80 FR 76067 - Endangered and Threatened Wildlife and Plants; 12-Month Finding for 7 Foreign Species of Elasmobranchs Under the Endangered Species Act
DEPARTMENT OF COMMERCE National Oceanic and Atmospheric Administration
Federal Register Volume 80, Issue 234 (December 7, 2015)
Page Range
76067-76115
FR Document
2015-30660
We, NMFS, have completed comprehensive status reviews under the Endangered Species Act (ESA) for seven foreign marine elasmobranch species in response to a petition to list those species. These seven species are the daggernose shark (Isogomphodon oxyrhynchus), Brazilian guitarfish (Rhinobatos horkelii), striped smoothhound shark (Mustelus fasciatus), narrownose smoothhound shark (Mustelus schmitti), spiny angel shark (Squatina guggenheim), Argentine angel shark (Squatina argentina), and graytail skate (Bathyraja griseocauda). Based on the best scientific and commercial information available, and after taking into account efforts being made to protect these species, we have determined that the daggernose shark (I. oxyrhynchus), Brazilian guitarfish (R. horkelii), striped smoothhound shark (Mustelus fasciatus), and Argentine angel shark (S. argentina) meet the definition of an endangered species under the ESA. We have determined that the narrownose smoothhound shark (M. schmitti) and spiny angel shark (S. guggenheim) meet the definition of a threatened species under the ESA. Therefore, we propose to list these six species under the ESA. Additionally, we have determined that the graytail skate (B. griseocauda) does not warrant listing under the ESA at this time. We are not proposing to designate critical habitat for any of the species proposed for listing because the geographical areas occupied by these species are entirely outside U.S. jurisdiction, and we have not identified any unoccupied areas within U.S. jurisdiction that are currently essential to the conservation of any of these species. We are soliciting comments on our proposal to list these six foreign marine elasmobranch species.
Federal Register, Volume 80 Issue 234 (Monday, December 7, 2015)
[Federal Register Volume 80, Number 234 (Monday, December 7, 2015)]
[Proposed Rules]
[Pages 76067-76115]
From the Federal Register Online [www.thefederalregister.org]
[FR Doc No: 2015-30660]
[[Page 76067]]
Vol. 80
Monday,
No. 234
December 7, 2015
Part II
Department of Commerce
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National Oceanic and Atmospheric Administration
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50 CFR Parts 223 and 224
Endangered and Threatened Wildlife and Plants; 12-Month Finding for 7
Foreign Species of Elasmobranchs Under the Endangered Species Act;
Proposed Rule
Federal Register / Vol. 80 , No. 234 / Monday, December 7, 2015 /
Proposed Rules
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DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration
50 CFR Parts 223 and 224
[Docket No. 150909839-5839-01]
RIN 0648-XE184
Endangered and Threatened Wildlife and Plants; 12-Month Finding
for 7 Foreign Species of Elasmobranchs Under the Endangered Species Act
AGENCY: National Marine Fisheries Service (NMFS), National Oceanic and
Atmospheric Administration (NOAA), Commerce.
ACTION: Proposed rule; 12-month petition finding; request for comments.
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SUMMARY: We, NMFS, have completed comprehensive status reviews under
the Endangered Species Act (ESA) for seven foreign marine elasmobranch
species in response to a petition to list those species. These seven
species are the daggernose shark (Isogomphodon oxyrhynchus), Brazilian
guitarfish (Rhinobatos horkelii), striped smoothhound shark (Mustelus
fasciatus), narrownose smoothhound shark (Mustelus schmitti), spiny
angel shark (Squatina guggenheim), Argentine angel shark (Squatina
argentina), and graytail skate (Bathyraja griseocauda). Based on the
best scientific and commercial information available, and after taking
into account efforts being made to protect these species, we have
determined that the daggernose shark (I. oxyrhynchus), Brazilian
guitarfish (R. horkelii), striped smoothhound shark (Mustelus
fasciatus), and Argentine angel shark (S. argentina) meet the
definition of an endangered species under the ESA. We have determined
that the narrownose smoothhound shark (M. schmitti) and spiny angel
shark (S. guggenheim) meet the definition of a threatened species under
the ESA. Therefore, we propose to list these six species under the ESA.
Additionally, we have determined that the graytail skate (B.
griseocauda) does not warrant listing under the ESA at this time. We
are not proposing to designate critical habitat for any of the species
proposed for listing because the geographical areas occupied by these
species are entirely outside U.S. jurisdiction, and we have not
identified any unoccupied areas within U.S. jurisdiction that are
currently essential to the conservation of any of these species. We are
soliciting comments on our proposal to list these six foreign marine
elasmobranch species.
DATES: Comments on this proposed rule must be received by February 5,
2016. Public hearing requests must be made by January 21, 2016.
ADDRESSES: You may submit comments on this document, identified by
NOAA-NMFS-2015-0161, by either of the following methods:
Electronic Submissions: Submit all electronic public
comments via the Federal eRulemaking Portal. Go to www.regulations.gov/#!docketDetail;D=NOAA-NMFS-2015-0161. Click the ``Comment Now'' icon,
complete the required fields, and enter or attach your comments.
Mail: Submit written comments to NMFS Office of Protected
Resources (F/PR3), 1315 East West Highway, Silver Spring, MD 20910,
USA.
Instructions: Comments sent by any other method, to any other
address or individual, or received after the end of the comment period,
may not be considered by NMFS. All comments received are a part of the
public record and will generally be posted for public viewing on
www.regulations.gov without change. All personally identifying
information (e.g., name, address, etc.), confidential business
information, or otherwise sensitive information submitted voluntarily
by the sender will be publicly accessible. NMFS will accept anonymous
comments (enter ``N/A'' in the required fields if you wish to remain
anonymous).
You can find the petition, status review report, Federal Register
notices, and the list of references electronically on our Web site at
http://www.nmfs.noaa.gov/pr/species/petition81.htm.
FOR FURTHER INFORMATION CONTACT: Maggie Miller, NMFS, Office of
Protected Resources (OPR), (301) 427-8403 or Chelsey Young, NMFS, OPR,
(301) 427-8491.
SUPPLEMENTARY INFORMATION:
Background
On July 15, 2013, we received a petition from WildEarth Guardians
to list 81 marine species as threatened or endangered under the
Endangered Species Act (ESA). This petition included species from many
different taxonomic groups, and we prepared our 90-day findings in
batches by taxonomic group. We found that the petitioned actions may be
warranted for 27 of the 81 species and announced the initiation of
status reviews for each of the 27 species (78 FR 63941, October 25,
2013; 78 FR 66675, November 6, 2013; 78 FR 69376, November 19, 2013; 79
FR 9880, February 21, 2014; and 79 FR 10104, February 24, 2014). This
document addresses the findings for 7 of those 27 species: daggernose
shark (Isogomphodon oxyrhynchus), Brazilian guitarfish (Rhinobatos
horkelii), striped smoothhound shark (Mustelus fasciatus), narrownose
smoothhound shark (Mustelus schmitti), spiny angel shark (Squatina
guggenheim), Argentine angel shark (Squatina argentina), and graytail
skate (Bathyraja griseocauda). The status of, and relevant Federal
Register notices for, the other 20 species can be found on our Web site
at http://www.nmfs.noaa.gov/pr/species/petition81.htm.
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 daggernose shark (I.
oxyrhynchus), Brazilian guitarfish (R. horkelii), striped smoothhound
shark (M. fasciatus), narrownose smoothhound shark (M. schmitti), spiny
angel shark (S. guggenheim), Argentine angel shark (S. argentina), and
graytail skate (B. griseocauda) are ``species'' under the ESA. There is
nothing in the scientific literature indicating that any 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
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one ``which is likely to become an endangered species within the
foreseeable future throughout all or a significant portion of its
range.'' We interpret an ``endangered species'' to be one that is
presently in danger of extinction. A ``threatened species,'' on the
other hand, is not presently in danger of extinction, but is likely to
become so in the foreseeable future (that is, at a later time). In
other words, the primary statutory difference between a threatened and
endangered species is the timing of when a species may be in danger of
extinction, either presently (endangered) or in the foreseeable future
(threatened).
When we consider whether 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.
Section 4(a)(1) of the ESA requires us to determine whether any
species is endangered or threatened due to any of the following
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. Under
section (4)(b)(1)(A), 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.
Status Reviews
Status reviews for the petitioned species addressed in this finding
were conducted by a contractor for the NMFS Southeast Fisheries Science
Center and are available at http://www.nmfs.noaa.gov/pr/species/petition81.htm or on the respective species pages found on the Office
of Protected Resources Web site (http://www.nmfs.noaa.gov/pr/species/index.htm). These status reviews compiled information on each species'
biology, ecology, life history, and threats from information contained
in the petition, our files, a comprehensive literature search, and
consultation with experts. The draft status review reports (Casselberry
and Carlson 2015 a-g) were submitted to independent peer reviewers and
comments and information received from peer reviewers were addressed
and incorporated as appropriate before finalizing the draft report. The
peer review report is available at http://www.cio.noaa.gov/services_programs/prplans/PRsummaries.html. These status reviews did
not include extinction risk analyses for the species; thus, the
extinction risk analyses for the seven species are included in this 12-
month finding. In addition to the status review reports, we considered
information submitted by the public in response to our petition finding
as well as information we compiled to assess the extinction risk of the
species to make our determinations.
Extinction Risk Analyses
We considered the best available information and applied
professional judgment in evaluating the level of risk faced by each of
the seven species. For each extinction risk analysis, we evaluated the
species' demographic risks (demographic risk analysis), such as low
abundance and productivity, and threats to the species including those
related to the factors specified by the ESA section 4(a)(1)(A)-(E)
(threats assessment), and then synthesized this information to estimate
the extinction risk of the species (risk of extinction).
The demographic risk analysis, mentioned above, is an assessment of
the manifestation of past threats that have contributed to the species'
current status and informs the consideration of the biological response
of the species to present and future threats. For this analysis, we
considered the demographic viability factors developed by McElhany et
al. (2000). The approach of considering demographic risk factors to
help frame the consideration of extinction risk has been used in many
of our status reviews, including for Pacific salmonids, Pacific hake,
walleye pollock, Pacific cod, Puget Sound rockfishes, Pacific herring,
scalloped and great hammerhead sharks, and black abalone (see http://www.nmfs.noaa.gov/pr/species/ for links to these reviews). In this
approach, the collective condition of individual populations is
considered at the species level according to four demographic viability
factors: Abundance, growth rate/productivity, spatial structure/
connectivity, and diversity. These viability factors reflect concepts
that are well-founded in conservation biology and that individually and
collectively provide strong indicators of extinction risk.
In conducting the threats assessment, we identified and summarized
the section 4(a)(1) factors that are currently operating on the species
and their likely impact on the biological status of the species. We
also looked for future threats (where the impact on the species has yet
to be manifested) and considered the reliability to which we could
forecast the effects of these threats and future events on the status
of these species.
Using the findings from the demographic risk analysis and threats
assessment, we evaluated the overall extinction risk of the species.
Because species-specific information (such as current abundance) is
sparse, qualitative ``reference levels'' of risk were used to describe
extinction risk. The definitions of the qualitative ``reference
levels'' of extinction risk were as follows: ``Low Risk''--a species is
at a low risk of extinction if it exhibits a trajectory indicating that
it is unlikely to be at a moderate level of extinction risk in the
foreseeable future (see description of ``Moderate Risk'' below). A
species may be at low risk of extinction due to its present
demographics (i.e., stable or increasing trends in abundance/population
growth, spatial structure and connectivity, and/or diversity) with
projected threats likely to have insignificant impacts on these
demographic trends; ``Moderate Risk''--a species is at moderate risk of
extinction if it exhibits a trajectory indicating that it will more
likely than not be at a high level of extinction risk in the
foreseeable future (see description of ``High Risk'' below). A species
may be at moderate risk of extinction due to its present demographics
(i.e., declining trends in abundance/population growth, spatial
structure and connectivity, and/or diversity and resilience) and/or
projected threats and its likely response to those threats; ``High
Risk''--a species is at high risk of extinction when it is at or near a
level of abundance, spatial structure and connectivity, and/or
diversity that place its persistence in question. The demographics of
the species may be strongly influenced by stochastic or depensatory
processes. Similarly, a species may be at high risk of extinction if it
faces clear and present threats (e.g., confinement to a small
geographic area; imminent destruction,
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modification, or curtailment of its habitat; or disease epidemic) that
are likely to create such imminent demographic risks.
Below we summarize information from the status review reports and
information we compiled on the seven foreign marine elasmobranch
species, analyze extinction risk of each species, assess protective
efforts to determine if they are adequate to mitigate existing threats
to each species, and propose determinations based on the status of each
of the seven foreign marine elasmobranch species.
