breeding programs for marine fish (Dawes, 2003). While quantitative
information is not currently available to estimate the number of A.
percula that are propagated in captivity, clownfish are widely
described among the industry as an easily cultured aquarium species. A
survey of marine aquarium hobbyists in 2003 revealed that only 16
percent of respondents had no concern over whether they purchased wild
vs. cultured organisms; the majority of respondents indicated a
preference for purchasing captive bred specimens (Moe, 2003). A more
recent study reports that 76 percent of respondents to the same
question indicated they would preferentially purchase cultured animals
and an additional 21 percent said it would depend on the price
difference (Murray and Watson, 2014).
Considering the estimated proportion of the population harvested
annually, the principles of fisheries management and population growth,
the ease and popularity of captive propagation of the species, and the
apparent consumer preference for captively-reared fish for home
aquaria, we have determined that overutilization due to collection for
the aquarium trade has a low likelihood of contributing significantly
to the extinction risk of the orange clownfish now or in the
foreseeable future.
Disease or Predation
We analyzed the threat of both disease and predation to the orange
clownfish. We conclude that disease has a very low likelihood of having
a significant effect on the species' risk of extinction now or in the
foreseeable future. We conclude that predation has a low likelihood of
having a significant effect on the species' risk of extinction now or
in the foreseeable future.
The available information on disease in A. percula indicates that
the spread of some diseases is of concern in captive culture facilities
(Ganeshamurthy et al., 2014; Siva et al., 2014); however, there is no
information available indicating that disease may be a concern in wild
populations. Because this is a well-studied species in at least parts
of its range, we find this compelling evidence that disease does not
currently pose a significant threat to the species. We therefore
conclude that the threat of disease has a very low likelihood of having
a significant effect on the species' risk of extinction now or in the
foreseeable future.
Orange clownfish, like many reef fish species, are most susceptible
to natural predation during the egg, pelagic larvae, and settlement
life stages. Natural mortality for juveniles and adults is low, ranging
from 2 percent (Elliott and Mariscal, 2001) to ~7 percent for ranks 1-3
(dominant breeding pair and first subordinate male) and ~30 percent for
ranks 4-6 (subsequent subordinate males) (Buston, 2003a). Shelter and
protection from predators is one of the primary benefits conferred to
post-settlement juvenile and adult orange clownfish by their symbiotic
relationship with host anemones. We found no information to indicate
elevated predation levels due to invasive species or other outside
influences in any part of the species' range is a cause for concern.
Moreover, we did not find any information to indicate that natural
predation rates for the species are of a magnitude that would cause
concern for their extinction risk now or in the foreseeable future.
There is some scientific evidence that indicates future levels of
ocean acidification have the potential to negatively affect predator
avoidance behavior for orange clownfish. However, it is unclear if or
how those effects may manifest themselves in the wild over the expected
timeframes of increasing acidification, and there is evidence that
trans-generational acclimation will play a role in allowing populations
to adapt over time. While the future effects of acidification are still
unclear, we allow for the potential for effects to predator avoidance
behavior from ocean acidification by concluding that the likelihood of
predation significantly contributing to the extinction risk for the
orange clownfish now or in the foreseeable future is low (instead of
very low).
Inadequacy of Existing Regulatory Mechanisms
Because the only threat that has a low-to-medium likelihood (higher
relative to all other threats which are low or very low) of
significantly contributing to extinction risk for the orange clownfish
is sedimentation and nutrient enrichment, we need only address the
inadequacy of regulatory mechanisms that could alleviate this threat. A
discussion of the adequacy of regulatory mechanisms for all other
threats can be found in the Status Review Report for the Orange
Clownfish (Maison and Graham 2015).
Based on the reasoning provided below, we conclude that the
inadequacy of regulatory mechanisms addressing sedimentation and
nutrient enrichment also has a low-to-medium likelihood of contributing
to extinction risk, meaning that it is possible but not necessarily
probable, that it contributes or will contribute significantly to
extinction risk for the species. Spanning the low and medium categories
indicates that the threat is likely to affect the species negatively
and may have visible consequences at the species level either now and/
or in the future, but we do not have enough confidence in the available
[[Page 51243]]
information to determine the negative effect is of a sufficient
magnitude to significantly increase extinction risk.
