[Federal Register Volume 80, Number 90 (Monday, May 11, 2015)]
[Notices]
[Pages 26899-26914]
From the Federal Register Online via the Government Publishing Office [www.gpo.gov]
[FR Doc No: 2015-11305]
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DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration
[Docket No. 150114043-5407-01]
RIN 0648-XD722
Endangered and Threatened Wildlife and Plants: Notice of 12-Month
Finding on a Petition To List the Undulate Ray and the Greenback
Parrotfish as Threatened or Endangered Under the Endangered Species Act
(ESA)
AGENCY: National Marine Fisheries Service (NMFS), National Oceanic and
Atmospheric Administration (NOAA), Commerce.
ACTION: Status review; notice of finding.
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SUMMARY: We, NMFS, have completed comprehensive status reviews under
the Endangered Species Act (ESA) for two foreign marine species in
response to a petition to list those species. These species are the
undulate ray (Raja undulata) and the greenback parrotfish (Scarus
trispinosus). We have determined that, based on the best scientific and
commercial data available, listing the undulate ray under the ESA is
not warranted and listing the greenback parrotfish under the ESA is not
warranted. We conclude that the undulate ray and the greenback
parrotfish are not currently in danger of extinction throughout all or
a significant portion of their respective ranges and are not likely to
become so within the foreseeable future.
DATES: The finding announced in this notice was made on May 11, 2015.
ADDRESSES: You can obtain the petition, status review reports, the 12-
month finding, and the list of references electronically on our NMFS
Web site at http://www.nmfs.noaa.gov/pr/species/petition81.htm.
FOR FURTHER INFORMATION CONTACT: Ronald Salz, NMFS, Office of Protected
Resources (OPR), (301) 427-8171.
SUPPLEMENTARY INFORMATION:
Background
On July 15, 2013, we received a petition from WildEarth Guardians
to list 81 marine species or subpopulations as threatened or endangered
under the Endangered Species Act (ESA). This petition included species
from many different taxonomic groups, and we prepared our 90-day
findings in batches by taxonomic group. We found that the petitioned
actions may be warranted for 24 of the species and 3 of the
subpopulations and announced the initiation of status reviews for each
of
[[Page 26900]]
the 24 species and 3 subpopulations (78 FR 63941, October 25, 2013; 78
FR 66675, November 6, 2013; 78 FR 69376, November 19, 2013; 79 FR 9880,
February 21, 2014; and 79 FR 10104, February 24, 2014). This document
addresses the 12-month findings for two of these species: undulate ray
(Raja undulata) and greenback parrotfish (Scarus trispinosus). Findings
for seven additional species and two subpopulations can be found at 79
FR 74853 (December 16, 2014), 80 FR 11363 (March 3, 2015), and 80 FR
15557 (March 24, 2015). The remaining 15 species and one subpopulation
will be addressed in subsequent findings.
We are responsible for determining whether species are threatened
or endangered under the ESA (16 U.S.C. 1531 et seq.). To make this
determination, we consider first whether a group of organisms
constitutes a ``species'' under the ESA, then whether the status of the
species qualifies it for listing as either threatened or endangered.
Section 3 of the ESA defines a ``species'' to include ``any subspecies
of fish or wildlife or plants, and any distinct population segment of
any species of vertebrate fish or wildlife which interbreeds when
mature.'' On February 7, 1996, NMFS and the U.S. Fish and Wildlife
Service (USFWS; together, the Services) adopted a policy describing
what constitutes a distinct population segment (DPS) of a taxonomic
species (the DPS Policy; 61 FR 4722). The DPS Policy identified two
elements that must be considered when identifying a DPS: (1) The
discreteness of the population segment in relation to the remainder of
the species (or subspecies) to which it belongs; and (2) the
significance of the population segment to the remainder of the species
(or subspecies) to which it belongs. As stated in the DPS Policy,
Congress expressed its expectation that the Services would exercise
authority with regard to DPSs sparingly and only when the biological
evidence indicates such action is warranted. Based on the scientific
information available, we determined that the undulate ray (Raja
undulata) and the greenback parrotfish (Scarus trispinosus) are both
``species'' under the ESA. There is nothing in the scientific
literature indicating that either of these species should be further
divided into subspecies or DPSs.
Section 3 of the ESA defines an endangered species as ``any species
which is in danger of extinction throughout all or a significant
portion of its range'' and a threatened species as one ``which is
likely to become an endangered species within the foreseeable future
throughout all or a significant portion of its range.'' We interpret an
``endangered species'' to be one that is presently in danger of
extinction. A ``threatened species,'' on the other hand, is not
presently in danger of extinction, but is likely to become so in the
foreseeable future. In other words, the primary statutory difference
between a threatened and endangered species is the timing of when a
species may be in danger of extinction, either presently (endangered)
or in the foreseeable future (threatened).
When we consider whether a species might qualify as threatened
under the ESA, we must consider the meaning of the term ``foreseeable
future.'' It is appropriate to interpret ``foreseeable future'' as the
horizon over which predictions about the conservation status of the
species can be reasonably relied upon. The foreseeable future considers
the life history of the species, habitat characteristics, availability
of data, particular threats, ability to predict threats, and the
reliability to forecast the effects of these threats and future events
on the status of the species under consideration. Because a species may
be susceptible to a variety of threats for which different data are
available, or which operate across different time scales, the
foreseeable future is not necessarily reducible to a particular number
of years. In determining an appropriate ``foreseeable future''
timeframe for the undulate ray and the greenback parrotfish, we
considered both the life history of the species and whether we could
project the impact of threats or risk factors through time. For the
undulate ray, we could not define a specific number of years as the
``foreseeable future'' due to uncertainty regarding life history
parameters of, and threats to, the species. For the greenback
parrotfish, the foreseeable future was defined as approximately 40
years, based on this species' relatively long life span (estimated at
23 years [Previero, 2014a]), which means threats can have long-lasting
impacts.
On July 1, 2014, NMFS and USFWS published a policy to clarify the
interpretation of the phrase ``significant portion of its range'' (SPR)
in the ESA definitions of ``threatened'' and ``endangered'' (the SPR
Policy; 76 FR 37578). Under this policy, the phrase ``significant
portion of its range'' provides an independent basis for listing a
species under the ESA. In other words, a species would qualify for
listing if it is determined to be endangered or threatened throughout
all of its range or if it is determined to be endangered or threatened
throughout a significant portion of its range. The policy consists of
the following four components:
(1) If a species is found to be endangered or threatened in only an
SPR, the entire species is listed as endangered or threatened,
respectively, and the ESA's protections apply across the species'
entire range.
(2) A portion of the range of a species is ``significant'' if its
contribution to the viability of the species is so important that,
without that portion, the species would be in danger of extinction or
likely to become so in the foreseeable future, throughout all of its
range.
(3) The range of a species is considered to be the general
geographical area within which that species can be found at the time
USFWS or NMFS makes any particular status determination. This range
includes those areas used throughout all or part of the species' life
cycle, even if they are not used regularly (e.g., seasonal habitats).
Lost historical range is relevant to the analysis of the status of the
species, but it cannot constitute an SPR.
(4) If a species is not endangered or threatened throughout all of
its range but is endangered or threatened within an SPR, and the
population in that significant portion is a valid DPS, we will list the
DPS rather than the entire taxonomic species or subspecies.
We considered this policy in evaluating whether to list the
undulate ray and greenback parrotfish as endangered or threatened under
the ESA.
Section 4(a)(1) of the ESA requires us to determine whether any
species is endangered or threatened due to any one or a combination of
the following five threat factors: The present or threatened
destruction, modification, or curtailment of its habitat or range;
overutilization for commercial, recreational, scientific, or
educational purposes; disease or predation; the inadequacy of existing
regulatory mechanisms; or other natural or manmade factors affecting
its continued existence. We are also required to make listing
determinations based solely on the best scientific and commercial data
available, after conducting a review of the species' status and after
taking into account efforts being made by any state or foreign nation
to protect the species.
In assessing extinction risk of these two species, we considered
the demographic viability factors developed by McElhany et al. (2000)
and the risk matrix approach developed by Wainwright and Kope (1999) to
organize and summarize extinction risk considerations. The approach of
considering demographic risk factors to
[[Page 26901]]
help frame the consideration of extinction risk has been used in many
of our status reviews (see http://www.nmfs.noaa.gov/pr/species for
links to these reviews). In this approach, the collective condition of
individual populations is considered at the species level according to
four demographic viability factors: abundance, growth rate/
productivity, spatial structure/connectivity, and diversity. These
viability factors reflect concepts that are well-founded in
conservation biology and that individually and collectively provide
strong indicators of extinction risk.
Scientific conclusions about the overall risk of extinction faced
by the undulate ray and greenback parrotfish under present conditions
and in the foreseeable future are based on our evaluation of the
species' demographic risks and section 4(a)(1) threat factors.
Assessment of overall extinction risk considered the likelihood and
contribution of each particular factor, synergies among contributing
factors, and the cumulative impact of all demographic risks and threats
on the species.
Status reviews for the undulate ray and the greenback parrotfish
were conducted by NMFS OPR staff. In order to complete the status
reviews, we compiled information on the species' biology, ecology, life
history, threats, and conservation status from information contained in
the petition, our files, a comprehensive literature search, and
consultation with experts. We also considered information submitted by
the public in response to our petition findings. Draft status review
reports were also submitted to independent peer reviewers; comments and
information received from peer reviewers were addressed and
incorporated as appropriate before finalizing the draft reports. The
undulate ray and greenback parrotfish status review reports are
available on our Web site (see ADDRESSES section). Below we summarize
information from these reports and the status of each species.
Status Reviews
Undulate Ray
The following section describes our analysis of the status of the
undulate ray, Raja undulata.
Species Description
The undulate ray, Raja undulata, is a member of the Family Rajidae
whose origin is from the Late Cretaceous period, about 100 to 66
million years ago. Species diversification within the Family Rajidae
occurred 15 to 2 million years ago in the northeast Atlantic and
Mediterranean, where undulate rays exist today (Valsecchi et al.,
2004). The undulate ray is part of the Rajini tribe, which is a
taxonomic category above the genus and below the family level. The
Rajini tribe is defined by two morphological characteristics: (1) Disc
free of denticles, and (2) crowns of alar thorns (sharp-pointed,
recurved thorns located on the outer aspect of pectoral fins of mature
males) with barbs (McEachran and Dunn, 1998).
The undulate ray gets its name from the leading edge of the disc,
which undulates from the snout to the wingtips during movement. Its
dorsal color ranges from almost black to light yellow-brown
interspersed with dark wavy bands lined by a twin row of white spots,
which may camouflage them against the seabed. The underbelly is white
with dark margins. The dorsal fins are widely spaced, normally with two
dorsal spines between them. The undulate ray is relatively large,
reaching 114 cm in total length (TL) as an adult (Ellis et al., 2012).
Growth rates, size and age at maturity, and seasonal patterns of
reproduction in undulate rays were determined from individuals taken
from trammel nets, beach seines, and fish markets in Portugal (Coelho
and Erzini, 2002; Coelho and Erzini, 2006; Moura et al., 2007). The
undulate ray exhibits rapid growth in the first year, but overall has a
slower growth rate compared to most species of Raja (n = 187; Von
Bertalanffy growth L[infin] = 110.22 cm, K = 0.11 per year and
t0 = -1.58 year) (Coelho and Erzini, 2002). Females appear
to become sexually mature later in life and at a larger body size than
males (Coelho and Erzini, 2006; Moura et al., 2007; Serra-Pereira et
al., 2013). In the Algarve estuary along the south coast of Portugal,
the mean age and body size at which half of the females became sexually
mature was 8.98 years and 76.2 cm TL. Half of the males became sexually
mature at 7.66 years and a body size of 73.6 cm TL (Coelho and Erzini,
2006). This means that half of the females in the Algarve estuary
became mature at 86.3 percent of their maximum size and 69.1 percent at
their maximum age and half of the males became mature at 88.5 percent
of maximum size and 63.8 percent at maximum age. This makes the
undulate ray, at least for this study area, a late maturing species
(Coelho and Erzini, 2006). Moura et al. (2007) found slightly larger
values for length at maturity for both females (83.8 cm TL) and males
(78.1 cm TL) in the Peniche region on the central coast of Portugal,
which may indicate two different populations of the undulate ray exist
on the Portuguese continental shelf (Moura et al., 2007). However, low
sample sizes and different survey methods may account for the
differences found between the study areas (Ellis, CEFAS, 2014 personal
communication). St[eacute]phan et al. (2013) reported the minimum
length at maturity for males captured in the English Channel and Bay of
Biscay was 74 cm TL, with 50 percent of the sample (n = 191) reaching
maturity at 80 cm TL.