Daggernose Shark (Isogomphodon oxyrhynchus)
Species Description
The daggernose shark (Isogomphodon oxyrhynchus) is the only species
in the genus Isogomphodon, in the family Carcharhinidae (Compagno
1988). It has a uniform gray or gray-brown color and white underside
(Compagno 1984; Compagno 1988; Grace 2001), and is identified by its
prominent, elongated snout. The pectoral fins of the species are very
large and paddle-shaped (Compagno 1984; Compagno 1988; Grace 2001).
Range and Habitat Use
The daggernose shark occurs in the central western Atlantic Ocean
and Caribbean Sea and has been reported along the coasts of Venezuela,
Trinidad, Guyana, Suriname, French Guiana, and northern Brazil (Lessa
et al. 2006a). The Brazilian range includes the states of Amap[aacute],
Par[aacute], and Maranh[atilde]o, with Tubar[atilde]o Bay in
Maranh[atilde]o as its easternmost limit (Silva 2004; Lessa et al.
1999a). The daggernose shark has one of the smallest ranges of any
elasmobranch species (Lessa et al. 2000). It is a coastal species that
is commonly found in estuaries and river mouths in tropical climates
and is most abundant in these areas during the Amazonian summer (i.e.,
the rainy season) (Compagno 1984; Compagno 1988; Lessa 1997; Lessa et
al. 1999a; Lessa et al. 2006b; Grace 2001). These sharks are often
found in association with mangrove coastlines, occur in highly turbid
waters and in low lying and indented coastlines that can have tide
changes that vary as much as 7 meters (m) (Martins-Juras et al. 1987;
Lessa et al. 1999a). Daggernose sharks occur in water depths between 8
m and 40 m, temperatures ranging from 21.5 [deg]C to 31.5 [deg]C and
salinities between 13.96 and 33.60 ppt (Lessa 1997; Lessa et al. 1999a,
b). Salinity is considered a determining factor for the distribution of
the species, but does not prevent the capture of daggernose sharks in
shallow waters during the rainy season when waters are less saline
(Lessa 1997). Specific winter habitats of the daggernose shark are
unknown.
Diet and Feeding
Little is known about the diet and feeding of the daggernose shark.
Bigelow and Schroeder (1948) and Compagno (1984) suggest that they feed
on schooling fishes, such as clupeids, sciaenids, herring, anchovies,
and croakers. It is speculated that their small eyes and elongated
snout emphasize the use of their rostral sense organs over eyesight
when hunting in turbid waters (Compagno 1984). In Maraj[oacute] Bay in
Brazil, daggernose sharks were found eating catfish (Family Ariidae)
(Barthem 1985).
Growth and Reproduction
Growth rates of daggernose sharks are similar between males and
females, with an estimated growth rate from birth to age 1 calculated
to be approximately 14 cm/year (Lessa et al. 2000). This rate then
slows to approximately 10 cm/year from age 1 to 5-6 for males and age 1
to 6-7 for females (Lessa et al. 2000). Thus, estimated ages at
maturity are 5-6 years for males and 6-7 years for females. In terms of
size, male daggernose sharks begin maturing between 90 cm and 110 cm
total length (TL), with fully adult males observed at sizes larger than
119 cm TL in the field (Lessa et al. 1999a). According to von
Bertalanffy growth parameters, size at maturity is 103 cm TL for males
and about 115 cm TL for females (Lessa et al. 2000), although the
smallest pregnant female recorded was 118 cm long (Lessa et al. 1999a).
After maturity is reached, growth rates decrease to less than 10 cm/
year (Lessa et al. 2000). Maximum age is estimated to be approximately
20 years based on converting the length of a 160 cm TL female with
parameters from the von Bertalanffy growth equation, although the
largest male caught was 144 cm TL, corresponding to an age of 13 years
old, and the oldest aged individuals from vertebrae analyses were of a
7 year old male and a 12 year old female (Lessa et al. 2000).
The reproductive cycle of daggernose sharks in Brazil is
synchronized with the rain cycle. The rainy season runs from January to
June and the dry season runs from July to December. A study by Lessa et
al. (1999a) found that 70 percent of the pregnant females collected
during the study in the rainy season were carrying a recently
fertilized egg or very small embryo, suggesting that the ovulation
period takes place at the end of the dry season or at the beginning of
the rainy season (Barthem 1985). The gestation period is approximately
12 months, with a protracted birthing period throughout the 6-month
rainy season (Lessa et al. 1999a; Lessa et al. 2006b). Mature females
captured with flaccid uteri and white follicles indicate that there is
a break in follicle development between two successive pregnancies,
which indicates a 2-year reproductive cycle (Lessa et al. 1999a).
Mating and gestation periods can also be postponed to compensate for
climate variability and changing environmental conditions across years
(Lessa et al. 1999a). Female fecundity is low, commonly ranging between
3 to 7 embryos per female, with the largest litter observed containing
7 embryos, and one report of a female with 8 embryos (Bigelow and
Schroeder 1948; Barthem 1985; Lessa et al. 1999a). There is no
significant relationship between female size and litter size in
daggernose sharks (Lessa et al. 1999a).
Genetics and Population Structure
Studies examining the genetics of the species or information on its
population structure could not be found.
Demography
Based on the above life history parameters, and following methods
in Cort[eacute]s (2002) for estimating survivorship, Casselberry and
Carlson (2015a) estimated productivity (as intrinsic rate of population
increase, ``r'') at 0.004 year-\1\ (median) within a range
of -0.040-0.038 (5 percent and 95 percent percentiles) (Carlson
unpublished). Median generation time was estimated at 10.6 years, the
mean age of parents of offspring of a cohort ([micro]1) was
10.7 years and the expected number of replacements (R0) was
1.05. Lessa et al. (2010) estimated annual population growth to be r =
-0.048 under natural mortality rates (of 0.28 using the Hoenig (1984)
method and 0.378 using the Pauly (1980) method), and a generation time
of 9 years. If fishing mortality rates were incorporated, the annual
population growth was estimated to be r = -0.074, with a generation
time of 8.4 years (Lessa et al. 2010). These demographic parameters
place daggernose sharks towards the slow growing end of the ``fast-
slow'' continuum of population parameters calculated for 38 species of
sharks by Cort[eacute]s (2002), which means this species generally has
a low potential to recover from exploitation.
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Historical and Current Distribution and Population Abundance
In Brazil, daggernose sharks were historically found in the states
of Amap[aacute], Par[aacute], and Maranh[atilde]o, and were first
formally recorded in surveys from the 1960s in the state of
Maranh[atilde]o (Lessa 1986). In 1999, daggernose sharks were
documented as occurring in two Marine Conservation Areas in northern
Brazil, the Parque Nacional Cabo Orange in Amap[aacute], and the
Reentr[acirc]ncias Maranhenses in Maranh[atilde]o (Lessa et al. 1999b).
However, in recent years, the absence of daggernose sharks in areas
where they were previously common has been noted. For example, in the
Bragan[ccedil]a fish market in northern Brazil (State of Par[aacute]),
daggernose sharks were once among the most common shark species sold in
the market. However, a genetic analysis of shark carcasses collected
from this fish market between 2005 and 2006 found no evidence of
daggernose sharks being sold in the market (Rodrigues-Filho et al.
2009). Although the species' absence in fish markets could indicate
obeyance of Brazilian law, which prohibited the catch of daggernose
sharks in 2004, it has been noted that these laws are poorly enforced
and frequently ignored (see discussion of Inadequacy of Existing
Regulatory Mechanisms below). Additionally, while daggernose sharks
were once caught abundantly in Maranh[atilde]o prior to 1992, they were
notably absent in research surveys conducted from November 2006 to
December 2007 (Almeida et al. 2011). Based on the species' life history
parameters and rates of fishing mortality, population abundance was
estimated to have declined by 18.4 percent per year for 10 years from
the mid-1990s to mid-2000, resulting in a total population decline of
over 90 percent (Santana and Lessa 2002; Rosa and Lima 2005; Kyne et
al. 2012).
Very little information is available on the distribution and
abundance of the daggernose shark outside of Brazil. While undated
catch records exist across the entire coastline of French Guiana,
records are scarce throughout Suriname, Guyana, and Trinidad and Tobago
(Bigelow and Schroeder 1948; Springer 1950; Compagno 1988; Global
Biodiversity Information Facility (GBIF) 2013). Additionally, although
Lessa et al. (1999a) includes Venezuela as part of the daggernose shark
range (citing Cervig[oacute]n 1968), no other information could be
found regarding the present existence of the daggernose shark in
Venezuela. Given the species' sensitive biological traits to
exploitation and evidence of high artisanal fishing pressure, it is
assumed that dramatic population declines have occurred in the last
decade throughout this part of the species' range, similar to the
levels documented in Brazil, but scientific data on population trends
are severely lacking for this region (Kyne et al. 2012).
Summary of Factors Affecting the Daggernose Shark
We reviewed the best available information regarding historical,
current, and potential threats to the daggernose shark species. We find
that the main threat to this species is overutilization for commercial
purposes. We consider the severity of this threat to be exacerbated by
the species' natural biological vulnerability to overexploitation,
which has led to significant declines in abundance and subsequent
extirpations from areas where the species was once commonly found. We
find current regulatory measures inadequate to protect the species from
further overutilization. Hence, we identify these factors as additional
threats contributing to the species' risk of extinction. We summarize
information regarding these threats and their interactions below
according to the factors specified in section 4(a)(1) of the ESA.
Available information does not indicate that habitat destruction or
modification, disease, predation or other natural or manmade factors
are operative threats on these species; therefore, we do not discuss
these factors further in this finding. See Casselbury and Carlson
(2015a) for discussion of these ESA section 4(a)(1) threat categories.
Overutilization for Commercial, Recreational, Scientific, or
Educational Purposes
Based on historical catch data and trends, the primary threat to
daggernose sharks is overutilization in artisanal fisheries. Given its
rather shallow depth distribution, in Brazil, the species is bycaught
in the artisanal gillnet fisheries for Spanish mackerel (Scomberomorus
brasiliensis) and king weakfish (Cynoscion acoupa), which operate
inside or near estuary mouths. Historically, the species was caught in
large numbers along the northern Brazilian coastline and represented a
significant component of the artisanal gillnet bycatch. For example, in
the State of Par[aacute], daggernose sharks represented close to 70
percent of the artisanal catch in the 1980s during the Amazonian summer
(Lessa et al. 2010). Farther south, off the Maranh[atilde]o coast,
harvest of daggernose sharks would begin in October and peak in
January, with the catch per unit effort (CPUE) of these sharks in
gillnets ranging from 6.04 kilogram (kg)/km/hour up to 71 kg/km/hour
(during the peak in the rainy season) in the early 1990s. However, due
to the species' sensitive life history traits, this high level of
fishing mortality was found to be unsustainable, causing the daggernose
shark population to decrease by 18.4 percent per year in the 1990s. By
1999, the percentage of daggernose sharks in the artisanal gillnet
bycatch along the Brazilian coast had significantly decreased, with
daggernose sharks comprising only around 7-10 percent of the
elasmobranch incidental catch (Lessa et al. 1999b; Lessa et al. 2000).
By 2004 and 2006 the species was no longer observed or recorded in the
states of Par[aacute] (Lessa et al. 2010) or Maranh[atilde]o (Almeida
et al. 2011), respectively, based on data from research surveys
conducted in these regions.
Artisanal fisheries operating off Brazil continue to exert
significant fishing pressure on the daggernose shark, which is likely
contributing to fishing mortality rates that historically resulted in
the substantial decline of the species. As such, overutilization
continues to be a threat to the species as these fisheries are still
highly active throughout its range. In fact, in the North region of
Brazil (which includes the States of Amap[aacute] and Par[aacute]), the
artisanal sector accounts for more than 80 percent of the total
landings from this region and represents around 40 percent of the total
artisanal landings for the entire country. These fisheries tend to be
concentrated in areas where the daggernose shark would most likely
occur, including the Amazon River estuary, small estuaries and bays,
and shallow coastal waters within the extensive mangrove area that
covers the northern coast of Brazil (Vasconcello et al. 2011). In the
Northwest region of Brazil (which includes the States of
Maranh[atilde]o south to Bahia), the artisanal sector is also the
dominant fishing sector, accounting for more than 60 percent of the
total landings from this region. The king weakfish fishery, which was
noted as one of the main artisanal gillnet fisheries responsible for
bycatching daggernose sharks, remains one of the most important
fisheries in Brazil as evidenced by the fact that the species was the
4th most landed marine fish in terms of volume in 2011 (21,074.2 t;
Minist[eacute]rio da Pesca e Aquicultura (MPA) 2011). Together, the
artisanal landings from these regions represent over 80 percent of the
total artisanal landings for the entire country (Minist[eacute]rio do
Meio Ambiente/Instituto Brasileiro do Meio Ambiente e dos
[[Page 76072]]
Recursos Naturais Renov[aacute]veis (MMA/IBAMA) 2007).
