Endangered and Threatened Wildlife and Plants; Notice of 12-Month Finding on a Petition To List the Humphead Wrasse as Threatened or Endangered Under the Endangered Species Act (ESA), 57875-57887 [2014-23034]
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Federal Register / Vol. 79, No. 187 / Friday, September 26, 2014 / Notices
Dated: September 23, 2014.
Emily H. Menashes,
Acting Director, Office of Sustainable
Fisheries, National Marine Fisheries Service.
[FR Doc. 2014–22932 Filed 9–25–14; 8:45 am]
BILLING CODE 3510–22–P
DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric
Administration
[Docket No. 121204680–4789–03]
RIN 0648–XC387
Endangered and Threatened Wildlife
and Plants; Notice of 12-Month Finding
on a Petition To List the Humphead
Wrasse as Threatened or Endangered
Under the Endangered Species Act
(ESA)
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.
AGENCY:
We, NMFS, announce a 12month finding on a petition to list the
humphead wrasse (Cheilinus undulatus)
as threatened or endangered under the
Endangered Species Act (ESA). We have
completed a comprehensive status
review of the humphead wrasse in
response to this petition. Based on the
best scientific and commercial
information available, including the
status review report (Graham et al.,
2014), we have determined that the
species does not warrant listing at this
time. We conclude that the humphead
wrasse 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.
We also announce the availability of the
humphead wrasse status review report.
DATES: This finding was made on
September 26, 2014.
ADDRESSES: The humphead wrasse
status review report is available
electronically at: https://
www.fpir.noaa.gov/PRD/prd_
humpheadwrasse.html. You may also
receive a copy by submitting a request
to the Protected Resources Division,
Pacific Islands Regional Office, NMFS,
1845 Wasp Blvd., Building 176,
Honolulu, HI 96818, Attention:
Humphead Wrasse 12-month Finding.
FOR FURTHER INFORMATION CONTACT:
Krista Graham, NMFS, Pacific Islands
Regional Office, (808) 725–5152; or Lisa
Manning, NMFS, Office of Protected
Resources, (301) 427–8466.
SUPPLEMENTARY INFORMATION:
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SUMMARY:
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Background
On October 31, 2012, we received a
petition from WildEarth Guardians to
list the humphead wrasse (Cheilinus
undulatus) as threatened or endangered
under the ESA throughout its entire
range. The petitioners also requested
that critical habitat be designated for the
humphead wrasse under the ESA. On
February 28, 2013, we published a
positive 90-day finding (78 FR 13614),
announcing that the petition presented
substantial scientific or commercial
information indicating the petitioned
action of listing the species may be
warranted and explained the basis for
that finding. 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.
Listing Species Under the Endangered
Species Act
Section 4(b)(3)(B) of the ESA requires
us to make a finding within 12-months
of the date of receipt of any petition that
was found to present substantial
information indicating that the
petitioned action may be warranted. The
12-month finding must provide a
determination of whether the petitioned
action is: (a) Not warranted; (b)
warranted; or (c) warranted but
precluded. In this case, we are
responsible for determining whether the
humphead wrasse warrants listing as
threatened or endangered under the
ESA (16 U.S.C. 1531 et seq.). To make
this determination, we first consider
whether a group of organisms
constitutes a ‘‘species’’ under section 3
of the ESA, then whether the status of
the species qualifies it for listing as
either threatened or endangered. Section
3 of the ESA defines species to include
‘‘any subspecies of fish or wildlife or
plants, and any distinct population
segment of any species of vertebrate fish
or wildlife which interbreeds when
mature.’’ On February 7, 1996, NMFS
and the U.S. Fish and Wildlife Service
(USFWS; together, the Services) adopted
a policy describing what constitutes a
distinct population segment (DPS) of a
taxonomic species (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.
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Section 3 of the ESA further defines
an ‘‘endangered species’’ as ‘‘any
species which is in danger of extinction
throughout all or a significant portion of
its range’’ and a ‘‘threatened species’’ as
one ‘‘which is likely to become an
endangered species within the
foreseeable future throughout all or a
significant portion of its range.’’ Thus,
in the context of the ESA, we interpret
an ‘‘endangered species’’ to be one that
is presently in danger of extinction. A
‘‘threatened species’’ is not presently at
risk of extinction, but is likely to
become so in the foreseeable future. The
key 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).
Section 4 of the ESA and
implementing regulations at 50 CFR part
424 require us to determine whether any
species is endangered or threatened as
a result of any one or a combination of
the following five factors: (A) The
present or threatened destruction,
modification, or curtailment of its
habitat or range; (B) overutilization for
commercial, recreational, scientific, or
educational purposes; (C) disease or
predation; (D) the inadequacy of
existing regulatory mechanisms; or (E)
other natural or manmade factors
affecting its continued existence (ESA
section 4(a)(1)(A)-(E)). Section 4(b)(1)(A)
of the ESA requires us to make listing
determinations based solely on the best
scientific and commercial data available
after conducting a review of the status
of the species and after taking into
account efforts being made by any State
or foreign nation or political subdivision
thereof to protect the species. We also
consider the comments received in
response to issuance of the 90-day
finding. In evaluating the efficacy of
existing protective efforts, we rely on
the Services’ joint Policy on Evaluation
of Conservation Efforts When Making
Listing Decisions (‘‘PECE’’; 68 FR 15100;
March 28, 2003). The PECE provides
direction for considering conservation
efforts that have not been implemented,
or have been implemented but not yet
demonstrated effectiveness.
Status Review
We appointed an Endangered Species
Biologist in the Protected Resources
Division of the NMFS Pacific Islands
Regional Office (PIRO) to gather and
review the best available data and
information on the life history and
ecology, distribution, abundance, and
threats to the humphead wrasse and to
document this review in a status review
report. Next, we convened a team of
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four biologists (hereinafter referred to as
the Extinction Risk Analysis (ERA)
Team) to conduct an extinction risk
analysis for the humphead wrasse, using
the information in the status review
report. The ERA Team was comprised of
three fishery biologists from NMFS’
Pacific Island Fisheries Science Center
and a fishery biologist with NMFS
PIRO’s Habitat Conservation Division.
The ERA Team had expertise in reef fish
biology and ecology, population
dynamics, and stock assessment
science. The ERA Team documented
their evaluation of possible DPSs for the
humphead wrasse and their professional
judgment of the extinction risk facing
the humphead wrasse in the status
review report (Graham et al., 2014). The
report makes no recommendation as to
the listing status of the species. The
status review report is available
electronically at https://
www.fpir.noaa.gov/PRD/prd_
humpheadwrasse.html.
The status review report was then
subjected to peer review as required by
the Office of Management and Budget
Final Information Quality Bulletin for
Peer Review (M–05–03; December 16,
2004). The status review report was peer
reviewed by three independent
specialists selected from the academic
and scientific community, with
expertise in reef fish biology,
conservation and management, and
knowledge of humphead wrasse. The
peer reviewers were asked to evaluate
the adequacy, appropriateness, and
application of data used in the status
review as well as evaluate the findings
made in the ‘‘Assessment of Extinction
Risk’’ section of the report. All peer
reviewer comments were addressed
prior to dissemination of the final status
review report and publication of this
determination.
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Life History, Biology, and Status of the
Petitioned Species
Below we summarize the key life
history and species information from
the status review report (Graham et al.,
2014). More detailed information is
available in the status review report,
which is available electronically at
https://www.fpir.noaa.gov/PRD/prd_
humpheadwrasse.html.
Species Description
The humphead wrasse is the largest
member of the family Labridae. Found
throughout the Indo-Pacific Ocean, the
humphead wrasse is distinguished from
other coral reef fishes, including other
wrasses, due primarily to its large size
along with its fleshy lips in adults
(Myers, 1999), prominent bulbous hump
that appears on the forehead in larger
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adults of both sexes, and intricate
markings around the eyes (Marshall,
1964; Bagnis et al., 1972; Sadovy et al.,
2003a).
The humphead wrasse has a reported
maximum length of 229 cm total length
(TL) (7.5 ft) and weight of 190.5 kg (420
lbs) (Marshall, 1964; Myers, 1989;
Lieske and Myers, 1994; Donaldson and
Sadovy, 2001; Westneat, 2001; Sadovy
et al., 2003a; Russell, 2004); however,
there are no confirmed records of this
species greater than 150 cm fork length
(FL) (Choat et al., 2006). (TL is
measured from the tip of the snout to
the tip of the longer lobe of the caudal
or tail fin; whereas, FL is measured from
the tip of the snout to the end of the
middle caudal fin rays (i.e., where the
fork of the tail begins). TL is longer than
FL). The maximum age of humphead
wrasse is estimated to be 30 years for
females and 25 years for males (Sadovy
et al., 2003a; Choat et al., 2006;
Andrews et al., in review).
The development of the cephalic
hump is related to body size and is
visible at 37 cm TL, with all individuals
≥75 cm TL exhibiting a distinctive
hump, irrespective of sex (Liu and
Sadovy de Mitcheson, 2011). Therefore,
C. undulatus does not show obvious
sexual dimorphism of the forehead
extension, meaning that it is not a
reliable criterion for differentiating
males and females. The species has 9
dorsal fin spines, 10 dorsal fin rays, 3
anal fin spines, and 8 anal fin rays
(Sadovy et al., 2003a). Juveniles are pale
gray/green with large dark spots on
some of the scales that produce a series
of broad dark bands, interspersed with
narrower white bands along the length
of the body and a pair of distinctive
parallel black lines before and after the
eye (Sadovy et al., 2003a). Colin (2006)
notes that juvenile C. undulatus
resemble juvenile C. trilobatus and C.
chlorurus, with similar shape, some
resemblance in coloration, similar swim
fashion, and can all occur in the same
habitat. The author notes that the
similarities with these two more
common species can result in confusion
and misidentification of juvenile C.
undulatus.
Adults are olive green to blue-green
with large scales. A narrow dark bar on
each scale breaks into irregular dark
lines anteriorly on the body with growth
(Randall, 2005). The head is a bluegreen to blue with irregularly wavy
yellowish lines (Sadovy et al., 2003)
with the same two slightly oblique black
lines extending posteriorly from the
lower half of the eye, often with two
more black lines extending from the eye
to the rear part of the upper lip (Randall,
2005). These distinctive patterns of lines
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makes identifying individual fish
possible if the head pattern and spots
can be seen or photographed. While
there is no apparent sexual
dichromatism or permanent difference
in color between sexes (Sadovy et al.,
2003a), temporary color differences
between males and females are seen
during reproduction (Colin, 2010).
Distribution
The humphead wrasse is widely
distributed on coral reefs and nearshore
habitats throughout much of the tropical
Indo-Pacific Ocean. The biogeographic
range of the humphead wrasse spans
from 30° N to 23° S latitude and
includes the Red Sea south to
Mozambique in the Indian Ocean, from
southern Japan in the northwest Pacific
south to New Caledonia in the south
Pacific and into the central Pacific
Ocean including French Polynesia. The
humphead wrasse has been recorded
from many islands of Oceania, but
appears to be absent from the Hawaiian
Islands, Johnston Island, Easter Island,
Pitcairn, Rapa, and Lord Howe Island
with the exception of occasional waifs
(Randall et al., 1978). In the United
States (U.S.), the species is found in the
territories of American Samoa, the
Commonwealth of the Northern Mariana
Islands (CNMI), and Guam. In the U.S.
Pacific Remote Island Areas, the species
is found in the Line (Palmyra Atoll,
Kingman Reef, and Jarvis Island) and
Phoenix (Howland and Baker) Islands,
and at Wake Atoll.
Habitat
The humphead wrasse is widely
distributed in low densities on all types
of coral reef environments and
nearshore habitats throughout much of
the tropical Indo-Pacific. Both coral
reefs and seagrass beds have been
reported to provide a nursery habitat for
post-settlement and juvenile humphead
wrasse (Sadovy et al., 2003a; Russell,
2004). Juveniles are also observed in
murky outer river areas with patch reefs,
shallow sandy areas adjacent to coral
reef lagoons, and in mangroves (Randall,
1955; Randall et al., 1978; Myers, 1989;
Sadovy et al., 2003a; Myers, 1999).
Unlike juveniles, adults are more
commonly observed inhabiting offshore
habitats along steep outer reef slopes,
reef drop offs, channel slopes, reef
passes, reef flats, and lagoonal reefs to
depths of up to at least 100 m (Randall,
1978; Myers, 1989; Sadovy et al., 2003a;
Zgliczynski et al., 2013). Fish size and
abundance are correlated with habitat
type, with the largest fish and most
dense groups of humphead wrasses
observed on barrier reefs and passes. In
coastal, middle reefs and lagoon areas,
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smaller fish (< 50 cm TL) are typically
observed among branching staghorn
corals (Acropora spp.) (Sadovy et al.,
2003a).
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Movement and Behavior
The numbers of fish found together
can vary. According to Sadovy et al.
(2003a), juveniles are typically solitary,
wary, and difficult to approach, though
they can be found in small groups.
Adults are typically observed solitary or
paired (Myers, 1989; Sadovy et al.,
2003a) but have also been noted in
groups of 3–7 individuals (Donaldson,
1995; Sadovy et al., 2003a).
Additionally, small social units can be
observed moving together in less
heavily fished areas, while lone and
more wary individuals are more often
noted in heavily fished areas (Sadovy et
al., 2003a).
Based on mensurative in situ
observations, humphead wrasse display
site fidelity and predictable home
ranges with the same individuals,
identifiable by distinct head markings,
observed along the same stretches of
reef for extended periods, although the
lengths of these periods are not defined.
Additionally, adults often use a
consistent resting place (i.e., cave or
crevice) at night or when threatened
(Bagnis et al., 1972; Myers, 1989;
Thaman, 1998; Myers, 1999; Donaldson
and Sadovy, 2001; Sadovy et al., 2003a;
Chateau and Wantiez, 2007).
Factors such as sex, age, and size of
the fish directly influence the home
range size of the humphead wrasse,
with smaller fish using a fraction of the
area occupied by adults (Sadovy et al.,
2003a citing T.J. Donaldson,
unpublished data). A single juvenile (45
cm FL) humphead wrasse that had been
surgically implanted with an ultrasonic
transmitter in New Caledonia moved at
least 20–200 m every day and had an
estimated home range size of at least
50,000 m2 (Chateau and Wantiez, 2007).
In Palmyra Atoll, 19 acoustically tagged
juveniles and adults (ranging in length
from 27 to 109 cm TL) had home range
sizes of 800 m 2 to 19,000 m 2, with the
smallest home ranges occupied by
juveniles, intermediate ranges for adult
males, and largest ranges occupied for
adult females (Weng et al., in press).
Foraging Ecology
The humphead wrasse is a diurnal
carnivore, feeding during the day and
sleeping at night (Durville et al., 2003;
Gillbrand et al., 2007). Much of its prey
is found in sand or rubble habitats
where it feeds on a variety of molluscs,
small fishes such as gobies, moray eels,
sea urchins, crustaceans, brittle stars,
starfish, and other invertebrates
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(Randall et al., 1978; Myers, 1989;
Randall et al., 1997; Thaman, 1998;
Sadovy et al., 2003a; Choat et al., 2006).
Similar to other wrasse (Labridae),
humphead wrasses forage by turning
over or crushing rocks and rubble to
reach cryptic organisms (Pogonoski et
al., 2002; Sadovy et al., 2003a citing P.S.
Lobel, pers. comm.). The thick fleshy
lips of the species appear to absorb sea
urchin spines, and the pharyngeal teeth
easily crush heavy-shelled sea snails in
the genera Trochus spp. and Turbo spp.
The humphead wrasse is also one of the
few predators of toxic animals such as
boxfishes (Ostraciidae), sea hares
(Aplysiidae), and crown-of-thorns
starfish (Acanthaster planci) (Randall,
1978; Myers, 1989; Thaman, 1998;
Sadovy et al., 2003a). Consumption of
toxic species in certain areas,
particularly Tahiti, Tuvalu, New
Caledonia, the Tuamotu Archipelago
(French Polynesia), Marshall Islands,
and the Federated States of Micronesia
can cause the humphead wrasse to be
ciguatoxic to humans (Randall, 1958;
Randall et al., 1978; Randall, 1979;
Lewis, 1986; Myers, 1989; Dalzell, 1992;
Dalzell, 1994; Sadovy, 1998; Myers,
1999; Sadovy et al., 2003b; Sadovy,
2006).
Reproduction and Growth
Field reports reveal variable
humphead wrasse spawning behavior,
depending on location (Sadovy et al.,
2003a; Colin, 2010). Spawning can
occur between several and all months of
the year, coinciding with certain phases
of the tidal cycle (usually after high
tide) and possibly lunar cycle (Sadovy
et al., 2003a; Colin, 2010). Spawning
can reportedly occur in small (< 10
individuals) or large (≤ 100 individuals)
groupings, which can take place daily in
a variety of reef types (Sadovy et al.,
2003a; Sadovy de Mitcheson et al.,
2008; Colin, 2010).
Data from captive rearing programs
indicates that egg diameter ranges from
0.62–0.67 mm, and newly hatched
larvae are 1.5–1.7 mm TL (Slamet and
Hutapea, 2005). Eggs are spherical and
lack pigment (Sadovy et al., 2003 citing
P.L. Colin, unpublished data). Little
information is available regarding larval
dispersal in the wild (Poh and Fanning,
2012). However, in unpublished work
P.L. Colin (pers. comm.) found that eggs
of humphead wrasse moved slowly off
the western barrier reef of Palau over a
few hours in tidal currents, and then
stalled before moving laterally along the
reef. Some eggs are brought back in over
the barrier reef, while others remain at
sea, all in the first 12 hours after
spawning.
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Humphead wrasse larvae settle out of
the plankton at a size of 8 to 15 mm TL,
with a mode of 12 mm TL (at an
unspecified larval duration), and reach
35 mm TL or greater within 2 to 3 weeks
post-settlement (Tupper, 2007 citing M.
Tupper, unpublished data). Slamet and
Hutapea (2005), however, indicate that
growth of larvae is actually much
slower. The authors report that captive
larvae reach 50–60 mm TL in 6 months.
Settlement varies among habitat types.
As is common in wrasses, the
humphead wrasse is a protogynous
hermaphrodite, capable of changing sex
from female to male around 9 years of
age (Choat et al., 2006; Sadovy de
Mitcheson et al., 2010). At around 6
months of age, juveniles are
approximately 5–6 cm TL (Slamet and
Hutapea, 2005), reaching 50 cm TL at
approximately 7 years of age. As females
reach sexual maturity growth slows,
with few individuals observed > 100 cm
TL. Male growth rates are approximately
double those of females, resulting in
relatively young but large males (Choat
et al., 1996; 2006).
Size at maturity for males and females
is difficult to compare across studies
because some measurements are
reported as TL and others as FL. Sadovy
et al. (2003a) estimates that females
reach sexual maturity at around 5 years
of age and 35–50 cm TL. Other
histological studies estimate that sexual
maturity is reached around 40–60 cm
TL, which is estimated to be about 5–
7 years of age (Pogonoski et al., 2002
and Russell, 2004 citing Sadovy,
unpublished data; Sadovy et al., 2011).
Another study analyzing early gonadal
development on 178 humphead wrasse
specimens revealed that minimum body
sizes for female and male sexual
maturation were 65 cm and 84.5 cm TL,
respectively (Sadovy de Mitcheson et
al., 2010). However, the authors note
that despite the results from this study,
based on available information, it is
suggested that the typical size of female
sexual maturation for the humphead
wrasse occurs at 40–50 cm TL (Sadovy
de Mitcheson et al., 2010). Choat et al.
(2006) estimated length at first maturity
as 45–50 cm FL for females (6–7 years)
and 70 cm FL (9 years) for males.