Estimated generation length (the age at which half of total
reproductive output is achieved by an individual) for this species
varies from 14.9 to 15.9 years in females and from 14.3 to 15.3 years
in males (Coelho et al., 2009). Based on an analysis of vertebral band
deposits of 187 undulate rays caught in commercial fisheries in the
Algarve estuary, the oldest individuals were estimated to be 13 years
old, but overall longevity for this species has been estimated to be
around 21-23 years (Coelho et al., 2002).
The undulate ray is a seasonal breeder; however, temporal
differences in breeding season were found between nursery areas (Moura
et al., 2007). Individuals from the Algarve region in south Portugal
were found to breed only in the winter (Coelho and Erzini, 2006), those
from Peniche in central Portugal were found to breed from February
through May (Moura et al., 2007; Serra-Pereira et al., 2013), and in
Portugal's north central coast, breeding occurred from December through
June (Serra-Pereira et al., 2013). Water temperatures in the Peniche
region are colder than those in the Algarve, which may explain the
longer breeding season observed there (Moura et al., 2007).
The undulate ray is oviparous, in that the fertilized egg, which is
encased in an egg capsule, hatches outside of the parental body (Moura
et al., 2008). Egg cases measure 70-90 mm long and 45-60 mm wide.
Typical reproductive output is unknown; however, one female was
observed to lay 88 egg cases over 52 days and the incubation period was
91 days (Shark Trust, 2009). In general, Rajidae exhibit protracted
incubation times ranging from 4 to 15 months (Serra-Pereira et al.,
2011).
Information on sex ratios in the population is sparse, but appears
to indicate a slight female bias in some areas and significant male
bias in other areas. In the eastern English Channel, individuals
collected in bottom trawl surveys were slightly female-biased at 57
percent female and 43 percent male (Martin et al., 2010). Undulate rays
caught in the Bay of Biscay, France, by fishermen, fishing guides, and
scientists
[[Page 26902]]
were generally 48 to 95 cm in total length and the sex ratio was 54
percent female and 46 percent male (Delamare et al., 2013). Other
studies have found a preponderance of males. During three gillnet
fisheries trips in May 2010 and two trips in February-March 2011 off
the Isle of Wight in the English Channel, the ratio of females to males
was 1:4.5 and 1:6.0, respectively, and all were mature adults (Ellis et
al., 2012).
Undulate ray habitat in the northeastern Atlantic Ocean includes
sandy and coarse bottoms from the shoreline to no deeper than 200 m,
but undulate rays are generally found in waters less than 50 m deep
(Saldnaha, 1997 as cited in Coelho and Erzini, 2006; Martin et al.,
2010; Martin et al., 2012; Ellis et al., 2012). Undulate rays,
especially juveniles, inhabit inshore waters, including lagoons, bays,
rias (defined as a coastal inlet formed by the partial submergence of a
river valley that is not covered in glaciers and remains open to the
sea), and outer parts of estuaries (Ellis et al., 2012).
The English Channel provides important habitat for the undulate ray
(Martin et al., 2010; Martin et al., 2012). The main predictors of
elasmobranch habitat in the English Channel were depth, bed shear
stress (an estimate of the pressure exerted across the seabed by tidal
forcing), and stability, followed by seabed sediment type and
temperature (Martin et al., 2010). The undulate ray was found more
frequently in the western area of the English Channel, particularly in
the area between the Cherbourg Peninsula and Isle of Wight, where the
seabed is hard (pebble) and tidal currents strong. However, the species
was also reported in patches of lower density in some shallower coastal
waters in the eastern part of the English Channel (Martin et al., 2010;
Martin et al., 2012). Based on counts of egg cases recorded on beaches
along the south coast of England, areas to the west and east of the
Isle of Wight may be important nursery areas for the undulate ray
(Dorset Wildlife Trust, 2010).
The Gironde estuary of France provides important sand and mud
bottom habitat for the undulate ray (Lobry et al., 2003). Tides are
strong within the estuary (average flow volume between 800 and 1,000
m\3\/s) and turbidity is high, frequently exceeding 400 mg/L. The
undulate ray is one of the most common species found in the coastal
waters of the Tagus estuary in the central and west coast of Portugal
(Prista et al., 2003). About 60 percent of the estuary is exposed at
low tide, revealing soft bottom habitat. However, specific data are
lacking on the undulate ray's distribution and association with
specific habitat within the estuary.
In waters off Portugal, the undulate ray diet changed as
individuals grew and matured. Smaller individuals had a generalized
diet, consuming a variety of semi-pelagic and benthic prey, including
shrimps and mysids. However, larger undulate rays began to specialize
on the brachyuran crab, Polybius henslowi, with the largest undulate
rays eating this prey item almost exclusively (Moura et al., 2008). The
shift in diet from semi-pelagic and benthic species to primarily
benthic crabs occurred at 55 cm TL, and the shift from more generalized
to specialized diet occurred at 75 cm TL. The first shift may be due to
juveniles migrating from nursery to foraging habitat, and the second
shift may be related to the onset of maturity (Moura et al., 2008).
Population Abundance, Distribution, and Structure
The undulate ray occurs on the continental shelf of the northeast
Atlantic Ocean, ranging in the north from southwest Ireland and the
English Channel, south to northwest Africa, west to the Canary Islands,
and east into the Mediterranean Sea (Serena, 2005; Coelho and Erzini,
2006; Ellis et al., 2012). The undulate ray exhibits a patchy
distribution throughout its range. According to ICES (2008), the patchy
distribution of the undulate ray may have existed as far back as the
1800s. It is locally abundant at sites in the central English Channel,
Ireland, France, Spain, and Portugal (Ellis et al., 2012). Within the
Mediterranean Sea, occasional records occur off Israel and Turkey, but
they are mainly recorded from the western region off southern France
and the Tyrrhenian Sea (Serena, 2005; Ellis et al. 2012). In 2001, a
few specimens were recorded in bottom trawl hauls on the continental
shelf of the Balearic Islands off the Iberian Peninsula (western
Mediterranean) (Massut[iacute] and Moranta, 2003; Massut[iacute] and
Re[ntilde]ones, 2005). Specimens have also been reported in the
southern North Sea and Bristol Channel, but these areas are outside the
normal distribution range (Ellis et al., 2012).
Few data exist regarding undulate ray population structure. Tagging
studies were conducted in French waters from 2012 through 2014 to
determine population structuring of the undulate ray in the English
Channel, central Bay of Biscay, Iroise Sea, South Brittany, and
Morocco, North Africa (Delamare et al., 2013). Preliminary data from
the Bay of Biscay and western English Channel indicate undulate rays do
not migrate great distances. In the central Bay of Biscay, 1,700
undulate rays were tagged from April 2012 through May 2013. Of the rays
tagged, 98 were recaptured within 450 days of tagging, mainly within 30
km of the tagging location; about two-thirds were recaptured within 10
km, indicating high site fidelity. The number of days between capture
and recapture did not affect the distances between the two points, also
supporting high site fidelity (Delamare et al., 2013). The central part
of the Bay of Biscay may host a closed population exhibiting a small
degree of emigration and immigration (Delamare et al., 2013). Mark and
recapture studies in the western English Channel around the Island of
Jersey also indicate high site fidelity (Ellis et al., 2011). Discrete
populations may also occur in the bays of southwest Ireland (ICES,
2007; ICES, 2013).
The ICES Working Group on Elasmobranch Fishes (2013) recommended
the species be managed as five separate stocks: (1) English Channel;
(2) southwest Ireland; (3) Bay of Biscay; (4) Cantabrian Sea; and (5)
Galicia and Portugal. However, the recommendation was based only on the
species' patchy distribution and not direct evidence of population
structure. Data are lacking on population structure based on
behavioral, morphological, and genetic characteristics.
Determining population size or trends is difficult due to the
patchy distribution of the species, variable survey effort and survey
methods over time, inconsistent metrics for reporting abundance,
temporally limited (less than 20 years) data sets, and species
misidentification. Prior to 2009, the undulate ray was often classified
at a higher taxonomic level, i.e. miscellaneous rays and skates
(LeBlanc et al., 2013); thus, the species was an unknown percentage of
a larger sample and was likely underrepresented in the landings data.
Trends based on fisheries landings have limited utility in
understanding true population trends. Restrictions and catch limits
have been implemented for the undulate ray at least since 2009; thus,
any reported decline in recent species-specific landings may be more
reflective of changes in fisheries practices, effort, and regulations
rather than changes in species abundance (see Ellis et al., 2010).
Fisheries-independent bottom trawl surveys were conducted in the
eastern English Channel each October from 1988 through 2008 (Martin et
al., 2010; Martin et al., 2012). During this period 1,800 hauls were
made and 16 different elasmobranch species were captured.
[[Page 26903]]
The undulate ray was the eighth most abundant elasmobranch in terms of
individuals caught and percent total biomass (Martin et al., 2010).
Mean densities of undulate ray fluctuated dramatically from 1988
through 2008, and no trend could be detected. The undulate ray was
present in 3.8 percent of the fisheries-independent bottom trawl survey
hauls from 1988-1996 and 3.8 percent of hauls from 1997-2008,
indicating stability in presence in the area (Martin et al., 2010).
Fisheries-independent beam trawl surveys have been conducted in the
eastern and western English Channel each year since 1989. In the
eastern English Channel survey, undulate ray catch rates were generally
low and variable, partly due to its patchy distribution. For the period
1993-2013, mean number of individuals caught per hour of survey effort
ranged from a low of zero (in 2006 and 2007) to between 0.25 and 0.30
(in 1996, 2009, 2012-2013) (ICES, 2014a). In the western English
Channel beam trawl survey, undulate ray catch rates were also generally
low and variable from 1989-2011 (Burt et al., 2013), with an apparent
decreasing trend after 2004. Mean relative abundance was zero in 6 out
of 7 years from 2005-2011. However, preliminary results from surveys
conducted in 2012-2013 of fishermen operating in the western English
Channel indicate that the undulate ray is a main species caught,
representing approximately 75 percent of the ray catch in trawl,
dredge, gillnet, and longline gear (LeBlanc et al., 2013). The English
Channel undulate ray stock status was considered uncertain and
classified by ICES as a ``data-limited stock'' with a precautionary
margin of 20 percent recommended for fishery management (ICES, 2012).
The ``precautionary margin'' is a 20 percent reduction to catch advice
that serves as a buffer when reference points for stock size or
exploitation (e.g., maximum sustainable yield) are unknown (ICES,
2012).