These artisanal fishing practices and effort levels, which caused
declines in daggernose shark populations off Brazil, are likely similar
in Venezuela, Trinidad and Tobago, Guyana, Suriname, and French Guiana
(which comprises the other half of the species' range). These countries
have a substantial artisanal fishing sector presence, with catches from
artisanal fishing comprising up to 80 percent of the total fish
landings. In French Guiana, sharks alone comprised 40.4 percent of the
annual artisanal landings for the local market (Harper et al. 2015).
However, as noted in the Inadequacy of existing regulatory mechanisms
section, due to minimal controls of these artisanal fisheries,
including lack of enforcement capabilities of existing regulations, the
available data indicate that many of these country's coastal marine
resources are fully to overexploited (Food and Agriculture Organization
of the United Nations (FAO) 2005a, 2005b, 2006, 2008). In Trinidad and
Tobago, for example, it is estimated that the artisanal fleet catches
between 75 and 80 percent of the total landings from these islands (FAO
2006). Of concern, as it relates to overutilization of the daggernose
shark, is the fact that Trinidad and Tobago have an open access fishery
for the artisanal sector, which means there are no restrictions on the
numbers and types of vessels, fishing gear, or trips (FAO 2006;
Mohammed and Lindop 2015). In other words, any local vessel is allowed
to enter the fishery and catch as much they can handle, with no
restriction on fishing effort (FAO 2006). Similarly, Guyana also
operates an open access fishery for its artisanal gillnet sector. Given
that artisanal fishing for groundfish in Guyana, which comprises one of
the country's two main fishing activities (the other being direct
exploitation of shrimp by trawlers), is predominantly conducted using
gillnets, open access fisheries cover a significant portion of the
fishery sector for the country (FAO 2005a).
As noted above, this essentially unregulated artisanal fishing
throughout the Atlantic Caribbean, employing unselective net gear and
concentrated in inshore coastal waters where daggernose sharks would
primarily occur, has led to the overexploitation of many marine
species, including sharks. However, there is virtually no information
available on daggernose shark catches from the Caribbean countries in
the daggernose shark range. These countries report general shark
landings to the FAO but, in addition to these catches being
significantly underestimated (on the order of 2.6 times for Trinidad
and Tobago (Mohammed and Lindop 2015); 1.6 times for Guyana (Macdonald
et al. 2015); 3.4 times for Suriname (Hornby et al. 2015); and 4 times
for French Guiana (Harper et al. 2015)), daggernose sharks are not
specifically identified in the catches (Shing 1999). However,
historical and more recent information suggests daggernose sharks were
and may still be utilized. Although the value of daggernose shark fins
is low, its meat has been sold in markets from artisanal fisheries for
decades (Lessa et al. 2006a), with Bigelow and Schroeder (1948)
recording daggernose shark meat in markets in Trinidad and Tobago and
noting its likelihood in markets in Guyana. Therefore, given the
evidence of utilization of the species, as well as the significant
fishing effort by artisanal fishing fleets throughout the daggernose
shark range, including unregulated access to fishing grounds where the
shark occurs, the observed absence of the daggernose shark in recent
years can likely be attributed to overutilization of the species to the
point where overutilization is significantly contributing to its risk
of extinction.
Inadequacy of Existing Regulatory Mechanisms
Throughout the species' range, species-specific protection for
daggernose sharks is only found in Brazil. In 2004, the daggernose
shark was first listed in Annex I of Brazil's endangered species list:
``Lista Nacional Oficial de Esp[eacute]cies da Fauna Amea[ccedil]adas
de Extin[ccedil][atilde]o--Peixes e Invertebrados Aqu[aacute]ticos''
(Silva 2004). An Annex I listing prohibits the catch of the species
except for scientific purposes, which requires a special license from
the Brazilian Institute of Environment and Renewable Resources (IBAMA)
(Silva 2004). This protection was renewed in December 2014, when the
daggernose shark was listed as ``critically endangered'' on the most
recent version of the Brazilian endangered species list approved by the
Ministry of the Environment (Directive No 445). ``Critically
endangered'' on this list is defined as a species that presents an
extremely high risk of extinction in the wild in the near future due to
profound environmental changes or high reduction in population, or
significant decrease in the taxon's range. In addition to the landing
prohibition, daggernose sharks also receive protection when they occur
within two of Brazil's marine protected areas (MPAs): The Parque
Nacional Cabo Orange and the Reentr[acirc]ncias Maranhenses (Lessa et
al. 1999b); however, the last time they were reported in these areas
was in 1999.
Although Brazil has a number of regulations in place to protect
endangered or threatened species, like the ones described above for
daggernose sharks, it is generally recognized that these regulations
are poorly enforced, particularly within artisanal fisheries (Lessa et
al. 1999b; Amaral and Jablonski 2005; Almeida et al. 2011; Rodrigues-
Filho et al. 2012). Poverty, lack of education within the artisanal
fisheries sector, and increased artisanal fishing effort, especially in
the State of Maranh[atilde]o, have already contributed to the decline
of many elasmobranch populations, including the daggernose shark (Lessa
et al. 1999b), despite the existence of protective legislation and
marine protected areas. As such, effective conservation appears to be
lacking in Brazil (Lessa et al. 1999b; Amaral and Jablonski 2005), with
existing regulatory mechanisms likely inadequate to protect the
daggernose shark from further fishery-related mortality.
In December 2014, the Brazilian Government's Chico Mendes Institute
for Biodiversity Conservation approved an FAO National Plan of Action
(NPOA) for the conservation of sharks (hereafter referred to as FAO
NPOA-sharks) for Brazil (No. 125). The plan considers the daggernose
shark to be one of the country's 12 species of concern and recommends a
moratorium on fishing with the prohibition of sales until there is
scientific evidence in support of recovery (Lessa et al. 2005).
Additionally, it proposes the expansion of the Reentr[acirc]ncias
Maranhenses (where daggernose sharks were observed in 1999) to include
the marine coastal zone and banks, providing additional protection to
the sharks from potential fishery-related mortality. The plan
recommends increased effort monitoring of vessels using nets in the
area and increased education to encourage the release of live
daggernose sharks and prevent the landing of the species. In general
the plan sets short term goals for improved data collection on landings
and discards, improved compliance and monitoring by the IBAMA,
supervision of elasmobranch landings to ensure fins are landed with
carcasses, the creation of a national port sampler program, and
intensified on-board observer monitoring programs. Mid-term goals
include increased monitoring and enforcement within protected areas as
well as the creation of new protected areas based on essential fish
habitat for the 12 species of concern. It also calls for improved
monitoring of fishing from beaches in coastal and estuarine
[[Page 76073]]
environments. Long term goals call for improved ecological data and
stock assessments for key species as well as mapping of elasmobranch
spatiotemporal distributions. This data will be used to better inform
the creation of protected areas and seasonal fishing closures. However,
as stated above, the plan was only just approved as of December 2014,
and will not be fully implemented for another 5 years. Even if the
recommendations outlined in the plan are implemented in the future, it
remains uncertain if they will be effective as the best available
information suggests that current regulatory measures in Brazil to
protect vulnerable species are poorly enforced, particularly within
artisanal fisheries.
Outside of Brazil, there is limited information on shark fishing
regulations or their adequacy for protecting daggernose sharks from
overutilization. In Guyana and Trinidad and Tobago, gillnet fisheries
are restricted to using nets of 900 ft or less with no more than a 15-
foot depth; however, currently, there are no minimum size restrictions
or catch quotas for sharks in either country (Shing 1999). As mentioned
previously, both countries have open access fisheries (however, in
Guyana the open access fishery only applies to the artisanal gillnet
fishery) (FAO 2005a, 2006). In the late 1990s a fisheries management
plan was drafted for Trinidad and Tobago, which prohibited the use of
monofilament gillnets less than 4.75'' stretch mesh and developed a
licensing system (Shing 1999); however, no further details about the
plan, including effectiveness or enforcement of these regulations,
could be found. According to Casselberry and Carlson (2015a), in the
summer of 2013, Guyana's Fisheries Department within the Ministry of
Agriculture passed a 5-year Fisheries Management Plan for Guyana to run
from 2013 to 2018, with one aspect of this plan meant to address shark
fishing, but no further details could be found at this time.
Enforcement of existing fishery regulations is also lacking due to
insufficient resources, with minimal control over the fisheries
resulting in increasing competition and conflicts among fishermen and
between fishing fleets and, consequently, overfishing of marine
resources (FAO 2005a, 2005b, 2006, 2008). No other pertinent
information could be found on shark fishing regulations or their
adequacy in controlling the exploitation of sharks, and more
specifically daggernose sharks.
Extinction Risk
Although accurate and precise population abundance and trend data
for the daggernose shark are lacking, best available information
provides multiple lines of evidence indicating that this species
currently faces a high risk of extinction. Below, we present the
demographic risk analysis, threats assessment, and overall risk of
extinction for the daggernose shark.
Demographic Risk Analysis
Abundance
There is a significant lack of abundance information for I.
oxyrhynchus throughout its range. In northern Brazil, the relatively
recent (2004-2009) absence of the species in fish markets where they
were once abundantly sold, in addition to their absence in fishery-
independent research surveys in areas where they were commonly caught
prior to 1992, suggests the species has suffered significant declines
in population abundance. Based on the daggernose shark's life history
parameters and rates of fishing mortality, the population abundance in
northern Brazil is estimated to have declined by 18.4 percent per year
from the mid-1990s to mid-2000, resulting in a total population decline
of at least 90 percent in approximately half of the species' known
range. Although abundance information from the other parts of the
species' range, including off Venezuela, Trinidad, Guyana, Suriname and
French Guiana, is presently unavailable, it is thought that these
populations have suffered similar declines based on the species'
biological vulnerability and susceptibility to artisanal fisheries
operating in these areas. Given the continued artisanal fishing
pressure throughout the species' range, coupled with the species'
present rarity and its potential extirpation in areas where it was
previously abundant, it is likely that the species is still in decline,
with current abundance trends and levels contributing significantly to
its risk of extinction.
Growth Rate/Productivity
The daggernose shark has extremely low productivity. Litter sizes
range from 2-8 pups, with a 1-year gestation period and a year of
resting between pregnancies. In other words, annual fecundity averages
only 1-4 pups because of the species' biennial reproductive
periodicity. Using these life history parameters, Casselberry and
Carlson (2015a) estimated a productivity (as the intrinsic rate of
population increase) of r = 0.004 year-\1\ (median) within a
range of -0.040-0.038 (Carlson unpublished). Under natural mortality
rates, Lessa et al. (2010) estimated annual population growth to be
negative, with an r = -0.048 and a generation time of 9 years. When
fishing mortality was considered, the estimate of r decreased even
further, to -0.074, with a generation time of 8.4 years. Considering
the daggernose shark has already undergone substantial population
declines, and is still susceptible to fishing mortality in the active
artisanal fisheries throughout its range, the species' extremely low
productivity (with estimates of negative annual population growth
rates) is likely significantly contributing to its risk of extinction.
Spatial Structure/Connectivity
Very limited information is available regarding spatial structure
and connectivity of the daggernose shark populations. The best
available information suggests the daggernose shark has a very
restricted range, one of the smallest of any elasmobranch species, and,
as such, an increased vulnerability to extinction from environmental or
anthropogenic perturbations. In addition, the substantial declines in
the Brazilian population and subsequent absence of the species in areas
it was previously known to occur, as well as its rarity throughout the
rest of its range, suggest the species likely exists as patchy and
small populations, which may limit connectivity. However, there is not
enough information to identify critically important populations to the
taxon as a whole, or determine whether the rates of dispersal among
populations, metapopulations, or habitat patches are presently posing a
risk of extinction.
Diversity
The loss of diversity can increase a species' extinction risk
through decreasing a species' capability of responding to episodic or
changing environmental conditions. This can occur through a significant
change or loss of variation in life history characteristics (such as
reproductive fitness and fecundity), morphology, behavior, or other
genetic characteristics. Although it is unknown if I. oxyrhynchus has
experienced a loss of diversity, the significant decline estimated for
the population in northern Brazil (comprising approximately half of its
known range), as well as the likely small populations elsewhere
throughout its range, suggest the species may be at an increased risk
of random genetic drift and could experience the fixing of
[[Page 76074]]
recessive detrimental genes, reducing the overall fitness of the
species.