Despite the apparent differences in
estimated minimum size of female
sexual maturation among the different
studies and locations, the age at first
maturity is relatively late, representing
about 20% of the female life span as
opposed to 5–6% of the female life span
observed in most other reef fishes with
life spans in excess of 30 years (Choat
and Robertson, 2002).
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Natural Mortality
Natural adult mortality is thought to
be low (Sadovy et al., 2003a). As for
mortality due to predation, little is
known though it is thought there is
refuge in size. Although adult
humphead wrasses are most vulnerable
during spawning, apex predators
including sharks are not known to prey
on adult humphead during this time
(Colin, 2010).
Population Structure
Very little published genetic research
is available on the humphead wrasse
other than the results of sequencing the
mitochondrial genome of the species (Qi
et al., 2013). Research is currently
underway to analyze 200 humphead
wrasse samples collected from the
eastern Indian Ocean to Pohnpei and
from the Great Barrier Reef to the
Marianas Islands. Preliminary analyses
of mitochondrial DNA from a subset of
samples from across the range suggest
no deep genetic differentiation on the
scale of ocean basins, though robust
conclusions await final analyses of the
complete dataset (Michael Dawson,
pers. comm.). Additionally, no tagging
or tracking studies of a scale sufficient
to define population structure have been
conducted. Although a number of
studies have provided abundance
estimates based on in situ surveys, there
are no current studies or references
describing population structure.
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Population Abundance
There are no historical estimates (pre1970s) of global or local abundance or
biomass of humphead wrasse. When
limited surveys first began on this
species in the early 1970s, the species
was generally characterized as being
naturally uncommon to rare in places
(Bagnis et al., 1972; Galzin et al., 1998;
Sadovy et al., 2003a and IUCN, 2008
citing Galzin, 1985; IUCN, 2008 citing
Tropical Research and Conservation
Centre—Malaysia (TRACC), 2004). For
example, in 1972 Taiaro lagoon, a 9 km2
uplifted lagoon (maximum depth of 27
m dominated by talus sand and small
dispersed patch reefs) of Taiaro Atoll in
Tuamotu Archipelago, French
Polynesia, where this species was not
fished and fish diversity was high,
abundance was estimated to be 1–2 fish
per 10,000 m2 (Galzin et al., 1998). This
abundance remained unchanged during
repeat surveys in 1992 and 1994 (Galzin
et al., 1998). In the Society Islands of
French Polynesia, humphead wrasses
were also reported to be uncommon in
the early 1970s (Bagnis et al., 1972;
IUCN, 2008 citing Galzin, 1985).
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Past catch records for some locations,
when compared to more current catch
records, although the data are sparse,
indicate that some populations were at
one time greater than present day (i.e.,
Australia, Fiji, Malaysia, Palau [IUCN,
2008]). However, inferences regarding
abundance from fishery dependent data
are subject to uncertainty from effects of
fishing methods, size selectivity, fishery
participation, regulation, and methods
of collecting data. Such uncertainty is
also true in relation to inferences made
from underwater surveys when habitat
information and survey methodology
are not known.
Efforts to estimate abundance and
density of humphead wrasse have been
completed in certain regions within the
species’ range (e.g., U.S. Pacific Islands)
using underwater visual census
techniques designed to quantify the
abundance of these relatively rare/
uncommon and wide-ranging fish.
Although humphead wrasses are widely
distributed, natural densities are
typically low, even in locations where
habitats are presumably intact. Unfished
or lightly fished areas have densities
ranging from 2–27 individuals per
10,000 m2 of reef (Sadovy et al., 2003a).
For example, at Wake Atoll where there
is zero fishing pressure for the species,
surveys that recorded primarily
juveniles (< 30 cm TL) reported the
naturally low abundance of the species
at 13–27 individuals per 10,000 m2
(Sadovy et al., 2003a and IUCN, 2008
citing P.S. Lobel, pers. comm., and
Lobel and Lobel, 2000). This is the
highest recorded abundance of any
location and one of the most protected
areas. Abundance of sub-adult and adult
humphead wrasse observed from toweddiver surveys of fore reef habitats (10–
15 m depth) at Wake Atoll conducted by
NMFS Pacific Islands Fisheries Science
Center (PIFSC) Coral Reef Ecosystem
Division (CRED) in 2005, 2007, 2009,
and 2011 is lower. Four years of
biannual surveys from this time period
report an average of 1.101 large (≤ 50 cm
TL) individuals per 10,000 m2 (NMFS
PIFSC CRED, unpublished). Palmyra
Atoll, also a U.S. Pacific Remote Island
Area where the species is completely
protected, had similarly naturally low
abundance levels despite decades of
complete protection. Abundance of
large (≤ 50 cm TL) humphead wrasse
observed from towed-diver surveys of
fore reef habitats (10–15 m depth) of
Palmyra Atoll conducted biannually
from 2001–2012 is 0.641 individuals per
10,000 m2 (NMFS PIFSC CRED,
unpublished).
At sites near human population
centers or at fished areas, densities are
typically lower by tenfold or more and
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in some locations humphead wrasse are
rarely observed (Sadovy et al., 2003a;
Colin, 2006; Sadovy, 2006b; Unsworth
et al., 2007). However, in some areas,
such as the previously mentioned
Tuamotu Archipelago, French
Polynesia, abundance of humphead
wrasse is low to non-existent, even
when fisheries exploitation is known to
be low or non-existent (Galzin et al.,
1998). Another example is the
northernmost uninhabited islands of the
Marianas Archipelago (Uracus, Maug,
and Asuncion), which are part of the
Marianas Trench Marine National
Monument. Here, where commercial
fishing is prohibited and recreational or
subsistence fishing is very rare given the
distance from most of the southern
inhabited areas of the island chain,
humphead wrasses were not observed.
However, in the southern inhabited part
of the chain where some protections for
the species exist, large (≤ 50 cm TL)
humphead wrasses are present though
abundance levels are low (i.e., biannual
towed-diver surveys of fore reef habitats
(10–15 m depth) from 2003–2011 of the
entire Marianas Archipelago reports an
average of 0.059 individuals per 10,000
m2 (Brainard et al., 2012; NMFS PIFSC
CRED, unpublished data)).
Status of the Species
Other than activities associated with
the live reef food fish trade (LRFFT),
there are few ‘‘directed’’ fisheries for the
humphead wrasse due to its natural
rarity and the inherent difficulty of
capturing the fish (Gillett, 2010). In
most countries where the fish occurs,
most of the catch of this species is for
domestic use. Commercially, the
humphead wrasse is caught in low
volume fisheries in different ways
according to its size and whether it is
needed alive or dead (Sadovy et al.,
2003a). The species is sold for domestic
consumption, exported for food for the
LRFFT, exported for mariculture until
the fish is large enough for
consumption, or exported for aquaria.
The LRFFT is a highly lucrative
industry that involves the capture of
reef fish that are kept alive for sale and
consumption. For about three decades,
the humphead wrasse has been a small
but significant component of the
commercial LRFFT as one of the
highest-valued luxury food items
(Sadovy et al., 2003a; Sadovy et al.,
2003b; Gillett, 2010). Indonesia,
Malaysia, and the Philippines are the
top three exporters of humphead wrasse
for the LRFFT, respectively. The major
importing countries for the species are
China (especially Hong Kong), Taiwan,
and Singapore (Sadovy et al., 2003a).
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In 1996, the humphead wrasse was
listed as ‘‘vulnerable’’ on the
International Union for the
Conservation of Nature (IUCN) Red List
of Threatened Species due to concerns
over rapidly declining numbers in many
areas. In 2004, the species was
reclassified to ‘‘endangered’’ on the
IUCN Red List. Also in 2004, the species
was included in Appendix II in the
Convention on International Trade in
Endangered Species of Wild Fauna and
Flora (CITES). Appendix II includes
species that are vulnerable to
overexploitation, but not at risk of
extinction under CITES criteria; trade
must be regulated to avoid exploitation
rates incompatible with species
survival.
Distinct Population Segment Analysis
As described earlier, the ESA’s
definition of ‘‘species’’ includes ‘‘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.’’ The
petitioners did not request that NOAA
consider listing a DPS; however, the
ERA Team was asked to evaluate
whether any populations of the species
might qualify as DPSs based on the
elements of discreteness and
significance as defined in the DPS
Policy. The ERA Team found support
for discreteness of the humphead wrasse
population within the ‘‘core-Coral
Triangle’’ area of Indonesia, Malaysia,
and the Philippines solely on the basis
that the population is delimited by
international governmental boundaries
within which regulation and governance
of threats are different from other
portions of the species’ range. There was
no support to conclusively subdivide
the species into discrete population
segments on the basis of genetics,
morphology, behavior, physical factors,
or other biological characteristics.
When evaluating whether the coreCoral Triangle DPS met the significance
criteria, the team found some support
for the ‘‘persistence of the discrete
population segment in an ecological
setting unusual or unique for the
taxon.’’ According to the Team (see
Appendix 1 of the Status Review
Report), this support was largely based
on the fact that the three countries
within the core-Coral Triangle area
contain approximately 50 percent of
mangroves and 30 percent of coral reefs
within the species range, both of which
provide important habitat for various
humphead wrasse life stages. However,
the team acknowledged that because
coral reef and mangrove habitats also
occur outside the range of the proposed
DPS, neither of those habitat types is
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unique to the core-Coral Triangle area,
nor did they identify any other unique
habitat features of this area. The ERA
Team did consider that the humphead
wrasse plays a relatively unique
ecosystem role in the core-Coral
Triangle area due to its co-occurrence
with two significant prey species that
likely have interdependent ecological
roles. However, the humphead wrasse
also overlaps with the two significant
prey species outside the range of the
proposed DPS, and although the overlap
may not be as widespread, the team
acknowledged that this ecological
structure is not truly unique to the coreCoral Triangle area. Thus, overall, the
significance criterion of the DPS Policy
is not well supported.
As stated in the DPS Policy, Congress
instructed the Services to exercise their
authority with regard to DPSs ‘‘. . .
sparingly and only when the biological
evidence indicates that such action is
warranted.’’ Given this direction from
Congress and the weak support for the
significance of the core-Coral Triangle
DPS, we declined to consider this DPS
further and asked the ERA Team to
conduct the extinction risk analysis on
the entire global population of the
humphead wrasse.
Assessment of Extinction Risk
When evaluating whether the
humphead wrasse meets the definition
of threatened or endangered, we
considered the best available
information and applied professional
judgment in evaluating the level of risk
faced by a species. We qualitatively
evaluated demographic risks, such as
low abundance and productivity, along
with other threats to the species. A
quantitative viability analysis (i.e.,
population modeling) was not
conducted for the humphead wrasse
because of the limited or inadequate
data on population size, definitive
trends in population size or apparent
abundance, intrinsic rate of increase,
mortality rates, or size structure. Lastly,
as required under section 4(b)(1)(A), we
also took into account conservation
efforts being made to protect the
species.
Methods
The term ‘‘foreseeable future’’ was
defined as the future timeframe over
which demographic risks and threats
can be reliably predicted to impact the
biological status of the humphead
wrasse. The Team took into account the
life history of the species, including the
longevity of the species (25–30 years),
and assumed 6–7 years for generation
time (which is defined as the time it
takes, on average, for a sexually mature
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female humphead wrasse to be replaced
by offspring with the same spawning
capacity). Considering all of this, the
Team agreed that it would likely take
several generation times for any
conservative management action to be
realized and reflected in population
abundance. Therefore, the ERA Team
chose to project threats in the
‘‘foreseeable future’’ out to eight
generations, or about 50 years.
Previous NMFS status reviews have
involved use of a risk matrix method to
organize and summarize the
professional judgment of a panel of
knowledgeable scientists. This approach
is described in detail by Wainright and
Kope (1999) and has been used in
Pacific salmonid status reviews as well
as in the status reviews of many other
species (see https://www.nmfs.noaa.gov/
pr/species for links to these reviews). In
the risk matrix approach, the collective
condition of individual populations is
summarized at the species level
according to four demographic risk
criteria: abundance, growth rate and
productivity, spatial structure and
connectivity, and diversity. These
viability criteria, outlined in McElhany
et al. (2000), reflect concepts that are
well founded in conservation biology
and that individually and collectively
provide strong indicators of extinction
risk. Using these concepts, the ERA
Team estimated demographic risks by
assigning a risk score to each of the four
demographic criteria. The scoring for
the demographic risk criteria
correspond to the following values: 1—
no risk, 2—low risk, 3—moderate risk,
4—high risk, and 5—very high risk. The
Team members also expressed their
certainty regarding evidence of
demographic risk using a ranking of
low, medium, and high. Detailed
definitions of the risk scores can be
found in the status review report.
The ERA Team then performed a
threats assessment for the humphead
wrasse by ranking the effect that each
threat was having on the extinction risk
of the species, both now and in the
foreseeable future. The four threat effect
levels ranged from ‘‘no effect,’’ ‘‘small
effect,’’ ‘‘moderate effect,’’ and
‘‘significant effect’’ on the extinction
risk to the humphead wrasse. To allow
individuals to express a distribution of
risk scores in assessing the impacts of
the threats to the species, the ERA Team
adopted the ‘‘likelihood point’’
(FEMAT) method using 8 ‘‘likelihood
points’’ per Team member for the four
threat effect levels. A similar approach
has been used in previous NMFS status
reviews (e.g., Pacific salmon, Puget
Sound rockfish, Pacific herring, black
abalone, great hammerhead shark) to
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structure the Team’s thinking and
express levels of risk as a distribution in
assigning threat risk categories. The
scores were then tallied (frequency,
range, mode, and median) and
summarized for each threat, and
considered in making the overall risk
determination. The Team members also
expressed their certainty regarding
evidence of potential threats using a
ranking of low, medium, and high.
Guided by the results from the
demographics risk analysis as well as
the threats assessment, the ERA Team
members used their informed
professional judgment to make an
overall extinction risk determination for
the humphead wrasse now and in the
foreseeable future (up to 50 years). For
these analyses, the ERA Team defined
five levels of overall extinction risk: 1—
no risk, 2—low risk, 3—moderate risk,
4—high risk, and 5—very high risk.
Detailed definitions of these risk levels
can be found in the status review report.
Again, the ERA Team adopted the
FEMAT method, distributing 10
‘‘likelihood points’’ per Team member
among the five levels of extinction risk.
The scores were then tallied (frequency,
mode, and median for likelihood points,
and mean and range for certainty) and
summarized. The Team members again
expressed their certainty in a ranking of
low, medium, and high.
Finally, the ERA Team drew scientific
conclusions about the overall risk of
extinction faced by the humphead
wrasse under present conditions and in
the foreseeable future based on an
evaluation of the species’ demographic
risks and assessment of threats. The
Team did not make recommendations as
to whether the species should be listed
as threatened or endangered, or if it did
not warrant listing.
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Evaluation of Demographic Risks
Abundance
Currently, there are no formal
estimates of population size throughout
most of the humphead wrasse’s range. It
is known that this species is uncommon
to rare throughout most of its range, in
some cases exhibiting low abundance in
areas where no anthropogenic stressors
are evident. In the CNMI, for example,
humphead wrasses appear to be more
prevalent in the southern populated
islands, as compared to the mostly
uninhabited or lightly populated islands
north of Saipan. In this case, several
factors may influence humphead wrasse
abundance such as total habitat
availability, fishing access to humphead
wrasse due to island size and/or
orientation, and restrictions on fishing
effort.
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Declines in abundance appear to be
restricted to particular areas where the
LRFFT has been active for several
decades. In some areas where no
apparent harvest occurs, the species has
not demonstrated any notable changes
between surveys. One aspect lacking in
many fishery-independent surveys is
meaningful time series of observations
incorporating standardized
methodological protocols. Without such
time series, drawing firm conclusions
based on temporally and/or spatially
distinct observations is simply not
possible. In addition, surveyed locations
(i.e., exact locations, habitat type, water
depth) and methods (i.e., stationary
point count, towed-diver surveys) are an
important descriptor in survey work, as
not all areas where the humphead
wrasse exists are equally accessible for
underwater visual census surveys. In
other words, it is difficult to draw
conclusions on abundance from survey
results across different locations and
time frames.
Existing information suggests that
humphead wrasse populations are most
abundant and stable in the Indian
Ocean. However, populations in the
core-Coral Triangle area, where harvest
has been significant near population
centers, appear to remain depressed to
a degree that is not quantifiable.
There are ‘‘pockets’’ of abundance in
Malaysia (e.g., Pulau Layang Layang,
West of Sabah, and Pulau Sipadan, as
well as Hoga Island in Wakatobi Marine
National Park) where either military or
management protection exists (IUCN,
2008 citing TRACC, 2004). These
pockets of abundance in the core-Coral
Triangle area should be considered
crucial as important potential source
populations to other core-Coral Triangle
populations. However, density estimates
from these protected locations are at
least a decade old, and no recent
information is available to indicate that
these densities have remained stable,
although there is no reason to expect
otherwise, especially in designated
military bases, where access is assumed
to be extremely limited.
There are many other foreign and
domestic areas where the species has
been protected by fishing regulations or
reserves, and the species continues to be
observed throughout the Pacific
wherever surveyed. Recent relative
abundance data suggest that many
populations, especially those in U.S.
waters, are either stable, show no clear
trend, or may be increasing (Graham et
al 2014).
Based on the very limited abundance
information available and its natural
rarity, along with depressed population
sizes in the center of the species’ range
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due to overharvest, the ERA Team
concluded that the demographic factor
of abundance had a low-to-moderate
likelihood of contributing to the
humphead wrasse’s risk of extinction
now, and a moderate-to-high likelihood
of contributing to the risk of extinction
in the foreseeable future. The ERA Team
was concerned that the species’ low
abundance levels, whether natural or
manmade, may pose a risk to its
continued existence if faced with other
demographic risks or threats, such as
overutilization, because a species that is
already at naturally low levels may not
be able to withstand heavy fishing
pressure. Of the four demographic
factors, abundance was considered by
the ERA Team to pose the highest
demographic risk to the species. Risk
was found to be higher in the
foreseeable future than now simply
because the increased chance that
declines in abundance may become
more serious with the passage of time,
unless regulations are effective and
enforced. Certainty of abundance
affecting the risk of extinction to the
humphead wrasse now was deemed
medium; certainty of abundance
affecting the risk of extinction to the
humphead wrasse in the foreseeable
future was deemed low.
Growth Rate and Productivity
Regarding the effect of the humphead
wrasses’ growth rate and productivity
on its risk of extinction, the ERA Team
expressed less concern compared to
their concern for abundance. The
intrinsic rate of increase, or
productivity, is a complex function of
fecundity, survival rates, age at
maturity, and longevity of a species.
Productivity determines a species’
ability to recover from low numbers, if
extrinsic factors are not limiting, as well
as the level of harvest that can be taken
from a population sustainably (Hudson
¨
and Brautigam, 2007). For the
humphead wrasse, productivity is
estimated to be 0.72 per year
(Fishbase.org). This places the
humphead wrasse towards the slow end
of the slow-to-fast growth continuum of
reef fishes. While the humphead wrasse
may be more productive than other reef
fish that are highly exploited in the
LRFFT, such as the giant grouper
(Epinephelus lanceolatus), it is not as
productive as the leopard coral grouper
(Plectropomus leopardus) or the
mangrove red snapper (Lutjanus
argentimaculatus), two species which
are also highly exploited in the LRFFT.
The Team recognized that being towards
the slow end of the continuum creates
some extinction risk compared with fish
that grow faster. As such, the ERA Team
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concluded that the demographic risks of
growth rate and productivity pose a low
risk to the humphead wrasse’s
continued existence now and a
moderate risk in the foreseeable future.