In the southern region of the North Sea, the undulate ray may be a
rare vagrant, but it is absent further north (Ellis et al., 2005). From
1990-1995, beam trawl surveys conducted in coastal waters of the
eastern North Sea, English Channel, Bristol Channel, and Irish Sea
indicated that the undulate ray was the least common of seven ray
species collected (Rogers et al., 1998a). Overall abundance in the
British Isles was low (<8 individuals per hour per ICES survey area)
(Ellis et al., 2005). The undulate ray was reported in trawl surveys
conducted from 1973 to 1997 along the south coasts of England (0.003
individuals per 1000 m\2\), but is absent from other parts of the
survey grid (Rogers and Millner, 1996; Rogers et al., 1998b). Juveniles
were infrequent catches in the surveys (Rogers et al., 1998b). Cooler
water temperatures may explain the absence of the undulate ray in
sampling stations along the more northern coast of England (Rogers and
Millner, 1996).
Catch of undulate ray was reported by two charter vessels from
Tralee Bay, southwestern Ireland, for the years 1981 through 2005
(ICES, 2007). Although effort data were not reported, the overall catch
trend suggests a decline in abundance. Undulate ray catch was at a high
of 80-100 fish per year in the first 2 years of reporting (1980-1981),
declined to 20-30 fish per year by the mid-1990s, increased to about
40-60 fish per year at the turn of the century, and declined again from
2001 through 2005, although catches fluctuated each year (ICES, 2007).
Tag and release data collected in the recreational fishery throughout
southwestern Ireland, including Tralee Bay, from 1972-2014 indicate a
decline since the 1970s, but potential changes in fishing effort were
not provided (ICES, 2014b).
The Tagus estuary, in the central and west coast of Portugal, was
surveyed between 1979 and 1981 and from 1995 through 1997 to determine
fish abundance and diversity (Cabral et al., 2001). The undulate ray
was a common species, usually in the top 3 to 5 most common species
found in the surveys over time. Mean density was similar or even
slightly increased over the sampling period (less than 0.01/1,000 m\2\
in 1979 and 1995; 0.01/1,000 m\2\ in 1996; 0.03/1,000 m\2\ in 1997)
(Cabral et al., 2001). More recent data reflecting the current status
of the undulate ray in the Tagus estuary were not available.
French landings data on the undulate ray for the Celtic Sea from
1995-2001 show a declining trend from a high of 12 t in 1995 to a low
of 0 t in 2000 and 2001 (ICES, 2007). However, not all French fisheries
reported skate landings at the species level. In coastal waters off
Spain, based on bycatch data from artisanal fisheries, there is no
evidence of a decreasing trend in undulate ray abundance (Ba[ntilde]on
et al., 2008 as cited in ICES, 2010). Data on undulate ray abundance
and trends in the western Mediterranean Sea and northwest coast of
Africa were not available.
Summary of Factors Affecting the Undulate Ray
Available information regarding current, historical, and potential
future threats to the undulate ray was thoroughly reviewed (Conant,
2015). We summarize information regarding threats below according to
the factors specified in section 4(a)(1) of the ESA. There is very
little information available on the impact of ``Disease or Predation''
or ``Other Natural or Manmade Factors'' on undulate ray survival. These
subjects are data poor, but there are no serious or known concerns
raised under these threat categories with respect to undulate ray
extinction risk; therefore, we do not discuss these further here. See
Conant (2015) for additional discussion of all ESA section 4(a)(1)
threat categories.
Present or Threatened Destruction, Modification, or Curtailment of Its
Habitat or Range
Data are limited on the undulate ray's habitat, and a comprehensive
review of the habitat characteristics that are important to the
undulate ray, and anthropogenic impacts on undulate ray habitat are not
available. Thus, the following section summarizes available data by
region on any habitat impacts, if known.
The Tagus estuary in Portugal has been subjected to industrial
development and urbanization (Cabral et al., 2001). Lisbon, which is on
the Tagus River and estuary, has experienced dramatic increases in
human population growth since the early 1900s. In 2000, the human
population living along the coast of the estuary was estimated at 2
million, which has resulted in high pollution loads in the estuary and
poor water quality (Cabral et al., 2001). The Tagus estuary is one of
the largest and most contaminated by anthropogenic mercury in Europe.
When released to the water column mercury can accumulate in aquatic
organisms, causing contamination within the food chain. Accumulation of
metals has been documented in other species, such as the European eel
(Anguilla anguilla), that were collected from the Tagus estuary (Neto
et al., 2011). However, data are lacking on specific contaminant loads
and effects on the undulate ray. In fact, abundance data in the Tagus
estuary reported by Cabral et al. (2001) indicate that the undulate ray
density slightly increased between 1979 and 1997.
The Gironde estuary is considered somewhat pristine and has
relatively fewer phosphates and nitrogen content compared to other
estuaries in France, such as the Seine, Loire, and Rh[ocirc]ne (Mauvais
and Guillaud, 1994 cited in Lobry et al., 2003). However, human impacts
have been documented for the estuary, including contamination,
[[Page 26904]]
nitrogen loads, and hypoxic conditions from upland activities (Dauvin,
2008).
The English Channel, and its local biodiversity, are also subject
to numerous anthropogenic impacts, including shipping, aggregate
extraction, aquaculture, and eutrophication (Dauvin, 2008; Martin et
al., 2010; Martin et al., 2012). Maritime traffic in the English
Channel is intense, with up to 600 vessels passing through the Dover
Straits each day. Transportation of oil is a major component of the
shipping industry in the English Channel.
Major oil spills have occurred in European seas, including off the
Brittany coast of France, Cornwall coast of England, and Galician coast
of Spain (Dauvin, 2008). In 2002, a spill of over 50,000 tons of heavy
oil occurred 250 miles from Spain's coast (Serrano et al., 2006). The
spill occurred during November, and the winter conditions dispersed and
sank the oil as tar aggregates along the continental shelf. These tar
aggregates were still detected on the continental shelf one month after
the spill, and oil was found in zooplankton species. Serrano et al.
(2006) sampled the area affected by the oil and compared it to pre-
spill data to determine if changes in biomass and benthic diversity had
occurred due to the oil spill. The undulate ray was one indicator
species in the study; however, the data were aggregated across taxa.
Although density of several taxa declined significantly in 2003, their
density increased to pre-oil spill numbers in 2004--two years after the
oil spill (Serrano et al., 2006). Also, the dissimilarity in species
abundance between 2002 and 2003 was not due to changes in any ray
species, including the undulate ray. The study found no effect on
biomass and benthic diversity due to the tar aggregation. Rather,
environmental variables such as depth, season, latitude, and sediment
characteristics influenced benthic community structure (Serrano et al.,
2006).
Overutilization for Commercial, Recreational, Scientific, or
Educational Purposes
With respect to commercial fishing, the undulate ray is mainly
bycaught in demersal fisheries using trawls, trammel nets, gillnets,
and longlines, but has been recorded as landings in other fisheries
operating within its range (Coehlo et al., 2009). Landings data are
generally reported as a generic ``skates and rays'' category and are
not species specific. By the early 1900s, the UK reported general skate
landings of 25,000-30,000 t per year (Ellis et al., 2010). Since 1958,
general skate landings have declined and have been less than 5,000 t
per year since 2005 (Ellis et al., 2010). Where landings are identified
to the undulate ray level, recent restrictions on fisheries need to be
considered in any interpretation on trends (Ellis et al., 2010). In
2009 and 2010, through Council Regulation EC No 43/2009 and Council
Regulation EU No 23/2010, respectively, the European Commission (EC)
banned the retention of the undulate ray in the European Union (EU) by
fishing vessels equipped for commercial exploitation of living aquatic
resources (EC 2371/2002). Prior to the retention ban, the species was a
relatively common commercial fish caught in the northeast Atlantic and
Mediterranean bays and estuaries (Costa et al., 2002). In the two years
preceding the 2009 retention ban on undulate rays, 60-100 t per year
were landed in the Bay of Biscay off the coast of France (Hennache,
2012 cited in Delamare et al., 2013). French landings data on the
undulate ray for the Celtic Seas were 12 t in 1995, 6 t in 1996, 10 t
in 1997, after which landings fell to 2 t in 1998, 1 t in 1999, and 0 t
in 2000-2006 (ICES, 2007), which may indicate overexploitation in this
area. However, it is unknown what percentage of French fisheries
reported skate landings to the species level. French landings data of
Rajidae from 1996 to 2006 were variable with no detectable trend and
ranged from 934 t in 2003 to 2,058 t in 1997 (ICES, 2007).
In Portugal, prior to the 2009 retention ban, over 90 percent of
the undulate rays caught in trammel nets were retained for commercial
purposes or for personal consumption (Coelho et al., 2002; Coelho et
al., 2005; Batista et al., 2009; Baeta et al., 2010). The undulate ray
was the most prominent elasmobranch species by weight (8.51 kg per 10
km of net), comprising almost 35 percent of the elasmobranch biomass
caught in the Portuguese artisanal trammel net fishery between October
2004 and August 2005 (Baeta et al., 2010). Catch per unit effort (CPUE)
was highest in shallow waters (0-25 m) and slightly increased in cooler
months. Raja spp. landings in Portuguese artisanal fisheries decreased
29.1 percent between 1988 and 2004 (Coelho et al., 2009). However,
landings data were not reported by species, so trends in undulate ray
landings data for this area are unknown.
In the Gulf of Cadiz off Spain, the undulate ray was the fifth most
common species discarded (Gon[ccedil]alves et al., 2007). The undulate
ray is also bycaught in the Spanish demersal trawl fleet operating in
the Cantabrian Sea located in the southern Bay of Biscay (ICES, 2007).
However, trawling is banned in waters shallower than 100m, so much of
the bycatch in the area occurs in small artisanal gillnet fisheries
operating in bays or shallow waters (ICES, 2010). The undulate ray is
an important species for artisanal fisheries operating in the coastal
waters of Galicia, and there is no evidence of a decreasing trend in
its abundance in the area (Ba[ntilde]on et al., 2008 as cited in ICES,
2010).
In the western Mediterranean, in 2001, one undulate ray was
recorded in a total of 131 bottom trawl hauls (Massut[iacute] and
Moranta, 2003) and two specimens were recorded in 88 hauls
(Massut[iacute] and Re[ntilde]ones, 2005) on the continental shelf of
the Balearic Islands off the Iberian Peninsula. Landings data are not
available for the northwestern coast of Africa, but the undulate ray's
preference for shallow waters may render it vulnerable to intensive
artisanal coastal fisheries operating in the area (Coelho et al.,
2009).
Inclusion of the undulate ray on the EC prohibited species list has
increased commercial discarding of this species, especially in areas
where it is locally common (ICES, 2013). Data are lacking on mortality
in the undulate ray as a result of discarding. Mortality may be high in
skates and rays discarded from fishing gear operating offshore where
soak times are relatively long (Ellis et al., 2010); however, skates
primarily caught in otter trawls, gillnets, and beam trawls by inshore
vessels operating in areas occupied by undulate rays have shown high
survival rates (Ellis, CEFAS, personal communication, 2014).
As discussed earlier, recreational catches have declined in Tralee
Bay and southwestern Ireland, which may indicate overexploitation in
this area, although fishing effort data are not available. The
International Game Fish Association (IGFA), which has 15,000 members in
over 100 countries, lists the undulate ray as a trophy fish (Shiffman
et al., 2014). Trophy fishing may result in catching large and fecund
fish. Although the IGFA undulate ray trophy fishery is a catch and
release program, some fish may die after being released (Shiffman et
al., 2014). Data are lacking on the number of undulate ray caught in
the IGFA program and on the recreational post-release mortality of
undulate rays.
In addition to commercial and recreational fishing, population
abundance research involving the tagging of undulate rays could have an
impact on the species. Petersen disk tags were tested for the level of
mortality
[[Page 26905]]
that may result from their use under controlled conditions in holding
tanks. Two of 34 tagged rays died, most likely due to the applied tags
(Delamare et al., 2013). The authors stated that although the mortality
is low, it is not negligible and needs to be accounted for in designing
and carrying out future studies involving tags. Mark recapture studies
using Petersen disk tags were conducted in 2013 in the western English
Channel and Bay of Biscay. A total of 1,700 undulate rays were tagged
and released during 6 sampling trips in the Atlantic, and 224 undulate
rays were tagged and released during 4 sampling in the English Channel
(St[eacute]phan et al., 2013). Fisheries independent surveys generally
result in low mortality of all species of rays caught (Ellis et al.,
2012).
