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), 26899-26914 [2015-11305]

Agencies

• DEPARTMENT OF COMMERCE
• National Oceanic and Atmospheric Administration

[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 https://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 https://www.nmfs.noaa.gov/pr/species for 
links to these reviews). In this approach, the collective condition of 
individual populations is considered at the species level according to 
four 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