Certainty of growth rate and
productivity affecting the risk of
extinction to the humphead wrasse now
was deemed medium; certainty in the
foreseeable future was deemed low.
Spatial Structure/Connectivity and
Diversity
The species’ population depends on
dispersal dynamics of individuals as
well as habitat quality and existing
spatial structure. Connectivity is
through spawning and planktonic larval
dispersal processes. Spatial structure
and genetic diversity are important as
they affect the species’ ability to survive
in diverse environments and enable the
population to respond to and survive
long-term environmental changes.
The humphead wrasse is known to
occur in waters around 48 countries,
from the Red Sea, east through the
tropical Indian and Pacific Oceans, to
French Polynesia. This geography
includes tens-of-thousands of islands
with diverse and varying bathymetry
(e.g., shallow coral reefs) along
mainland coasts, most within close
proximity and presumed easy dispersal
reach of pelagic larvae of this species.
Essentially very little is known
regarding the spatial structure and
genetic diversity of the humphead
wrasse. It is not known if there are any
manmade or ecological factors that
could significantly alter gene flow in the
species, nor is it known if the
humphead wrasse consists of more than
one population throughout its range or
if any genetically distinct populations
exist. Without definitive genetic
information, the Team assumed that the
species does not appear to be at risk of
a genetic bottleneck, meaning that the
humphead wrasse is likely able to adapt
overtime to changing environments.
Although data are either completely
lacking or inadequate, it can be
reasonably presumed that, across its
entire range, the characteristics of
spatial structure/connectivity and
genetic diversity, by themselves, are
unlikely to contribute to an extinction
risk for the humphead wrasse.
Therefore, the ERA Team concluded
that the demographic factor of spatial
structure and connectivity posed no-tolow risk to the humphead wrasse’s
continued existence both now and in
the foreseeable future, with certainty
deemed low for both timeframes. The
Team also concluded that diversity
posed a low risk to the humphead
wrasse’s continued existence both now
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and in the foreseeable future, with
certainty deemed low for both
timeframes.
Summary of Factors Affecting the
Humphead Wrasse
As described above, section 4(a)(1) of
the ESA and NMFS implementing
regulations (50 CFR part 424) state that
we must determine whether a species is
endangered or threatened because of
any one or a combination of the
following five ESA factors: (A) The
present or threatened destruction,
modification, or curtailment of its
habitat or range; (B) overutilization for
commercial, recreational, scientific, or
educational purposes; (C) disease or
predation; (D) inadequacy of existing
regulatory mechanisms; or (E) other
natural or man-made factors affecting its
continued existence. The ERA Team
evaluated whether and the extent to
which each of the foregoing factors
contributed to the overall extinction risk
of the global humphead wrasse
population. This section briefly
summarizes the ERA Team’s findings
and our conclusions regarding threats to
the humphead wrasse. More details can
be found in the status review report
(Graham et al., 2014).
(A) The Present or Threatened
Destruction, Modification, or
Curtailment of its Habitat or Range
The ERA Team evaluated habitat
destruction as a potential threat to the
humphead wrasse and found this threat
may have a small effect on the
extinction risk of the humphead wrasse
now, meaning that it is unlikely that it
is presently increasing the species’ risk
of extinction. In the foreseeable future,
the Team found that it is moderately
likely that this threat is increasing the
species’ extinction risk. Certainty of the
potential effects of habitat destruction
on the extinction risk of the species was
deemed medium for both now and in
the foreseeable future.
With regard to destructive fishing
practices, cyanide fishing is the major
practice that is used to target this
wrasse, although a relatively small
number of mostly small-sized fish of
this species might occasionally be killed
incidentally during blast fishing for
other reef fishes in open-reef
environments. The intent in using
cyanide is to stun juvenile wrasse and
capture them alive for subsequent growout for sale in the LRFFT; however,
some and perhaps a substantial
proportion of cyanide-fished wrasse die
prior to actually contributing product to
the industry. Cyanide fishing is still a
major fishing method in Southeast Asia,
but cyanide fishing is presently much
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less of a concern throughout the rest of
the Indo-Pacific region (Sadovy de
Mitcheson and Yin, in press), and thus
of less concern to the species
throughout its range. In addition to its
deleterious effects on humphead wrasse,
the cyanide released into and near the
reef substrate has substantial acute
mortality and delayed health effects on
other fishes in and near the reef and on
the non-fish motile, sessile, and other
biota including corals.
Regarding the loss and modification
of juvenile nursery areas, burgeoning
coastal development and poor land
management (e.g., sedimentation) in
developing tropical countries appears to
be the major threat to the seagrass and
branching coral and macroalgal habitats
that provide juvenile nursery habitat.
The cutting of mangroves for firewood
used to fuel open-fire cooking stoves is
another increasing problem reflecting
exponential human population growth
in many of these developing countries.
Approximately one-third of all
mangroves worldwide have been lost in
the past 50 years.
Regarding the loss and modification
of adult habitat, the major threat to the
primary habitat of forereef and openlagoons appears to be climate changeinduced coral bleaching and
acidification, both of which are
impacting corals and other organisms
with carbonate skeletons, although at
varying degrees according to
susceptibility. Although adult
humphead wrasses use caves and other
structures in rock and dead coral
limestone substrates to a great extent
and are not directly dependent on living
corals, humphead wrasses are most
numerous near abundant live coral.
Moreover, in geological time even
consolidated dead coral limestone
substrates will decline because of
weathering if the replenishment rates of
stony corals decline. Concern over this
factor and coastal development over a
longer term was influential in the
conclusion that habitat loss could have
moderate effects on extinction risk in
the foreseeable future.
Based on the best available
information, we do not find that habitat
destruction, modification, or
curtailment are threats that are
presently, or in the foreseeable future,
placing the species at an increased risk
of extinction. Cyanide has recently been
banned in a number of countries
throughout the species’ range, and
illegal use appears to be waning and is
much less of a concern outside of the
Coral Triangle region. The magnitude of
direct and indirect threats to juvenile
and adult habitats is variable with no
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evidence of substantial or widespread
habitat loss or destruction.
(B) Overutilization for Commercial,
Recreational, Scientific or Educational
Purposes
The ERA Team identified
overutilization as a threat with a smallto-moderate effect on the extinction risk
of the humphead wrasse now, and a
moderate effect on the extinction risk to
the species in the foreseeable future.
Certainty of the potential effects of
overutilization on the extinction risk of
the species was deemed medium for
now and low for the foreseeable future.
Estimates of overutilization have been
hampered by a dearth of information
regarding landings data and illegal,
unregulated, and unreported fishing.
Fisheries that land humphead wrasse
appear to lack detailed temporal
information pertaining to fishing effort,
fishing power, harvest location, seasonal
changes in landings, as well as the
institution of management protocols.
For example, IUCN (2008) notes a 10fold decrease in market landings from
Palau from the mid 1980s to mid-1990s,
though fails to note that scuba
spearfishing was banned in the early
1990s and may be directly linked to that
stated decline. Although declines in
landings were noted in some
jurisdictions, information indicating no
changes in landings is either not noted
or not available. This may be a result of
humphead wrasse representing a minor
component of most coral reef fisheries
throughout its range because of its
natural rarity.
Anecdotal evidence, in particular
from within LRFFT participating
countries, indicates that areas where at
some past time period humphead
wrasses were observed to have been
present in naturally low densities are no
longer found since the start of the
LRFFT.
Although overutilization appears to
be an issue in some jurisdictions and
locales (e.g., core-Coral Triangle area)
(Sadovy et al., 2003a; IUCN, 2008),
amounting to moderate effects on
extinction risk now and in the
foreseeable future, it cannot be
considered a significant or overriding
impact on the species throughout its
entire range in either time frame. In
jurisdictions where scuba spearfishing
has been banned (Fiji, Palau, the U.S.
jurisdictions of American Samoa and
CNMI), there is reasonable expectation
that older and larger fish benefit from
depth refugia. In the CNMI, scuba
spearfishing is banned; it is still
permitted in Guam. As a result, there
exists considerable disparity in the size
frequency distributions of landed
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humphead wrasse between the
jurisdictions, which falls in line with
the conclusions of Lindley et al. (2014)
that the banning of scuba spearfishing
results in depth refugia for many coral
reef fish species.
While there is some concern for
overutilization of the species,
particularly for commercial purposes
resulting in population declines in some
areas such as the Coral Triangle region,
the current evidence indicates that
many populations are either stable,
show no clear trend, or may be
increasing. The current global
population size is likely sufficient to
maintain population viability into the
foreseeable future. Based on the best
available information, we do not find
that overutilization of the species is
presently, or in the foreseeable future,
placing the species at an increased risk
of extinction.
(C) Disease or Predation
The ERA Team evaluated disease and
predation as potential threats to the
humphead wrasse, but noted that
available information on either threat is
sparse. The ERA Team found that the
little information available indicates
that this threat may have a small effect
on the extinction risk of the species,
meaning that it is unlikely that disease
or predation are increasing the
extinction risk to the species, either now
or in the foreseeable future. Certainty of
the potential effects of disease or
predation on the extinction risk of the
species was deemed medium for both
time frames.
Very little is known about diseases of
the humphead wrasse other than fish
leech infestation (Hirundinea spp.),
parasitic infestations (protozoa, worms,
etc.), and bacterial infections that have
been documented. Parasitic infestations
have been reported as occurring in the
fins, gill operculum, body surface, eyes,
and mouth cavity (Koesharyani et al.,
2005; Zafran et al., 2005). Zafran et al.
(2005) report that cryptocaryoniosis, or
white spot disease because it causes
numerous white spots on the body
surface, is the most dangerous parasitic
disease in many marine fishes in
aquaria or mariculture facilities. This
disease, which can spread rapidly to
other healthy fish and lead to a high
mortality, has been documented at the
Gondol Research Station in Indonesia.
The Gondol Research Station has also
reported the presence of the parasitic
disease oodiniasis (Amyloodinium
ocellatum, a dinoflagellate protozoan)
infecting captive humphead wrasse at
their facility (Zafran et al., 2005), as well
as capsalid monogenean, or so-called
skin flukes, which are the most common
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external parasites in mariculture finfish
(Koesharyani et al., 2005). Vibriosis, the
most common bacterial disease in
marine finfish, has also been
documented in broodstock and young
humphead wrasse at the Gondol
Research Station. The infected fish were
those that were captured with cage traps
and transported to the station; mortality
occurred within a week after the
transportation (Zafran et al., 2005).
Wada et al. (1993) documented the
first known report of a simultaneous
infection with an acid-fast bacterium
(Mycobacterium sp.) and an imperfect
fungus in a humphead wrasse that was
captured in Indonesia and reared in a
commercial fish dealer’s concrete
aquarium in Japan. They speculate that
the male fish became infected while in
captivity. No other information has been
found to indicate that disease,
particularly in the wild, is a factor
influencing mortality of humphead
wrasse.
There are no known major predators
of adult humphead wrasse, even in
vulnerable locations such as at
spawning aggregations. Colin (2010)
reports that no instances of predation on
spawning adults were observed despite
the presence of grey reef (Carcharhinus
amblyrhynchos) and white tip
(Trianodon obesus) reef sharks.
Additionally, few other piscivorous reef
fishes are capable of taking even a
moderate-sized humphead wrasse
(Colin, 2010). The predators of juvenile
humphead wrasse are unknown but
likely to be sharks and other largebodied piscivorous species such as
grouper (Serranidae), Jacks (Carangidae),
and snapper (Lutjanidae) that are
commonly found on Indo-Pacific coral
reefs.
Based on the best available
information, we agree that neither
disease nor predation is increasing the
species’ extinction risk presently, or in
the foreseeable future.
(D) The Inadequacy of Existing
Regulatory Mechanisms
The ERA Team evaluated existing
regulatory mechanisms to determine
whether they may be inadequate to
address threats to the humphead wrasse.
Existing regulatory mechanisms may
include Federal, state, and international
regulations. Below is a brief description
and evaluation of current and relevant
domestic and international management
measures that affect the humphead
wrasse. More information on these
domestic and international management
measures can be found in the status
review report (Graham et al., 2014).
Across the wide Indo-Pacific range of
the humphead wrasse, there exists a
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diversity of regulations. In U.S. waters,
most jurisdictions have regulations that
afford partial to complete protection for
the species, and these are, in general,
reliably enforced. These include Federal
annual catch limits based on what little
is known of abundance, prohibitions on
non-selective and destructive fishing
gear (e.g., American Samoa and CNMI
both ban scuba spearfishing, while
Guam presently does not but is
considering such a ban), an assortment
of no-take marine protected areas
(MPAs) around CNMI and Guam, and
full prohibition on take around
American Samoa and the Pacific Remote
Island Areas.
Internationally, of the 48 countries
where humphead wrasses occur, only
about 18 have implemented regulations.
This lack of consistent regulation may
be due to abundance data being
unknown, undocumented, or not
attended to (e.g., Cambodia, Egypt,
Kenya, Saudi Arabia, Somalia, Sudan,
etc.), or the country does not participate
in the legal international trade (e.g.,
Djibouti, Eritrea, Israel, Madagascar,
Mayotte, Myanmar). Of countries that
have regulations, most prohibit nonselective and destructive gear types,
regulate minimum size limits,
significantly reduce or ban export
quotas, and/or have tightened
enforcement loopholes—all within the
last few years (Gillett, 2010; Sadovy,
2010; IUCN, 2013; Sadovy,
unpublished). Only 12 countries are
known to participate (or have
participated) in the legal trade of the
species, while the number of countries
participating in the illegal trade is
unquantified. International regulation
and effectiveness was the primary
concern in finding that inadequate
existing regulations have a moderate
effect on extinction risk of the species.
Other international regulatory
authorities include CITES, which lists
the humphead wrasse under Appendix
II with the following provisions: Legal
trade is regulated, an export permit is
required to show fish were legally
acquired and harvesting is not
detrimental to survival of the species,
and the exporting country must have a
functional management plan and
associated monitoring. In addition, the
importing country must closely monitor
its imports. Sanctions or complete bans
on exports provide strong incentive to
comply. Additionally, the IUCN lists the
humphead wrasse as ‘‘endangered’’
while affording no regulatory
protection; the hope is to promote
awareness of the status of the species.
As previously mentioned, 12
countries report legally trading the
species, ranging from live humphead
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wrasse to bodies, derivatives, and meat;
of these 12 countries, only 10 countries
report exporting live humphead wrasse.
According to CITES (2014) trade data,
from 2005–2011, 81,848 live humphead
wrasse were legally traded by 10
countries, whereas in 2012, only 1,691
live humphead wrasse were legally
traded, and only by 5 of the countries.
Zero bodies, meat, or derivatives of the
species were traded in 2012 (CITES,
2014).
Legal trade has significantly
decreased due to reduced or zero export
quotas, especially from the main
exporting countries of Indonesia,
Malaysia, and the Philippines. For
example, Indonesia decreased their
export quota of humphead wrasse from
8,000 in 2005 to 1,800 in 2012 (IUCN,
2013), and legally traded only 1,653 in
2012 (CITES, 2014). In 2010, Malaysia
reached and has maintained a zero
export quota of the species (Sadovy,
2010; IUCN, 2013; CITES, 2014). This is
significant since Malaysia legally
exported ∼53,000 live humphead wrasse
from 2007–2009 (CITES, 2014).
Moreover, Hong Kong is now believed
to be better controlling trade where it
checks imports and re-exports, and
coordinates verification of permits with
Malaysia and Indonesia (Sadovy, 2010).
Additionally, countries that formerly
exported for the LRFFT have now
banned the export of the species (e.g.,
Australia, Federated States of
Micronesia, New Caledonia, Niue, and
Palau) (Gillett, 2010). In other countries,
national regulations have been tightened
(e.g., Palau and Fiji), helping to close
enforcement loopholes (Sadovy, 2010).
In Indonesia, recent field surveys at
seven ‘‘baseline’’ sites found increased
densities of humphead wrasse at four
sites 4–5 years later. Most fish were
juveniles, but the increase in numbers is
encouraging and has occurred in areas
where fishing pressure has evidently
declined (IUCN, 2013). At least a decade
is believed to be a conservative time
scale for these heavily exploited
populations to begin recovery from
fishing pressure following adequate
protection (Colin, 2010).
In the geographic center of the
species’ range—the Coral Triangle
Region—the humphead wrasse is one of
the most valuable species in the LRFFT,
and has been for the past few decades.
Countries within the Coral Triangle
region are characterized by large and
growing populations, particularly in
coastal areas, where many consider
fishing an occupation of last resort.
Many nearshore fish stocks are heavily
harvested, and recent declines in
humphead wrasse landings probably
reflect this fact more so than
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effectiveness of new regulations. In
areas of this region where the LRFFT is
not currently operating, any catch of
this species would bring a good price at
local markets. Local regulations to
manage the trade that are contradictory
to national regulations also exist in the
area and where illegal export is
reportedly rampant (e.g., Philippines).
Misreporting continues to be an
illegal, unregulated, and unreported
fishing issue for the LRFFT in Southeast
Asia, including mislabeled fish or fish
hidden in exports (CITES, 2010a; CITES,
2010b; Sadovy et al., 2011).
Undocumented shipments continue
through Singapore. However, Hong
Kong, the largest importer, has recently
committed to controlling imports, reexports, and possession within the
territory, thus enabling a more secure
system of trade (CITES, 2010a).
Additionally, most countries ban the
use of cyanide, though it does continue
in areas due to lack of enforcement and
corruption (Erdman and Pet-Soede,
1997; Pet and Pet-Soede, 1999; Yan,
2011).
Numerous MPAs exist throughout the
range of the humphead wrasse. If
adequately enforced, these sufficiently
large MPAs might help reduce threats
from the loss and modification of adult
or juvenile habitat, destructive fishing
practices, and overutilization. For
example, in areas including Australia,
Maldives, and Wake Atoll where some
degree of protection for the species is
afforded (e.g., take and possession
prohibited, ban on exports, etc.) and
adequately enforced, the risk of local
‘‘stock’’ depletion has been reduced and
abundance of humphead wrasse in the
area is stable or increasing (Sadovy et
al., 2003 citing Sluka, 2000; NMFS
PIFSC CRED, unpublished data).
In summary, when considered across
the entire range of the species, it is
reasonably likely that the various
existing regulatory measures will
continue to benefit the humphead
wrasse globally by appreciably reducing
the threats to the species, presuming
they are adequately enforced. The
greatest threat—the LRFFT—appears to
have decreased substantially, according
to recent CITES trade data available
through 2012 (CITES, 2014). This
reduction in legal trade may be due to
either reduced or zero export quotas, or
reduced population sizes of humphead
wrasse stocks within the three main
exporting countries of Indonesia,
Malaysia, and Philippines. It can be
hoped that with time more countries
will follow suit, implement, and
effectively enforce regulatory
mechanisms to prevent the decline of
the species and allow any overexploited
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populations to rebuild. However, it is
believed that much illegal and
unreported trade still continues,
particularly in the several countries of
the Coral Triangle region. In spite of
local pockets of questionable regulatory
compliance, we agree that based on the
best available information, it is unlikely
that inadequate existing regulatory
mechanisms alone contribute more than
moderately to the extinction risk for the
humphead wrasse across its wide IndoPacific range either now, or in the
foreseeable future. The recent
implementation of, increased adherence
to, and enforcement of existing
regulatory mechanisms throughout the
species’ range appear effective in
addressing the most important threat to
the species, which is overharvest.
Certainty of the potential effects of
inadequate existing regulatory
mechanisms on the extinction risk of
the species was deemed medium for
now and low in the foreseeable future.
Accordingly, we do not find that
inadequacy of existing regulatory
mechanisms is presently, or in the
foreseeable future, placing the species at
an increased risk of extinction.