Threats Assessment
The primary threat to the daggernose shark is overutilization in
artisanal fisheries. In Brazil, the species is bycaught in the
artisanal gillnet fisheries for Spanish mackerel and king weakfish.
Historically, the species comprised up to around 70 percent of the
artisanal catch during the Amazonian summer in the State of
Par[aacute], and was caught in large numbers by the artisanal gillnet
fisheries operating on the Maranh[atilde]o coast in Brazil. However,
given the extremely low productivity of the species and vulnerability
to depletion, this level of exploitation resulted in substantial
declines (estimated at over 90 percent) to the point where the species
is no longer found in fish markets or observed in trawl and research
survey data. The artisanal gillnet fisheries that were responsible for
this decline are still active throughout the species' range and likely
exerting similar fishing pressure that historically resulted in the
substantial decline of the daggernose shark populations. In fact,
together, the artisanal landings from the North region of Brazil (which
includes the States of Amap[aacute] and Par[aacute]) and Northwest
region (which includes the States of Maranh[atilde]o south to Bahia),
the areas where daggernose sharks were once historically abundant,
represent over 80 percent of the total artisanal landings for the
entire country, indicating the importance and, hence, likely
continuation of this type of fishing in these regions. Notably, the
king weakfish fishery, which was reported as one of the two main
artisanal gillnet fisheries responsible for bycatching daggernose
sharks, remains one of the most important fisheries in Brazil.
Artisanal gillnet fisheries are also active in the other parts of
the species' range, including Venezuela, Trinidad and Tobago, Guyana,
Suriname, and French Guiana, with likely similar fishing practices.
Although landings data from these countries are unknown, the available
information suggests that artisanal fishing pressure is high and that
the species has been taken in small numbers by local fishermen in these
countries, with daggernose sharks historically sold in markets in
Trinidad and likely Guyana. Given the species' susceptibility to
depletion from even low levels of fishing mortality, it is highly
likely that overutilization by artisanal fisheries operating throughout
the species' range is a threat that is significantly contributing to
its risk of extinction.
In 2004, the daggernose shark was listed on Brazil's endangered
species list, and as of 2014, was classified as ``critically
endangered.'' Additionally, it is listed as one of 12 species of
concern under Brazil's FAO NPOA-sharks. However, the implementation and
effectiveness of the recommendations outlined in this plan remain
uncertain, with the best available information indicating that current
regulatory measures in Brazil to protect vulnerable species are poorly
enforced, particularly in artisanal fisheries (the fishery sector that
poses the biggest threat of overutilization of the species). In
addition, there appears to be a lack of adequate fishing regulations to
control the exploitation of the daggernose shark in the other parts of
its range, and, as such, the inadequacy of existing regulatory measures
is a threat that further contributes to the extinction risk of the
species.
Risk of Extinction
Although there is significant uncertainty regarding the current
abundance of the species, the species' population growth rate and
productivity estimates indicate that the species has likely suffered
significant population declines (of up to 90 percent) throughout its
range and will continue to decrease without adequate protection from
overutilization. The species' restricted coastal range, combined with
its recent (2004-2009) absence in areas where it was once commonly
found, as well as its present rarity throughout the rest of its range
(with the last record of the species from 1999) indicate potential
local extirpations and suggest an increased likelihood that the species
is strongly influenced by stochastic or depensatory processes. This
vulnerability is further exacerbated by the present threats of
overutilization and inadequacy of existing regulatory measures that
will significantly contribute to the decline of the existing
populations (based on its demographic risks) into the future,
compromising the species' long-term viability. Therefore, based on the
best available information and the above analysis, we conclude that I.
oxyrhynchus is presently at a high risk of extinction throughout its
range.
Protective Efforts
With the exception of the recommendations within Brazil's FAO NPOA-
sharks (discussed above), we were unable to find any other information
on protective efforts for the conservation of daggernose sharks in
Brazil, Venezuela, Trinidad and Tobago, Guyana, Suriname, or French
Guiana that would potentially alter the extinction risk for the
species. We seek additional information on other conservation efforts
in our public comment process (see below).
Proposed Determination
Based on the best available scientific and commercial information
as presented in the status review report and this finding, we find that
the daggernose shark is presently in danger of extinction throughout
its range. We assessed the ESA section 4(a)(1) factors and conclude
that that the species faces ongoing threats from overutilization and
inadequacy of existing regulatory mechanisms throughout its range. The
species' natural biological vulnerability to overexploitation and
present demographic risks (e.g., low and declining abundance, negative
population growth rates, small, fragmented and likely isolated
populations, extremely restricted distribution, and very low
productivity) are currently exacerbating the negative effects of the
aforementioned threats, placing this species in danger of extinction.
We also found no evidence of protective efforts for the conservation of
daggernose shark that would reduce the level of extinction risk faced
by the species. We therefore propose to list the daggernose shark as an
endangered species.
Brazilian Guitarfish (Rhinobatos horkelii)
Species Description
The Brazilian guitarfish (Rhinobatos horkelii) is a member of the
order Rajiformes and the family Rhinobatidae (Lessa and Vooren 2007).
The species within the family Rhinobatidae are very similar
morphologically, which can make them difficult to distinguish from each
other (De-Franco et al. 2010). The Brazilian guitarfish has long
nostrils with transversely flat or a slightly convex crown and has a
median row of tubercles (nodules) on its dorsal surface that are large
and thorn-like (Lessa and Vooren 2005). The disc width is about 5/6 of
the body length, with dorsal fins that are triangular and similar in
size (Bigelow and Schroeder 1953). The dorsal side of the Brazilian
guitarfish is olive grey or chocolate brown in color and lacks light or
dark markings. Additionally, its snout has a ``sooty'' oval patch
(Lessa and Vooren 2005).
Range and Habitat Use
The Brazilian guitarfish is found along the coast of South America
in the southwestern Atlantic from Bahia, Brazil to Mar del Plata,
Argentina (Figueiredo 1977; Lessa and Vooren 2005, 2007; GBIF 2013).
Newborns and
[[Page 76075]]
juveniles live year round in coastal waters less than 20 m deep. Adults
coexist with immature individuals in shallow waters between November
and March, when pupping and mating occur, but spend the rest of the
year offshore in waters greater than 40 m depth. In the winter,
individuals can be found in water temperatures as low as 9 [deg]C,
while in the summer, individuals are found in average water
temperatures of 26 [deg]C (Lessa and Vooren 2005). Brazilian guitarfish
are commonly found in salinities ranging from 24-28 ppt in northern
Argentina (Jaureguizar et al. 2006).
Diet and Feeding
There is very little information on the diet or feeding behavior of
Brazilian guitarfish. Refi (1973) recorded the stomach contents of six
individuals caught in Mar del Plata, Argentina and found that stomachs
contained the Patagonian octopus (Octopus tehuelchus), shrimp
(Hymenopeneus muelleri), decapods, isopods, and polychaetes. No other
information on diet or feeding could be found.
Growth and Reproduction
Based on a yearly vertebral annulus formation in September, Vooren
et al. (2005a; citing Lessa (1982)) report the von Bertalanffy growth
rate (k) for Brazilian guitarfish to be 0.0194, with a theoretical
maximum size of 135.5 cm TL and age at maturity between 7 and 9 years
for females and 5 and 6 years for males. Similar results were estimated
by Caltabellota (2014), with a theoretical maximum size of 121.71 cm TL
and k = 0.21. No significant differences were found in growth between
the sexes. Using two different methods, Caltabellota (2014) also
estimated theoretical longevity of 18.24 and 14.17 years for females,
and 13.86 and 10.90 years for males. Vooren et al. (2005a) found
longevity to be longer for both females and males, with estimates of 28
years and 15 years, respectively.
Size at maturity for Brazilian guitarfish is between 90 cm and 120
cm TL for both sexes; the smallest pregnant females recorded were
between 91-92 cm TL, and all captured females larger than 119 cm TL
were pregnant (Lessa et al. 2005a; Lessa and Vooren 2005). The
Brazilian guitarfish has an annual reproductive cycle, with
lecithotrophic development (i.e., larva depend on the egg's yolk
reserve supplied by the mother), and a gestation period lasting
approximately 11-12 months (Lessa et al. 2005a; Lessa and Vooren 2005).
Gravid females live at depths greater than 20 m for most of the year,
but migrate into the shallows in the spring and summer to give birth.
Litter sizes range from 4-12 pups and increase with female size (Lessa
and Vooren 2005).
Genetics and Population Structure
Studies examining the genetics of the species or information on its
population structure could not be found.
Demography
Total natural mortality for Brazilian guitarfish was estimated by
Caltabellota (2014) using an age at maturity of 5 years (i.e., an
earlier age of maturity than what was reported by Vooren et al.
(2005a)), and found the estimated total natural mortality from catch
curves to be 0.692 for males and 0.751 for females. Modeling of various
exploitation scenarios found that under natural conditions, with no
fishing mortality, the population would increase by 9 percent each
year, with a population doubling time of 7.41 years (Caltabellota
2014). In the presence of fishing mortality and an age at first capture
of 2 years, the Brazilian guitarfish population would decline by 25
percent every 2.73 years; however, if the age at first capture was
after the age at first maturity (assumed to be 5 years for these
models), the population would increase by 4 percent each year
(Catabellota 2014). Based on the life history parameters discussed
previously, these demographic parameters indicate that the Brazilian
guitarfish generally has a low potential to recover from exploitation,
particularly if the species is experiencing fishing pressure on
neonates and juveniles.
Historical and Current Distribution and Population Abundance
The Brazilian guitarfish is distributed along the coast of South
America, from Bahia, Brazil to Mar del Plata, Argentina. The species'
center of distribution lies between 28[deg] and 34[deg] S. and also
corresponds to the area where it is most abundant. This area is known
as the Plataforma Sul, which includes the continental shelf of southern
Brazil and extends from Cabo de Santa Marta Grande (28[deg]36' S.) to
Arroio Chu[iacute] (33[deg]45' S.). In historical bottom trawl surveys
between latitudes 28[deg]00' S. and 34[deg]30' S., R. horkelii was
common across the Plataforma Sul south of latitude 29[deg]40' S.
(Vooren et al. 2005a). Annual catch of Brazilian guitarfish in this
area was approximately 636 t-1803 t from 1975-1987 (Miranda and Vooren
2003). Research surveys conducted between Chu[iacute] and
Solid[atilde]o (Rio Grande do Sul, Brazil) in February 2005 found an
average CPUE of 1.68 kg/hr (Vooren et al. 2005b), but no follow-up
surveys were conducted after 2005.
Throughout the rest of its range, there is little information on
the abundance of R. horkelli, with the species considered to be a rare
occurrance. In northern Argentina (34[deg] S.-43[deg] S.), estimated
mean biomass of Brazilian guitarfish was 0.1240 t/nm\2\ between 1981
and 1999, with R. horkelli comprising only 0.44 percent of the biomass
of demersal fish on the northern Argentine continental shelf
(Jaureguizar et al. 2006). In 1981, biomass of Brazilian guitarfish was
calculated to be 0.010 t/nm\2\ in 1981. Estimated biomass then peaked
at 0.441 t/nm\2\ in 1994 before falling steadily to 0.007 t/nm\2\ in
1999 (Jaureguizar et al. 2006). Biomass estimates reported in
Argentina's FAO NPOA-sharks for the coast of Buenos Aires province and
Uruguay were 2,597 t in 1994, 661 t in 1998, and 91 t in 1999
(Argentina FAO NPOA-sharks 2009). Along the oceanic coast of Uruguay,
R. horkelii occurs with low density, with annual catches around 3 t in
2000 and 2001 (Meneses 1999; Paesch and Sunday 2003).
Summary of Factors Affecting the Brazilian Guitarfish (Rhinobatos
horkelii)
We reviewed the best available information regarding historical,
current, and potential threats to the Brazilian guitarfish species. We
find that the main threat to this species is overutilization for
commercial purposes. We consider the severity of this threat to be
exacerbated by the species' natural biological vulnerability to
overexploitation, which has led to significant declines in abundance of
all life stages, particularly neonates. We find current regulatory
measures inadequate to protect the species from further
overutilization. Hence, we identify these factors as additional threats
contributing to the species' risk of extinction. We summarize
information regarding these threats and their interactions below
according to the factors specified in section 4(a)(1) of the ESA.
Available information does not indicate that habitat destruction or
curtailment, disease, predation or other natural or manmade factors are
operative threats on these species; therefore, we do not discuss these
factors further in this finding. See Casselbury and Carlson (2015b) for
discussion of these ESA section 4(a)(1) threat categories.