Inadequacy of Existing Regulatory Mechanisms
As described above, in 2009, through Council Regulation (EC No 43/
2009), and in 2010, through Council Regulation (EU No 23/2010), the EC
designated the undulate ray as a prohibited species that could not be
fished, retained, transshipped or landed in the EU. Member countries of
the EU include France, Spain, Portugal, UK, and Ireland--all countries
where the undulate ray occurs. The justification for the ban was based
largely on ICES's findings that the state of conservation in the Celtic
Sea was ``uncertain but with cause for concern'' and recommendation of
no targeted fishing for this species (ICES, 2014b). The prohibited
species designations have been controversial and some EU countries have
questioned the rationale behind them (ICES, 2013; ICES, 2014). In 2010,
the EC asked ICES to comment on the listing of the undulate ray as a
prohibited species. ICES (2010) stated that the undulate ray would be
better managed under local management measures and ``should not appear
on the prohibited species list in either the Celtic Seas or the Biscay/
Iberia ecoregion.'' ICES classified the undulate ray as a ``data-
limited stock'' and recommended a precautionary approach to the
exploitation of this species (ICES, 2012). In 2014, the undulate ray
was removed from the prohibited species list in ICES Sub-Area VII,
which includes Ireland and the English Channel (ICES, 2014b), although
it remains as a species that should be returned to the water unharmed
to the maximum extent practicable and cannot be landed in this area.
In England and Wales, the undulate ray is designated as a species
of principal importance in conserving biodiversity under sections 41
and 42 of the Natural Environment and Rural Communities Act of 2006.
Thus, England and Wales must take into consideration the undulate ray
in conserving biodiversity when performing government functions such as
providing funds for development.
Other fishing regulations apply generally to skates and rays. Local
English and Welsh minimum landing sizes are in effect in some inshore
areas (Ellis et al., 2010). In 1999, a total allowable catch (TAC) set
at 6,060 t was established for skates and rays in the North Sea (ICES
Division IIa and sub-area IV). The TAC was reduced by 20 percent (to
4,848 t) for the period 2001-2002, and has been further reduced by
between 8 percent and 25 percent in subsequent years. In 2010, the TAC
was at a record low of 1,397 t (Ellis et al., 2010). Other measures
include bycatch quotas for skates and rays, whereby skates and rays may
not exceed 25 percent live weight of the catch retained on board larger
vessels. In Portugal, a maximum of 5 percent bycatch, in weight, of any
skate species belonging to the Rajidae family is allowed per fishing
trip (ICES, 2013). In 2011, Portugal adopted a law (Portaria No. 315/
2011) that prohibits landing any Rajidae species during May within the
nation's exclusive economic zone. In 1998, mesh size restrictions were
implemented for fisheries targeting skates and rays (Ellis et al.,
2010). Other technical measures have been implemented that may benefit
skate and ray populations, including height of static nets,
delimitation of fishing grounds and depths, and duration of soak time
(e.g., European Council Regulations EC No 3071/95, 894/97, 850/98)
(Gon[ccedil]alves et al., 2007). Portuguese legislation limits trammel
net soak times to 24 hours, unless nets are set deeper than 300m, for
which the soak time can be 72 hours (Baeta et al., 2010).
Information on regulatory mechanisms is lacking for the non-EU
Mediterranean Sea and northwest Africa, which represents a large part
of the undulate ray's overall range.
Extinction Risk Assessment
Several demographic characteristics of the undulate ray, which are
intrinsic to elasmobranchs, may increase the species' vulnerability to
extinction (Dulvy et al., 2014; Musick, 2014, Virginia Institute of
Marine Science, personal communication). The undulate ray is a large-
bodied skate that exhibits the following life-history characteristics:
Delayed age to sexual maturity; long generation length; and long life
span. For these reasons, we conclude that demographic characteristics
related to growth rate and productivity have a moderate to high
likelihood of contributing to the extinction of the undulate ray.
Historical abundance data are lacking for the undulate ray. Prior
to the ban on retention, fisheries landings data indicate that it was a
common species caught in the Celtic Seas off west Ireland, Portugal,
and the English Channel, but was uncommon elsewhere. Fisheries
dependent data from France showed a decline in undulate ray catch over
the period of 1995 through 2001. In the Tagus estuary, Portugal, the
undulate ray mean density was stable or slightly increasing from 1979
through 1997. In coastal waters off Spain there is no evidence of a
decreasing trend in the abundance of the undulate ray in the area.
Thus, in some areas population abundance may be declining, while in
other areas the population appears to be stable or increasing. For
these reasons, we conclude that demographic characteristics related to
population abundance have a low likelihood of contributing to the
extinction of the undulate ray.
The distribution of the undulate ray is patchy, and few data exist
on the undulate ray population structure. Preliminary data indicate
undulate rays do not migrate great distances and exhibit high site
fidelity. Similar to other large skates, these life-history
characteristics may increase the undulate ray's vulnerability to
exploitation, reduce their rate of recovery, and increase their risk of
extinction (ICES, 2007; Rogers et al., 1999). However, localized
declines of this species are not widespread. Based on the limited
information available, we conclude spatial structure and connectivity
characteristics have a low likelihood of contributing to the extinction
of the undulate ray.
Because there is insufficient information on genetic diversity, we
conclude this characteristic presents an unknown likelihood of
contributing to the extinction of the undulate ray.
Information on specific threat factors contributing to the undulate
ray extinction risk is limited. Regarding habitat related threats,
several estuaries inhabited by the undulate ray have been degraded by
human activities, yet others appear somewhat pristine (e.g., Gironde
estuary). However, systematic data are lacking on impacts to habitat
features specific to the undulate ray and/or threats that result in
curtailment of the undulate ray's range. For these reasons, we conclude
habitat destruction, modification, and curtailment of habitat or range
has an unknown to low likelihood (given some undulate ray
[[Page 26906]]
habitat areas are not highly impacted by human activities) of
contributing to the extinction of the undulate ray. Predictions of how
threats to habitat may impact the undulate ray in the foreseeable
future would be largely speculative.
Overexploitation of the undulate ray by commercial fishing has
occurred in some areas, but does not appear widespread. Fisheries
independent data indicate undulate ray populations are uncommon in some
areas, and stable or possibly increasing in other areas over time. Some
mortality may also occur as a result of tags used in scientific
research activities, although the number of rays tagged is relatively
low and unlikely to represent a large portion of the overall
population. For these reasons, we conclude that overutilization for
commercial, recreational, or scientific purposes has a low likelihood
of contributing to the extinction of the undulate ray. Predictions of
how the threat of overutilization may impact the undulate ray in the
foreseeable future would be largely speculative.
With respect to the inadequacy of existing regulatory mechanisms,
retention of the undulate ray is banned in most areas of the EU.
Although the ban on retention of the undulate ray is being re-examined,
a precautionary approach to fisheries management is still advised for
the undulate ray and is likely to continue into the foreseeable future.
Other fisheries regulations for skates and rays in general will reduce
the impact of fishing on the undulate ray population and are also
likely to continue into the foreseeable future. In conclusion, there is
a low likelihood that the inadequacy of existing regulatory mechanisms
contributes or will contribute in the foreseeable future to the
extinction of the undulate ray.
Conant (2015) concluded that the undulate ray is presently at a low
risk of extinction, with no information to indicate that this will
change in the foreseeable future. Although one of the demographic
characteristics (growth rate/productivity) of the undulate ray has a
moderate to high likelihood of contributing to extinction, the species
does not appear to be negatively impacted by threats now, and
information does not indicate the species' response to threats will
change in the future. In addition, known threats pose a very low to low
likelihood of contributing to the extinction of the undulate ray. After
reviewing the best available scientific data and the extinction risk
assessment, we agree with Conant (2015) and conclude that the undulate
ray's risk of extinction is low both now and in the foreseeable future.
Significant Portion of Its Range
Though we find that the undulate ray is not in danger of extinction
now or in the foreseeable future throughout its range, under the SPR
Policy, we must go on to evaluate whether the species is in danger of
extinction, or likely to become so in the foreseeable future, in a
``significant portion of its range'' (79 FR 37578; July 1, 2014).
The SPR Policy explains that it is necessary to fully evaluate a
particular portion for potential listing under the ``significant
portion of its range'' authority only if substantial information
indicates that the members of the species in a particular area are
likely both to meet the test for biological significance and to be
currently endangered or threatened in that area. Making this
preliminary determination triggers a need for further review, but does
not prejudge whether the portion actually meets these standards such
that the species should be listed. To identify only those portions that
warrant further consideration, we will determine whether there is
substantial information indicating that (1) the portions may be
significant and (2) the species may be in danger of extinction in those
portions or likely to become so within the foreseeable future. We
emphasize that answering these questions in the affirmative is not a
determination that the species is endangered or threatened throughout a
significant portion of its range--rather, it is a step in determining
whether a more detailed analysis of the issue is required (79 FR 37578,
at 37586; July 1, 2014).
Thus, the preliminary determination that a portion may be both
significant and endangered or threatened merely requires NMFS to engage
in a more detailed analysis to determine whether the standards are
actually met (79 FR 37578, at 37587). Unless both are met, listing is
not warranted. The policy further explains that, depending on the
particular facts of each situation, NMFS may find it is more efficient
to address the significance issue first, but in other cases it will
make more sense to examine the status of the species in the potentially
significant portions first. Whichever question is asked first, an
affirmative answer is required to proceed to the second question. Id.
(``[I]f we determine that a portion of the range is not `significant,'
we will not need to determine whether the species is endangered or
threatened there; if we determine that the species is not endangered or
threatened in a portion of its range, we will not need to determine if
that portion was `significant''' (79 FR 37578, at 37587). Thus, if the
answer to the first question is negative--whether that regards the
significance question or the status question--then the analysis
concludes and listing is not warranted.
Applying the policy to the undulate ray, we first evaluated whether
there is substantial information indicating that any particular portion
of the species' range is ``significant.'' The undulate ray exhibits a
patchy distribution throughout its range and may have been patchily
distributed since at least the 1800s (ICES, 2008). It is locally
abundant at sites in the central English Channel, Ireland, France,
Spain, and Portugal (Ellis et al., 2012). Within the Mediterranean Sea,
occasional records occur off Israel and Turkey, but undulate rays are
mainly recorded from the western region off southern France and the
Tyrrhenian Sea (Ellis et al. 2012; Serena 2005). Few data exist on the
undulate ray population structure and studies have just begun that
would improve our understanding of whether the species migrates and
mixes/interbreeds among populations. Studies to date indicate that this
species does not migrate great distances and that it exhibits high site
fidelity (ICES 2007; Ellis et al., 2011; ICES, 2013; Delamare et al.,
2013).
The undulate ray is broadly distributed, with locally abundant
populations in five countries, indicating a level of representation
that would increase resiliency against environmental catastrophes or
random variations in environmental conditions. Limited data indicate
discrete populations may exist (e.g., Bay of Biscay, Tralee Bay), but
no data support that any particular population's contribution to the
viability of the species is so important that, without the members in
that portion of the range, the spatial structure of the entire species
could be disrupted, resulting in fragmentation that could preclude
individuals from moving and repopulating other areas. The preliminary
data on possible discrete populations in some areas are too limited to
support a conclusion that undulate ray populations would become
isolated and fragmented, and demographic and population-dynamic
processes within the species would be disrupted to the extent that the
entire species would be at higher risk of extinction. Data on genetic
diversity are lacking; thus, it is unknown how this characteristic
would affect the species' resiliency against extinction should any
particular population be extirpated. While historical abundance data
are lacking, limited fishery-independent
[[Page 26907]]
and fishery-dependent data indicate that in some areas population
abundance may be declining, but in other areas the population appears
to be stable or increasing. And as noted above, we have no reason to
conclude that the extirpation of any particular portion of the range
would cause the entire species to be in danger of extinction now or in
the foreseeable future.