(E.) Other Natural or Manmade Factors
Affecting Its Continued Existence
The Status Review Report describes
the life history characteristics,
information on competition, and
substantial concerns with regard to
climate change and pollution
considered by the ERA Team. The Team
concluded that other natural or
manmade threats would likely have
some small effects on the extinction risk
of the species now and moderate effects
over the foreseeable future, the latter
due to concerns of increased climate
change and pollution-related impacts on
the species. Certainty of the potential
effects of other natural or manmade
factors on the extinction risk of the
species was deemed medium for now
and low in the foreseeable future.
The humphead wrasse may be
susceptible to natural and human
perturbations due to particular life
history characteristics that include slow
growing, long-lived, and delayed
reproductive development (Choat et al.,
2006; Tupper, 2007; Sadovy de
Mitcheson et al., 2008; Colin, 2010).
Additionally, adults often occupy
consistent home ranges, have
predictable sleeping sites, have discrete
spawning locations, and may form mass
aggregations during spawning (Sadovy
et al., 2003a).
As for competition with other species
for prey, humphead wrasses are
opportunistic diurnal carnivores with a
wide-ranging diet. As previously
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mentioned, much of its prey is found in
sand or rubble habitats where it feeds on
a variety of molluscs, small fishes such
as gobies, moray eels, sea urchins,
crustaceans, brittle stars, starfish, and
other invertebrates (Randall et al., 1978;
Myers, 1989; Randall et al., 1997;
Thaman, 1998; Sadovy et al., 2003a;
Choat et al., 2006). As generalists, the
humphead wrasse is less susceptible to
competition for prey from other
predators or fisheries with more
specialized diets.
Large-scale impacts such as global
climate change may pose a threat to the
humphead wrasse because the species
uses inshore habitats and coral reefs out
to depths of up to at least 100 m
(Randall, 1978; Sadovy et al., 2003a;
Russell, 2004; Zgliczynski et al., 2013).
The Status Review Report describes the
potential threats, including ocean
acidification, increased ocean
temperatures, sea level rise, and extreme
weather, in detail. These threats are
summarized below.
Although the impacts of ocean
acidification specifically to humphead
wrasse are unknown, the threat is
anticipated to be greatest to marine taxa
that build skeletons, shells, and tests of
biogenic calcium carbonate such as
coral (e.g., Fabry et al., 2008; Guinotte
and Fabry, 2008; Pandolfi et al., 2011).
In a meta-analysis, abundances of
species reliant on live coral for food or
shelter consistently declined (e.g.,
Wilson et al., 2006; Pratchett et al.,
2008), while abundance of some species
that feed on invertebrates, algae and/or
detritus increased (e.g., Wilson et al.,
2006). As previously discussed,
branching corals are one of several
important habitats to various stages of
the humphead wrasse life cycle.
Vulnerability of a coral species to a
threat is a function of susceptibility and
exposure, considered at the appropriate
spatial and temporal scales. With regard
to localized variability, recent papers
identify various mechanisms that can
offset or buffer changes in seawater pH
around coral reefs from ocean
acidification, such as photosynthetic
uptake of CO2 by sea grasses and
macroalgae in adjacent areas (Palacios
and Zimmerman, 2007; Manzello et al.,
2012; Anthony et al., 2013), and
biogeochemical processes within coral
reef communities (Andersson et al.,
2013). Other papers identify
mechanisms that can exacerbate
changes in seawater pH around coral
reefs from ocean acidification, such as
diurnal variability, that can amplify CO2
in seawater around coral reefs (Shaw et
al., 2013). Ultimately, the future effects
of ocean acidification on coral reefs will
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be highly variable across coral taxa,
space, and time.
Other direct and indirect linkages of
ocean acidification effects to the
humphead wrasse remain tenuous. The
adult humphead wrasse does not appear
to be food limited or space limited in
any portions of its range. The species
also appears to be adaptable to a variety
of biotic and abiotic conditions given its
wide geographic range and observations
of it residing (foraging, sleeping) in both
shallow and deep water. Additionally,
some researchers have pointed out that
increased CO2 (lower pH) leading to
ocean acidification could enhance
seagrass productivity (Palacios and
Zimmerman, 2007; Guinotte and Fabry,
2008; Poloczanska et al., 2009), which
may benefit juvenile humphead wrasse
that rely on seagrass beds as nursery
areas.
Increased ocean temperatures on large
spatial and temporal scales could
generally impact current flow,
productivity, physiological performance
and behavior of coral reef fishes and
survival of corals. For example, larval
production and survival rates could be
negatively impacted (e.g., Lo-Yat et al.,
2010). However, small temperature
increases might accelerate larval
development and competency to settle,
though larger temperature increases may
be detrimental (Munday et al., 2008).
Brainard et al. (2011) discusses how
coral adaptation and acclimatization to
increased ocean temperatures is
possible; that there is intra-genus
variation in susceptibility of coral to
bleaching, ocean acidification, and
sedimentation; that at least some coral
species have already expanded their
range in response to climate change; and
that not all coral species are seriously
affected by ocean acidification. Such
adaptation and acclimation could
reduce the impact of warming
temperatures and allow populations to
persist across their current range
(Donelson et al., 2011; Logan et al.,
2013). The exceptional complexity,
extent, and diversity of coral reef habitat
defy simplistic modeling of reef
responses to climate change threats.
Likewise, many aspects of the biology of
reef-building corals contribute to
complex responses to ocean warming.
This includes capacity for
acclimatization and adaptation to ocean
warming, range expansion in response
to ocean warming (Yamano et al., 2011;
Yara et al., 2011), and contrasting
ecological interactions resulting from
ocean warming (Hughes et al., 2012;
Cahill et al., 2013). All of these
contribute to highly variable, complex
and uncertain responses of reef-building
coral species and in turn, coral reefs to
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climate change threats like ocean
warming.
The impacts of sea level rise to coral
reef ecosystems also remains uncertain.
Theoretically, a rise in sea level could
potentially provide additional habitat
for corals living near the sea surface.
There are now studies documenting that
during periods of higher water levels,
coral cover increases on reef flats
´
(Brown et al., 2011; Scopelitis et al.,
2011). On the other hand, if coral
growth is unable to keep pace with sea
level rise, there will most likely be
negative consequences.
As for the effects of climate change to
prey species of the humphead wrasse,
direct and indirect effects are again
variable and complex. Climate change
can affect marine organisms both
directly via physiological stress and
indirectly via changing relationships
among species (Harley, 2011). Shifts in
distribution and abundance of prey can
potentially be driven by changes in
temperature and ocean chemistry
(Harley et al., 2006). Although
humphead wrasses do not feed directly
on corals, many of their prey do rely on
corals, sea grass beds, or mangroves for
their own food or shelter. The wide
variety of humphead wrasse prey is
found in various habitats and across a
vast depth range of a few meters to at
least 100 m. Coral communities found at
greater depths have shown thermal
refuge from increased temperatures
while those found in more shallow areas
are more impacted (e.g., Graham et al.,
2008; Bridge et al., 2014). For example,
sea urchin fertilization may be
compromised by warmer temperatures
(Byrne et al., 2009). While urchins
found in more shallow areas may have
reduced or compromised fertilization
and development, urchins found at
deeper depths may be less impacted.
Urchins are also less susceptible to
increased ocean acidification (Byrne et
al., 2009). In another example of
variable impacts, Harley (2011)
conducted an experiment and found
that prey species were able to occupy a
hot, extralimital site if predation
pressure was experimentally reduced.
As a result, local species richness more
than doubled, suggesting that
anthropogenic climate change can alter
interspecific interactions and produce
unexpected changes in species
distribution, community structure, and
diversity (Harley, 2011). Overall, some
humphead wrasse prey may likely be
negatively impacted by climate change;
however, not all prey will be impacted
equally. Given that humphead wrasse
are foraging generalists and feed on a
wide variety of prey found in various
habitats and depths, impacts are likely
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to be less than if they were foraging
specialists like other reef fish species
(i.e., bumphead parrotfish) that feed
primarily on corals.
In summary, the extent of potential
direct and indirect effects of climate
change on the humphead wrasse are
unknown or speculative as the threats
described in the literature are broad and
general, and typically use another
species as a proxy to infer vulnerability.
Lastly, contaminants such as fuel and
crude oil from spills, land-based
pollution from agriculture, etc. that find
its way into the marine environment,
sewage effluent from areas with
insufficient sanitation systems, and
marine debris from discarded or lost
fishing gear are all potential sources of
pollution that could directly and
indirectly affect the humphead wrasse.
However, such events including oil and
sewage spills are typically episodic and
localized. Other types of pollution such
as land-based contaminants and marine
debris may also impact the humphead
wrasse, but the direct extent of the
effects to the humphead wrasse and its
habitat are speculative at this time. As
such, the Team determined that these
other natural and manmade factors
collectively would likely have some
small effects on the extinction risk of
the species now and moderate effects
over the foreseeable future.
Therefore, based on the best available
information, although the Team
identified the threat of other natural or
manmade factors, such as climate
change and pollution, as having a smallto-moderate effect on the species’ risk of
extinction, we do not find that other
natural or manmade factors are
presently, or in the foreseeable future,
placing the species at an increased risk
of extinction.
Significant Portion of Its Range
The definitions of both ‘‘threatened’’
and ‘‘endangered’’ under the ESA
contain the term ‘‘significant portion of
its range’’ (SPOIR) as an area smaller
than the entire range of the species that
must be considered when evaluating a
species’ risk of extinction. With regard
to SPOIR, the Services proposed a
‘‘Draft Policy on Interpretation of the
Phrase ‘Significant Portion of Its Range’
in the Endangered Species Act’s
Definitions of ‘Endangered Species’ and
‘Threatened Species’ ’’ (76 FR 76987;
December 9, 2011), which is consistent
with our past practice as well as our
understanding of the statutory
framework and language. The Draft
Policy was recently finalized on July 1,
2014, (79 FR 37578), and the Services
are now to consider the interpretations
and principles contained in the Final
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Policy as binding guidance in making
individual listing determinations, while
taking into account the unique
circumstances of the species under
consideration. However, the policy
remained in the draft form when the
ERA Team discussed whether the data
indicated if any portion of the
humphead wrasse’s range is more
significant than another portion.
The ERA Team considered whether a
portion of the species’ range is more
important than any other portion, and
that without that portion, the species
would be in danger of extinction. With
this in mind, the ERA Team agreed that
of the entire range of the species, the
primary region that has exhibited a
decline of the humphead wrasse, which
comprises the three countries in the
core-Coral Triangle area, might meet the
definition of a SPOIR. These countries
are Indonesia, Malaysia, and the
Philippines, and have large and growing
human populations with coincident
agricultural expansion and coastal
development impacts on humphead
wrasse habitat. As this area is the center
of the species’ range, the Team also
discussed physical, ecological, and
behavioral factors in relation to
recruitment between the potential
SPOIR area and the rest of the species’
range. The Team concluded that local
extinction of humphead wrasse in these
three countries would not cause the
remainder of the species to become in
danger of extinction. Islands and
archipelagoes outside the core-Coral
Triangle area (i.e., Papua New Guinea
and the Solomon Islands in the east or
Australia to the south) are
comparatively healthy with fewer
impacts to the species. Humphead
wrasse in these other areas are not
dependent on aggregations in Indonesia,
Malaysia, or the Philippines for larval
recruitment or other aspects of survival;
in fact, the ERA Team concluded that
these nearby areas could provide
recruits to recolonize the core-Coral
Triangle portion of the range in the
event that local extirpations were to
occur inside that area. Thus, the status
of the rest of the species was not
considered to be dependent on the
continued existence of the population in
these three countries of Indonesia,
Malaysia, and the Philippines. The main
purpose for improved conservation in
this core area of the species’ range
would be the recovery of the
populations located there, and not the
status of the rest of the population.
Therefore, after a review of the best
available information, the ERA Team
concluded, and we agree, that data do
not indicate any portion of the
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humphead wrasse’s range meets the
definition of a SPOIR. As such, when
considering the overall extinction risk of
the species, we considered it throughout
the species’ entire range.
Under the Final SPOIR Policy, the
definition of ‘‘significant’’ has been
revised to a lower threshold and now
states ‘‘A portion of the range of a
species is ‘significant’ if the species is
not currently endangered or threatened
throughout its range, but the portion’s
contribution to the viability of the
species is so important that, without the
members in that portion, the species
would be in danger of extinction or
likely to become so in the foreseeable
future, throughout all of its range’’
(emphasis added). Despite this revision,
we continue to find that the data do not
indicate any portion of the humphead
wrasse’s range meets the definition of a
SPOIR. Thus, the overall extinction risk
of the species is considered throughout
the species’ entire range.
Overall Risk Summary
As a final step in their analysis, the
ERA Team voted on the overall risk of
extinction to the humphead wrasse
based on the information the Team
reviewed in its demographic risk
analysis, as modified by the information
reviewed in the threats assessment.
Likelihood points attributed to the
current level of extinction risk
categories were as follows, with the first
number representing the total votes by
Team members and the second number
representing the total possible votes,
which was 40: No Risk (25/40), Low
Risk (13/40), Moderate Risk (2/40).
None of the Team members placed a
likelihood point in either the ‘‘High
Risk’’ or ‘‘Very High Risk’’ categories,
indicating their strong consensus that
the species is not currently at a high or
very high risk of extinction. Thus, the
Team found, and we agree, that the
species is not presently at risk of
extinction. The Team expressed this
view with a high relative certainty with
regard to the available information.
For the level of extinction risk of the
humphead wrasse in the foreseeable
future, the ERA Team found, and we
agree, that the species would be at low
overall risk of extinction. Likelihood
points attributed to each risk category in
the foreseeable future were as follows:
No Risk (15/40), Low Risk (18/40),
Moderate Risk (7/40). Again, none of the
Team members placed a likelihood
point in either the ‘‘High Risk’’ or ‘‘Very
High Risk’’ categories, indicating their
strong consensus that the species will
not be at a high or very high risk of
extinction in the foreseeable future. The
Team viewed the certainty of
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information for the foreseeable future as
being low.
Overall, there was a high degree of
consensus among the members of the
Team, and we agree, that the humphead
wrasse’s risk of extinction presently and
in the foreseeable future is no-to-low
risk. Although the humphead wrasse is
naturally rare throughout its range and
in some places abundance has declined,
this no-to-low risk of extinction is based
primarily on the species’ sustained
widespread distribution throughout
most of its known range, and its recent
effective protection from exploitation at
a variety of localities under both U.S.
and foreign jurisdiction.
Final Determination
Section 4(b)(1) of the ESA requires
that NMFS make listing determinations
based solely on the best scientific and
commercial data available after
conducting a review of the status of the
species and taking into account those
efforts, if any, being made by any state
or foreign nation, or political
subdivisions thereof, to protect and
conserve the species. We have
independently reviewed the best
available scientific and commercial
information including the petition,
public comments submitted on the 90day finding (78 FR 13614; February 28,
2013), the status review report (Graham
et al., 2014), and other published and
unpublished information, and have
consulted with species experts and
individuals familiar with humphead
wrasse. We considered each of the five
ESA statutory factors to determine
whether it presented an extinction risk
to the species on its own. Additionally,
we do not find that the combination of
factors poses an extinction risk. As
required by the ESA, section 4(b)(1)(a),
we also took into account efforts to
protect humphead wrasse by territories,
foreign nations, and others and
evaluated whether those efforts provide
a conservation benefit to the species. As
previously explained, no portion of the
species’ range is considered significant
and we did not find biological evidence
that would indicate that any population
segment of the humphead wrasse would
qualify as a DPS under the DPS Policy.
Therefore, our determination set forth
below is based on a synthesis and
integration of the foregoing information,
factors and considerations, and their
effects on the status of the species
throughout its entire range.
We conclude that the humphead
wrasse is not presently in danger of
extinction, nor is it likely to become so
in the foreseeable future throughout all
of its range. We summarize the factors
supporting this conclusion as follows:
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(1) The species is made up of a single
population over a broad geographic
range, with no barrier to dispersal; (2)
its current range is unaltered from the
range identified by surveys since the
1970s and although there are some
concerns related to the species’ habitat,
there is no evidence of substantial or
widespread habitat loss or destruction;
(3) although the species has predictable
home ranges and sleeping sites, and
possesses life history characteristics that
may increase its vulnerability to impacts
of fishing in reef fish assemblages, its
risk of extinction due to low
productivity is not of significant
concern; (4) the best available
information indicates that abundance is
naturally low across the species’ range,
and although populations have declined
in some areas because of fishing
mortality, many populations, especially
those in U.S. waters, are either stable,
show no clear trend, or may be
increasing; (5) although there is no
formal estimate on the current global
population size, it is likely sufficient to
maintain population viability into the
foreseeable future; (6) the main threat to
the species is overutilization in the live
reef food fish trade; however, legal trade
of the species has decreased
substantially over recent years due to
reduced or zero export quotas,
especially from the three main exporting
countries within the Coral Triangle
region; (7) there is no evidence that
disease or predation is contributing to
increasing the risk of extinction of the
species; (8) recent implementation of,
increased adherence to, and
enforcement of existing regulatory
mechanisms throughout the species’
range appear effective in addressing the
most important threat to the species
(overharvest); and (9) although there is
some concern with regard to effects
from other natural or manmade factors,
such as climate change and pollution,
the evidence does not suggest that the
species is at risk of extinction from
these factors.
Based on these findings, we conclude
that the humphead wrasse is not
presently in danger of extinction
throughout all or a significant portion of
its range nor is it likely to become so
within the foreseeable future.
Accordingly, the humphead wrasse does
not meet the definition of a threatened
or endangered species and therefore the
humphead wrasse does not warrant
listing as threatened or endangered at
this time. However, it will remain on
our Species of Concern list and we will
encourage research on the status of the
species for use in future status reviews.
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Federal Register / Vol. 79, No. 187 / Friday, September 26, 2014 / Notices
References
A complete list of all references cited
herein is available upon request (see FOR
FURTHER INFORMATION CONTACT).
Authority
The authority for this action is the
Endangered Species Act of 1973, as
amended (16 U.S.C. 1531 et seq.).
Dated: September 22, 2014.
Samuel D. Rauch, III.,
Deputy Assistant Administrator for
Regulatory Programs, National Marine
Fisheries Service.
[FR Doc. 2014–23034 Filed 9–25–14; 8:45 am]
BILLING CODE 3510–22–P
DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric
Administration
RIN 0648–XD517
Fisheries of the South Atlantic; South
Atlantic Fishery Management Council
(SAFMC); Public Meeting
National Marine Fisheries
Service (NMFS), National Oceanic and
Atmospheric Administration (NOAA),
Commerce.
ACTION: Notice of a public meeting.
AGENCY:
The South Atlantic Fishery
Management Council (Council) will
hold a Visioning Workshop, October
14–16, 2014 in North Charleston, SC.
DATES: The workshop will be held 1
p.m.–5 p.m., Tuesday, October 14, 2014;
8:30 a.m.–5 p.m., Wednesday, October
15, 2014; and 8:30 a.m.–3 p.m.,
Thursday, October 16, 2014. Public
comment will be held 4:30 p.m.–5 p.m.,
Tuesday, October 14, 2014; 4:30 p.m.–
5 p.m., Wednesday, October 15, 2014;
1:30 p.m.–2 p.m., Thursday, October 16,
2014.
ADDRESSES:
Meeting address: Crowne Plaza
Charleston Airport-Convention Center,
4381 Tanger Outlet Boulevard, N.
Charleston, SC 29418; telephone: (843)
744–4422.
Council address: South Atlantic
Fishery Management Council, 4055
Faber Place Drive, Suite 201, N.
Charleston, SC 29405.