[[Page 76076]]
Overutilization for Commercial, Recreational, Scientific, or
Educational Purposes
Based on historical catch data and trends, the primary threat to
Brazilian guitarfish is overutilization in industrial and artisanal
fisheries. Before landings were prohibited in Brazil in 2004, the
Brazilian guitarfish was considered to be the only economically
important species of the order Rajiformes in southern Brazil, where
they were fished and caught in otter trawls, pair trawls, shrimp
trawls, beach seines, and bottom gillnets (Haimovici 1997; Mazzoleni
and Schwingel 1999; Martins and Schwingel 2003; Lessa and Vooren 2005).
Commercial catches of the Brazilian guitarfish primarily occurred
between 28[deg] S.-34[deg] S. in Brazil, where the species is most
heavily concentrated (Martins and Schwingel 2003; Lessa and Vooren
2005). The pair and simple trawl fleets, which operate on the inner
continental shelf and outer shelf, respectively, were responsible for
the majority of the commercial R. horkelli catch in the 1970s and 1980s
(Vooren et al. 2005a). Based on historical data, CPUE for the pair
trawling fleet was highest from December to March, when adults of the
species would concentrate in coastal waters during the summer for
birthing and reproduction purposes (making them, as well as their
young, more susceptible to being caught in large numbers by the
trawlers) (Miranda and Vooren 2003; Vooren et al. 2005a). In the winter
(April to September), the simple trawl fleet saw an increase in CPUE as
both juvenile and adult Brazilian guitarfish migrated to the outer
shelf; however, as the species was able to spread out more on the outer
shelf, the CPUE of the simple trawl fleet tended to be half of what the
pair trawling fleet experienced (Miranda and Vooren 2003; Vooren et al.
2005a). Regardless, given the effort and complementary spatial and
temporal operations of these fleets, the adult population of Brazilian
guitarfish was under high fishing pressure year-round. Consequently,
this level of exploitation led to significant decreases in the
abundance of the species, as evidenced by the substantial declines in
landings and CPUE from both of these fleets. From 1975 to 1986,
Brazilian guitarfish were common in the landings of these two fleets
that were operating from Rio Grande do Sul, averaging more than 100 t
annually in the simple trawl fleet and more than 200 t annually in the
pair trawl fleet (Klippel et al. 2005). The simple trawl fleet saw
maximum landings of Brazilian guitarfish in the years 1976 (228 t) and
1984 (219 t) and the pair trawl fleet landed a Brazilian industrial
fishing record amount of 1,014 t of R. horkelli in 1984 (Klippel et al.
2005). However, both fleets saw a significant drop in landings and CPUE
after 1986. After 1987, landings oscillated between 50 t and 200 t
annually for the pair trawl fleet, and from 1991-2000, annual landings
did not exceed 10 t for the single trawl fleet (Klippel et al. 2005).
In terms of CPUE, the simple trawl fleet saw an 84 percent decline
between 1975-1986 and 1993-1999, with CPUE decreasing from 0.55 t/trip
(range: 0.41-0.94) to 0.09 t/trip (range: 0.04-0.15) for the respective
time periods (Vooren et al. 2005a). Similarly, the pair trawl fleet
CPUE decreased from 1.07 t/trip (range: 0.43-2.38) to 0.18 t/trip
(range: 0.09-0.30), an 83 percent decline between the two time periods
(Vooren et al. 2005a). Based on these landings and CPUE data, the
Brazilian guitarfish population on the Plataforma Sul is thought to
have collapsed after 1986, with the abundance of the species after 1993
estimated to be around 16 percent of its 1986 level (Vooren et al.
2005a).
From 2000 to 2002, increases in CPUE of R. horkelli were recorded
off Santa Catarina, Brazil, in both pair trawls (from 0.11 t/trip in
2000 to 0.15 t/trip in 2002) and single trawls (from 0.63 t/trip in
2001 to 1.0 t/trip in 2002) (Martins and Schwingel 2003). However,
these increases were assumed to be a reflection of changes in
operational fishing strategy as opposed to an increase in guitarfish
abundance (Martins and Schwingel 2003). In 2000, the single and pair
trawl fleets operating out of Itajai (Santa Catarina, Brazil) began
fishing in depths of 100 m-200 m on the outer continental shelf and
slope between 28[deg] S.-30[deg] S., which was previously unexplored
fishing grounds by these trawl fleets (Martins and Schwingel 2003;
Vooren et al. 2005a). These fleets subsequently caught large amounts of
Brazilian guitarfish in the autumn and winter, of which the majority
were juveniles (Vooren et al. 2005a; Klippel et al. 2005). In fact,
based on a sample of landings data between 2002 and 2003, juveniles
(<90 cm) comprised around 81 to 94 percent of the R. horkelli catch
from the industrial trawl fleets, and 76 percent in the bottom gillnet
fleet (Klippel et al. 2005). This increase in R. horkelli catch by the
industrial fleets was attributed to their fishing in a previously
unexplored outer shelf and slope habitat that likely constituted a
haven for part of the Plataforma Sul population of Brazilian guitarfish
(Martins and Schwingel 2003). Although it was determined that these
fleets were not specifically targeting R. horkelli (based on the fact
that the species comprised only around 1-2.5 percent of the total catch
in 2002 and 2003), decreases in the CPUE of R. horkelli between 2002
and 2003 suggest that the population was already being impacted by the
increase in fishing pressure in this area (Vooren et al. 2005a).
Specifically, the R. horkelli CPUE of these fleets declined from 663
kg/trip in 2002 to 456 kg/trip in 2003 (Vooren et al. 2005a), which
equates to a decline of 31 percent and is concerning for a population
that has already been fished to such low levels. In fact, in July 2010,
the state of S[atilde]o Paulo, Brazil declared the stock of Brazilian
guitarfish collapsed due to intense exploitation, with biomass and the
stock's reproductive potential at such a level that severely comprises
recovery.
In addition to the contribution of the industrial fisheries to the
overutilization of the species, artisanal fisheries were also known for
catching large quantities of the Brazilian guitarfish in beach seines
and fixed nets (Miranda and Vooren 2003; Lessa and Vooren 2005). In
fact, before the prohibition of the species, artisanal fisheries,
combined with the industrial pair trawl fisheries, caught over 70
percent of the Brazilian guitarfish (Miranda and Vooren 2003). Because
these artisanal fisheries operate on the inshore pupping grounds of the
species, the guitarfish catch consists primarily of aggregations of
pregnant females (around 98 percent of the catch) (Lessa and Vooren
2005). In the 1980s, annual artisanal catches of guitarfish wavered
around 600 t-800 t but declined soon after (Lessa, 1982; Miranda and
Vooren 2003). In 1992, artisanal landings were estimated at 330 t and
by 1997, landings dropped to only 125 t, a decrease that was attributed
to a reduction in catches specifically of R. horkelli (Miranda and
Vooren 2003). Monitoring of 20 artisanal beach seine fishing operations
in 2002/2003 documented only a single haul containing R. horkelli, and
artisanal fishermen now report that catches of Brazilian guitarfish are
rare (Vooren et al. 2005a). Due to this significant decline in
abundance of the species, artisanal fishermen have shifted their focus
to fishing for mullet (Vooren et al. 2005a). However, they still
operate within the R. horkelli inshore pupping grounds on the
Plataforma Sul, and, as such, the species remains susceptible to
incidental capture in beach seines and fixed net fishing gear (Vooren
et al. 2005a). Recent data also indicate that when Brazilian guitarfish
are caught by
[[Page 76077]]
artisanal fishermen, the species is not usually released, despite its
prohibited status (Vooren et al. 2005a; Vieira 2014). For example, from
November 2013 to March 2014, Vieira (2014) monitored four artisanal
fishing boat operations (off Rio Grande do Sul) that made 50 sets over
20 fishing trips in depths of 5 m to 21 m using primarily gillnets. The
Brazilian guitarfish was the second most abundant species caught by
gillnets, with 125 individuals captured, representing 17.5 percent of
elasmobranch catch. Its frequency of occurrence per fishing trip was 40
percent. The author noted that all of the caught sharks (either as
catch or bycatch) were sold, whereas out of all the caught rays, only
R. horkelli was sold. Additionally, although the CPUE was estimated to
be relatively low for the elasmobranchs in the study, given the area
where these artisanal fisheries operate, the majority of the R. hokelli
catch consisted of immature individuals and breeding adults (with
observations of pregnant females initiating abortion on the boats)
which likely compromises recruitment to the already at risk population
(Vieira 2014).
The substantial abundance declines of R. horkelli on the Plataforma
Sul due to overutilization by fisheries, as indicated by the commercial
and artisanal fisheries data, is further confirmed by CPUE data from
fishery-independent surveys of the region. On the Plataforma Sul, a
number of research cruises dating back to 1972 have surveyed the area
using bottom trawl gear (from depths of around 10 m to over 500 m). In
an analysis of this time series set, Vooren et al. (2005a) note that
between the periods of 1975-1986 and 1993-1999, CPUE of R. horkelli
showed similar declines as those observed in the commercial CPUE over
the same period. Based on the CPUE trends, abundance of R. horkelli on
the Plataforma Sul in depths of 20 m-200 m is estimated to have
decreased by about 85 percent between 1975 and 1999 (Vooren et al.
2005a).
Overall, based on the above commercial and artisanal fishing data,
it is estimated that over the period of 1975-1986, around 100,000
mature R. horkelli females and 100,000 mature R. horkelli males were
caught annually (Vooren et al. 2005a). The removal of these
reproductively active adults from the population translated to a loss
of around 600,000 newborns per year, or 6.7 million newborns over the
course of the 11-year period of fishing, and led to recruitment
overfishing of the species (Vooren et al. 2005a). As a result of this
overutilization, abundance of the species on the Plataforma Sul
significantly declined, causing the stock to collapse after 1986.
Overutilization still remains a threat to the species as fishing by
the industrial and artisanal fleets continues to occur at high efforts
on the Plataforma Sul and especially within important nursery habitats
for the species (Vooren et al. 2005a; Klippel et al. 2005; Vooren and
Klippel 2005c). In 2007, the industrial fleets operating off southern
Brazil, where R. horkelli is most concentrated, and specifically from
the States of Parana, Santa Catarina, and Rio Grande du Sol (identified
as Brazil's ``South Region''), were responsible for landing around 54
percent (151,154 mt) of the total industrial fish catch for all of
Brazil (277,364.5 mt). Within Brazil's South Region, the industrial
fleet comprised 59.3 percent of the total fish landings from the region
(255,080.5 mt). In 2011, the South Region's marine fish landings (not
including aquaculture) amounted to 158,515.4 mt, representing 47
percent of the total fish production from that region and 28.6 percent
of the national total of marine fish landings. In terms of artisanal
fisheries, fishing pressure (and related mortality) on R. horkelli is
likely high given that the mullet fishery, the target of artisanal
fisheries operating within R. horkelli nursery habitats, is an
important fishery in Brazil. According to Lemos et al. (2014), catches
of mullets (Mugil liza) in Rio Grande do Sul and Santa Catarina between
1997 and 2010 were around 95 percent of the total catch from all other
Brazilian states, Uruguay, and Argentina. In 2011, mullets were the 2nd
most landed fish (in terms of volume) in the artisanal fisheries in Rio
Grande do Sul (IBAMA/Centro de Pesquisa e Gest[atilde]o dos Recursos
Pesqueiros Lagunares e Estuarinos (CEPERG) 2012) and the 5th most
landed marine fish species for all of Brazil, with landings totaling
18,045 t (MPA 2011), suggesting that this significant fishing effort by
artisanal fisheries in the inshore pupping grounds of Brazilian
guitarfish is unlikely to decrease in the foreseeable future.
Additionally, the relatively recent expansion and operation of the Rio
Grande do Sul and Itajai trawl fleets on the outer shelf and continued
operation of the pair trawl fleet on the inner continental shelf
suggest overutilization (in the form of bycatch mortality) is still a
threat to the species. Areas that previously served as offshore refugia
for the Plataforma Sul population from fishing pressure are no longer
protected from exploitation, with both juveniles and adults susceptible
to fishery-related mortality over their entire habitat.
Inadequacy of Existing Regulatory Mechanisms
Like the daggernose shark, the Brazilian guitarfish was also listed
on Brazil's endangered species list in 2004, and as of 2014, was
classified as ``critically endangered.'' In 2007, Lessa and Vooren
noted that the 2004 prohibition on catching the species was gradually
becoming more effectively enforced, but genetic studies indicate that
enforcement was still relatively poor as recently as 2009. Of 267
guitarfish samples that were collected at ports throughout southeastern
and southern Brazil between 2008 and 2009, 55.8 percent were
genetically identified as Brazilian guitarfish (De-Franco et al. 2012).