Finally, threats occur throughout the species' range and there is
no one particular geographic area where the species appears to be
exposed to heightened threats. This, coupled with the lack of data on
the undulate ray population structure and diversity, precludes us from
identifying any particular portion of the species' range where the loss
of individuals within that portion would adversely affect the viability
of the species to such a degree as to render it in danger of
extinction, or likely to be in the foreseeable future, throughout all
of its range.
After a review of the best available information, we could identify
no particular portion of the undulate ray range where its contribution
to the viability of the species is so important that, without the
members in that portion, the species would be at risk of extinction, or
likely to become so in the foreseeable future, throughout all of its
range. Therefore, we find that there is no portion of the undulate ray
range that qualifies as ``significant'' under the SPR Policy, and thus
our SPR analysis ends.
Determination
Based on our consideration of the best available data, as
summarized here and in Conant (2015), we determine that the undulate
ray, Raja undulata, faces a low risk of extinction throughout its range
both now and in the foreseeable future, and that there is no portion of
the undulate ray's range that qualifies as ``significant'' under the
SPR Policy. We therefore conclude that listing this species as
threatened or endangered under the ESA is not warranted. This is a
final action, and, therefore, we do not solicit comments on it.
Greenback Parrotfish
The following section describes our analysis of the status of the
greenback parrotfish, Scarus trispinosus.
Species Description
The greenback parrotfish, Scarus trispinosus, is a valid taxonomic
species within the parrotfish family Scaridae. Parrotfishes are
considered a monophyletic group but are often classified as a subfamily
or tribe (Scarinae) of the wrasse family (Labridae). Currently, there
are 100 species of parrotfish (family Scaridae) in 10 genera (Parenti
and Randall, 2011; Rocha et al., 2012). Parrotfishes are distinguished
from other labroid fishes based upon their unique dentition (dental
plates derived from fusion of teeth), loss of predorsal bones, lack of
a true stomach, and extended length of intestine (Randall, 2005). The
greenback parrotfish is one of the largest Brazilian parrotfish
species, with maximum sizes reported around 90 cm (Previero, 2014a).
The greenback parrotfish has six predorsal scales, two scales on the
third cheek row, and roughly homogeneously-colored scales on flanks
(Moura et al., 2001). Juveniles are similarly colored to adults, but
bear a yellowish area on the nape (Moura et al., 2001).
Greenback parrotfish are endemic to Brazil and range from Manuel
Luiz Reefs off the northern Brazilian coast to Santa Catarina on the
southeastern Brazilian coast (Moura et al., 2001; Ferreira et al.,
2010). Greenback parrotfish are widely distributed in reef environments
throughout their range (Bender et al., 2012). Their range includes the
Abrolhos reef complex, located in southern Bahia state (southeastern
Brazil), which is considered the largest and richest coral reef system
in the South Atlantic (Francini-Filho et al., 2008). This reef complex
encompasses an area of approximately 6,000 km\2\ on the inner and
middle continental shelf of the Abrolhos Bank (Kikuchi et al., 2003).
The majority of parrotfishes inhabit coral reefs, but many can also
be found in a variety of other habitats, including subtidal rock and
rocky reefs, submerged seagrass, and macroalgal and kelp beds (Comeros-
Raynal, 2012). There is little evidence that scarids have strict
habitat requirements (Feitosa and Ferreira, 2014). Instead, they appear
to be habitat ``generalists'' and their biomass is weakly related to
the cover of particular reef feeding substrata (Gust, 2002). Greenback
parrotfish have been recorded dwelling in coral reefs, algal reefs,
seagrass beds, and rocky reefs at depths ranging from 1 m to at least
30 m (Moura et al. 2001).
The following von Bertalanffy growth parameters were estimated for
greenback parrotfish: L[infin] = 84.48 cm, K = 0.17 and t0 =
1.09 (Previero, 2014a). Previero (2014a) estimated a maximum life span
for this species of 23 years. Based on a similar ``sister'' species
Scarus guacamaia, a generation length of 7 to 10 years has been
inferred for the greenback parrotfish (Padovani-Ferreira et al., 2012).
Previero (2014b) assessed greenback parrotfish productivity using an
index designed for data deficient and small scale fisheries (from
Hobday et al., 2007). Productivity was measured based on the following
seven attributes: Average age at maturity, average maximum age,
fecundity, average size at maturity, average maximum size, reproductive
strategy, and trophic level. Each attribute was given a score from 1
(high productivity) to 3 (low productivity). Data for this analysis
were obtained from greenback parrotfish sampled from Abrolhos Bank
artisanal fishery landings from 2010 to 2011. Productivity scores for
greenback parrotfish ranged from 1 to 2 with a mean score across all
seven attributes of 1.71. This overall score reflects a species with
average productivity.
Parrotfish typically exhibit the following reproductive
characteristics: Sexual change, divergent sexual dimorphism, breeding
territories, and harems (Streelman et al., 2002). Territories of larger
male parrotfish have been shown to contain more females, suggesting
that male size is an important factor in reproductive success (Hawkins
and Roberts, 2003). Although parrotfish are usually identified as
protogynous hermaphrodites (Choat and Robertson, 1975; Choat and
Randall, 1986), evidence of gonochromism has been reported for three
species within the parrotfish family (Hamilton et al., 2007).
Freitas et al. (2012) studied reproduction of greenback parrotfish
on Abrolhos Bank. From 2006-2013 they sampled a total of 1,182 fish, of
which they collected gonads and prepared histological sections for 304.
Based on a strong female biased sex ratio (282 females; 22 males),
histological evidence, and the distribution of males only in the
largest size classes, Freitas et al. (2012) concluded that the
greenback parrotfish is a protogynous hermaphrodite (changing from
female to male). Greenback parrotfish size at first maturity (i.e., 50
percent mature) is estimated at 39.1 cm, with 100 percent maturity
achieved at 48.0 cm (Freitas et al., 2012). Spawning season for
greenback parrotfish is thought to occur between December and March
(Freitas et al., 2013).
Most parrotfish species are considered ``generalists'' in feeding
behavior--they can rely on food types other than algae, such as
detritus, crustaceans, sponges, gorgonians, and dead or live coral
(Feitosa and Ferreira, 2014). Greenback parrotfish are classified as
either detritivores or roving herbivores but do occasionally graze on
live coral (Francini-Filho et al., 2008c; Comeros-Raynal, 2012). The
foraging plasticity of greenback parrotfish acting either as scraper,
excavator, or browser suggests that, depending on environmental
heterogeneity, this species has the
[[Page 26908]]
capacity to exercise some level of selectivity over their primary food,
and are thus adapted to foraging in different modes (Ferreira and
Goncalves, 2006; Francini-Filho et al., 2008c). Larger males will
establish feeding territories which both attract harems and are grazed
continuously over a period of time (Francini-Filho et al., 2008c).
Population Abundance, Distribution, and Structure
There are no historical or current abundance estimates for
greenback parrotfish. Several studies have reported average densities
and relative abundance of greenback parrotfish at specific reef
locations in Brazil using underwater visual census (UVC) techniques.
Previero (2014b) reported average densities of greenback parrotfish by
size class from 2001-2009 at five Abrolhos Bank sites. Average
densities fluctuate considerably during this time series, with no
strong trends detected for any of the size classes. For the largest
size class (40-100 cm), that would be most targeted by fishing, the
years 2006-2009 represent four out of the five largest mean densities
of greenback parrotfish in the nine year time series. Ferreira (2005)
conducted a baseline study of reef fish abundance at six different
sites within the Abrolhos Reef complex in 2005. The mean density of
greenback parrotfish ranged from 0.80 (Southern Reefs) to 6.04
(Timbebas Reefs) fish per 100 m\2\ across the six sites. The relative
abundance of greenback parrotfish among all fishery targeted species
ranged from 3.05 percent (Southern Reefs) to 15.25 percent (Timbebas
Reefs) (Ferreira, 2005). Francini-Filho and Moura (2008b) found that
greenback parrotfish accounted for 28.3 percent of the total fish
biomass across a diverse range of Brazilian reefs surveyed from 2001-
2005. On the Itacolomis Reef alone, greenback parrotfish accounted for
37.4 percent of the total fish biomass and 45.6 percent of the total
target fish biomass (Francini-Filho and Moura, 2008a). Kikucki et al.
(2012) conducted a rapid assessment of Abrolhos reef fish communities
within the Abrolhos National Marine Park and on the fringing reef off
Santa B[aacute]rbara Island. Average mean density recorded for
greenback parrotfish was 11.8 individuals per 100 m\2\ and this species
was ranked 8th in mean density among all species recorded.
Two studies reported mean densities of greenback parrotfish on
northeastern Brazilian reefs. In 2006, Medeiros et al. (2007) evaluated
reef fish assemblage structure on two shallow reefs located 1.5 km off
the coast of Jo[atilde]o Pessoa in Para[iacute]ba state. Greenback
parrotfish densities were lower on the recreationally exploited reefs
(0.15 fish per 100 m\2\) than on unexploited reefs (0.85 fish per 100
m\2\). In this study, greenback parrotfish accounted for 0.04 percent
of all fish recorded on the exploited reefs and 0.56 percent of all
fish recorded on the unexploited reefs. Feitosa and Ferreira (2014)
studied reef fish distribution on the shallow, fringing reef complex at
Tamandare (northeastern coast) between December 2010 and May 2012. Four
visually different habitats were selected for sampling: Macroalgal
beds; back reef; reef flat; and fore reef. Greenback parrotfish were
only observed on the fore reef, where the mean density was 2.0 fish
(standard error +/- 0.55) per 100 m\2\.
Results indicate that the greenback parrotfish is not only the most
abundant species of parrotfish on Abrolhos Bank, but is also one of the
dominant reef species overall in terms of fish biomass at some sites
within this reef complex (Ferreira, 2005; Francini-Filho and Moura,
2008b; Kikucki et al. 2012). Based on limited data, mean densities and
relative abundance of greenback parrotfish reported from studies on
northeastern Brazilian reefs were generally lower that those reported
on Abrolhos reefs (Medeiros et al., 2007; Feitosa and Ferreira, 2014).
It is unclear whether differences in greenback parrotfish mean
densities across study sites are due primarily to different levels of
fishery exploitation or to the natural distribution of this species.
Time series datasets for detecting trends in greenback parrotfish
abundance over time are limited. Three studies (Francini-Filho and
Moura, 2008b; Bender et al., 2014; Previero, 2014b) reported mean
densities at particular reef sites over multiple years. Only one of
these studies indicated a declining trend in greenback parrotfish
abundance over time (Bender et al., 2014). UVC surveys, combined with
interviews with local fishermen, suggest that the greenback parrotfish
was once abundant at Arraial do Cabo (Rio de Janeiro state) and are now
thought to be locally extirpated from this area (Floeter et al., 2007;
Bender et al., 2014). Arraial do Cabo is a relatively small (1,000
m\2\) marine extractive reserve with heavy exploitation due to its
proximity to a traditional fishing village and general lack of
enforcement of fishing regulations (Floeter et al., 2006; Bender et
al., 2014).
Summary of Factors Affecting the Greenback Parrotfish
Available information regarding current, historical, and potential
future threats to the greenback parrotfish was thoroughly reviewed
(Salz, 2015). We summarize information regarding threats below
according to the factors specified in section 4(a)(1) of the ESA. There
is very little information available on the impact of ``Disease or
Predation'' or ``Other Natural or Manmade Factors'' on greenback
parrotfish survival. These subjects are data poor, but there are no
serious or known concerns raised under these threat categories with
respect to greenback parrotfish extinction risk; therefore, we do not
discuss these further here. See Salz (2015) for additional discussion
of all ESA section 4(a)(1) threat categories.