Regulatory mechanisms for the four countries within A. percula's
range that address land based-sources of pollution like sedimentation
and nutrient enrichment are described in greater detail in the NMFS
coral management report (NMFS, 2012b), but we summarize them here. In
Papua New Guinea, most legislation does not specifically refer to
marine systems, which has generated some uncertainty as to how it
should be applied to coral reefs. Also, laws relevant to different
sectors (e.g., fisheries, mining, environmental protection) are not
fully integrated, which has led to confusion over which laws have
priority, who is responsible for management, and the rights of the
various interest groups. In the Solomon Islands, the Fisheries Act of
1998 states that marine biodiversity, coastal and aquatic environments
of the Solomon Islands shall be protected and managed in a sustainable
manner and calls for the application of the precautionary approach to
the conservation, management, and exploitation of fisheries resources
in order to protect fisheries resources and preserve the marine
environment (Aqorau, 2005). In Vanuatu, each cultural group has its own
traditional approaches to management, which may include the
establishment of MPAs, initiating taboo sites, or periodic closures.
These traditional management schemes have been supplemented by various
legislative initiatives, including the Foreshore Development Act, which
regulates coastal development (Naviti and Aston, 2000). In Australia,
A. percula occurs mostly, if not entirely, within the Great Barrier
Reef Marine Park. In addition to the park, the Australian government
has developed a National Cooperative Approach to Integrated Coastal
Zone Management (Natural Resource Management Ministerial Council,
2006). In response to recent reports showing declining water quality
within the marine park, the State of Queensland recently developed and
published a Reef Water Quality Protection Plan, outlining actions to
secure the health and resilience of the Great Barrier Reef and adjacent
catchments (State of Queensland, 2013).
Under the discussion of ``Present or Threatened Destruction,
Modification, or Curtailment of its Habitat or Range'' above, we
evaluated the threat of sedimentation and nutrient enrichment on A.
percula and determined that it has a low-to-medium likelihood of
significantly contributing to extinction risk for the species now and
in the foreseeable future. While some regulations exist to address
land-based sources of pollution throughout A. percula's range, overall,
there is little information available on the enforcement or
effectiveness of these regulations. As such, it is difficult to
determine the overall likelihood of the inadequacy of regulatory
mechanisms contributing significantly to the extinction risk for this
species. In analyzing whether regulatory mechanisms addressing this
threat are adequate, we conclude, from what little information we could
find, that although regulations do exist, there are varying levels of
efficacy and enforcement, and this is an ongoing threat that is likely
to increase as economies within the species' range continue to grow.
Marine protected areas are often categorized as conservation
efforts but because they are almost always regulatory in nature
(establishment and enforcement via regulations), in the context of an
ESA listing determination we evaluate them here in the ``Inadequacy of
Existing Regulatory Mechanisms'' section. Although we cannot determine
the overall benefit to the species from the network of protected areas
throughout its entire range, the existence and enforcement of a large
number of MPAs throughout the species' range is likely to confer at
least some benefit and is unlikely to contribute significantly to the
extinction risk for the orange clownfish now or in the foreseeable
future. There is a significant number of (MPAs) of varying degrees of
size, management, and success that exist throughout A. percula's range,
including at least 22 MPAs in Papua New Guinea, MPAs in all 9 provinces
of the Solomon Islands, and over 55 MPAs in Vanuatu, and nearly all of
A. percula's range in Australia is found within the Great Barrier Reef
Marine National Park. While there are relatively little empirical data
on the effectiveness of these particular MPAs other than for Australia,
the general consensus is that these MPAs do provide some conservation
benefits for marine species (Day, 2002; McClanahan et al., 2006; McCook
et al., 2010). In Vanuatu, Hickey and Johannes (2002) report success of
locally managed MPAs due to a variety of reasons, including
enforcement. The authors report that there is an increasing use of
state police to informally support decisions made by the village
chiefs. Individuals who break these village taboos, including taboos
relating to marine resource management activities, may be turned over
to the police. More specifically regarding orange clownfish, findings
suggest that the MPA network in Kimbe Bay, Papua New Guinea, might
function to sustain resident orange clownfish populations both by local
replenishment and through larval dispersal from other reserves (Almany
et al., 2007; Green et al., 2009; Planes et al., 2009; Berumen et al.,
2012).