Of the 85 samples from boats operating off Santa Catarina, 100 percent
of the guitarfish were Brazilian guitarfish (De-Franco et al. 2012).
When the fishermen were asked about their landings during sample
collection, many of them denied harvest of guitarfish, suggesting that
fishermen are aware of the capture prohibition of Brazilian guitarfish
(De-Franco et al. 2012). However, because fishermen commonly remove the
head and gut of any guitarfish before arriving in port, distinguishing
the Brazilian guitarfish from the other two guitarfish species in the
area (R. percellens and Zapteryx brevirostris) is difficult, which,
when coupled with the lack of adequate government inspections, may be
encouraging fishermen to disregard the law for economic gain (De-Franco
et al. 2012). Similarly, and most recently, a 2013 investigation by Sea
Shepherd Brazil into the illegal trade of elasmobranchs by the
S[atilde]o Paulo General Warehousing and Centers Company led to the
seizure of 700 kg of illegal elasmobranch species by federal police.
Included in the illegal haul were Brazilian guitarfish, again
suggesting that poor enforcement of present regulations is likely
contributing to the continued exploitation and, consequently,
overutilization of the species.
Although the Brazilian guitarfish occurs in several MPAs within
Brazilian waters, including APA de Canan[eacute]ia-Iguape-
Peru[iacute]be (S[atilde]o Paulo; 234,000 hectares), PARNA do Superagui
(Parana; 33,988 hectares), REBIO do Arvoredo (Santa Catarina; 17,600
hectares) and RESEX Marinha do Pirjuba[eacute] (Santa Catarina; 1,712
hectares) (Rosa and Lima 2005), these MPAs only protect the species
from exploitation when they occur within these areas. In addition, the
coverage of these MPAs compared to
[[Page 76078]]
the range of the species is very small and also located north of the
center of distribution and concentration of the species and, therefore,
unlikely to significantly decrease the threat of overutilization to the
species.
Another regulation in place in Brazil to control the exploitation
of marine resources is a prohibition on trawl fishing within three
nautical miles (nm) from the coast of southern Brazil. This prohibition
may help decrease fishery-related mortality of R. horkelli in the
nearshore areas primarily used as nursery habitat by the species;
however, according to Chiaramonte and Vooren (2007), enforcement of
this prohibition has been noted as difficult. In addition, the species
is still susceptible to being caught as bycatch in the legally
permitted coastal gillnet fisheries (which also operate in nursery
areas) and in the offshore trawl and gillnet fisheries and vulnerable
to the associated bycatch mortality (Lessa and Vooren 2007). Therefore,
the adequacy of the trawl prohibition in decreasing fishery-related
mortality of R. horkelli to the point where the extinction risk of the
species is significantly lowered is unclear.
Like the daggernose shark, the Brazilian guitarfish is one of
Brazil's 12 species of concern identified in their FAO NPOA-sharks. The
plan recommends a moratorium on fishing with a prohibition of sales
until there is scientific evidence in support of recovery, and proposes
a fishing exclusion area over a large region of the coast of Rio Grande
do Sul at depths of 20 m to protect nursery areas (No 125, Lessa et al.
2005). As noted in the daggernose shark analysis above, this plan will
not be fully implemented for another 5 years and it remains uncertain
whether the recommendations will be implemented and effective, as the
best available information suggests that current regulatory measures in
Brazil to protect the Brazilian guitarfish are poorly enforced.
Similar to Brazil, Uruguay also lists the Brazilian guitarfish as a
species of high priority in its FAO NPOA-sharks (Domingo et al. 2008).
The plan sets short-term goals (12-18 months) to investigate
distribution and habitat use and generate time-series of effort and
catch; mid-term goals (24-30 months) to conduct an abundance assessment
and determine maximum sustainable catch limits; and long term goals
(36-48 months) to conduct age, growth, reproduction, and diet studies.
In its plan, Uruguay made it a priority to: Review current fishing
licenses that allow for the catch of Brazilian guitarfish and possibly
modify them; no longer grant new licenses that would allow for such
fishing; forbid processing and marketing of the species; and promote
safe release if possible. However, updated results from the goals and
priorities of this plan could not be found. As such, their
implementation and overall effectiveness at decreasing the threats to
the species remains highly uncertain.
Extinction Risk
The best available information provides multiple lines of evidence
indicating that the R. horkelli currently faces a high risk of
extinction. Below, we present the demographic risk analysis, threats
assessment, and overall risk of extinction for the Brazilian
guitarfish.
Demographic Risk Analysis
Abundance
There is very limited information regarding abundance estimates for
R. horkelli throughout its range. The majority of the Brazilian
guitarfish population and center of distribution is concentrated
between 28[deg] S. and 34[deg] S. in southern Brazil, and it is scarce
elsewhere. On the northern Argentine continental shelf, between 34[deg]
S. and 43[deg] S., which appears to be the southern extent of the
species' range, mean biomass of R. horkelli has fluctuated over the
years. In 1981, biomass was estimated to be 0.010 t/nm\2\. Biomass
peaked in 1994 at 0.441 t/nm\2\ before falling to 0.007 t/nm\2\ in 1999
(Jaureguizar et al. 2006). This represents a 98 percent decrease from
peak biomass between 1994-1999, but only a decrease of around 30
percent from estimates in 1981. While mean abundance estimates from the
presumed center of the species' distribution are not available, we can
infer significant historical population declines from a variety of
fishery effort, catch and landings data from this region. Based on both
fishery-independent sampling and commercial fleet CPUE data from 1975-
1986 and 1993-2002, the population of Brazilian guitarfish along the
southern coast of Brazil has significantly decreased in size. Data from
the single and pair trawl fleets operating on the Plataforma Sul
indicate that CPUE declined by 61 percent and 74 percent, respectively,
between the periods of 1975-1986 and 1993-2002 (Klippel et al. 2005).
The population is assumed to have collapsed after 1986. Since 1993, the
population is estimated to be about 16 percent of its 1986 level. Due
to species identification issues, there is some level of uncertainty
regarding the accuracy of the available data; however, based on the
best available information (including fisheries-independent survey
data), it appears that the species has likely undergone significant
declines throughout its range. Given the continued high fishing
pressure in the species' nursery grounds and presence of the species in
recent landings data despite its prohibited status, abundance has
likely continued to decline.
Growth Rate/Productivity
Lessa and Vooren (2005) estimated the growth rate of R. horkelii as
(k) = 0.194, and more recently, Caltabellota (2014) reported similar
results, with an estimated k = 0.21 (with no significant difference in
growth rates between sexes). The species is thought to reproduce
annually, with a long gestation period (~1 year) and low fecundity
(litter sizes range from 4 to 12 pups). Females have also been observed
aborting embryos upon capture in fishing gear, further decreasing the
reproductive output of the species. In addition, based on the data, it
appears that both males and females of the species do not reach
reproductive maturity until they have grown to approximately 74-89
percent of their maximum size. These reproductive characteristics
suggest the species has relatively low productivity, similar to other
elasmobranch species, which likely hinders its ability to quickly
rebound from threats that decrease its abundance (such as
overutilization).
Under natural mortality, Caltabellota (2014) estimated that the
population would increase by 9 percent each year, doubling every 7.41
years. However, if individuals of the species are fished before
reaching maturity (assumed to be 5 years), the Brazilian guitarfish
population will decline by 25 percent every 2.73 years (Caltabellota
2014). Given the historical declines in CPUE and levels of neonate and
juvenile landings, the species was likely subject to this exploitation
scenario and subsequently experienced a negative population growth rate
to the point where the population collapsed after 1986. With the
continued fishing pressure by the mullet fisheries operating in the
nursery habitats and the industrial fisheries on the Plataforma Sul,
the available data on growth rate and productivity of the species
indicates that current exploitation levels will likely continue to
cause population declines in the species, with no information to
suggest this trend is reversing.
Spatial Structure/Connectivity
The species is thought to have a continuous distribution along the
[[Page 76079]]
Plataforma Sul (where the species is most abundant) (Vooren et al.
2005a); however, there is no information on the connectivity among
other R. horkelii populations throughout the rest of its range,
including the importance of the Plataforma Sul population to the taxon
as a whole. Based on the available data, there is not enough
information to identify critical populations or determine whether the
rates of dispersal among populations, metapopulations, or habitat
patches are posing a risk of extinction to the species.
Diversity
The loss of diversity can increase a species' extinction risk
through decreasing a species' capability of responding to episodic or
changing environmental conditions. This can occur through a significant
change or loss of variation in life history characteristics (such as
reproductive fitness and fecundity), morphology, behavior, or other
genetic characteristics. Although it is unknown if R. horkelli has
experienced a loss of diversity, the significant reduction in
population size on the Plataforma Sul, as well as the likely small
populations elsewhere throughout its range, suggest the species may be
at an increased risk of random genetic drift and could experience the
fixing of recessive detrimental genes, reducing the overall fitness of
the species.
Threats Assessment
Present threats to the species include overutilization by fisheries
and inadequate regulatory mechanisms. The artisanal and industrial
fisheries that historically contributed to the decline in R. horkelii
are still active throughout the species' range and significantly
contribute to national marine fish production. In fact, in Brazil in
2007, the industrial fleets were responsible for landing over half of
the marine fish from the country's South Region, where R. horkelli is
most concentrated, with artisanal fisheries responsible for 10 percent.
The most recent statistics from 2011 show that marine fish landings
from the South Region represent almost half of the fish production from
that region and 28.6 percent of the Brazilian national total of marine
fish landings. Because these artisanal and industrial fleets primarily
operate in locations where R. horkelii would occur, and use rather
unselective fishing gear, their operations are likely contributing
significantly to the fishery-related mortality rates of the species and
impacting the status of the species.
Although trawl fishing in Brazil is prohibited within 3 nm of the
coast (<10 m depth), the shallow nursery areas, where neonates are
found year-round and where adults are concentrated during the pupping
and mating season, are still accessible to and heavily fished by
artisanal fisheries using gillnets and beach seines. For example, in
the mullet fishery, fishermen use beach seines to trap the mullets;
however, due to the low selectivity of the fishing gear, these seines
may also catch large numbers of juvenile and pregnant female guitarfish
as evidenced by the historical data from beach seine operations on the
coast of Rio Grande do Sul (Miranda and Vooren 2003; Lessa and Vooren
2005; Vooren et al. 2005a). The mullet fishery remains an important
fishery in Brazil and in 2011, mullets were the 2nd most landed fish in
the Rio Grande do Sul artisanal fisheries and the 5th most landed
marine fish in all of Brazil. Additionally, the artisanal gillnet
fisheries operating off Rio Grande do Sul are also known to bycatch and
sell pregnant females, mature males, and juvenile Brazilian guitarfish,
despite its prohibited status. Based on the modeled exploitation
scenarios and resultant population growth rates described in the
demographic analysis above, continued fishing pressure by both
artisanal fisheries targeting mullet, as well as other gillnet
fisheries, and subsequent fishery-related mortality of immature
Brazilian guitarfish, is likely contributing to the significant decline
of the species and is a threat that places the species at a high risk
of extinction.
In addition to the threat from artisanal fishing operations,
juveniles and adults of the species are also at risk of bycatch-related
mortality by the industrial trawl and gillnet fleets operating off Rio
Grande do Sul and Santa Catarina. These fleets focus trawling efforts
on the inner and outer continental shelf (between 29[deg] S. and
34[deg] S.), essentially covering the entire seasonal adult migratory
corridor. Of concern is the fact that the R. horkelli catch from these
industrial fleets are predominantly juveniles, with estimates of
juveniles comprising around 76 to 94 percent of the landings from these
fleets. Again, based on the modeled exploitation scenarios, this level
of juvenile catch is likely contributing to significant declines in the
population. Additionally, the relatively recent expansion and operation
of the Rio Grande do Sul and Itajai trawl fleets into previously
unexplored depths of 100 m-200 m on the outer shelf 28[deg] S.-30[deg]
S., and the subsequent large catches of Brazilian guitarfish, also
suggest that areas that previously served as offshore refugia for the
Rio Grande do Sul population from fishing pressure are no longer
protected from exploitation.
In July 2010, the State of S[atilde]o Paulo, Brazil, declared the
stock of Brazilian guitarfish collapsed due to intense exploitation.