Present or Threatened Destruction, Modification, or Curtailment of Its
Habitat or Range
The adverse effects of global coral loss and habitat degradation
(including declines in species abundance and diversity, reduced
physiological condition, decreased settlement, change in community
structure, etc.) on species dependent upon coral reefs for food and
habitat have been well documented (Comeros-Raynal et al., 2012).
Anthropogenic threats to Brazil's coastal zone include industrial
pollution, urban development, agricultural runoff, and shrimp farming
(Diegues, 1998; Le[atilde]o and Dominguez, 2000; Cordell, 2006).
In 2008, as part of the International Coral Reef Initiative, coral
reef experts worldwide were asked to assess the threat status of reefs
in their regions due to human pressures and global climate change
(Wilkinson, 2008). For purposes of this assessment, reefs were
categorized into one of three groups: (1) Not threatened--reefs at very
low risk of decline in the short term (5-10 years); (2) Threatened--
reefs under high risk of decline in the mid-long term (> 10 years); or
(3) Critical--reefs under high risk of decline in the short term (5-10
years). In the Atlantic Eastern Brazil Region, experts classified 40
percent of the reefs as ``Not Threatened,'' 50 percent as
``Threatened,'' and 10 percent as ``Critical'' (Wilkinson, 2008).
The Brazilian National Coral Reef Monitoring Program, which
includes all major reef areas in Brazil, conducts annual surveys at 90
different sites within 12 reef systems (Wilkinson, 2008). Reef Check
(www.reefcheck.org) compatible methodology was used to monitor eight
locations in northeastern and eastern Brazil from 2003 to 2008
(Wilkinson, 2008). Results showed that
[[Page 26909]]
due to chronic land-based stresses, the nearshore, shallow reefs, less
than 1 km from the coast, were in poor condition, with less than 5
percent mean coral cover; reefs further than 5 km from the coast, or
deeper than 6 m, showed an increase in algal cover but also some local
coral recovery (Wilkinson, 2008). Atlantic and Gulf Rapid Reef
Assessment (AGRRA; www.agrra.org) monitoring methods have been used at
five eastern Brazilian reefs since 1999. Monitoring via the AGRRA
methodology showed that reefs less than 5 km from the coast were in
poor condition, with a mean of less than 4 percent coral cover and more
than 40 percent cover of macroalgae (Wilkinson, 2008). The poor
condition of nearshore reefs was attributed to damage from sewage
pollution, increased sedimentation and water turbidity, as well as
damage by tourists and over-exploitation (Wilkinson, 2008). Reefs more
than 5 km offshore and in no-take reserves had more than 10 percent
coral cover and less than 10 percent algal cover (Wilkinson, 2008).
Francini-Filho and Moura (2008b) found up to 30 times greater biomass
of target fish on deep reefs (25-35 m) on the Abrolhos Bank compared to
reefs in shallow coastal areas.
The Itacolomis reef, the largest reef complex within the Corumbau
Marine Extractive Reserve on Abrolhos Bank, has a rich coral fauna as
well as relatively high cover, particularly of Orbicella cavernosa, M.
brazilensis, and Siderastrea stellata, which are biologically
representative of the range of Abrolhos corals (Cordell, 2006).
Biological surveys of species diversity, coralline cover, and condition
of colonies, carried out before and after the creation of the reserve
in 2000 indicated that the Itacolomis reefs were still in a good state
of conservation as of 2006 (Conservation International--Brazil, 2000;
Conservation International--Brazil, 2006).
Coral reef area loss and decline is widespread globally, including
many reef areas along the Brazilian coastline. However, there is
considerable variation in the reliance of different species on coral
reefs based on species' feeding and habitat preferences--i.e., some
species spend the majority of their life stages on coral reef habitat,
while others primarily utilize seagrass beds, mangroves, algal beds,
and rocky reefs. The greenback parrotfish is considered a ``mixed
habitat'' species, found on rocky reefs, algal beds, seagrass beds, and
coral reefs (Comeros-Raynal et al., 2012; Freitas et al., 2012), that
feeds mainly on detritus and algae and only occasionally grazes on live
coral (Francini-Filho et al. 2008c).
Impacts of ocean acidification to coral abundance and/or diversity
are arguably significant; however, the direct linkages between ocean
acidification and greenback parrotfish extinction risk remain tenuous.
As discussed above, the ability of greenback parrotfish to occupy
multiple habitat types should make this species less vulnerable to
climate change and ocean acidification compared to other reef species
that are more dependent on coral for food and shelter. Similarly, there
is no evidence directly linking increased ocean temperatures or sea
level rise with greenback parrotfish survival.
Overutilization for Commercial, Recreational, Scientific, or
Educational Purposes
Several studies suggest that overutilization of fish populations is
leading to significant changes in the community structure and balance
of Brazilian reef ecosystems (Costa et al., 2003; Gasparini et al.,
2005; Ferreira and Maida, 2006; Previero, 2014b). An estimated 20,000
fishermen currently use the natural resources of Brazil's Abrolhos
Region as their main source of income (Dutra et al., 2011). Their
activity is predominantly artisanal, performed with small and medium-
sized boats. Small-scale artisanal fisheries account for an estimated
70 percent of total fish landings on the eastern Brazilian coast
(Cordell, 2006), where coral reefs are concentrated (Lea[otilde] et
al., 2003). A growing number of larger and industrial fishing boats
have moved into this region in the last few years, increasing the
pressure on target species and competing with artisanal fishing
(Francini-Filho and Moura, 2008b; Dutra et al., 2011).
Greenback parrotfish were not considered a traditional fishery
resource by most fishermen in Brazil as recently as 20 years ago
(Francini-Filho and Moura, 2008b). Although fishermen from some
localities have reported landing greenback parrotfish as far back as
the late 1970s (Bender et al., 2014; Previero, 2014b), the importance
of this species to Brazil's artisanal fisheries has increased greatly
only in the past two decades or so. Since about the mid-1990s,
parrotfish have increasingly contributed to fishery yields in Brazil,
as other traditional resources such as snappers, groupers, and sea
basses are becoming more scarce (Costa et al., 2005; Previero, 2014b).
This is part of a global phenomenon described by Pauly et al. (1998) as
``fishing down the food web.'' As populations of top oceanic predators
collapse due to overfishing, other large-bodied species at lower
trophic levels become new targets. Some boats now exclusively target
these non-traditional reef fishes, whereas others target them only
during periods of low productivity or during closed seasons of higher
priority target species (Cunha et al., 2012). Greenback parrotfish are
now considered an important fishery resource that is sold to regional
markets in nearby large cities (e.g., Vitoria and Porto Seguro) and
even to overseas markets (Francini-Filho and Moura, 2008b; Cunha et
al., 2012; Previero, 2014b). In general, parrotfishes may be highly
susceptible to harvest due to their conspicuous nature, relatively
shallow depth distributions, small home ranges, and vulnerability at
night (Taylor et al., 2014). Primary fishing methods used in Brazil to
capture parrotfish are spearfishing and seine nets (Ferreira, 2005;
Araujo and Previero, 2013).
Previero (2014b) conducted a quantitative assessment of the
greenback parrotfish commercial fishery on Abrolhos Bank. Fishery
dependent data were collected over 13 months between 2010 and 2011 from
the main fishing ports that exploit reef fish: Caravelas; Prado;
Corumbau Marine Extractive Reserve (MERC); and Alcobaca. The Alcobaca
fleet was characterized by relatively large vessels (some over 12 m)
equipped with freezer space for the preservation of fish over long
periods. These vessels targeted parrotfish on more distant fishing
grounds during extended fishing trips (average duration 11.7 days). By
comparison, fishermen from Caravelas mainly took day trips targeting
greenback parrotfish closer to shore and from smaller vessels. Prado
fishing vessels also traveled longer distances, but greenback
parrotfish were considered a less important target species by fishermen
at this port (compared to either Alcobaca or Caravelas) and landings
were considerably lower as a result. Alcobaca fishermen caught
greenback parrotfish only with harpoons, often with air compressors to
increase bottom time at greater depths; Caravelas fishermen used a
combination of harpoons and nets. Greenback parrotfish landings ranged
in size from 28 cm to 91 cm TL and the fishery was dominated by 8 and 9
year-old fish. The oldest fish sampled was 11 years old--less than half
the estimated maximum life span of 23 years for this species (Previero,
2014a). Significantly larger specimens were landed at Alcobaca compared
to Caravelas (Previero, 2014b). Length frequency data suggest that a
relatively large portion of the greenback parrotfish
[[Page 26910]]
landings, particularly from the near-shore Caravelas fleet, were fish
that had not yet reached maturity (Freitas et al., 2012; Previero,
2014b). Total landings of greenback parrotfish recorded for 13 months
at Caravelas was 24.80 metric tons (average 1.90 tons per month). Total
landings for 7 months of monitoring at the MERC and Alcobaca were 1.93
and 9.21 metric tons, respectively (average 0.27 tons per month at MERC
and 1.31 tons per month at Alcobaca). The CPUE for Caravelas ranged
from 0.911 to 1.92 kg per fisherman/hour/day and for the MERC from 0.65
to 1.25 kg per fisherman/hour/day. The following parameters were
estimated for the Abrolhos Bank greenback parrotfish fishery: Fishing
mortality = 0.68; natural mortality = 0.19; total mortality = 0.87; and
survival rate = 0.42 (Previero, 2014b).
The potential vulnerability of the greenback parrotfish population
to commercial fishery exploitation was evaluated by Previero (2014b)
using a Productivity and Susceptibility Analysis (PSA) index designed
for data deficient and small scale fisheries (Hobday et al., 2007). The
PSA is a semi-quantitative approach based on the assumption that the
vulnerability to a species will depend on two characteristics: (1) The
species' productivity, which will determine the rate at which the
population can sustain fishing pressure or recover from depletion due
to the fishery; and (2) the susceptibility of the population to fishing
activities (Hobday et al., 2007). Seven productivity attributes
(described in ``Species Description'' section above) and the following
four susceptibility attributes were evaluated: (1) Availability--
overlap of fishing effort with the species' distribution, (2)
Encounterability--the likelihood that the species will encounter
fishing gear that is deployed within its geographic range, (3)
Selectivity--the potential of the gear to capture or retain the species
and the desirability (value) of the fishery, and (4) Post Capture
Mortality--the condition and subsequent survival of a species that is
captured and released (or discarded) (Hobday et al., 2007).
Susceptibility attributes were derived mainly from sampling data
obtained at major ports and from interviews with fishermen. The
productivity and susceptibility rankings determine relative
vulnerability and are each given a score: 1 to 3 for high to low
productivity, respectively; and 1 to 3 for low to high susceptibility,
respectively. The average productivity score of greenback parrotfish on
Abrolhos Bank across seven different attributes was 1.71 and the
average susceptibility score across four attributes was 3.00. This
combination of very high susceptibility and average productivity places
the greenback parrotfish in the PSA zone of ``high potential risk'' of
overfishing. The PSA results, in combination with an estimated high
fishing mortality, strongly suggest that greenback parrotfish are
heavily exploited by artisanal fishing on Abrolhos Bank (Previero,
2014b).
Greenback parrotfish may be particularly vulnerable to
spearfishing, due to their size and reproductive traits. Spearfishing
is a highly size-selective, efficient gear--fishermen target individual
fish, typically the largest, most valuable individuals. For protogynous
hermaphrodites, the largest individuals are (in order) terminal males,
individuals undergoing sexual transition, and the largest females.