Other Natural or Manmade Factors Affecting Continued Existence
Among the other natural or human factors affecting the orange
clownfish, we analyzed the potential future physiological and
behavioral effects of ocean acidification and ocean warming. The orange
clownfish, along with several other pomacentrid species, has been the
subject of several laboratory-based studies on both ocean acidification
and ocean warming. The field of study is relatively new, but we
conclude that the threats of physiological or behavioral effects from
ocean acidification and ocean warming each have a low likelihood of
having a significant effect on the species' risk of extinction now or
in the foreseeable future.
Research thus far has focused on the effects of acidification on
two aspects of physiology for A. percula: (1) Growth and development,
and (2) sensory capabilities that affect behavior. In one study,
increased acidification at levels expected to occur circa 2100 had no
detectable effect on embryonic duration, egg survival, or size at
hatching and, in fact, increased larval growth rate in A. percula
(Munday et al., 2009a). Similarly, there was no effect on otolith size,
shape, symmetry, or elemental chemistry when A. percula larvae were
reared at CO2 levels predicted by the year 2100 (Munday et
al., 2011b).
When it comes to behavioral impairment, laboratory research has
shown more consequential results regarding the potential effects of
future ocean acidification. An elevated CO2 environment can
affect auditory sensory capabilities for juvenile A. percula, even in
the absence of effects on otolith growth. This indicates other possible
mechanisms for this interference, such as deterioration of neural
transmitters or compromised processing of sensory information (Simpson
et al., 2011). Auditory sensory capabilities guide larval fish during
settlement as nocturnal reef sounds promote settlement and daytime
predator-rich noises discourage settlement (Simpson et al., 2011).
Increased CO2 levels may affect olfactory cues used by
larval clownfish
[[Page 51244]]
to identify anemones and avoid predators. Larval clownfish use
olfactory cues, such as odors from anemones, to locate suitable reef
habitat for settlement (Munday et al., 2009b). Larval A. percula reared
at CO2 levels comparable to those predicted by the end of
this century showed no observable response to olfactory cues of
different habitat types, whereas those reared in the control
environment showed a strong preference for anemone olfactory cues over
other habitat olfactory cues (Munday et al., 2009b). Newly hatched A.
percula larvae also innately detect predators using olfactory cues, and
they retain this ability through settlement (Dixson et al., 2010). When
tested for behavioral responses to olfactory cues from predators, A.
percula larvae raised in both the control environment (390 parts per
million (ppm) CO2) and the lower of the two intermediate
environments tested (550 ppm CO2) showed strong avoidance of
predator cues. However, larvae reared at 700 ppm CO2 showed
variation in their responses, with half showing avoidance of predator
cues and the other half showing preference for predator cues (Munday et
al., 2010). In this same study, larvae reared at 850 ppm showed strong
preference for predator cues, indicating that 700 ppm may be a
threshold at which adaptation is possible or natural selection will
take effect because of the mixed responses to olfactory cues (Munday et
al., 2010). Additionally, Dixson et al. (2010) report that
CO2 exposure at the egg stage does not appear to affect
olfactory sensory capabilities of hatched larvae, but these
capabilities are affected when settlement stage larvae are exposed to
elevated CO2.
The results discussed above indicate that ocean acidification
associated with climate change has the potential to affect behavioral
responses of A. percula to certain cues during critical life stages.