FOR FURTHER INFORMATION CONTACT: Kim
Iverson, Public Information Officer,
4055 Faber Place Drive, Suite 201, North
Charleston, SC 29405; telephone: (843)
571–4366 or toll free (866) SAFMC–10;
fax: (843) 769–4520; email:
kim.iverson@safmc.net.
SUPPLEMENTARY INFORMATION: This
workshop is being held for Council
members to discuss the further
mstockstill on DSK4VPTVN1PROD with NOTICES
SUMMARY:
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development of a Vision Blueprint
(long-term strategic plan) for the South
Atlantic snapper grouper fishery. The
outcome of the workshop will consist of
a draft Vision Blueprint document
outlining strategic goals, objectives, and
strategies for managing the snapper
grouper fishery going forward. The draft
document will be provided to the
Council at the December 2014 Council
meeting and then open for public
comment. Topics of discussion include:
1. Visioning exercise to develop key
concepts for each sector of the
snapper grouper fishery.
2. Breakout Group Discussion to
develop strategies on key topics to
include:
a. Sub-regional Management
b. Reporting/Data Collection
c. Reducing Discards
d. Access to the Fishery
e. Stakeholder Engagement
f. Habitat/Ecosystems
g. Allocation
3. Plenary session to summarize
breakout group discussions, and
4. Public Comment/Outreach
Approaches for draft Vision
Blueprint.
Although non-emergency issues not
contained in this agenda may come
before these groups for discussion, those
issues may not be the subject of formal
action during these meetings. Action
will be restricted to those issues
specifically listed in this notice and any
issues arising after publication of this
notice that require emergency action
under section 305(c) of the MagnusonStevens Act, provided the public has
been notified of the Council’s intent to
take final action to address the
emergency.
Special Accommodations
This meeting is accessible to people
with disabilities. Requests for auxiliary
aids should be directed to the SAFMC
office (see ADDRESSES) at least 5
business days prior to the meeting.
Note: The times and sequence specified in
this agenda are subject to change.
Authority: 16 U.S.C. 1801 et seq.
Dated: September 23, 2014.
Tracey L. Thompson,
Acting Deputy Director, Office of Sustainable
Fisheries, National Marine Fisheries Service.
[FR Doc. 2014–22957 Filed 9–25–14; 8:45 am]
BILLING CODE 3510–22–P
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57887
DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric
Administration
RIN 0648–XD518
Western Pacific Fishery Management
Council; Public Meetings
National Marine Fisheries
Service (NMFS), National Oceanic and
Atmospheric Administration (NOAA),
Commerce.
ACTION: Notice of public meetings and
hearings.
AGENCY:
The Western Pacific Fishery
Management Council (Council) will
hold meetings of its 117th Scientific and
Statistical Committee (SSC) and its
161st Council meeting to take actions on
fishery management issues in the
Western Pacific Region. The Council
will also convene meetings of the
Council’s Education Steering
Committee, Fishery Data Collection and
Research Committee, Pelagic Standing
Committee, and Executive and Budget
Standing Committee.
DATES: The meetings will be held
Monday, October 13, 2014 through
Thursday, October 23, 2014. For specific
dates, times and agendas, see
SUPPLEMENTARY INFORMATION.
ADDRESSES: The Education Steering
Committee, 117th SSC, the Fishery Data
Collection and Research Committee and
Standing Committee meetings will be
held at the Council office, 1164 Bishop
Street, Suite 1400, Honolulu, HI 96813;
telephone: (808) 522–8220.
The 161st Council meeting will be
held at the Laniakea YWCA-Fuller Hall,
1040 Richards Street, Honolulu, HI
96813; telephone: (808) 538–7061.
The Fishers Forum will be held at the
Harbor View Center, Pier 38, 1129 North
Nimitz Highway, Honolulu, HI 96817;
telephone: (808) 983–1200.
Background documents will be
available from, and written comments
should be sent to, Mr. Edwin Ebisui,
Acting Chair, Western Pacific Fishery
Management Council, 1164 Bishop
Street, Suite 1400, Honolulu, HI 96813;
telephone: (808) 522–8220 or fax: (808)
522–8226.
FOR FURTHER INFORMATION CONTACT:
Kitty M. Simonds, Executive Director;
telephone: (808) 522–8220.
SUPPLEMENTARY INFORMATION: The
Education Steering Committee will meet
on October 13, 2014, between 3 p.m.
and 5 p.m.; 117th SSC meeting on
October 14–16, 2014, between 8:30 a.m.
and 5 p.m.; Fishery Data Collection and
Research Committee October 20, 2014,
between 10 a.m. and 12 noon; the
SUMMARY:
E:\FR\FM\26SEN1.SGM
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Agencies
[Federal Register Volume 79, Number 187 (Friday, September 26, 2014)]
[Notices]
[Pages 57875-57887]
From the Federal Register Online via the Government Printing Office [www.gpo.gov]
[FR Doc No: 2014-23034]
-----------------------------------------------------------------------
DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration
[Docket No. 121204680-4789-03]
RIN 0648-XC387
Endangered and Threatened Wildlife and Plants; Notice of 12-Month
Finding on a Petition To List the Humphead Wrasse as Threatened or
Endangered Under the Endangered Species Act (ESA)
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.
-----------------------------------------------------------------------
SUMMARY: We, NMFS, announce a 12-month finding on a petition to list
the humphead wrasse (Cheilinus undulatus) as threatened or endangered
under the Endangered Species Act (ESA). We have completed a
comprehensive status review of the humphead wrasse in response to this
petition. Based on the best scientific and commercial information
available, including the status review report (Graham et al., 2014), we
have determined that the species does not warrant listing at this time.
We conclude that the humphead wrasse 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. We also announce
the availability of the humphead wrasse status review report.
DATES: This finding was made on September 26, 2014.
ADDRESSES: The humphead wrasse status review report is available
electronically at: https://www.fpir.noaa.gov/PRD/
prdhumpheadwrasse.html. You may also receive a copy by
submitting a request to the Protected Resources Division, Pacific
Islands Regional Office, NMFS, 1845 Wasp Blvd., Building 176, Honolulu,
HI 96818, Attention: Humphead Wrasse 12-month Finding.
FOR FURTHER INFORMATION CONTACT: Krista Graham, NMFS, Pacific Islands
Regional Office, (808) 725-5152; or Lisa Manning, NMFS, Office of
Protected Resources, (301) 427-8466.
SUPPLEMENTARY INFORMATION:
Background
On October 31, 2012, we received a petition from WildEarth
Guardians to list the humphead wrasse (Cheilinus undulatus) as
threatened or endangered under the ESA throughout its entire range. The
petitioners also requested that critical habitat be designated for the
humphead wrasse under the ESA. On February 28, 2013, we published a
positive 90-day finding (78 FR 13614), announcing that the petition
presented substantial scientific or commercial information indicating
the petitioned action of listing the species may be warranted and
explained the basis for that finding. 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.
Listing Species Under the Endangered Species Act
Section 4(b)(3)(B) of the ESA requires us to make a finding within
12-months of the date of receipt of any petition that was found to
present substantial information indicating that the petitioned action
may be warranted. The 12-month finding must provide a determination of
whether the petitioned action is: (a) Not warranted; (b) warranted; or
(c) warranted but precluded. In this case, we are responsible for
determining whether the humphead wrasse warrants listing as threatened
or endangered under the ESA (16 U.S.C. 1531 et seq.). To make this
determination, we first consider whether a group of organisms
constitutes a ``species'' under section 3 of the ESA, then whether the
status of the species qualifies it for listing as either threatened or
endangered. Section 3 of the ESA defines species to include ``any
subspecies of fish or wildlife or plants, and any distinct population
segment of any species of vertebrate fish or wildlife which interbreeds
when mature.'' On February 7, 1996, NMFS and the U.S. Fish and Wildlife
Service (USFWS; together, the Services) adopted a policy describing
what constitutes a distinct population segment (DPS) of a taxonomic
species (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.
Section 3 of the ESA further defines an ``endangered species'' as
``any species which is in danger of extinction throughout all or a
significant portion of its range'' and a ``threatened species'' as one
``which is likely to become an endangered species within the
foreseeable future throughout all or a significant portion of its
range.'' Thus, in the context of the ESA, we interpret an ``endangered
species'' to be one that is presently in danger of extinction. A
``threatened species'' is not presently at risk of extinction, but is
likely to become so in the foreseeable future. The key 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).
Section 4 of the ESA and implementing regulations at 50 CFR part
424 require us to determine whether any species is endangered or
threatened as a result of any one or a combination of the following
five factors: (A) The present or threatened destruction, modification,
or curtailment of its habitat or range; (B) overutilization for
commercial, recreational, scientific, or educational purposes; (C)
disease or predation; (D) the inadequacy of existing regulatory
mechanisms; or (E) other natural or manmade factors affecting its
continued existence (ESA section 4(a)(1)(A)-(E)). Section 4(b)(1)(A) of
the ESA requires us to make listing determinations based solely on the
best scientific and commercial data available after conducting a review
of the status of the species and after taking into account efforts
being made by any State or foreign nation or political subdivision
thereof to protect the species. We also consider the comments received
in response to issuance of the 90-day finding. In evaluating the
efficacy of existing protective efforts, we rely on the Services' joint
Policy on Evaluation of Conservation Efforts When Making Listing
Decisions (``PECE''; 68 FR 15100; March 28, 2003). The PECE provides
direction for considering conservation efforts that have not been
implemented, or have been implemented but not yet demonstrated
effectiveness.
Status Review
We appointed an Endangered Species Biologist in the Protected
Resources Division of the NMFS Pacific Islands Regional Office (PIRO)
to gather and review the best available data and information on the
life history and ecology, distribution, abundance, and threats to the
humphead wrasse and to document this review in a status review report.
Next, we convened a team of
[[Page 57876]]
four biologists (hereinafter referred to as the Extinction Risk
Analysis (ERA) Team) to conduct an extinction risk analysis for the
humphead wrasse, using the information in the status review report. The
ERA Team was comprised of three fishery biologists from NMFS' Pacific
Island Fisheries Science Center and a fishery biologist with NMFS
PIRO's Habitat Conservation Division. The ERA Team had expertise in
reef fish biology and ecology, population dynamics, and stock
assessment science. The ERA Team documented their evaluation of
possible DPSs for the humphead wrasse and their professional judgment
of the extinction risk facing the humphead wrasse in the status review
report (Graham et al., 2014). The report makes no recommendation as to
the listing status of the species. The status review report is
available electronically at https://www.fpir.noaa.gov/PRD/
prdhumpheadwrasse.html.
The status review report was then subjected to peer review as
required by the Office of Management and Budget Final Information
Quality Bulletin for Peer Review (M-05-03; December 16, 2004). The
status review report was peer reviewed by three independent specialists
selected from the academic and scientific community, with expertise in
reef fish biology, conservation and management, and knowledge of
humphead wrasse. The peer reviewers were asked to evaluate the
adequacy, appropriateness, and application of data used in the status
review as well as evaluate the findings made in the ``Assessment of
Extinction Risk'' section of the report. All peer reviewer comments
were addressed prior to dissemination of the final status review report
and publication of this determination.
Life History, Biology, and Status of the Petitioned Species
Below we summarize the key life history and species information
from the status review report (Graham et al., 2014). More detailed
information is available in the status review report, which is
available electronically at https://www.fpir.noaa.gov/PRD/
prdhumpheadwrasse.html.
Species Description
The humphead wrasse is the largest member of the family Labridae.
Found throughout the Indo-Pacific Ocean, the humphead wrasse is
distinguished from other coral reef fishes, including other wrasses,
due primarily to its large size along with its fleshy lips in adults
(Myers, 1999), prominent bulbous hump that appears on the forehead in
larger adults of both sexes, and intricate markings around the eyes
(Marshall, 1964; Bagnis et al., 1972; Sadovy et al., 2003a).
The humphead wrasse has a reported maximum length of 229 cm total
length (TL) (7.5 ft) and weight of 190.5 kg (420 lbs) (Marshall, 1964;
Myers, 1989; Lieske and Myers, 1994; Donaldson and Sadovy, 2001;
Westneat, 2001; Sadovy et al., 2003a; Russell, 2004); however, there
are no confirmed records of this species greater than 150 cm fork
length (FL) (Choat et al., 2006). (TL is measured from the tip of the
snout to the tip of the longer lobe of the caudal or tail fin; whereas,
FL is measured from the tip of the snout to the end of the middle
caudal fin rays (i.e., where the fork of the tail begins). TL is longer
than FL). The maximum age of humphead wrasse is estimated to be 30
years for females and 25 years for males (Sadovy et al., 2003a; Choat
et al., 2006; Andrews et al., in review).
The development of the cephalic hump is related to body size and is
visible at 37 cm TL, with all individuals >=75 cm TL exhibiting a
distinctive hump, irrespective of sex (Liu and Sadovy de Mitcheson,
2011). Therefore, C. undulatus does not show obvious sexual dimorphism
of the forehead extension, meaning that it is not a reliable criterion
for differentiating males and females. The species has 9 dorsal fin
spines, 10 dorsal fin rays, 3 anal fin spines, and 8 anal fin rays
(Sadovy et al., 2003a). Juveniles are pale gray/green with large dark
spots on some of the scales that produce a series of broad dark bands,
interspersed with narrower white bands along the length of the body and
a pair of distinctive parallel black lines before and after the eye
(Sadovy et al., 2003a). Colin (2006) notes that juvenile C. undulatus
resemble juvenile C. trilobatus and C. chlorurus, with similar shape,
some resemblance in coloration, similar swim fashion, and can all occur
in the same habitat. The author notes that the similarities with these
two more common species can result in confusion and misidentification
of juvenile C. undulatus.
Adults are olive green to blue-green with large scales. A narrow
dark bar on each scale breaks into irregular dark lines anteriorly on
the body with growth (Randall, 2005). The head is a blue-green to blue
with irregularly wavy yellowish lines (Sadovy et al., 2003) with the
same two slightly oblique black lines extending posteriorly from the
lower half of the eye, often with two more black lines extending from
the eye to the rear part of the upper lip (Randall, 2005). These
distinctive patterns of lines makes identifying individual fish
possible if the head pattern and spots can be seen or photographed.
While there is no apparent sexual dichromatism or permanent difference
in color between sexes (Sadovy et al., 2003a), temporary color
differences between males and females are seen during reproduction
(Colin, 2010).
Distribution
The humphead wrasse is widely distributed on coral reefs and
nearshore habitats throughout much of the tropical Indo-Pacific Ocean.
The biogeographic range of the humphead wrasse spans from 30[deg] N to
23[deg] S latitude and includes the Red Sea south to Mozambique in the
Indian Ocean, from southern Japan in the northwest Pacific south to New
Caledonia in the south Pacific and into the central Pacific Ocean
including French Polynesia. The humphead wrasse has been recorded from
many islands of Oceania, but appears to be absent from the Hawaiian
Islands, Johnston Island, Easter Island, Pitcairn, Rapa, and Lord Howe
Island with the exception of occasional waifs (Randall et al., 1978).
In the United States (U.S.), the species is found in the territories of
American Samoa, the Commonwealth of the Northern Mariana Islands
(CNMI), and Guam. In the U.S. Pacific Remote Island Areas, the species
is found in the Line (Palmyra Atoll, Kingman Reef, and Jarvis Island)
and Phoenix (Howland and Baker) Islands, and at Wake Atoll.
Habitat
The humphead wrasse is widely distributed in low densities on all
types of coral reef environments and nearshore habitats throughout much
of the tropical Indo-Pacific. Both coral reefs and seagrass beds have
been reported to provide a nursery habitat for post-settlement and
juvenile humphead wrasse (Sadovy et al., 2003a; Russell, 2004).
Juveniles are also observed in murky outer river areas with patch
reefs, shallow sandy areas adjacent to coral reef lagoons, and in
mangroves (Randall, 1955; Randall et al., 1978; Myers, 1989; Sadovy et
al., 2003a; Myers, 1999).
Unlike juveniles, adults are more commonly observed inhabiting
offshore habitats along steep outer reef slopes, reef drop offs,
channel slopes, reef passes, reef flats, and lagoonal reefs to depths
of up to at least 100 m (Randall, 1978; Myers, 1989; Sadovy et al.,
2003a; Zgliczynski et al., 2013). Fish size and abundance are
correlated with habitat type, with the largest fish and most dense
groups of humphead wrasses observed on barrier reefs and passes. In
coastal, middle reefs and lagoon areas,
[[Page 57877]]
smaller fish (< 50 cm TL) are typically observed among branching
staghorn corals (Acropora spp.) (Sadovy et al., 2003a).
Movement and Behavior
The numbers of fish found together can vary. According to Sadovy et
al. (2003a), juveniles are typically solitary, wary, and difficult to
approach, though they can be found in small groups. Adults are
typically observed solitary or paired (Myers, 1989; Sadovy et al.,
2003a) but have also been noted in groups of 3-7 individuals
(Donaldson, 1995; Sadovy et al., 2003a). Additionally, small social
units can be observed moving together in less heavily fished areas,
while lone and more wary individuals are more often noted in heavily
fished areas (Sadovy et al., 2003a).
Based on mensurative in situ observations, humphead wrasse display
site fidelity and predictable home ranges with the same individuals,
identifiable by distinct head markings, observed along the same
stretches of reef for extended periods, although the lengths of these
periods are not defined. Additionally, adults often use a consistent
resting place (i.e., cave or crevice) at night or when threatened
(Bagnis et al., 1972; Myers, 1989; Thaman, 1998; Myers, 1999; Donaldson
and Sadovy, 2001; Sadovy et al., 2003a; Chateau and Wantiez, 2007).
Factors such as sex, age, and size of the fish directly influence
the home range size of the humphead wrasse, with smaller fish using a
fraction of the area occupied by adults (Sadovy et al., 2003a citing
T.J. Donaldson, unpublished data). A single juvenile (45 cm FL)
humphead wrasse that had been surgically implanted with an ultrasonic
transmitter in New Caledonia moved at least 20-200 m every day and had
an estimated home range size of at least 50,000 m\2\ (Chateau and
Wantiez, 2007). In Palmyra Atoll, 19 acoustically tagged juveniles and
adults (ranging in length from 27 to 109 cm TL) had home range sizes of
800 m \2\ to 19,000 m \2\, with the smallest home ranges occupied by
juveniles, intermediate ranges for adult males, and largest ranges
occupied for adult females (Weng et al., in press).
Foraging Ecology
The humphead wrasse is a diurnal carnivore, feeding during the day
and sleeping at night (Durville et al., 2003; Gillbrand et al., 2007).
Much of its prey is found in sand or rubble habitats where it feeds on
a variety of molluscs, small fishes such as gobies, moray eels, sea
urchins, crustaceans, brittle stars, starfish, and other invertebrates
(Randall et al., 1978; Myers, 1989; Randall et al., 1997; Thaman, 1998;
Sadovy et al., 2003a; Choat et al., 2006). Similar to other wrasse
(Labridae), humphead wrasses forage by turning over or crushing rocks
and rubble to reach cryptic organisms (Pogonoski et al., 2002; Sadovy
et al., 2003a citing P.S. Lobel, pers. comm.). The thick fleshy lips of
the species appear to absorb sea urchin spines, and the pharyngeal
teeth easily crush heavy-shelled sea snails in the genera Trochus spp.
and Turbo spp. The humphead wrasse is also one of the few predators of
toxic animals such as boxfishes (Ostraciidae), sea hares (Aplysiidae),
and crown-of-thorns starfish (Acanthaster planci) (Randall, 1978;
Myers, 1989; Thaman, 1998; Sadovy et al., 2003a). Consumption of toxic
species in certain areas, particularly Tahiti, Tuvalu, New Caledonia,
the Tuamotu Archipelago (French Polynesia), Marshall Islands, and the
Federated States of Micronesia can cause the humphead wrasse to be
ciguatoxic to humans (Randall, 1958; Randall et al., 1978; Randall,
1979; Lewis, 1986; Myers, 1989; Dalzell, 1992; Dalzell, 1994; Sadovy,
1998; Myers, 1999; Sadovy et al., 2003b; Sadovy, 2006).