Continued removal of terminal males, individuals undergoing sexual
transition, and the largest females at high rates can lead to decreased
productivity and increased risk of extinction over time. Thus,
protogynous hermaphrodites, such as the greenback parrotfish, may be
particularly susceptible to over-fishing (Francis, 1992; Hawkins and
Roberts, 2003). With continued heavy exploitation from fishing, it is
plausible that the proportion of male greenback parrotfish could fall
below some critical threshold needed for successful reproduction in
some localities. If sex change is governed by social (exogenous)
mechanisms, then transition would be expected to occur earlier in the
life cycle when larger individuals are selectively removed by fishing
(Armsworth, 2001; Hawkins and Roberts, 2003). This would cause the mean
size and age of females to decrease for protogynous species and could
result in a reduction in egg production (Armsworth, 2001). Sexual
transition takes time and energy, including energy expended on social
interactions and competition among females vying for dominance. Since
removal of terminal males by fishing will result in more sexual
transitions, overall population fitness may be negatively impacted.
Greenback parrotfish are also targeted by recreational
spearfishermen in Brazil, but the impact of this activity on the
resource is largely unknown (Costa Nunes et al., 2012). Medeiros et al.
(2007) studied the effects of other recreational activities (i.e.,
snorkeling, SCUBA, and fish feeding) on a tropical shallow reef off the
northeastern coast of Brazil by comparing its fish assemblage structure
to a nearby similar control reef where tourism does not occur.
Greenback parrotfish were found to be less abundant on the
recreationally exploited reef compared to the control reef (0.15 versus
0.85 individuals per 100 m\2\), although the relative abundance of this
species was very low on both reefs (0.04 percent versus 0.56 percent of
all fish individuals recorded) and results were based on very small
sample sizes of fish observed.
Several studies have linked localized declines of greenback
parrotfish populations to increased fishing effort (Floeter et al.,
2007; Pinheiro et al., 2010; Costa Nunes et al., 2012; Bender et al.,
2014). As previously discussed (see above in ``Population Abundance,
Distribution, and Structure''), studies suggest that the greenback
parrotfish was once abundant at Arraial do Cabo and are now thought to
be locally extirpated from this small area due to fishing pressure
(Floeter et al., 2007; Bender et al., 2014). Pinheiro et al. (2010)
studied the relationships between reef fish frequency of capture
(rarely, occasionally, or regularly), intensity at which species are
targeted by fisheries (highly targeted, average, or non-targeted), and
UVC counts off Franceses island (central coast of Brazil) between 2005
and 2006. Greenback parrotfish were one of 19 species classified as
both ``highly targeted'' (by spearfishing) and ``rarely caught.'' The
authors attributed these results to the overexploitation by fishing of
the Franceses island reef fish community. Similarly, Feitosa and
Ferreira (2014) attributed low observed abundance of greenback
parrotfish outside of no-take areas on Tamandare reefs (northeastern
coast of Brazil) to heavy fishing pressure in this region.
Artisanal and commercial fishing pressure on greenback parrotfish
will likely increase in the future as the country's coastal population
grows and more traditional target species become less available due to
overfishing. As easily accessible nearshore and shallower reefs become
more depleted, fishing effort will likely shift to currently less-
utilized, more remote, and deeper reefs. This is already evident in
landings for the fishing port of Alcobaca, where a fleet of larger,
freezer-equipped vessels return from long duration trips (up to several
weeks) specifically targeting large greenback parrotfish on offshore
reefs (Previero, 2014b). This level of fishing capacity and
sophistication suggests that, over time, greenback parrotfish may
become over-exploited throughout their range, including in more remote
areas that were at one time considered inaccessible to local fishermen.
This is
[[Page 26911]]
supported by the PSA results, which rated greenback parrotfish as
``highly susceptible'' to overfishing on all four susceptibility
criteria: Availability, encounterability, selectivity, and post capture
mortality (Previero, 2014b).
It is likely that greenback parrotfish are being overfished
(Previero, 2014b) and that overfishing will continue into the future
unless additional regulatory mechanisms are implemented and adequately
enforced. In one very small area (Arraial do Cabo), fishing has led to
the local extirpation of this species, although the contribution of
this area to the population as a whole is likely minimal. As a
protogynous hermaphrodite, the greenback parrotfish may be more
susceptible to fishing methods that selectively target the largest
individuals in the population. In addition, as one of the largest
parrotfish species and with relatively late maturation, greenback
parrotfish may be more vulnerable to overexploitation than smaller,
faster-maturing parrotfish species (Taylor et al., 2014). However, the
lack of baseline information and a time series of fishery dependent
data, combined with limitations of the available studies, make it
difficult to estimate the magnitude of this threat or to quantitatively
assess its impact on greenback parrotfish abundance.
Inadequacy of Existing Regulatory Mechanisms
Several marine protected areas (MPAs) have been established in
Brazil on reefs inhabited by greenback parrotfish. Brazil's MPAs vary
considerably in terms of size, ecosystem type, zoning regulations,
management structure, fishing pressure, and level of compliance and
enforcement. The Abrolhos National Marine Park was established by the
Brazilian government in 1983 as a ``no-take'' protected area with
limited use allowed by non-extractive activities (Cordell, 2006).
Effective conservation policy was not implemented in the national park
until the mid-1990s (Ferreira, 2005). The park, which covers an area of
approximately 88,000 hectares, is divided into two discontinuous
portions: (1) The coastal Timbebas Reef, which is considered poorly
enforced, and (2) the offshore reefs of Parcel dos Abrolhos and
fringing reefs of the Abrolhos Archipelago, which are more intensively
enforced (Ferreira and Goncalves, 1999; Francini-Filho et al., 2013).
The Corumbau Marine Extractive Reserve (MERC), located in the northern
portion of Abrolhos Bank in eastern Brazil, was established in 2000 and
covers 89,500 hectares (930 km\2\) of nearshore habitats and coralline
reefs (Francini-Filho et al., 2013). Extractive reserves are co-
managed, multi-use areas in Brazil established by the initiative of
local communities with support from the Federal Protected Areas Agency
(ICMBio) and non-governmental organizations (Francini-Filho and Moura,
2008a). Exploitation of marine resources within the MERC is only
allowed for locals, with use rules (e.g., zoning and gear restrictions)
defined by a deliberative council made up of more than 50 percent
fishermen (Francini-Filho and Moura, 2008a). Handlining, spearfishing,
and various types of nets are allowed, while destructive fishing
practices (e.g., drive-nets above reefs and collections for aquarium
trade) are prohibited (Francini-Filho and Moura, 2008a). The MERC
management plan, approved in November 2001, created several no-take
zones; the main one (~ 10 km\2\) covering about 20 percent of the
largest reef complex within the MERC-Itacolomis Reef (Francini-Filho
and Moura, 2008a). Besides those on Abrolhos Bank, there are a few
other no-take reserves with reef habitat within the greenback
parrotfish range. Laje de Santos State Marine Park on the southeastern
coast of Brazil (S[atilde]o Paulo state) is a no-take reserve
consisting mainly of rocky reefs (Wilkinson, 2008; Luiz et al., 2008).
Established in 1993, Laje de Santos was initially considered a ``paper
park'' with inadequate (or non-existent) enforcement to eradicate
poaching in this heavily populated region (Luiz et al., 2008). In the
past 10 years, significant efforts have been made to protect the park
from illegal and extractive activities (Luiz et al., 2008). Costa dos
Corais, located in Northern Brazil (Pernambuco state), was established
in 1997 as a sustainable multi-use MPA. This area includes coral reef
habitat and is used for tourism, fisheries, and coral reef conservation
(Gerhardinger et al., 2011).
Several studies have evaluated the effectiveness of Brazil's MPAs
in protecting and restoring populations of overexploited reef species.
Francini-Filho and Moura (2008a) estimated fish biomass and body size
within the Itacolomis Reef no-take zone and at unprotected sites on the
reef before (2001) and after initiation of protection (2002-2005).
Greenback parrotfish was the dominant species found on the Itacolomis
Reef in terms of biomass (37.4 percent of total biomass), and
considered a major fishery resource in the study area. Biomass of this
species increased significantly inside the reserve and also in
unprotected reefs close (0-400 m) to its boundary (i.e., ``spillover
effect'') between 2001 and 2002, soon after the reserve establishment
and banning of the parrotfish fishery from the entire MERC (Francini-
Filho and Moura, 2008a). The initial greenback parrotfish biomass
increase on the unprotected reefs was followed by a statistically
significant decrease from 2002 to 2003 after local fishermen decided to
re-open the parrotfish fishery. Greenback parrotfish biomass inside the
no-take reserve also decreased starting in 2004, although this decline
was not statistically significant. The authors attributed this decline
to increased poaching by some local spearfishermen who were strongly
resistant to regulatory controls despite the apparent positive effects
on fish biomass in the first few years after the reserve was
established.
Francini-Filho and Moura (2008b) compared fish biomass from 2001-
2005 across several reef areas with different levels of protection.
Their results varied depending on species considered and were sometimes
confounded by year effects. For the greenback parrotfish, biomass was
statistically higher within the newly established Itacolomis Reef's no-
take reserve than in any of the following areas: Itacolomis Reef multi-
use area, no-take reserves within Abrolhos National Marine Park, and
other open access areas. Greenback parrotfish biomass within the
Abrolhos National Marine Park no-take areas was not statistically
different than biomass found at either the multi-use or open access
sites surveyed. This may be partially due to the lack of enforcement at
the Timbebas Reef no-take area (located within the national park) for
many years after it was established in 1983 (Floeter et al., 2006).
Floeter et al. (2006) compared abundances of reef fishes across
areas with varying levels of protection and enforcement along the
Brazilian coastline. They found that heavily fished species, including
greenback parrotfish, were significantly more abundant in areas with
greater protection. Study sites with full protection (i.e., no-take
areas with adequate enforcement and/or little fishing pressure) also
produced significantly more large parrotfish (>21 cm) than did sites
with only partial protection from fishing (Floeter et al., 2006).
Similarly, Ferreira (2005) found that reefs within the fully protected
and enforced areas of the Abrolhos National Marine Park contained
greater numbers of large-sized parrotfish compared to unprotected reefs
on Abrolhos Bank.
The studies cited above provide ample evidence that, when fully
protected and enforced, no-take reserves
[[Page 26912]]
can have positive effects on greenback parrotfish abundance and size
within the reserve boundaries, and possibly outside due to
``spillover'' effects. For MPAs to work as a fishery management tool,
fully protected (no-take) areas must be sufficiently large in area and
include a variety of habitats critical to the various life history
stages of the target species (Dugan and Davis, 1993). MPAs cover an
estimated 3.85 percent of the greenback parrotfish total range
(Comeros-Raynal et al., 2012). UVC data indicate that within this
range, the reefs with the greatest abundance of greenback parrotfish
are located within Abrolhos Bank (Ferreira, 2005; Francini-Filho and
Moura, 2008a). At present, about 2 percent of the Abrolhos Bank is
designated as a ``no-take'' marine reserve (Francini-Filho and Moura,
2008a). Afonso et al. (2008) found that for the parrotfish Sparisoma
cretense in the Azore Islands, haremic adults displayed very high site
fidelity with minimal dispersion from established male territories that
could last for several years. This study suggests that a network of
small to medium sized, well-enforced no-take marine reserves can
effectively protect ``core'' populations of reef fish (Afonso et al.,
2008) and possibly serve as a buffer from extinction risk.
Magris et al. (2013) conducted a gap analysis to evaluate how well
MPAs in Brazil meet conservation objectives. Coral reef ecosystems were
subdivided into four ecoregions: Eastern Brazil, Northeastern Brazil,
Amazon, and Fernando de Noronha and Atoll das Rocas islands (note:
Greenback parrotfish are not found in the latter two ecoregions). No-
take areas exceeded 20 percent coverage in three out of the four coral
reef ecoregions, but accounted for less than 2 percent of coral reef
areas in Northeastern Brazil. While a large portion of coral reef
ecosystems in Brazil are designated as no-take, only a few of these
areas are greater than 10 km\2\ (Magris et al., 2013). Pressey et al.