However, if or how these effects will manifest themselves at the
population level in the natural environment requires an understanding
of additional factors. All of the aforementioned authors acknowledge
that the potential for acclimation or adaptation was not factored into
their studies because it is generally unknown or hard to predict.
Murray et al. (2014) assert that there is mounting evidence of an
important but understudied link between parent and offspring
generations, known as parental conditioning or trans-generational
plasticity, which may comprise a short-term adaptation mechanism to
environmental acidification. This type of plasticity describes the
ability of the parental environment prior to fertilization to influence
offspring reaction norms without requiring changes in DNA sequence
(Salinas and Munch, 2012). Trans-generational plasticity in
CO2 resistance as a potential adaptation for coping with
highly variable aquatic CO2 environments may be common
(Salinas and Munch, 2012; Dupont et al., 2013). One recent study found
that the effects associated with rearing larval clownfish (A.
melanopus) at high CO2 levels, including smaller length and
mass of fish and higher resting metabolic rates, were absent or
reversed when both parents and offspring were reared in elevated
CO2 levels (Miller et al., 2012). These results show that
non-genetic parental effects can have a significant influence on the
performance of juveniles exposed to high CO2 levels with the
potential to fully compensate for the observed effects caused by acute
(within generation) exposure to increased CO2 levels (Miller
et al., 2012).
In addition to the potential for acclimation and trans-generational
plasticity, it is difficult to interpret the results of laboratory
studies of acute exposure in terms of what is likely to happen in the
foreseeable future in the wild or to predict potential population level
effects for a species. The acute nature of the exposure and acclimation
in the studies above is noteworthy because most species will not
experience changes in acidification so acutely in their natural
habitats. Rather, they are likely to experience a gradual increase in
average CO2 levels over several generations, and therefore
parental effects could be highly effective in moderating overall
effects. Moreover, there is ample evidence that coral reef ecosystems
naturally experience wide fluctuations in pH on a diurnal basis
(Gagliano et al., 2010; Gray et al., 2012; Price et al., 2012). Price
et al. (2012) found that reefs experienced substantial diel
fluctuations in temperature and pH similar to the magnitudes of warming
and acidification expected over the next century. The pH of ocean
surface water has decreased from an average of 8.2 to 8.1 since the
beginning of the industrial era (IPCC, 2013). The pH of reef water can
vary substantially throughout the day, sometimes reaching levels below
8.0 in the early morning due to accumulated respiration of reef
organisms in shallow water overnight (Ohde and van Woesik, 1999;
Kuffner et al., 2007). Primary producers, including zooxanthellae in
corals, uptake dissolved CO2 and produce O2 and
organic matter during the day, while at night respiration invokes net
CO2 release into the surrounding sea water. In fact, Ohde
and van Woesik (1999) found one site that fluctuated between pH 8.7 and
7.9 over the course of a single day.
Studies clearly show that in a controlled setting, an increased
CO2 environment can impair larval sensory capabilities that
are required to make important decisions during critical life stages.
However, a disconnect exists between these experimental results and
what can be expected to occur in the wild over time, or even what is
currently experienced on a daily basis on natural reefs. There is
uncertainty associated with A. percula's likely level of exposure to
this threat in the foreseeable future given the uncertainty in future
ocean acidification rates and the heterogeneity of the species' habitat
and current environmental conditions across its range. There is also
evidence that susceptibility to acute changes in ocean pH may decrease
or disappear over several generations. Even though projections for
future levels of acidification go out to the year 2100, we do not
consider the effects of this potential threat to be foreseeable over
that timeframe due to the variable and uncertain nature of effects
shown in laboratory studies versus what the species is likely to
experience in nature over several generations. The best available
information does not indicate that ocean acidification is currently
creating an extinction risk for the species in the wild through effects
to fitness of a significant magnitude. We therefore conclude that the
threat of physiological effects from ocean acidification has a low
likelihood of having a significant effect on the species' risk of
extinction now or in the foreseeable future.