Despite the species' listing under Brazil's endangered species list
since 2004, which effectively prohibits catching this species, R.
horkelli continues to be brought into ports throughout southeastern and
southern Brazil. In both Brazil and Uruguay, R. horkelli is considered
a species of high priority under the country's respective FAO NPOA-
sharks. However, the implementation and effectiveness of the
recommendations outlined in these plans remain uncertain, with the best
available information indicating that current regulatory measures to
protect vulnerable species are poorly enforced, particularly within
artisanal fisheries. Overall, the best available information suggests
heavy exploitation of R. horkelli, particularly in the area where it
was historically most abundant, and a significant lack of adequate
regulatory mechanisms to protect the species from overutilization
throughout its range.
Risk of Extinction
Although there is significant uncertainty regarding the current
abundance of the species, the best available information indicates that
the species has suffered significant historical population declines,
with no indication that these trends have stabilized or reversed. Based
on the species' demographic risks, without adequate protection, these
severely depleted populations are likely to be strongly influenced by
stochastic or depensatory processes. This vulnerability is further
exacerbated by the present threats of overutilization and inadequacy of
existing regulatory measures that continue to contribute to the decline
of the existing populations, compromising the species' long-term
viability. Therefore, based on the best available information and the
above analysis, we conclude that the R. horkelli is presently at a high
risk of extinction throughout its range.
Protective Efforts
With the exception of the recommendations within Brazil and
Uruguay's FAO NPOA-sharks plans discussed above, we were unable to find
any other information on protective efforts for the conservation of
Brazilian guitarfish in Brazil, Uruguay, or Argentina that would
potentially alter the extinction risk for the species. We seek
additional information on other conservation efforts in our public
comment process (see below).
[[Page 76080]]
Proposed Determination
Based on the best available scientific and commercial information
as presented in the status review report and this finding, we find that
the Brazilian guitarfish is presently in danger of extinction
throughout its range. We assessed the ESA section 4(a)(1) factors and
conclude that the species faces ongoing threats from overutilization
and inadequacy of existing regulatory mechanisms throughout its range.
The species' natural biological vulnerability to overexploitation and
present demographic risks (e.g., low and declining abundance, negative
population growth rates, and likely small and/or isolated populations
at an increased risk of random genetic drift) are currently
exacerbating the negative effects of the aforementioned threats,
placing this species in danger of extinction. We also found no evidence
of protective efforts for the conservation of Brazilian guitarfish that
would reduce the level of extinction risk faced by the species. We
therefore propose to list the Brazilian guitarfish as an endangered
species.
Smoothhound Sharks
Smoothhound sharks are members of the family Triakidae and genus
Mustelus. The Mustelus species are often difficult to distinguish due
to their conserved morphology and highly variable intraspecific
meristic characteristics. This problem is compounded in the
southwestern Atlantic, with very few specimens, particularly of larger
individuals, leading to a lack of comparative ontogenetic observations
that can be used for species diagnosis (Rosa and Gadig 2010). To date,
there are at least five species of the genus Mustelus that occur with
overlapping ranges in the southwestern Atlantic: M. canis, M. higmani,
M. norrisi, M. fasciatus and M. schmitti (Rosa and Gadig 2010). Two of
these species, M. fasciatus and M. schmitti, are elasmobranchs that are
being considered for listing in this finding.
Striped Smoothhound Shark (Mustelus fasciatus)
Species Description
The striped smoothhound is one of the most distinctive Mustelus
species. Its head is large, with very small eyes and a sharply pointed
snout (Compagno 1984; Rosa and Gadig 2010). Labial folds are present,
and are longer on the upper jaw than on the lower jaw (Heemstra 1997;
Rosa and Gadig 2010). The striped smoothhound's teeth are small and
uniform in size and are similar in adults and juveniles (Heemstra 1997;
Vooren and Klippel 2005b; Rosa and Gadig 2010). The first dorsal fin is
short, broad, and triangular with a large base and is located closer to
the pelvic fins than the pectoral fins (Compagno 1984; Rosa and Gadig
2010). The second dorsal fin base is generally slightly smaller than
the first dorsal fin base, and a dermal ridge is present between the
two fins (Vooren and Klippel 2005b). The pectoral and pelvic fins have
posterior margins that are nearly straight, and the caudal fin is not
well developed, with a small and rounded ventral lobe (Rosa and Gadig
2010). The striped smoothhound is grey or grey-brown on its dorsal side
and white on its ventral side (Compagno 1984). Newborns and juveniles
have dark bars of irregular widths running across the dorsal surface of
their head and body (Heemstra 1997). The distinguishing vertical bars
are still present in adults, but are not nearly as defined as they are
in juveniles (Sadowski 1977; Heemstra 1997; Lorenz et al. 2010; Rosa
and Gadig 2010). Overall, the striped smoothhound stands out from the
other Mustelus species in the southwestern Atlantic because of its
triangular dorsal and pectoral fins, underdeveloped caudal fin, unique
tooth morphology, wide head, and small eyes (Rosa and Gadig 2010).
Range and Habitat Use
The striped smoothhound is a demersal shark species, found at
depths between 1 m and 250 m along the continental shelf and slope of
the Southwestern Atlantic in Brazil, Uruguay, and Argentina (Soto
2001). The species has a very restricted coastal distribution, ranging
from Santa Catarina in southern Brazil to Bah[iacute]a Blanca in Buenos
Aires Province, Argentina, which covers about 1,500 km of coastline
(Lopez Cazorla and Menni 1983; Vooren and Klippel 2005b; Lorenz et al.
2010). During the winter, adult biomass is concentrated on the
Plataforma Sul between Rio Grande and Chu[iacute] off Rio Grande do
Sul, Brazil (Vooren 1997; Vooren and Klippel 2005b). During the summer,
a portion of the population migrates from Brazil to Uruguay and
Argentine waters, while the rest of the population remains on the
Plataforma Sul off Rio Grande do Sul as year-round residents (Vooren
1997; Vooren and Klippel 2005b). Outside of Brazil, the striped
smoothhound occurs only occasionally, with sporadic observations from
the Mar del Plata, Argentina, near the southern boundary of its range
(Lopez Cazorla and Menni 1983).
Striped smoothhounds display clear ontogenetic (i.e., life-stage
based) depth distributions. In Rio Grande do Sul, neonates are common
in inshore areas between Cassino Beach and Chu[iacute] in depths less
than 20 m, with the greatest frequencies between 2 m-5 m depth from
November to January (summer months; Vooren and Klippel 2005b). As such,
these shallow areas likely function as important nursery areas for the
species (Vasconcellos and Vooren 1991; Soto 2001; Vooren and Klippel
2005b). Adults are found mainly in water depths between 50 m-100 m in
autumn and winter but move to shallower depths (<=50 m) in spring and
summer (Vooren and Klippel 2005b). In the summer, males are much more
common at depths between 20 m and 50 m, and are only rarely caught in
waters less than 20 m deep, whereas females can be found in waters less
than 20 m deep as they move into coastal waters for pupping during the
summer months (Vooren and Klippel 2005b). Striped smoothhound are
generally found in cooler water temperatures (11 [deg]C-15 [deg]C for
juveniles during winter months, and >16 [deg]C for adults; Vooren and
Klippel 2005b) and prefer water salinities between 33.3 ppt and 33.6
ppt (Lopez Cazorla and Menni 1983).
Diet and Feeding
Knowledge of the striped smoothhound's diet is limited. Soto (2001)
studied the stomach contents of 17 specimens captured off Parcel da
Solid[atilde]o in Rio Grande do Sul, Brazil. Crustaceans were the most
abundant prey group, making up 82.4 percent of the diet, while fishes
and mollusks were present in lower numbers (11.8 percent and 5.9
percent, respectively). Box crabs (Heptus pudibundus) were the most
prevalent crustacean, occurring in 52.9 percent of the stomachs
examined (Soto 2001).
Growth and Reproduction
There is scant information on striped smoothhound life history. Age
and growth studies are not available and conflicting data exist for
sizes at birth and maturity in Rio Grande do Sul. For example, one
study reported that size at birth is between 39 cm and 43 cm TL, and
that sexual maturity is reached at 130 cm and 135 cm TL for males and
females, respectively (Vasconcellos and Vooren 1991). More recent
studies report smaller sizes, with birth estimated between 35 cm and 38
cm TL and size at maturity estimated at 119 cm TL for males and 121 cm
TL for females (Soto 2011; Vooren and Klippel 2005b). The smaller size
at maturity seen in the more recent studies could be a
[[Page 76081]]
compensatory response to the high levels of fishing mortality the
species has experienced since the early 1980s (see Overutilization for
Commercial, Recreational, Scientific or Educational Purposes section).
The maximum observed sizes for striped smoothhound are 162 cm TL (17.5
kg) for males and 177 cm TL (29.7 kg) for females (Lorenz et al. 2010).
Striped smoothhound have placental viviparous reproduction (Vooren
1997) and a gestation period that lasts between 11 and 12 months (Soto
2001; Lorenz et al. 2010). Pregnant females migrate into shallow waters
(<20 m) along the Rio Grande do Sul coast to give birth from October to
December (Vasconcellos and Vooren 1991; Vooren 1997; Lorenz et al.
2010). Vooren and Klippel (2005b) report that pupping takes place from
November to January, but Soto (2001) reports that it occurs earlier,
from September to November. Striped smoothhounds have 4-14 pups per
litter, with an average of 8 pups (Vasconcellos and Vooren 1991).
Newborns are seen in high frequency in November, along with females
with mature follicles and postpartum uteri, suggesting an annual
reproductive cycle (Vasconcellos and Vooren 1991). After pupping,
females move to deeper waters to mate (Soto 2001; Vooren and Klippel
2005b; Lorenz et al. 2010). One study found a positive relationship of
litter size and maternal size (Soto 2001); however, two other studies
found no correlation (Vasconcellos and Vooren 1991; Heemstra 1997).
Genetics and Population Structure
Studies examining the genetics of the species or information on its
population structure could not be found.
Demography
The striped smoothhound is generally thought to have low fecundity,
with a long gestation time (~1 year), and an average of only eight pups
(range = 4-14 pups). Information regarding natural mortality rates or
the intrinsic rate of population increase (r) of the striped
smoothhound is unavailable; however, based on the life history
parameters described previously, the species likely has low
productivity, which may hinder its ability to recover from
exploitation.
Historical and Current Distribution and Population Abundance
The striped smoothhound is distributed from Santa Catarina in
southern Brazil to the Bah[iacute]a Blanca in Buenos Aires Province,
Argentina. While striped smoothhound were once considered a dominant
permanent resident in Rio Grande do Sul in the early 1970s and 1980s,
and displayed predictable abundance changes throughout the year (Vooren
1997), they are now considered sporadic in this area and rare in the
northern and southern portions of their range (Soto 2001). Prior to
fisheries exploitation, it is thought that the striped smoothhound had
naturally low abundance based on their relatively low frequency of
occurrence in fishery research surveys (Vooren and Klippel 2005b). For
example, in research trawl surveys on the Plataforma Sul, conducted
from 1972-2005 with over 1,500 hauls, striped smoothhound occurred at a
frequency of only 10 percent in the trawl hauls from the 10 m-100 m
depth range (Vooren and Klippel 2005b) and comprised only 2 to 4
percent of the total elasmobranch CPUE for the period of 1980-1984.
Despite this low frequency of occurrence, Vooren and Klippel (2005b)
note that neonates of the species were relatively abundant in the 1980s
in the summer and commonly observed along the 10,688 km of the Rio
Grande do Sul coastline. In fact, for the period of 1981-1985,
estimated CPUE from artisanal fisheries operating off Rio Grande do Sul
ranged from 1.9 individuals/haul for beach seines to 18.5 individuals/
haul for gillnet fishing gear. In research trawl surveys conducted in
shallow waters of 10 m-20 m depths in 1981 and 1982, juvenile M.
fasciatus occurred at a frequency of 54-86 percent in trawl hauls with
a CPUE of 2.55-3.95 kg/hour. However, in follow-up surveys conducted
nearly two decades later, juveniles and neonates were mostly absent
from hauls, despite significant sampling in habitats where they had
been known to occur. In 2005, neonates were noted as abundant along
only 395 km of the Rio Grande do Sul coastline, corresponding to an
estimated 95 percent decline in occupied area by neonates between 1981
and 2005 (Vooren and Klippel 2005b).
In Uruguay and Argentina, current catches by fishermen are
infrequent. Additionally, trawl surveys conducted along the coastal
region of the Bonaerensean (Buenos Aires) District of northern
Argentina and Uruguay indicate a 96 percent decline in biomass of the
species between 1994 and 1999 (Hozbor et al. 2004). Striped
smoothhounds were also absent from Argentine research surveys conducted
in the 1990s and are currently rarely caught by the commercial fleet,
suggesting that the Argentine sea represents the periphery of its
distribution (Massa 2013).