Reproduction and Growth
Field reports reveal variable humphead wrasse spawning behavior,
depending on location (Sadovy et al., 2003a; Colin, 2010). Spawning can
occur between several and all months of the year, coinciding with
certain phases of the tidal cycle (usually after high tide) and
possibly lunar cycle (Sadovy et al., 2003a; Colin, 2010). Spawning can
reportedly occur in small (< 10 individuals) or large (> 100
individuals) groupings, which can take place daily in a variety of reef
types (Sadovy et al., 2003a; Sadovy de Mitcheson et al., 2008; Colin,
2010).
Data from captive rearing programs indicates that egg diameter
ranges from 0.62-0.67 mm, and newly hatched larvae are 1.5-1.7 mm TL
(Slamet and Hutapea, 2005). Eggs are spherical and lack pigment (Sadovy
et al., 2003 citing P.L. Colin, unpublished data). Little information
is available regarding larval dispersal in the wild (Poh and Fanning,
2012). However, in unpublished work P.L. Colin (pers. comm.) found that
eggs of humphead wrasse moved slowly off the western barrier reef of
Palau over a few hours in tidal currents, and then stalled before
moving laterally along the reef. Some eggs are brought back in over the
barrier reef, while others remain at sea, all in the first 12 hours
after spawning.
Humphead wrasse larvae settle out of the plankton at a size of 8 to
15 mm TL, with a mode of 12 mm TL (at an unspecified larval duration),
and reach 35 mm TL or greater within 2 to 3 weeks post-settlement
(Tupper, 2007 citing M. Tupper, unpublished data). Slamet and Hutapea
(2005), however, indicate that growth of larvae is actually much
slower. The authors report that captive larvae reach 50-60 mm TL in 6
months. Settlement varies among habitat types.
As is common in wrasses, the humphead wrasse is a protogynous
hermaphrodite, capable of changing sex from female to male around 9
years of age (Choat et al., 2006; Sadovy de Mitcheson et al., 2010). At
around 6 months of age, juveniles are approximately 5-6 cm TL (Slamet
and Hutapea, 2005), reaching 50 cm TL at approximately 7 years of age.
As females reach sexual maturity growth slows, with few individuals
observed > 100 cm TL. Male growth rates are approximately double those
of females, resulting in relatively young but large males (Choat et
al., 1996; 2006).
Size at maturity for males and females is difficult to compare
across studies because some measurements are reported as TL and others
as FL. Sadovy et al. (2003a) estimates that females reach sexual
maturity at around 5 years of age and 35-50 cm TL. Other histological
studies estimate that sexual maturity is reached around 40-60 cm TL,
which is estimated to be about 5-7 years of age (Pogonoski et al., 2002
and Russell, 2004 citing Sadovy, unpublished data; Sadovy et al.,
2011). Another study analyzing early gonadal development on 178
humphead wrasse specimens revealed that minimum body sizes for female
and male sexual maturation were 65 cm and 84.5 cm TL, respectively
(Sadovy de Mitcheson et al., 2010). However, the authors note that
despite the results from this study, based on available information, it
is suggested that the typical size of female sexual maturation for the
humphead wrasse occurs at 40-50 cm TL (Sadovy de Mitcheson et al.,
2010). Choat et al. (2006) estimated length at first maturity as 45-50
cm FL for females (6-7 years) and 70 cm FL (9 years) for males. Despite
the apparent differences in estimated minimum size of female sexual
maturation among the different studies and locations, the age at first
maturity is relatively late, representing about 20% of the female life
span as opposed to 5-6% of the female life span observed in most other
reef fishes with life spans in excess of 30 years (Choat and Robertson,
2002).
[[Page 57878]]
Natural Mortality
Natural adult mortality is thought to be low (Sadovy et al.,
2003a). As for mortality due to predation, little is known though it is
thought there is refuge in size. Although adult humphead wrasses are
most vulnerable during spawning, apex predators including sharks are
not known to prey on adult humphead during this time (Colin, 2010).
Population Structure
Very little published genetic research is available on the humphead
wrasse other than the results of sequencing the mitochondrial genome of
the species (Qi et al., 2013). Research is currently underway to
analyze 200 humphead wrasse samples collected from the eastern Indian
Ocean to Pohnpei and from the Great Barrier Reef to the Marianas
Islands. Preliminary analyses of mitochondrial DNA from a subset of
samples from across the range suggest no deep genetic differentiation
on the scale of ocean basins, though robust conclusions await final
analyses of the complete dataset (Michael Dawson, pers. comm.).
Additionally, no tagging or tracking studies of a scale sufficient to
define population structure have been conducted. Although a number of
studies have provided abundance estimates based on in situ surveys,
there are no current studies or references describing population
structure.
Population Abundance
There are no historical estimates (pre-1970s) of global or local
abundance or biomass of humphead wrasse. When limited surveys first
began on this species in the early 1970s, the species was generally
characterized as being naturally uncommon to rare in places (Bagnis et
al., 1972; Galzin et al., 1998; Sadovy et al., 2003a and IUCN, 2008
citing Galzin, 1985; IUCN, 2008 citing Tropical Research and
Conservation Centre--Malaysia (TRACC), 2004). For example, in 1972
Taiaro lagoon, a 9 km\2\ uplifted lagoon (maximum depth of 27 m
dominated by talus sand and small dispersed patch reefs) of Taiaro
Atoll in Tuamotu Archipelago, French Polynesia, where this species was
not fished and fish diversity was high, abundance was estimated to be
1-2 fish per 10,000 m\2\ (Galzin et al., 1998). This abundance remained
unchanged during repeat surveys in 1992 and 1994 (Galzin et al., 1998).
In the Society Islands of French Polynesia, humphead wrasses were also
reported to be uncommon in the early 1970s (Bagnis et al., 1972; IUCN,
2008 citing Galzin, 1985).
Past catch records for some locations, when compared to more
current catch records, although the data are sparse, indicate that some
populations were at one time greater than present day (i.e., Australia,
Fiji, Malaysia, Palau [IUCN, 2008]). However, inferences regarding
abundance from fishery dependent data are subject to uncertainty from
effects of fishing methods, size selectivity, fishery participation,
regulation, and methods of collecting data. Such uncertainty is also
true in relation to inferences made from underwater surveys when
habitat information and survey methodology are not known.
Efforts to estimate abundance and density of humphead wrasse have
been completed in certain regions within the species' range (e.g., U.S.
Pacific Islands) using underwater visual census techniques designed to
quantify the abundance of these relatively rare/uncommon and wide-
ranging fish. Although humphead wrasses are widely distributed, natural
densities are typically low, even in locations where habitats are
presumably intact. Unfished or lightly fished areas have densities
ranging from 2-27 individuals per 10,000 m\2\ of reef (Sadovy et al.,
2003a). For example, at Wake Atoll where there is zero fishing pressure
for the species, surveys that recorded primarily juveniles (< 30 cm TL)
reported the naturally low abundance of the species at 13-27
individuals per 10,000 m\2\ (Sadovy et al., 2003a and IUCN, 2008 citing
P.S. Lobel, pers. comm., and Lobel and Lobel, 2000). This is the
highest recorded abundance of any location and one of the most
protected areas. Abundance of sub-adult and adult humphead wrasse
observed from towed-diver surveys of fore reef habitats (10-15 m depth)
at Wake Atoll conducted by NMFS Pacific Islands Fisheries Science
Center (PIFSC) Coral Reef Ecosystem Division (CRED) in 2005, 2007,
2009, and 2011 is lower. Four years of biannual surveys from this time
period report an average of 1.101 large (> 50 cm TL) individuals per
10,000 m\2\ (NMFS PIFSC CRED, unpublished). Palmyra Atoll, also a U.S.
Pacific Remote Island Area where the species is completely protected,
had similarly naturally low abundance levels despite decades of
complete protection. Abundance of large (> 50 cm TL) humphead wrasse
observed from towed-diver surveys of fore reef habitats (10-15 m depth)
of Palmyra Atoll conducted biannually from 2001-2012 is 0.641
individuals per 10,000 m\2\ (NMFS PIFSC CRED, unpublished).
At sites near human population centers or at fished areas,
densities are typically lower by tenfold or more and in some locations
humphead wrasse are rarely observed (Sadovy et al., 2003a; Colin, 2006;
Sadovy, 2006b; Unsworth et al., 2007). However, in some areas, such as
the previously mentioned Tuamotu Archipelago, French Polynesia,
abundance of humphead wrasse is low to non-existent, even when
fisheries exploitation is known to be low or non-existent (Galzin et
al., 1998). Another example is the northernmost uninhabited islands of
the Marianas Archipelago (Uracus, Maug, and Asuncion), which are part
of the Marianas Trench Marine National Monument. Here, where commercial
fishing is prohibited and recreational or subsistence fishing is very
rare given the distance from most of the southern inhabited areas of
the island chain, humphead wrasses were not observed. However, in the
southern inhabited part of the chain where some protections for the
species exist, large (> 50 cm TL) humphead wrasses are present though
abundance levels are low (i.e., biannual towed-diver surveys of fore
reef habitats (10-15 m depth) from 2003-2011 of the entire Marianas
Archipelago reports an average of 0.059 individuals per 10,000 m\2\
(Brainard et al., 2012; NMFS PIFSC CRED, unpublished data)).
Status of the Species
Other than activities associated with the live reef food fish trade
(LRFFT), there are few ``directed'' fisheries for the humphead wrasse
due to its natural rarity and the inherent difficulty of capturing the
fish (Gillett, 2010). In most countries where the fish occurs, most of
the catch of this species is for domestic use. Commercially, the
humphead wrasse is caught in low volume fisheries in different ways
according to its size and whether it is needed alive or dead (Sadovy et
al., 2003a). The species is sold for domestic consumption, exported for
food for the LRFFT, exported for mariculture until the fish is large
enough for consumption, or exported for aquaria.
The LRFFT is a highly lucrative industry that involves the capture
of reef fish that are kept alive for sale and consumption. For about
three decades, the humphead wrasse has been a small but significant
component of the commercial LRFFT as one of the highest-valued luxury
food items (Sadovy et al., 2003a; Sadovy et al., 2003b; Gillett, 2010).
Indonesia, Malaysia, and the Philippines are the top three exporters of
humphead wrasse for the LRFFT, respectively. The major importing
countries for the species are China (especially Hong Kong), Taiwan, and
Singapore (Sadovy et al., 2003a).
[[Page 57879]]
In 1996, the humphead wrasse was listed as ``vulnerable'' on the
International Union for the Conservation of Nature (IUCN) Red List of
Threatened Species due to concerns over rapidly declining numbers in
many areas. In 2004, the species was reclassified to ``endangered'' on
the IUCN Red List. Also in 2004, the species was included in Appendix
II in the Convention on International Trade in Endangered Species of
Wild Fauna and Flora (CITES). Appendix II includes species that are
vulnerable to overexploitation, but not at risk of extinction under
CITES criteria; trade must be regulated to avoid exploitation rates
incompatible with species survival.
Distinct Population Segment Analysis
As described earlier, the ESA's definition of ``species'' includes
``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.'' The petitioners did not request that NOAA
consider listing a DPS; however, the ERA Team was asked to evaluate
whether any populations of the species might qualify as DPSs based on
the elements of discreteness and significance as defined in the DPS
Policy. The ERA Team found support for discreteness of the humphead
wrasse population within the ``core-Coral Triangle'' area of Indonesia,
Malaysia, and the Philippines solely on the basis that the population
is delimited by international governmental boundaries within which
regulation and governance of threats are different from other portions
of the species' range. There was no support to conclusively subdivide
the species into discrete population segments on the basis of genetics,
morphology, behavior, physical factors, or other biological
characteristics.
When evaluating whether the core-Coral Triangle DPS met the
significance criteria, the team found some support for the
``persistence of the discrete population segment in an ecological
setting unusual or unique for the taxon.'' According to the Team (see
Appendix 1 of the Status Review Report), this support was largely based
on the fact that the three countries within the core-Coral Triangle
area contain approximately 50 percent of mangroves and 30 percent of
coral reefs within the species range, both of which provide important
habitat for various humphead wrasse life stages. However, the team
acknowledged that because coral reef and mangrove habitats also occur
outside the range of the proposed DPS, neither of those habitat types
is unique to the core-Coral Triangle area, nor did they identify any
other unique habitat features of this area. The ERA Team did consider
that the humphead wrasse plays a relatively unique ecosystem role in
the core-Coral Triangle area due to its co-occurrence with two
significant prey species that likely have interdependent ecological
roles. However, the humphead wrasse also overlaps with the two
significant prey species outside the range of the proposed DPS, and
although the overlap may not be as widespread, the team acknowledged
that this ecological structure is not truly unique to the core-Coral
Triangle area. Thus, overall, the significance criterion of the DPS
Policy is not well supported.
As stated in the DPS Policy, Congress instructed the Services to
exercise their authority with regard to DPSs ``. . . sparingly and only
when the biological evidence indicates that such action is warranted.''
Given this direction from Congress and the weak support for the
significance of the core-Coral Triangle DPS, we declined to consider
this DPS further and asked the ERA Team to conduct the extinction risk
analysis on the entire global population of the humphead wrasse.
Assessment of Extinction Risk
When evaluating whether the humphead wrasse meets the definition of
threatened or endangered, we considered the best available information
and applied professional judgment in evaluating the level of risk faced
by a species. We qualitatively evaluated demographic risks, such as low
abundance and productivity, along with other threats to the species. A
quantitative viability analysis (i.e., population modeling) was not
conducted for the humphead wrasse because of the limited or inadequate
data on population size, definitive trends in population size or
apparent abundance, intrinsic rate of increase, mortality rates, or
size structure. Lastly, as required under section 4(b)(1)(A), we also
took into account conservation efforts being made to protect the
species.
Methods
The term ``foreseeable future'' was defined as the future timeframe
over which demographic risks and threats can be reliably predicted to
impact the biological status of the humphead wrasse. The Team took into
account the life history of the species, including the longevity of the
species (25-30 years), and assumed 6-7 years for generation time (which
is defined as the time it takes, on average, for a sexually mature
female humphead wrasse to be replaced by offspring with the same
spawning capacity). Considering all of this, the Team agreed that it
would likely take several generation times for any conservative
management action to be realized and reflected in population abundance.
Therefore, the ERA Team chose to project threats in the ``foreseeable
future'' out to eight generations, or about 50 years.
Previous NMFS status reviews have involved use of a risk matrix
method to organize and summarize the professional judgment of a panel
of knowledgeable scientists. This approach is described in detail by
Wainright and Kope (1999) and has been used in Pacific salmonid status
reviews as well as in the status reviews of many other species (see
https://www.nmfs.noaa.gov/pr/species for links to these reviews). In the
risk matrix approach, the collective condition of individual
populations is summarized at the species level according to four
demographic risk criteria: abundance, growth rate and productivity,
spatial structure and connectivity, and diversity. These viability
criteria, outlined in McElhany et al. (2000), reflect concepts that are
well founded in conservation biology and that individually and
collectively provide strong indicators of extinction risk. Using these
concepts, the ERA Team estimated demographic risks by assigning a risk
score to each of the four demographic criteria. The scoring for the
demographic risk criteria correspond to the following values: 1--no
risk, 2--low risk, 3--moderate risk, 4--high risk, and 5--very high
risk. The Team members also expressed their certainty regarding
evidence of demographic risk using a ranking of low, medium, and high.
Detailed definitions of the risk scores can be found in the status
review report.
The ERA Team then performed a threats assessment for the humphead
wrasse by ranking the effect that each threat was having on the
extinction risk of the species, both now and in the foreseeable future.
The four threat effect levels ranged from ``no effect,'' ``small
effect,'' ``moderate effect,'' and ``significant effect'' on the
extinction risk to the humphead wrasse. To allow individuals to express
a distribution of risk scores in assessing the impacts of the threats
to the species, the ERA Team adopted the ``likelihood point'' (FEMAT)
method using 8 ``likelihood points'' per Team member for the four
threat effect levels. A similar approach has been used in previous NMFS
status reviews (e.g., Pacific salmon, Puget Sound rockfish, Pacific
herring, black abalone, great hammerhead shark) to
[[Page 57880]]
structure the Team's thinking and express levels of risk as a
distribution in assigning threat risk categories. The scores were then
tallied (frequency, range, mode, and median) and summarized for each
threat, and considered in making the overall risk determination. The
Team members also expressed their certainty regarding evidence of
potential threats using a ranking of low, medium, and high.
Guided by the results from the demographics risk analysis as well
as the threats assessment, the ERA Team members used their informed
professional judgment to make an overall extinction risk determination
for the humphead wrasse now and in the foreseeable future (up to 50
years). For these analyses, the ERA Team defined five levels of overall
extinction risk: 1--no risk, 2--low risk, 3--moderate risk, 4--high
risk, and 5--very high risk. Detailed definitions of these risk levels
can be found in the status review report. Again, the ERA Team adopted
the FEMAT method, distributing 10 ``likelihood points'' per Team member
among the five levels of extinction risk. The scores were then tallied
(frequency, mode, and median for likelihood points, and mean and range
for certainty) and summarized. The Team members again expressed their
certainty in a ranking of low, medium, and high.
Finally, the ERA Team drew scientific conclusions about the overall
risk of extinction faced by the humphead wrasse under present
conditions and in the foreseeable future based on an evaluation of the
species' demographic risks and assessment of threats. The Team did not
make recommendations as to whether the species should be listed as
threatened or endangered, or if it did not warrant listing.
Evaluation of Demographic Risks
Abundance
Currently, there are no formal estimates of population size
throughout most of the humphead wrasse's range. It is known that this
species is uncommon to rare throughout most of its range, in some cases
exhibiting low abundance in areas where no anthropogenic stressors are
evident. In the CNMI, for example, humphead wrasses appear to be more
prevalent in the southern populated islands, as compared to the mostly
uninhabited or lightly populated islands north of Saipan. In this case,
several factors may influence humphead wrasse abundance such as total
habitat availability, fishing access to humphead wrasse due to island
size and/or orientation, and restrictions on fishing effort.
Declines in abundance appear to be restricted to particular areas
where the LRFFT has been active for several decades. In some areas
where no apparent harvest occurs, the species has not demonstrated any
notable changes between surveys. One aspect lacking in many fishery-
independent surveys is meaningful time series of observations
incorporating standardized methodological protocols. Without such time
series, drawing firm conclusions based on temporally and/or spatially
distinct observations is simply not possible. In addition, surveyed
locations (i.e., exact locations, habitat type, water depth) and
methods (i.e., stationary point count, towed-diver surveys) are an
important descriptor in survey work, as not all areas where the
humphead wrasse exists are equally accessible for underwater visual
census surveys. In other words, it is difficult to draw conclusions on
abundance from survey results across different locations and time
frames.
Existing information suggests that humphead wrasse populations are
most abundant and stable in the Indian Ocean. However, populations in
the core-Coral Triangle area, where harvest has been significant near
population centers, appear to remain depressed to a degree that is not
quantifiable.
There are ``pockets'' of abundance in Malaysia (e.g., Pulau Layang
Layang, West of Sabah, and Pulau Sipadan, as well as Hoga Island in
Wakatobi Marine National Park) where either military or management
protection exists (IUCN, 2008 citing TRACC, 2004). These pockets of
abundance in the core-Coral Triangle area should be considered crucial
as important potential source populations to other core-Coral Triangle
populations. However, density estimates from these protected locations
are at least a decade old, and no recent information is available to
indicate that these densities have remained stable, although there is
no reason to expect otherwise, especially in designated military bases,
where access is assumed to be extremely limited.