Regarding the threat of physiological and behavioral effects from
ocean warming, the best available information does not indicate that
ocean warming is currently creating an extinction risk for the orange
clownfish in the wild through effects to fitness of a significant
magnitude. In other words, the current magnitude of impact from ocean
warming is likely not affecting the ability of the orange clownfish to
survive to reproductive age, successfully find a mate, and produce
offspring. While it has yet to be studied specifically for the orange
clownfish, researchers have begun to explore the potential effect of
increasing temperature on the physiology of other pomacentrid reef fish
species. Dascyllus reticulatus adults exposed to a high temperature
(32[deg]C) environment in a laboratory setting displayed
[[Page 51245]]
significantly reduced swimming and metabolic performance (Johansen and
Jones, 2011). Other results include reduced breeding success of
Acanthochromis polyacanthus (Donelson et al., 2010) and increased
mortality rates among juvenile Dascyllus aruanus (Pini et al., 2011) in
response to increased water temperatures that may be experienced later
this century. However, multiple references on the subject state that
the effects of temperature changes appear to be species-specific
(Nilsson et al., 2009; Lo-Yat et al., 2010; Johansen and Jones, 2011);
therefore, these results are not easily applied to orange clownfish.
With regard to ocean warming effects to respiratory and metabolic
processes, Nilsson et al. (2009) and Johansen and Jones (2011) compared
results of exposure to increased temperatures across multiple families
or genera and species of reef fish. Both studies reported negative
responses, but the magnitude of the effect varied greatly among closely
related species and genera. As such, it is difficult to draw analogies
to unstudied species like orange clownfish. As with acidification,
Price et al. (2012) found that reefs currently already experience
substantial diel fluctuations in temperature similar to the magnitude
of warming expected over the next century. In addition, trans-
generational plasticity in temperature-dependent growth was recently
documented for two fish species, where offspring performed better at
higher temperatures if the parents had experienced these temperatures
as well (Donelson et al., 2011; Salinas and Munch, 2012).
There is epistemic uncertainty associated with the threat of future
ocean warming to orange clownfish. Susceptibility of reef fish that
have been studied varies widely, but there is evidence that trans-
generational plasticity may play a role in acclimation over time, at
least for some species (Donelson et al., 2011; Salinas and Munch,
2012). In addition, we cannot predict the exposure of the species to
this threat over time given the uncertainty in future temperature
predictions and the heterogeneity of the species' habitat and current
environmental conditions across its range. Further, we do not have
sufficient information to suggest future ocean warming will
significantly affect the extinction risk for orange clownfish in the
foreseeable future. Therefore, acknowledging these uncertainties, we
conclude that the threat of ocean warming has a low likelihood of
significantly contributing to extinction risk for A. percula now, or in
the foreseeable future.
Extinction Risk Assessment
In assessing four demographic risks for the orange clownfish--
abundance, growth rate/productivity, spatial structure/connectivity,
and diversity--we determined that the likelihood of three of these
risks individually contributing significantly to the extinction risk
for the species both now and in the foreseeable future is low
(abundance, growth rate/productivity, diversity), and unknown for the
fourth (spatial structure/connectivity). On a local scale, spatial
structure/connectivity does not appear to be a cause for concern for
this species but, because global genetic structure is unknown, we
cannot assign a likelihood that this factor is contributing
significantly to extinction risk for A. percula.
We acknowledge that uncertainties exist regarding how these
demographic risks may affect the species on an individual and
population level. However, we conclude that the species' estimated wild
abundance of 13-18 million individuals is at a level sufficient to
withstand demographic stochasticity. Moreover, productivity appears to
be at or above replacement levels, rates of dispersal and recruitment
at the local scale appear sufficient to sustain meta-population
structure (although global genetic structure is unknown), and species
diversity may allow for trans-generational adaptation to long term,
global environmental change. As such, even with acknowledgement of
uncertainties, we conclude that these demographic risks have a low or
unknown likelihood of contributing in a significant way to the
extinction risk of the orange clownfish.