(2014) followed up on the Magris et al. (2013) study by more finely
delineating coral reef ecosystems based on reef type (nearshore bank,
bank off the coast, fringing, patch, mushroom reef, and atoll), depth
(deep and shallow), and tidal zone (subtidal and intertidal). They
found that protection of coral reef ecosystems by no-take areas was
very uneven across the 23 ecosystems delineated. Coverage ranged from 0
percent to 99 percent with a mean of 28 percent, with 13 of 23
ecosystems having no coverage (mostly nearshore banks and patch reefs
located in the Northeastern ecoregion). Vila-Nova et al. (2014)
developed a spatial dataset that overlays Brazil's reef fish hotspots
with MPA coverage and protection levels. Hotspots were identified as
areas with either high species richness, endemism, or number of
threatened species. Results showed a mismatch between no-take coverage
and reef hotspots in the Northeast region from Para[iacute]ba state to
central Bahia state. Reef fish hotspots for total richness, endemics,
and targeted species were found in this region which does not have any
designated no-take areas (only multi-use MPAs). The state of
Esp[iacute]rito Santo was also identified as a hotspot for endemic,
threatened, and targeted reef fish species despite being the least
protected region along the Brazilian coast.
Several researchers have noted the prevalence of high levels of
poaching and inadequate enforcement within Brazilian ``no-take''
reserves (Ferreira and Goncalves, 1999; Cordell, 2006; Floeter et al.,
2006; Wilkinson, 2008; Francini-Filho and Moura, 2008a; Luiz et al.,
2008; Francini-Filho et al., 2013). Although these reports are based
largely on anecdotal information, and quantitative data are lacking,
illegal fishing activity is consistently cited as a factor that could
undermine the effectiveness of ``no-take'' marine reserves in Brazil.
Management and enforcement of at least some Brazilian no-take areas has
been reported as improving within the past decade (Luiz et al., 2008;
Floeter et al., 2006). The success of a national MPA system in Brazil
will depend on the capacity to overcome pervasive lack of enforcement,
frequent re-structuring and re-organization of government environmental
agencies, and difficulties with the practicality of implementing
management plans (Wilkinson, 2008).
Aside from establishing no-take protected areas, few actions have
been taken by the Brazilian government to manage reef fisheries.
Traditional fishery management controls (e.g., annual quotas, daily
catch limits, limited entry, seasonal closures, and size limits) on
coastal fisheries are typically not implemented either at the state or
national level (Cordell, 2006; Wilkinson, 2008). For years, the only
marine management practices that limited access to fishing grounds were
unofficial, informal ones: Local sea tenure systems based on artisanal
fishers' knowledge, kinship and social networks, contracts, and a
collective sense of ``use rights'' (Begossi, 2006; Cordell, 2006).
While local sea tenure systems and informal agreements, such as the
short-lived ban on parrotfish harvest within the MERC (Francini-Filho
and Moura, 2008a), could reduce the threat of overexploitation, without
legal authority and regulatory backing, such arrangements may be viewed
as tenuous or unstable.
Extinction Risk Assessment
Studies indicating a declining trend in greenback parrotfish
abundance over time are lacking. Increased fishing pressure on this
species in the past two decades has likely reduced overall abundance
(Previero, 2014b), but available data are insufficient to assess the
magnitude of this decline. Despite the likely negative impact of
fishing on abundance, mean densities recorded for greenback parrotfish
are very high when compared to mean densities recorded for similar
sized species in the north-western tropical Atlantic (Debrot et al.,
2007). In parts of their range, greenback parrotfish are still a
commonly occurring species and represent a large proportion of the
total fish biomass on some reefs. UVC time series data indicate that
greenback parrotfish have been locally extirpated from a relatively
small reef near the species' southern range (Rio de Janeiro state).
However, the impact of this localized decline on the greenback
parrotfish population as a whole may be small. Based on the available
scientific and commercial information, we conclude that it is unlikely
that demographic factors related to abundance contribute significantly
to the current extinction risk of this species.
As a large-bodied, protogynous hermaphrodite with relatively late
maturation, greenback parrotfish may be particularly susceptible to the
effects of fishing on population growth rate or productivity. However,
information indicating a significant decline in greenback parrotfish
productivity is lacking. Greenback parrotfish productivity scores based
on a Productivity and Susceptibility Analysis (PSA) are indicative of a
species with average productivity (Previero, 2014b). Therefore, we
conclude that it is unlikely that demographic factors related to growth
rate/productivity contribute significantly to the current extinction
risk of this species. Based on the limited available information, we
find no evidence to suggest that demographic factors related to spatial
structure/connectivity pose an extinction risk to the greenback
parrotfish. This species is widely distributed throughout its range,
can recruit to a variety of habitats, and shows little evidence of
population fragmentation. We conclude that it is very unlikely that
demographic factors related to spatial structure/connectivity
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contribute significantly to the current extinction risk of this
species. Because there is insufficient information on genetic
diversity, we conclude that this factor presents an unknown likelihood
of contributing to the extinction of the greenback parrotfish.
Although there is evidence that some portion of greenback
parrotfish habitat has been modified and degraded, studies indicating
that habitat associated changes are contributing significantly to the
extinction risk of this species are lacking. Therefore, based on the
available scientific and commercial information, we conclude that it is
unlikely that the threat of destruction, modification, or curtailment
of greenback parrotfish habitat or range contributes or will contribute
significantly to the extinction risk of this species either now or in
the foreseeable future.
The cumulative research indicates that greenback parrotfish are
heavily exploited by fishing throughout much of their range, fishing
pressure has reduced the abundance of greenback parrotfish, and in some
localities the reduction has been significant. Based on the information
available, and taking into account the scientific uncertainty
associated with this threat, we conclude that the threat of
overutilization from artisanal and commercial fishing is somewhat
likely to contribute to the extinction risk of this species both now
and in the foreseeable future. Given the systemic problems associated
with enforcement of no-take MPAs in Brazil and the general lack of
traditional fishing regulations designed to limit catch and effort of
reef fishes, we also conclude that the threat of inadequate existing
regulatory mechanisms is somewhat likely to contribute to the
extinction risk of this species both now and in the foreseeable future.
The extinction risk analysis of Salz (2015) found that the
greenback parrotfish currently faces a low risk of extinction
throughout its range. Fishing overutilization and the inadequacy of
existing fishing regulations were identified as threats that are
somewhat likely to contribute to the risk of greenback parrotfish
extinction. However, while fishing has resulted in a decline in
abundance, greenback parrotfish are still a commonly occurring species
on many Brazilian reefs, and represent a relatively large proportion of
the total fish biomass on some reefs. All of the demographic factors
evaluated were categorized as either unlikely or very unlikely to
contribute significantly to the current extinction risk. There are no
indications that the greenback parrotfish is currently at risk of
extinction based on demographic viability criteria. After reviewing the
best available scientific data and the extinction risk evaluation, we
agree with Salz (2015) and conclude that the present risk of extinction
for the greenback parrotfish is low.
Salz (2015) found that the greenback parrotfish's risk of
extinction in the foreseeable future is between low and moderate. It is
likely that fishing overutilization will further reduce greenback
parrotfish abundance in the future, thus increasing the overall risk of
extinction. However, as mentioned above, there are no indications that
the greenback parrotfish is at risk of extinction based on demographic
viability criteria. This species is still relatively abundant in parts
of its range, and the available information does not indicate that
fishing overutilization will reduce abundance to the point at which the
greenback parrotfish would be in danger of extinction in the
foreseeable future. Based on the best available scientific data and the
extinction risk evaluation, we agree with Salz (2015) and conclude that
the greenback parrotfish's risk of extinction in the foreseeable future
is between low and moderate--i.e., greater than low but less than
moderate.
Significant Portion of Its Range
Though we find that the greenback parrotfish is not in danger of
extinction now or in the foreseeable future throughout its range, under
the SPR Policy, we must go on to evaluate whether the species is in
danger of extinction, or likely to become so in the foreseeable future,
in a significant portion of its range (79 FR 37578; July 1, 2014). To
make this determination, we followed the SPR Policy, as described above
in the ``Significant Portion of Its Range'' section for the undulate
ray, and first evaluated whether substantial information indicates that
the members of the species in a particular area are likely both to meet
the test for biological significance and to be currently endangered or
threatened in that area.
Applying the policy to the greenback parrotfish, we first evaluated
whether there is substantial information indicating that any particular
portion of the species' range is ``significant.'' Greenback parrotfish
are found only in Brazilian waters and are considered widely
distributed throughout their range from the Manuel Luiz Reefs off the
northern coast to Santa Catarina on the southeastern coast (Moura et
al., 2001; Ferreira et al., 2010; Bender et al., 2012). Although
studies on greenback parrotfish spatial structure and connectivity are
lacking, there is no information indicating that the loss of any
particular portion of its range would isolate the species to the point
where the remaining portions would be at risk of extinction from
demographic processes. Similarly, we did not find any information
suggesting that loss of any particular portion would severely fragment
and isolate this species to the point that vulnerability to threats
would increase as a result. The ability of greenback parrotfish to
recruit to a variety of habitats (Moura et al., 2001; Comeros-Raynal,
2012) may improve spatial connectivity among local reef populations.
Parrotfish in general exhibit broad larval dispersal capabilities which
should aid in the repopulation of reefs where they have been eliminated
due to fishing. There is no information indicating that the loss of
genetic diversity from one portion of the greenback parrotfish range
would result in the remaining population lacking enough genetic
diversity to allow for adaptations to changing environmental
conditions. There is also no evidence of a particular portion of the
greenback parrotfish range that is critically important to specific
life history events (e.g., spawning, breeding, feeding) such that the
loss of that portion would severely impact the growth, reproduction, or
survival of the entire species.
After a review of the best available information, we could identify
no particular portion of the greenback parrotfish range where its
contribution to the viability of the species is so important that,
without the members in that portion, the species would be at risk of
extinction, or likely to become so in the foreseeable future,
throughout all of its range. Therefore, we find that there is no
portion of the greenback parrotfish range that qualifies as
``significant'' under the SPR Policy, and thus our SPR analysis ends.
Determination
Based on our consideration of the best available data, as
summarized here and in Salz (2015), we determine that the present risk
of extinction for the greenback parrotfish is low, and that the
greenback parrotfish's risk of extinction in the foreseeable future is
between low and moderate--i.e., greater than low but less than
moderate, and that there is no portion of the greenback parrotfish's
range that qualifies as ``significant'' under the SPR Policy. We
therefore conclude that listing this species as threatened or
endangered under the ESA is not warranted. This is a final action, and,
therefore, we do not solicit comments on it.
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References
A complete list of the references used in this proposed rule is
available upon request (see ADDRESSES).
Classification
National Environmental Policy Act
The 1982 amendments to the ESA, in section 4(b)(1)(A), restrict the
information that may be considered when assessing species for listing.
Based on this limitation of criteria for a listing decision and the
opinion in Pacific Legal Foundation v. Andrus, 675 F. 2d 825 (6th Cir.
1981), NMFS has concluded that ESA listing actions are not subject to
the environmental assessment requirements of the National Environmental
Policy Act (NEPA) (See NOAA Administrative Order 216-6).
Authority
The authority for this action is the Endangered Species Act of
1973, as amended (16 U.S.C. 1531 et seq.).
Dated: May 5, 2015.
Samuel D. Rauch III,
Deputy Assistant Administrator for Regulatory Programs, National Marine
Fisheries Service.
[FR Doc. 2015-11305 Filed 5-8-15; 8:45 am]
BILLING CODE 3510-22-P