There are many other foreign and domestic areas where the species
has been protected by fishing regulations or reserves, and the species
continues to be observed throughout the Pacific wherever surveyed.
Recent relative abundance data suggest that many populations,
especially those in U.S. waters, are either stable, show no clear
trend, or may be increasing (Graham et al 2014).
Based on the very limited abundance information available and its
natural rarity, along with depressed population sizes in the center of
the species' range due to overharvest, the ERA Team concluded that the
demographic factor of abundance had a low-to-moderate likelihood of
contributing to the humphead wrasse's risk of extinction now, and a
moderate-to-high likelihood of contributing to the risk of extinction
in the foreseeable future. The ERA Team was concerned that the species'
low abundance levels, whether natural or manmade, may pose a risk to
its continued existence if faced with other demographic risks or
threats, such as overutilization, because a species that is already at
naturally low levels may not be able to withstand heavy fishing
pressure. Of the four demographic factors, abundance was considered by
the ERA Team to pose the highest demographic risk to the species. Risk
was found to be higher in the foreseeable future than now simply
because the increased chance that declines in abundance may become more
serious with the passage of time, unless regulations are effective and
enforced. Certainty of abundance affecting the risk of extinction to
the humphead wrasse now was deemed medium; certainty of abundance
affecting the risk of extinction to the humphead wrasse in the
foreseeable future was deemed low.
Growth Rate and Productivity
Regarding the effect of the humphead wrasses' growth rate and
productivity on its risk of extinction, the ERA Team expressed less
concern compared to their concern for abundance. The intrinsic rate of
increase, or productivity, is a complex function of fecundity, survival
rates, age at maturity, and longevity of a species. Productivity
determines a species' ability to recover from low numbers, if extrinsic
factors are not limiting, as well as the level of harvest that can be
taken from a population sustainably (Hudson and Br[auml]utigam, 2007).
For the humphead wrasse, productivity is estimated to be 0.72 per year
(Fishbase.org). This places the humphead wrasse towards the slow end of
the slow-to-fast growth continuum of reef fishes. While the humphead
wrasse may be more productive than other reef fish that are highly
exploited in the LRFFT, such as the giant grouper (Epinephelus
lanceolatus), it is not as productive as the leopard coral grouper
(Plectropomus leopardus) or the mangrove red snapper (Lutjanus
argentimaculatus), two species which are also highly exploited in the
LRFFT. The Team recognized that being towards the slow end of the
continuum creates some extinction risk compared with fish that grow
faster. As such, the ERA Team
[[Page 57881]]
concluded that the demographic risks of growth rate and productivity
pose a low risk to the humphead wrasse's continued existence now and a
moderate risk in the foreseeable future. Certainty of growth rate and
productivity affecting the risk of extinction to the humphead wrasse
now was deemed medium; certainty in the foreseeable future was deemed
low.
Spatial Structure/Connectivity and Diversity
The species' population depends on dispersal dynamics of
individuals as well as habitat quality and existing spatial structure.
Connectivity is through spawning and planktonic larval dispersal
processes. Spatial structure and genetic diversity are important as
they affect the species' ability to survive in diverse environments and
enable the population to respond to and survive long-term environmental
changes.
The humphead wrasse is known to occur in waters around 48
countries, from the Red Sea, east through the tropical Indian and
Pacific Oceans, to French Polynesia. This geography includes tens-of-
thousands of islands with diverse and varying bathymetry (e.g., shallow
coral reefs) along mainland coasts, most within close proximity and
presumed easy dispersal reach of pelagic larvae of this species.
Essentially very little is known regarding the spatial structure
and genetic diversity of the humphead wrasse. It is not known if there
are any manmade or ecological factors that could significantly alter
gene flow in the species, nor is it known if the humphead wrasse
consists of more than one population throughout its range or if any
genetically distinct populations exist. Without definitive genetic
information, the Team assumed that the species does not appear to be at
risk of a genetic bottleneck, meaning that the humphead wrasse is
likely able to adapt overtime to changing environments.
Although data are either completely lacking or inadequate, it can
be reasonably presumed that, across its entire range, the
characteristics of spatial structure/connectivity and genetic
diversity, by themselves, are unlikely to contribute to an extinction
risk for the humphead wrasse. Therefore, the ERA Team concluded that
the demographic factor of spatial structure and connectivity posed no-
to-low risk to the humphead wrasse's continued existence both now and
in the foreseeable future, with certainty deemed low for both
timeframes. The Team also concluded that diversity posed a low risk to
the humphead wrasse's continued existence both now and in the
foreseeable future, with certainty deemed low for both timeframes.
Summary of Factors Affecting the Humphead Wrasse
As described above, section 4(a)(1) of the ESA and NMFS
implementing regulations (50 CFR part 424) state that we must determine
whether a species is endangered or threatened because of any one or a
combination of the following five ESA factors: (A) The present or
threatened destruction, modification, or curtailment of its habitat or
range; (B) overutilization for commercial, recreational, scientific, or
educational purposes; (C) disease or predation; (D) inadequacy of
existing regulatory mechanisms; or (E) other natural or man-made
factors affecting its continued existence. The ERA Team evaluated
whether and the extent to which each of the foregoing factors
contributed to the overall extinction risk of the global humphead
wrasse population. This section briefly summarizes the ERA Team's
findings and our conclusions regarding threats to the humphead wrasse.
More details can be found in the status review report (Graham et al.,
2014).
(A) The Present or Threatened Destruction, Modification, or Curtailment
of its Habitat or Range
The ERA Team evaluated habitat destruction as a potential threat to
the humphead wrasse and found this threat may have a small effect on
the extinction risk of the humphead wrasse now, meaning that it is
unlikely that it is presently increasing the species' risk of
extinction. In the foreseeable future, the Team found that it is
moderately likely that this threat is increasing the species'
extinction risk. Certainty of the potential effects of habitat
destruction on the extinction risk of the species was deemed medium for
both now and in the foreseeable future.
With regard to destructive fishing practices, cyanide fishing is
the major practice that is used to target this wrasse, although a
relatively small number of mostly small-sized fish of this species
might occasionally be killed incidentally during blast fishing for
other reef fishes in open-reef environments. The intent in using
cyanide is to stun juvenile wrasse and capture them alive for
subsequent grow-out for sale in the LRFFT; however, some and perhaps a
substantial proportion of cyanide-fished wrasse die prior to actually
contributing product to the industry. Cyanide fishing is still a major
fishing method in Southeast Asia, but cyanide fishing is presently much
less of a concern throughout the rest of the Indo-Pacific region
(Sadovy de Mitcheson and Yin, in press), and thus of less concern to
the species throughout its range. In addition to its deleterious
effects on humphead wrasse, the cyanide released into and near the reef
substrate has substantial acute mortality and delayed health effects on
other fishes in and near the reef and on the non-fish motile, sessile,
and other biota including corals.
Regarding the loss and modification of juvenile nursery areas,
burgeoning coastal development and poor land management (e.g.,
sedimentation) in developing tropical countries appears to be the major
threat to the seagrass and branching coral and macroalgal habitats that
provide juvenile nursery habitat. The cutting of mangroves for firewood
used to fuel open-fire cooking stoves is another increasing problem
reflecting exponential human population growth in many of these
developing countries. Approximately one-third of all mangroves
worldwide have been lost in the past 50 years.
Regarding the loss and modification of adult habitat, the major
threat to the primary habitat of forereef and open-lagoons appears to
be climate change-induced coral bleaching and acidification, both of
which are impacting corals and other organisms with carbonate
skeletons, although at varying degrees according to susceptibility.
Although adult humphead wrasses use caves and other structures in rock
and dead coral limestone substrates to a great extent and are not
directly dependent on living corals, humphead wrasses are most numerous
near abundant live coral. Moreover, in geological time even
consolidated dead coral limestone substrates will decline because of
weathering if the replenishment rates of stony corals decline. Concern
over this factor and coastal development over a longer term was
influential in the conclusion that habitat loss could have moderate
effects on extinction risk in the foreseeable future.
Based on the best available information, we do not find that
habitat destruction, modification, or curtailment are threats that are
presently, or in the foreseeable future, placing the species at an
increased risk of extinction. Cyanide has recently been banned in a
number of countries throughout the species' range, and illegal use
appears to be waning and is much less of a concern outside of the Coral
Triangle region. The magnitude of direct and indirect threats to
juvenile and adult habitats is variable with no
[[Page 57882]]
evidence of substantial or widespread habitat loss or destruction.
(B) Overutilization for Commercial, Recreational, Scientific or
Educational Purposes
The ERA Team identified overutilization as a threat with a small-
to-moderate effect on the extinction risk of the humphead wrasse now,
and a moderate effect on the extinction risk to the species in the
foreseeable future. Certainty of the potential effects of
overutilization on the extinction risk of the species was deemed medium
for now and low for the foreseeable future.
Estimates of overutilization have been hampered by a dearth of
information regarding landings data and illegal, unregulated, and
unreported fishing. Fisheries that land humphead wrasse appear to lack
detailed temporal information pertaining to fishing effort, fishing
power, harvest location, seasonal changes in landings, as well as the
institution of management protocols. For example, IUCN (2008) notes a
10-fold decrease in market landings from Palau from the mid 1980s to
mid-1990s, though fails to note that scuba spearfishing was banned in
the early 1990s and may be directly linked to that stated decline.
Although declines in landings were noted in some jurisdictions,
information indicating no changes in landings is either not noted or
not available. This may be a result of humphead wrasse representing a
minor component of most coral reef fisheries throughout its range
because of its natural rarity.
Anecdotal evidence, in particular from within LRFFT participating
countries, indicates that areas where at some past time period humphead
wrasses were observed to have been present in naturally low densities
are no longer found since the start of the LRFFT.
Although overutilization appears to be an issue in some
jurisdictions and locales (e.g., core-Coral Triangle area) (Sadovy et
al., 2003a; IUCN, 2008), amounting to moderate effects on extinction
risk now and in the foreseeable future, it cannot be considered a
significant or overriding impact on the species throughout its entire
range in either time frame. In jurisdictions where scuba spearfishing
has been banned (Fiji, Palau, the U.S. jurisdictions of American Samoa
and CNMI), there is reasonable expectation that older and larger fish
benefit from depth refugia. In the CNMI, scuba spearfishing is banned;
it is still permitted in Guam. As a result, there exists considerable
disparity in the size frequency distributions of landed humphead wrasse
between the jurisdictions, which falls in line with the conclusions of
Lindley et al. (2014) that the banning of scuba spearfishing results in
depth refugia for many coral reef fish species.
While there is some concern for overutilization of the species,
particularly for commercial purposes resulting in population declines
in some areas such as the Coral Triangle region, the current evidence
indicates that many populations are either stable, show no clear trend,
or may be increasing. The current global population size is likely
sufficient to maintain population viability into the foreseeable
future. Based on the best available information, we do not find that
overutilization of the species is presently, or in the foreseeable
future, placing the species at an increased risk of extinction.
(C) Disease or Predation
The ERA Team evaluated disease and predation as potential threats
to the humphead wrasse, but noted that available information on either
threat is sparse. The ERA Team found that the little information
available indicates that this threat may have a small effect on the
extinction risk of the species, meaning that it is unlikely that
disease or predation are increasing the extinction risk to the species,
either now or in the foreseeable future. Certainty of the potential
effects of disease or predation on the extinction risk of the species
was deemed medium for both time frames.
Very little is known about diseases of the humphead wrasse other
than fish leech infestation (Hirundinea spp.), parasitic infestations
(protozoa, worms, etc.), and bacterial infections that have been
documented. Parasitic infestations have been reported as occurring in
the fins, gill operculum, body surface, eyes, and mouth cavity
(Koesharyani et al., 2005; Zafran et al., 2005). Zafran et al. (2005)
report that cryptocaryoniosis, or white spot disease because it causes
numerous white spots on the body surface, is the most dangerous
parasitic disease in many marine fishes in aquaria or mariculture
facilities. This disease, which can spread rapidly to other healthy
fish and lead to a high mortality, has been documented at the Gondol
Research Station in Indonesia. The Gondol Research Station has also
reported the presence of the parasitic disease oodiniasis (Amyloodinium
ocellatum, a dinoflagellate protozoan) infecting captive humphead
wrasse at their facility (Zafran et al., 2005), as well as capsalid
monogenean, or so-called skin flukes, which are the most common
external parasites in mariculture finfish (Koesharyani et al., 2005).
Vibriosis, the most common bacterial disease in marine finfish, has
also been documented in broodstock and young humphead wrasse at the
Gondol Research Station. The infected fish were those that were
captured with cage traps and transported to the station; mortality
occurred within a week after the transportation (Zafran et al., 2005).
Wada et al. (1993) documented the first known report of a
simultaneous infection with an acid-fast bacterium (Mycobacterium sp.)
and an imperfect fungus in a humphead wrasse that was captured in
Indonesia and reared in a commercial fish dealer's concrete aquarium in
Japan. They speculate that the male fish became infected while in
captivity. No other information has been found to indicate that
disease, particularly in the wild, is a factor influencing mortality of
humphead wrasse.
There are no known major predators of adult humphead wrasse, even
in vulnerable locations such as at spawning aggregations. Colin (2010)
reports that no instances of predation on spawning adults were observed
despite the presence of grey reef (Carcharhinus amblyrhynchos) and
white tip (Trianodon obesus) reef sharks. Additionally, few other
piscivorous reef fishes are capable of taking even a moderate-sized
humphead wrasse (Colin, 2010). The predators of juvenile humphead
wrasse are unknown but likely to be sharks and other large-bodied
piscivorous species such as grouper (Serranidae), Jacks (Carangidae),
and snapper (Lutjanidae) that are commonly found on Indo-Pacific coral
reefs.
Based on the best available information, we agree that neither
disease nor predation is increasing the species' extinction risk
presently, or in the foreseeable future.
(D) The Inadequacy of Existing Regulatory Mechanisms
The ERA Team evaluated existing regulatory mechanisms to determine
whether they may be inadequate to address threats to the humphead
wrasse. Existing regulatory mechanisms may include Federal, state, and
international regulations. Below is a brief description and evaluation
of current and relevant domestic and international management measures
that affect the humphead wrasse. More information on these domestic and
international management measures can be found in the status review
report (Graham et al., 2014).
Across the wide Indo-Pacific range of the humphead wrasse, there
exists a
[[Page 57883]]
diversity of regulations. In U.S. waters, most jurisdictions have
regulations that afford partial to complete protection for the species,
and these are, in general, reliably enforced. These include Federal
annual catch limits based on what little is known of abundance,
prohibitions on non-selective and destructive fishing gear (e.g.,
American Samoa and CNMI both ban scuba spearfishing, while Guam
presently does not but is considering such a ban), an assortment of no-
take marine protected areas (MPAs) around CNMI and Guam, and full
prohibition on take around American Samoa and the Pacific Remote Island
Areas.
Internationally, of the 48 countries where humphead wrasses occur,
only about 18 have implemented regulations. This lack of consistent
regulation may be due to abundance data being unknown, undocumented, or
not attended to (e.g., Cambodia, Egypt, Kenya, Saudi Arabia, Somalia,
Sudan, etc.), or the country does not participate in the legal
international trade (e.g., Djibouti, Eritrea, Israel, Madagascar,
Mayotte, Myanmar). Of countries that have regulations, most prohibit
non-selective and destructive gear types, regulate minimum size limits,
significantly reduce or ban export quotas, and/or have tightened
enforcement loopholes--all within the last few years (Gillett, 2010;
Sadovy, 2010; IUCN, 2013; Sadovy, unpublished). Only 12 countries are
known to participate (or have participated) in the legal trade of the
species, while the number of countries participating in the illegal
trade is unquantified. International regulation and effectiveness was
the primary concern in finding that inadequate existing regulations
have a moderate effect on extinction risk of the species.
Other international regulatory authorities include CITES, which
lists the humphead wrasse under Appendix II with the following
provisions: Legal trade is regulated, an export permit is required to
show fish were legally acquired and harvesting is not detrimental to
survival of the species, and the exporting country must have a
functional management plan and associated monitoring. In addition, the
importing country must closely monitor its imports. Sanctions or
complete bans on exports provide strong incentive to comply.
Additionally, the IUCN lists the humphead wrasse as ``endangered''
while affording no regulatory protection; the hope is to promote
awareness of the status of the species.
As previously mentioned, 12 countries report legally trading the
species, ranging from live humphead wrasse to bodies, derivatives, and
meat; of these 12 countries, only 10 countries report exporting live
humphead wrasse. According to CITES (2014) trade data, from 2005-2011,
81,848 live humphead wrasse were legally traded by 10 countries,
whereas in 2012, only 1,691 live humphead wrasse were legally traded,
and only by 5 of the countries. Zero bodies, meat, or derivatives of
the species were traded in 2012 (CITES, 2014).
Legal trade has significantly decreased due to reduced or zero
export quotas, especially from the main exporting countries of
Indonesia, Malaysia, and the Philippines. For example, Indonesia
decreased their export quota of humphead wrasse from 8,000 in 2005 to
1,800 in 2012 (IUCN, 2013), and legally traded only 1,653 in 2012
(CITES, 2014). In 2010, Malaysia reached and has maintained a zero
export quota of the species (Sadovy, 2010; IUCN, 2013; CITES, 2014).
This is significant since Malaysia legally exported ~53,000 live
humphead wrasse from 2007-2009 (CITES, 2014). Moreover, Hong Kong is
now believed to be better controlling trade where it checks imports and
re-exports, and coordinates verification of permits with Malaysia and
Indonesia (Sadovy, 2010). Additionally, countries that formerly
exported for the LRFFT have now banned the export of the species (e.g.,
Australia, Federated States of Micronesia, New Caledonia, Niue, and
Palau) (Gillett, 2010). In other countries, national regulations have
been tightened (e.g., Palau and Fiji), helping to close enforcement
loopholes (Sadovy, 2010). In Indonesia, recent field surveys at seven
``baseline'' sites found increased densities of humphead wrasse at four
sites 4-5 years later. Most fish were juveniles, but the increase in
numbers is encouraging and has occurred in areas where fishing pressure
has evidently declined (IUCN, 2013). At least a decade is believed to
be a conservative time scale for these heavily exploited populations to
begin recovery from fishing pressure following adequate protection
(Colin, 2010).
In the geographic center of the species' range--the Coral Triangle
Region--the humphead wrasse is one of the most valuable species in the
LRFFT, and has been for the past few decades. Countries within the
Coral Triangle region are characterized by large and growing
populations, particularly in coastal areas, where many consider fishing
an occupation of last resort. Many nearshore fish stocks are heavily
harvested, and recent declines in humphead wrasse landings probably
reflect this fact more so than effectiveness of new regulations. In
areas of this region where the LRFFT is not currently operating, any
catch of this species would bring a good price at local markets. Local
regulations to manage the trade that are contradictory to national
regulations also exist in the area and where illegal export is
reportedly rampant (e.g., Philippines).
Misreporting continues to be an illegal, unregulated, and
unreported fishing issue for the LRFFT in Southeast Asia, including
mislabeled fish or fish hidden in exports (CITES, 2010a; CITES, 2010b;
Sadovy et al., 2011). Undocumented shipments continue through
Singapore. However, Hong Kong, the largest importer, has recently
committed to controlling imports, re-exports, and possession within the
territory, thus enabling a more secure system of trade (CITES, 2010a).
Additionally, most countries ban the use of cyanide, though it does
continue in areas due to lack of enforcement and corruption (Erdman and
Pet-Soede, 1997; Pet and Pet-Soede, 1999; Yan, 2011).