We also assessed 12 current and predicted threats to the species
and determined that the likelihood of these individual threats
contributing to the extinction risk of the species throughout its range
vary between very low and low-to-medium (one threat was very low; nine
threats were low; and two threats were low-to-medium). We again
acknowledge uncertainties in predicting the breadth of the threats and
the extent of the species' exposure and response, but we can assume
that these threats are reasonably certain to occur at some magnitude.
For some threats, such as anemone bleaching, evidence indicates these
events will become more severe and more frequent over the next few
decades (van Hooidonk et al., 2013). However, anemone susceptibility
and response is variable, and A. percula is known to associate with
five anemone hosts, indicating that the species may be resilient to
this threat. Additionally, the species may exhibit resiliency and
adaptation to threats such as ocean acidification and ocean warming via
trans-generational plasticity. While it is unknown how much adaptation
the species will undergo, we anticipate such threats to occur gradually
over space and time rather than acutely.
Of the 12 identified current and predicted threats, our two
greatest concerns relate to the species' susceptibility and exposure to
sedimentation and nutrients, as well as the inadequacy of regulatory
mechanisms to address this threat, especially since juveniles and
adults occur in shallow water and are non-migratory once they have
settled into a host anemone. Therefore, we conservatively assigned a
low-to-medium likelihood that both this threat and the inadequate
regulatory mechanisms to address this threat may contribute
significantly to the extinction risk for the orange clownfish.
Considering the demographic risks analysis (three low, one unknown)
and the current and predicted threats assessment (one very low, nine
low, two low-to-medium), we have determined that overall extinction
risk for the orange clownfish is low, both now and in the foreseeable
future. We recognize that some of the demographic risks and threats to
the species may work in combination to produce cumulative effects. For
example, increased ocean acidification may affect the olfactory and
auditory sensory capabilities of the species and potentially affect
predation rates; ocean warming may affect the aerobic capacity of the
species or the rates of disease; and harvest of sea anemones may
eliminate habitat that is essential for the species and potentially
increase the likelihood of predation; and therefore, interactions
within and among these threats may affect individuals of the species.
However, despite our acknowledged uncertainties, even these synergistic
effects that can be reasonably expected to occur from multiple threats
and/or demographic risks are expected to be limited to cumulative
effects on a local scale at most and not anticipated to rise to the
level of significantly affecting the extinction risk for this species.
While individuals may be affected, we do not anticipate the overlap of
these threats to be widespread throughout the species' range at any
given time because all threats are occurring and will continue to occur
with significant variability over space and time. Therefore, we do not
expect the species to respond to cumulative threats in a way that may
[[Page 51246]]
cause measurable effects at the population level.
Based on the species' exposure and response to threats, resilient
life history characteristics, potential for trans-generational adaptive
capabilities, and estimated global wild abundance of 13-18 million
individuals, it is unlikely that these threats will contribute
significantly to the extinction risk of the orange clownfish.
Therefore, we conclude that the species is not endangered or threatened
throughout its range.
Significant Portion of Its Range
Though we find that the orange clownfish is not in danger of
extinction now or in the foreseeable future throughout its range, under
the SPR Policy, we must go on to evaluate whether the species in in
danger of extinction, or likely to become so in the foreseeable future,
in a ``significant portion of its range'' (79 FR 37578; July 1, 2014).
The SPR Policy explains that it is necessary to fully evaluate a
particular portion for potential listing under the ``significant
portion of its range'' authority only if substantial information
indicates that the members of the species in a particular area are
likely both to meet the test for biological significance and to be
currently endangered or threatened in that area. Making this
preliminary determination triggers a need for further review, but does
not prejudge whether the portion actually meets these standards such
that the species should be listed. To identify only those portions that
warrant further consideration, we will determine whether there is
substantial information indicating that (1) the portions may be
significant and (2) the species may be in danger of extinction in those
portions or likely to become so within the foreseeable future. We
emphasize that answering these questions in the affirmative is not a
determination that the species is endangered or threatened throughout a
significant portion of its range--rather, it is a step in determining
whether a more detailed analysis of the issue is required (79 FR 37578,
at 37586; July 1, 2014).
Thus, the preliminary determination that a portion may be both
significant and endangered or threatened merely requires NMFS to engage
in a more detailed analysis to determine whether the standards are
actually met (79 FR 37578, at 37587). Unless both standards are met,
listing is not warranted. The policy further explains that, depending
on the particular facts of each situation, NMFS may find it is more
efficient to address the significance issue first, but in other cases
it will make more sense to examine the status of the species in the
potentially significant portions first. Whichever question is asked
first, an affirmative answer is required to proceed to the second
question. Id. ``[I]f we determine that a portion of the range is not
`significant,' we will not need to determine whether the species is
endangered or threatened there; if we determine that the species is not
endangered or threatened in a portion of its range, we will not need to
determine if that portion is `significant' '' (79 FR 37578, at 37587).
Thus, if the answer to the first question is negative--whether that
regards the significance question or the status question--then the
analysis concludes and listing is not warranted.
Applying the policy to the orange clownfish, we first evaluated
whether there is substantial information indicating that any particular
portion of the species' range is ``significant.'' We considered the
best available information on abundance, productivity, spatial
distribution, and diversity in portions of the species' range in the
Indo-Pacific Ocean. We did not find information indicating that any of
these four factors show any type of spatial pattern that would allow
for delineation of portions of the species' range in order to evaluate
biological significance. The range of the species is somewhat
restricted to the eastern-most portion of the coral triangle and
northern Australia. Abundance and density of A. percula are highly
variable throughout the species' range and are likely highest in Papua
New Guinea. However, we do not have information on abundance and
density in other portions of the species' range and were only able to
estimate an overall global population size of 13-18 million (based on
De Brauwer, 2014). We do not have information on historical abundance
or recent population trends for the orange clownfish, nor can we
estimate population growth rates in any particular portions of the
species' range. The best available information on spatial distribution
indicates that the orange clownfish likely has variable connectivity
between and within meta-populations throughout its range. We do not
have information on the global phylogeography of orange clownfish and
cannot delineate any particular portion of the species' range that may
be significant because of its spatial distribution or connectivity
characteristics. Multiple reports of geographic color variations at
sites in Papua New Guinea indicate there is genetic diversity at those
sites. Levels of phenotypic and genetic diversity in other portions of
the species' range are largely unknown. Based on their pelagic
dispersal and variable levels of self-recruitment, orange clownfish are
likely arranged in meta-population structures like the ones studied in
Kimbe Bay, Papua New Guinea, throughout their geographic range, thus
providing opportunity for genetic mixing.
After a review of the best available information, and because of
the scale at which most of the information exists, there is no
supportable way to evaluate demographic factors for any portions
smaller than the entire population. We are unable to identify any
particular portion of the species' range where its contribution to the
viability of the species is so important that, without the members in
the portion, the species would be at risk of extinction, or likely to
become so in the foreseeable future, throughout all of its range. We
find that there is no portion of the species' range that qualifies as
``significant'' under the SPR Policy, and thus our SPR analysis ends.
Determination
Based on our consideration of the best available information, as
summarized here and in Maison and Graham (2015), we determine that the
orange clownfish, Amphiprion percula, faces a low risk of extinction
throughout its range both now and in the foreseeable future, and that
there is no portion of the orange clownfish's range that qualifies as
``significant'' under the SPR Policy. We therefore conclude that
listing this species as threatened or endangered under the ESA is not
warranted. This is a final action, and, therefore, we do not solicit
comments on it.
References
A complete list of all references cited herein is available at our
Web site (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 (See NOAA Administrative Order 216-6).
[[Page 51247]]
Authority
The authority for this action is the Endangered Species Act of
1973, as amended (16 U.S.C. 1531 et seq.).
Dated: August 18, 2015.
Samuel D. Rauch III,
Deputy Assistant Administrator for Regulatory Programs, National Marine
Fisheries Service.
[FR Doc. 2015-20754 Filed 8-21-15; 8:45 am]
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