Numerous MPAs exist throughout the range of the humphead wrasse. If
adequately enforced, these sufficiently large MPAs might help reduce
threats from the loss and modification of adult or juvenile habitat,
destructive fishing practices, and overutilization. For example, in
areas including Australia, Maldives, and Wake Atoll where some degree
of protection for the species is afforded (e.g., take and possession
prohibited, ban on exports, etc.) and adequately enforced, the risk of
local ``stock'' depletion has been reduced and abundance of humphead
wrasse in the area is stable or increasing (Sadovy et al., 2003 citing
Sluka, 2000; NMFS PIFSC CRED, unpublished data).
In summary, when considered across the entire range of the species,
it is reasonably likely that the various existing regulatory measures
will continue to benefit the humphead wrasse globally by appreciably
reducing the threats to the species, presuming they are adequately
enforced. The greatest threat--the LRFFT--appears to have decreased
substantially, according to recent CITES trade data available through
2012 (CITES, 2014). This reduction in legal trade may be due to either
reduced or zero export quotas, or reduced population sizes of humphead
wrasse stocks within the three main exporting countries of Indonesia,
Malaysia, and Philippines. It can be hoped that with time more
countries will follow suit, implement, and effectively enforce
regulatory mechanisms to prevent the decline of the species and allow
any overexploited
[[Page 57884]]
populations to rebuild. However, it is believed that much illegal and
unreported trade still continues, particularly in the several countries
of the Coral Triangle region. In spite of local pockets of questionable
regulatory compliance, we agree that based on the best available
information, it is unlikely that inadequate existing regulatory
mechanisms alone contribute more than moderately to the extinction risk
for the humphead wrasse across its wide Indo-Pacific range either now,
or in the foreseeable future. The recent implementation of, increased
adherence to, and enforcement of existing regulatory mechanisms
throughout the species' range appear effective in addressing the most
important threat to the species, which is overharvest. Certainty of the
potential effects of inadequate existing regulatory mechanisms on the
extinction risk of the species was deemed medium for now and low in the
foreseeable future. Accordingly, we do not find that inadequacy of
existing regulatory mechanisms is presently, or in the foreseeable
future, placing the species at an increased risk of extinction.
(E.) Other Natural or Manmade Factors Affecting Its Continued Existence
The Status Review Report describes the life history
characteristics, information on competition, and substantial concerns
with regard to climate change and pollution considered by the ERA Team.
The Team concluded that other natural or manmade threats would likely
have some small effects on the extinction risk of the species now and
moderate effects over the foreseeable future, the latter due to
concerns of increased climate change and pollution-related impacts on
the species. Certainty of the potential effects of other natural or
manmade factors on the extinction risk of the species was deemed medium
for now and low in the foreseeable future.
The humphead wrasse may be susceptible to natural and human
perturbations due to particular life history characteristics that
include slow growing, long-lived, and delayed reproductive development
(Choat et al., 2006; Tupper, 2007; Sadovy de Mitcheson et al., 2008;
Colin, 2010). Additionally, adults often occupy consistent home ranges,
have predictable sleeping sites, have discrete spawning locations, and
may form mass aggregations during spawning (Sadovy et al., 2003a).
As for competition with other species for prey, humphead wrasses
are opportunistic diurnal carnivores with a wide-ranging diet. As
previously mentioned, much of its prey is found in sand or rubble
habitats where it feeds on a variety of molluscs, small fishes such as
gobies, moray eels, sea urchins, crustaceans, brittle stars, starfish,
and other invertebrates (Randall et al., 1978; Myers, 1989; Randall et
al., 1997; Thaman, 1998; Sadovy et al., 2003a; Choat et al., 2006). As
generalists, the humphead wrasse is less susceptible to competition for
prey from other predators or fisheries with more specialized diets.
Large-scale impacts such as global climate change may pose a threat
to the humphead wrasse because the species uses inshore habitats and
coral reefs out to depths of up to at least 100 m (Randall, 1978;
Sadovy et al., 2003a; Russell, 2004; Zgliczynski et al., 2013). The
Status Review Report describes the potential threats, including ocean
acidification, increased ocean temperatures, sea level rise, and
extreme weather, in detail. These threats are summarized below.
Although the impacts of ocean acidification specifically to
humphead wrasse are unknown, the threat is anticipated to be greatest
to marine taxa that build skeletons, shells, and tests of biogenic
calcium carbonate such as coral (e.g., Fabry et al., 2008; Guinotte and
Fabry, 2008; Pandolfi et al., 2011). In a meta-analysis, abundances of
species reliant on live coral for food or shelter consistently declined
(e.g., Wilson et al., 2006; Pratchett et al., 2008), while abundance of
some species that feed on invertebrates, algae and/or detritus
increased (e.g., Wilson et al., 2006). As previously discussed,
branching corals are one of several important habitats to various
stages of the humphead wrasse life cycle. Vulnerability of a coral
species to a threat is a function of susceptibility and exposure,
considered at the appropriate spatial and temporal scales. With regard
to localized variability, recent papers identify various mechanisms
that can offset or buffer changes in seawater pH around coral reefs
from ocean acidification, such as photosynthetic uptake of
CO2 by sea grasses and macroalgae in adjacent areas
(Palacios and Zimmerman, 2007; Manzello et al., 2012; Anthony et al.,
2013), and biogeochemical processes within coral reef communities
(Andersson et al., 2013). Other papers identify mechanisms that can
exacerbate changes in seawater pH around coral reefs from ocean
acidification, such as diurnal variability, that can amplify
CO2 in seawater around coral reefs (Shaw et al., 2013).
Ultimately, the future effects of ocean acidification on coral reefs
will be highly variable across coral taxa, space, and time.
Other direct and indirect linkages of ocean acidification effects
to the humphead wrasse remain tenuous. The adult humphead wrasse does
not appear to be food limited or space limited in any portions of its
range. The species also appears to be adaptable to a variety of biotic
and abiotic conditions given its wide geographic range and observations
of it residing (foraging, sleeping) in both shallow and deep water.
Additionally, some researchers have pointed out that increased
CO2 (lower pH) leading to ocean acidification could enhance
seagrass productivity (Palacios and Zimmerman, 2007; Guinotte and
Fabry, 2008; Poloczanska et al., 2009), which may benefit juvenile
humphead wrasse that rely on seagrass beds as nursery areas.
Increased ocean temperatures on large spatial and temporal scales
could generally impact current flow, productivity, physiological
performance and behavior of coral reef fishes and survival of corals.
For example, larval production and survival rates could be negatively
impacted (e.g., Lo-Yat et al., 2010). However, small temperature
increases might accelerate larval development and competency to settle,
though larger temperature increases may be detrimental (Munday et al.,
2008).
Brainard et al. (2011) discusses how coral adaptation and
acclimatization to increased ocean temperatures is possible; that there
is intra-genus variation in susceptibility of coral to bleaching, ocean
acidification, and sedimentation; that at least some coral species have
already expanded their range in response to climate change; and that
not all coral species are seriously affected by ocean acidification.
Such adaptation and acclimation could reduce the impact of warming
temperatures and allow populations to persist across their current
range (Donelson et al., 2011; Logan et al., 2013). The exceptional
complexity, extent, and diversity of coral reef habitat defy simplistic
modeling of reef responses to climate change threats. Likewise, many
aspects of the biology of reef-building corals contribute to complex
responses to ocean warming. This includes capacity for acclimatization
and adaptation to ocean warming, range expansion in response to ocean
warming (Yamano et al., 2011; Yara et al., 2011), and contrasting
ecological interactions resulting from ocean warming (Hughes et al.,
2012; Cahill et al., 2013). All of these contribute to highly variable,
complex and uncertain responses of reef-building coral species and in
turn, coral reefs to
[[Page 57885]]
climate change threats like ocean warming.
The impacts of sea level rise to coral reef ecosystems also remains
uncertain. Theoretically, a rise in sea level could potentially provide
additional habitat for corals living near the sea surface. There are
now studies documenting that during periods of higher water levels,
coral cover increases on reef flats (Brown et al., 2011;
Scop[eacute]litis et al., 2011). On the other hand, if coral growth is
unable to keep pace with sea level rise, there will most likely be
negative consequences.
As for the effects of climate change to prey species of the
humphead wrasse, direct and indirect effects are again variable and
complex. Climate change can affect marine organisms both directly via
physiological stress and indirectly via changing relationships among
species (Harley, 2011). Shifts in distribution and abundance of prey
can potentially be driven by changes in temperature and ocean chemistry
(Harley et al., 2006). Although humphead wrasses do not feed directly
on corals, many of their prey do rely on corals, sea grass beds, or
mangroves for their own food or shelter. The wide variety of humphead
wrasse prey is found in various habitats and across a vast depth range
of a few meters to at least 100 m. Coral communities found at greater
depths have shown thermal refuge from increased temperatures while
those found in more shallow areas are more impacted (e.g., Graham et
al., 2008; Bridge et al., 2014). For example, sea urchin fertilization
may be compromised by warmer temperatures (Byrne et al., 2009). While
urchins found in more shallow areas may have reduced or compromised
fertilization and development, urchins found at deeper depths may be
less impacted. Urchins are also less susceptible to increased ocean
acidification (Byrne et al., 2009). In another example of variable
impacts, Harley (2011) conducted an experiment and found that prey
species were able to occupy a hot, extralimital site if predation
pressure was experimentally reduced. As a result, local species
richness more than doubled, suggesting that anthropogenic climate
change can alter interspecific interactions and produce unexpected
changes in species distribution, community structure, and diversity
(Harley, 2011). Overall, some humphead wrasse prey may likely be
negatively impacted by climate change; however, not all prey will be
impacted equally. Given that humphead wrasse are foraging generalists
and feed on a wide variety of prey found in various habitats and
depths, impacts are likely to be less than if they were foraging
specialists like other reef fish species (i.e., bumphead parrotfish)
that feed primarily on corals.
In summary, the extent of potential direct and indirect effects of
climate change on the humphead wrasse are unknown or speculative as the
threats described in the literature are broad and general, and
typically use another species as a proxy to infer vulnerability.
Lastly, contaminants such as fuel and crude oil from spills, land-
based pollution from agriculture, etc. that find its way into the
marine environment, sewage effluent from areas with insufficient
sanitation systems, and marine debris from discarded or lost fishing
gear are all potential sources of pollution that could directly and
indirectly affect the humphead wrasse. However, such events including
oil and sewage spills are typically episodic and localized. Other types
of pollution such as land-based contaminants and marine debris may also
impact the humphead wrasse, but the direct extent of the effects to the
humphead wrasse and its habitat are speculative at this time. As such,
the Team determined that these other natural and manmade factors
collectively would likely have some small effects on the extinction
risk of the species now and moderate effects over the foreseeable
future.
Therefore, based on the best available information, although the
Team identified the threat of other natural or manmade factors, such as
climate change and pollution, as having a small-to-moderate effect on
the species' risk of extinction, we do not find that other natural or
manmade factors are presently, or in the foreseeable future, placing
the species at an increased risk of extinction.
Significant Portion of Its Range
The definitions of both ``threatened'' and ``endangered'' under the
ESA contain the term ``significant portion of its range'' (SPOIR) as an
area smaller than the entire range of the species that must be
considered when evaluating a species' risk of extinction. With regard
to SPOIR, the Services proposed a ``Draft Policy on Interpretation of
the Phrase `Significant Portion of Its Range' in the Endangered Species
Act's Definitions of `Endangered Species' and `Threatened Species' ''
(76 FR 76987; December 9, 2011), which is consistent with our past
practice as well as our understanding of the statutory framework and
language. The Draft Policy was recently finalized on July 1, 2014, (79
FR 37578), and the Services are now to consider the interpretations and
principles contained in the Final Policy as binding guidance in making
individual listing determinations, while taking into account the unique
circumstances of the species under consideration. However, the policy
remained in the draft form when the ERA Team discussed whether the data
indicated if any portion of the humphead wrasse's range is more
significant than another portion.
The ERA Team considered whether a portion of the species' range is
more important than any other portion, and that without that portion,
the species would be in danger of extinction. With this in mind, the
ERA Team agreed that of the entire range of the species, the primary
region that has exhibited a decline of the humphead wrasse, which
comprises the three countries in the core-Coral Triangle area, might
meet the definition of a SPOIR. These countries are Indonesia,
Malaysia, and the Philippines, and have large and growing human
populations with coincident agricultural expansion and coastal
development impacts on humphead wrasse habitat. As this area is the
center of the species' range, the Team also discussed physical,
ecological, and behavioral factors in relation to recruitment between
the potential SPOIR area and the rest of the species' range. The Team
concluded that local extinction of humphead wrasse in these three
countries would not cause the remainder of the species to become in
danger of extinction. Islands and archipelagoes outside the core-Coral
Triangle area (i.e., Papua New Guinea and the Solomon Islands in the
east or Australia to the south) are comparatively healthy with fewer
impacts to the species. Humphead wrasse in these other areas are not
dependent on aggregations in Indonesia, Malaysia, or the Philippines
for larval recruitment or other aspects of survival; in fact, the ERA
Team concluded that these nearby areas could provide recruits to
recolonize the core-Coral Triangle portion of the range in the event
that local extirpations were to occur inside that area. Thus, the
status of the rest of the species was not considered to be dependent on
the continued existence of the population in these three countries of
Indonesia, Malaysia, and the Philippines. The main purpose for improved
conservation in this core area of the species' range would be the
recovery of the populations located there, and not the status of the
rest of the population. Therefore, after a review of the best available
information, the ERA Team concluded, and we agree, that data do not
indicate any portion of the
[[Page 57886]]
humphead wrasse's range meets the definition of a SPOIR. As such, when
considering the overall extinction risk of the species, we considered
it throughout the species' entire range.
Under the Final SPOIR Policy, the definition of ``significant'' has
been revised to a lower threshold and now states ``A portion of the
range of a species is `significant' if the species is not currently
endangered or threatened throughout its range, but the portion's
contribution to the viability of the species is so important that,
without the members in that portion, the species would be in danger of
extinction or likely to become so in the foreseeable future, throughout
all of its range'' (emphasis added). Despite this revision, we continue
to find that the data do not indicate any portion of the humphead
wrasse's range meets the definition of a SPOIR. Thus, the overall
extinction risk of the species is considered throughout the species'
entire range.
Overall Risk Summary
As a final step in their analysis, the ERA Team voted on the
overall risk of extinction to the humphead wrasse based on the
information the Team reviewed in its demographic risk analysis, as
modified by the information reviewed in the threats assessment.
Likelihood points attributed to the current level of extinction risk
categories were as follows, with the first number representing the
total votes by Team members and the second number representing the
total possible votes, which was 40: No Risk (25/40), Low Risk (13/40),
Moderate Risk (2/40). None of the Team members placed a likelihood
point in either the ``High Risk'' or ``Very High Risk'' categories,
indicating their strong consensus that the species is not currently at
a high or very high risk of extinction. Thus, the Team found, and we
agree, that the species is not presently at risk of extinction. The
Team expressed this view with a high relative certainty with regard to
the available information.
For the level of extinction risk of the humphead wrasse in the
foreseeable future, the ERA Team found, and we agree, that the species
would be at low overall risk of extinction. Likelihood points
attributed to each risk category in the foreseeable future were as
follows: No Risk (15/40), Low Risk (18/40), Moderate Risk (7/40).
Again, none of the Team members placed a likelihood point in either the
``High Risk'' or ``Very High Risk'' categories, indicating their strong
consensus that the species will not be at a high or very high risk of
extinction in the foreseeable future. The Team viewed the certainty of
information for the foreseeable future as being low.
Overall, there was a high degree of consensus among the members of
the Team, and we agree, that the humphead wrasse's risk of extinction
presently and in the foreseeable future is no-to-low risk. Although the
humphead wrasse is naturally rare throughout its range and in some
places abundance has declined, this no-to-low risk of extinction is
based primarily on the species' sustained widespread distribution
throughout most of its known range, and its recent effective protection
from exploitation at a variety of localities under both U.S. and
foreign jurisdiction.
Final Determination
Section 4(b)(1) of the ESA requires that NMFS make listing
determinations based solely on the best scientific and commercial data
available after conducting a review of the status of the species and
taking into account those efforts, if any, being made by any state or
foreign nation, or political subdivisions thereof, to protect and
conserve the species. We have independently reviewed the best available
scientific and commercial information including the petition, public
comments submitted on the 90-day finding (78 FR 13614; February 28,
2013), the status review report (Graham et al., 2014), and other
published and unpublished information, and have consulted with species
experts and individuals familiar with humphead wrasse. We considered
each of the five ESA statutory factors to determine whether it
presented an extinction risk to the species on its own. Additionally,
we do not find that the combination of factors poses an extinction
risk. As required by the ESA, section 4(b)(1)(a), we also took into
account efforts to protect humphead wrasse by territories, foreign
nations, and others and evaluated whether those efforts provide a
conservation benefit to the species. As previously explained, no
portion of the species' range is considered significant and we did not
find biological evidence that would indicate that any population
segment of the humphead wrasse would qualify as a DPS under the DPS
Policy. Therefore, our determination set forth below is based on a
synthesis and integration of the foregoing information, factors and
considerations, and their effects on the status of the species
throughout its entire range.
We conclude that the humphead wrasse is not presently in danger of
extinction, nor is it likely to become so in the foreseeable future
throughout all of its range. We summarize the factors supporting this
conclusion as follows: (1) The species is made up of a single
population over a broad geographic range, with no barrier to dispersal;
(2) its current range is unaltered from the range identified by surveys
since the 1970s and although there are some concerns related to the
species' habitat, there is no evidence of substantial or widespread
habitat loss or destruction; (3) although the species has predictable
home ranges and sleeping sites, and possesses life history
characteristics that may increase its vulnerability to impacts of
fishing in reef fish assemblages, its risk of extinction due to low
productivity is not of significant concern; (4) the best available
information indicates that abundance is naturally low across the
species' range, and although populations have declined in some areas
because of fishing mortality, many populations, especially those in
U.S. waters, are either stable, show no clear trend, or may be
increasing; (5) although there is no formal estimate on the current
global population size, it is likely sufficient to maintain population
viability into the foreseeable future; (6) the main threat to the
species is overutilization in the live reef food fish trade; however,
legal trade of the species has decreased substantially over recent
years due to reduced or zero export quotas, especially from the three
main exporting countries within the Coral Triangle region; (7) there is
no evidence that disease or predation is contributing to increasing the
risk of extinction of the species; (8) recent implementation of,
increased adherence to, and enforcement of existing regulatory
mechanisms throughout the species' range appear effective in addressing
the most important threat to the species (overharvest); and (9)
although there is some concern with regard to effects from other
natural or manmade factors, such as climate change and pollution, the
evidence does not suggest that the species is at risk of extinction
from these factors.
Based on these findings, we conclude that the humphead wrasse is
not presently in danger of extinction throughout all or a significant
portion of its range nor is it likely to become so within the
foreseeable future. Accordingly, the humphead wrasse does not meet the
definition of a threatened or endangered species and therefore the
humphead wrasse does not warrant listing as threatened or endangered at
this time. However, it will remain on our Species of Concern list and
we will encourage research on the status of the species for use in
future status reviews.
[[Page 57887]]
References
A complete list of all references cited herein is available upon
request (see FOR FURTHER INFORMATION CONTACT).
Authority
The authority for this action is the Endangered Species Act of
1973, as amended (16 U.S.C. 1531 et seq.).
Dated: September 22, 2014.
Samuel D. Rauch, III.,
Deputy Assistant Administrator for Regulatory Programs, National Marine
Fisheries Service.
[FR Doc. 2014-23034 Filed 9-25-14; 8:45 am]
BILLING CODE 3510-22-P