Summary of Factors Affecting Striped Smoothhound (Mustelus fasciatus)
We reviewed the best available information regarding historical,
current, and potential threats to the striped smoothhound species. We
find that the main threat to this species is overutilization for
commercial purposes. We consider the severity of this threat to be
exacerbated by the species' natural biological vulnerability to
overexploitation, which has led to significant declines in abundance of
all life stages, particularly neonates. We find current regulatory
measures inadequate to protect the species from further
overutilization. Hence, we identify these factors as additional threats
contributing to the species' risk of extinction. We summarize
information regarding these threats and their interactions below
according to the factors specified in section 4(a)(1) of the ESA.
Available information does not indicate that habitat destruction,
modification or curtailment, disease, predation or other natural or
manmade factors are operative threats on these species; therefore, we
do not discuss these factors further in this finding. See Casselbury
and Carlson (2015c) for discussion of these ESA Section 4(a)(1) threat
categories.
Overutilization for Commercial, Recreational, Scientific, or
Educational Purposes
The greatest threat to striped smoothhound is overutilization in
commercial fisheries, particularly by those fisheries operating on the
Plataforma Sul off Rio Grande do Sul. The Plataforma Sul comprises
approximately one-third of the species' geographic distribution and is
the area where the species was historically most concentrated. In fact,
striped smoothhound were commonly caught as bycatch in the 1970s and
1980s on the Plataforma Sul in Brazil, albeit in low numbers (Soto
2001; Vooren and Klippel 2005b). Estimates of CPUE of M. fasciatus on
the shelf in the early 1980s varied between 2 kg/hr and 7 kg/hr (in
areas of low density) and 8 kg/hr to 33 kg/hr (in areas where the
species was more highly concentrated) (Vooren and Klippel 2005b).
Although the presumed naturally low abundance of striped smoothhound
prohibited a directed fishery from developing for this species on the
Plataforma Sul, they were and continue to be caught as part of the
multispecies smoothhound fisheries and as bycatch in fisheries for
other species such as drums, flounders, and mullets (Haimovici and
Mendon[ccedil]a 1996; Vooren and Klippel 2005b). Striped
[[Page 76082]]
smoothhounds have been reported in landings from the industrial pair
and double-rig trawl fleets, bottom longline and gillnet fleets and
artisanal fisheries (Mazzoleni and Schwingel 1999). When caught, large
striped smoothhound weighing more than 4 kg are generally retained and
those less than 4 kg are discarded (Haimovici and Maceira 1981), but
the rate of discard mortality is unknown. However, as both industrial
and artisanal fishing intensified on the Plataforma Sul in the 1980s
and continued through the 1990s, with the heavy use of trawls, gillnets
and beach seines within the habitat of the striped smoothhound shark,
the rates of fishery-related mortality experienced by the species
clearly led to dramatic declines in its abundance (Soto 2001; Hozbor et
al. 2004).
The intense coastal commercial and artisanal fishing off Rio Grande
do Sul that takes place in nearshore waters along the coast (see
additional discussion of these fisheries in the Brazilian guitarfish
assessment) has likely had, and continues to have, the greatest impact
on the species. These coastal fisheries primarily use beach seines,
gillnet and trawl gear in the nearshore locations where striped
smoothhound neonates and juveniles are found year-round. This level of
fishing effort exerts constant pressure on the species before it
reaches maturity (Soto 2001; Vooren and Klippel 2005b), and
consequently, affects the recruitment of juvenile sharks into the
population (Vooren 1997). Significant declines in neonate and juvenile
populations have already been observed. Between the areas of
Chu[iacute] and Torres of Rio Grande do Sul, Brazil, for example,
neonates were abundant in the summer in the 1980s, along the coast from
depths of 2 m-20 m, representing an area of occupancy of about 10,688
km\2\. According to Hozbor et al. (2004), gillnets set off beaches in
this area would capture neonate striped smoothhound in large numbers
(10-100 per set) in the 1980s; however, by 2003, this level of removal
had led to substantial declines in the population, with striped
smoothhound currently caught only sporadically and in much smaller
numbers. Similarly, off of Cassino Beach (located close to the mid-
point between Chu[iacute] and Torres) Vooren and Klippel (2005b)
estimated that CPUE of neonate striped smoothhound decreased by up to
99 percent in the artisanal fisheries during this time period.
Specifically, the CPUE of neonate striped smoothhound and frequency of
its occurrence in the artisanal gillnet fishery sets went from 18.5
(individuals/set) and 75 percent, respectively, in 1981-1985 to 0.2
(individuals/set) and 13 percent in 2002-2003. In 2005, neonates
remained common only in the inner edge of their former 10,688 km\2\
occupied area, in depths between 2 m-5 m: An area of only 395 km\2\.
This significant reduction in occupied area translates to an estimated
95 decline in neonate production and is likely a result of the intense
artisanal and industrial fishing pressure and overutilization of the
species within this area. Trawl surveys conducted in the same area but
in depths of 10 m-20 m showed a similar decline in the CPUE of juvenile
striped smoothhounds, from 2.55 kg/hour in 1981 and 3.95 kg/hour in
1982 to 0.02 kg/hour in 2005, an estimated 99 percent decrease in
abundance (Vooren and Klippel 2005b).
In addition to the coastal artisanal and industrial fisheries, the
intense fishing by the Plataforma Sul trawl fisheries that operate
between the coastal waters and inner continental shelf (see description
of the pair trawl fleet in the Brazilian guitarfish assessment) also
affected and continues to impact the reproductive capacity of the
striped smoothhound population in southern Brazil. These trawl
fisheries, whose area of operation intersects with the spring migration
of female M. fasciatus, incidentally catch both pregnant females and
adult male striped smoothhounds on the inner shelf (Haimovici and
Mendon[ccedil]a 1996; Vooren and Klippel 2005b). As such, all life-
stages of the species as well as both sexes are subject to constant
fishing pressure year-round, which Vooren and Klippel (2005b) point to
as the primary cause for the significant decline and present rarity of
the resident striped smooth population on the Plataforma Sul. As
discussed in the Brazilian guitarfish assessment, fishing by the
industrial and artisanal fleets continues to occur at high efforts on
the Plataforma Sul and especially within the important coastal nursery
and inner shelf habitats for the species (which overlap with R.
horkelli). In fact, total marine fish landings from Rio Grande do Sul
(where striped smoothhound are most concentrated on the Plataforma Sul)
have increased substantially in recent years, from 23,594 t in 2007 to
34,385 t in 2011 (an increase of 46 percent over 4 years) (MMA/IBAMA
2007; IBAMA/CEPERG 2012). Out of the 27 Brazilian States, Rio Grande do
Sul reports the 6th highest level of marine fish landings and Santa
Catarina (which represents the northern periphery of the species' range
in Brazil) reports the highest level of marine fish landings (121,960 t
in 2011) (IBAMA/CEPERG 2012). Based on the trends in the available
fishing data, it is unlikely that the industrial and artisanal fishing
on the Plataforma Sul, and particularly off the coast of Rio Grande do
Sul within striped smoothhound habitat, will decrease in the
foreseeable future, indicating that overutilization (in the form of
bycatch mortality) is still a threat to the species.
Outside of Brazil, off Uruguay and Argentina, striped smoothhound
are caught sporadically as bycatch in gillnets, bottom longlines, and
trawls in fisheries targeting Brazilian flathead (Percophis
brasiliensis), Argentinian sandperch (Pseudopercis semifasciata), apron
rays (Discopyge tschudii), striped weakfish (Cynoscion guatucupa) and
whitemouth croaker (Micropogonias funieri) (Chiaramonte 1998; Lasta et
al. 1998; Domingo et al. 2008). Bycatch levels and the associated
fishery-related mortality of striped smoothhound in these fisheries
have resulted in marked declines in the population, with trawl surveys
conducted in the coastal region of the Bonaerensean District of
northern Argentina and Uruguay indicating a 96 percent decline in the
biomass of striped smoothhound between 1994 and 1999 (Hozbor et al.
2004). In the early 2000s, annual landings of smoothhounds (primarily
M. schmitti, but also M. fasciatus and M. canis) in Uruguay increased
dramatically, from fewer than 350 t in the 1990s to a peak of 1,300 t
in 2000 and remained above 1,000 t through 2005; however, the cause for
this reported increase in landings is unknown and, since 2000, landings
have progressively declined (Domingo et al. 2008). In Uruguay's latest
2013 Fishery Statistics Bulletin, there were no reported landings of M.
fasciatus (Direcci[oacute]n Nacional de Recursos Acu[aacute]ticos
(DINARA) 2014). Similarly, in Argentina, striped smoothhounds are also
currently a rare occurrence (Casselberry and Carlson 2015c).
Inadequacy of Existing Regulatory Mechanisms
Like the daggernose shark and Brazilian guitarfish, the striped
smoothhound is also listed as critically endangered under Annex I of
Brazil's endangered species list. Aside from authorized conservation
research purposes, the capture, transport, storage, and handling of
striped smoothhounds is prohibited. There is also a prohibition of
trawl fishing within three nautical miles of the coast of southern
Brazil, although the enforcement of this prohibition has been noted as
difficult
[[Page 76083]]
(Chiaramonte and Vooren 2007). In addition, the species is still
susceptible to being caught as bycatch in the legally permitted coastal
gillnet fisheries and offshore trawl and gillnet fisheries and
vulnerable to the associated bycatch mortality (Lessa and Vooren 2007).
While the striped smoothhound is not listed as one of the 12 species of
concern under Brazil's FAO NPOA-sharks, the plan does call for a
fishing exclusion area over a large region of the coast of Rio Grande
do Sul at depths of 20 m to protect nursery areas (which would include
the striped smoothhound nursery habitat) (Lessa et al. 2005). The plan
also proposes a fishing closure between 32[deg] S. and 34[deg] S.,
where adults of the species now seem to be found in greatest abundance
(Vooren and Klippel 2005b). However, as mentioned previously, the plan
was only just approved as of December 2014, and will not be fully
implemented for another 5 years. Thus, the implementation and
effectiveness of the recommendations outlined in the plan remain
uncertain, with the best available information indicating that current
regulatory measures in Brazil to protect vulnerable species are poorly
enforced.
In contrast to Brazil, Uruguay's FAO NPOA-sharks does list the
striped smoothhound as a species of high priority (Domingo et al.
2008), and, as stated previously, has set goals to collect the
necessary information on its priority species in order to conduct
abundance assessments, review current fishing licenses, and promote
public awareness to release captured individuals. However, no updated
results from the goals and priorities of this plan could be found. As
such, their implementation and overall effectiveness at decreasing the
threats to the striped smoothhound remains highly uncertain.
Additionally, in 2013, the National Directorate of Aquatic Resources
(DINARA), the state agency responsible for regulating and controlling
fishing and aquaculture in Uruguay, passed a resolution authorizing
fishing with gillnets and longlines in the Rio de la Plata and Atlantic
Ocean at a distance less than 300 m from the coast, between March 1 and
October 31 of each year. This type of fishing was previously prohibited
in 2008; however, due to concerns brought forth by the artisanal
fishermen, primarily of the socio-economic nature, DINARA revised the
prohibition to allow for this seasonal fishing (Resolution No. 24/04/
2013 MGAP). Although this seasonal restriction should provide some
protection for the population of migrating pupping females (which moves
inshore to pup primarily from October to December), it does little to
decrease fisheries-related mortality of young striped smoothhounds
which remain in these coastal waters following birth. In other words,
given that the depth distribution of M. fasciatus extends from shallow
coastal waters out to 100 m depths, and fishery records from Uruguay
show that the species is primarily bycaught in the artisanal longline
and gillnet fisheries (Domingo et al. 2008), this new resolution is
unlikely to adequately decrease the threat of overutilization to
striped smoothhounds.
Extinction Risk
The best available information provides multiple lines of evidence
indicating that the M. fasciatus currently faces a high risk of
extinction. Below, we present the demographic risk analysis, threats
assessment, and overall risk of extinction for the striped smoothhound
shark.
Demographic Risk Analysis
Abundance
While there are no quantitative abundance estimates available for
M. fasciatus, qualitative information and historical catch data can
provide some insight into the current abundance of the species. Based
on data from research trawl surveys, it is thought that the striped
smoothhound naturally occurred at low abundance before they were
exploited in fisheries (Vooren and Klippel 2005b), and were once
considered a dominant permanent resident species on the Plataforma Sul.
However, presently, the species is rarely observed anywhere in its
range and caught only sporadically. Historical data from artisanal
gillnet and beach seine fisheries suggest neonate production on the
Plataforma Sul has decreased by 95 percent since the 1980s.
Additionally, research trawl survey data estimate a decline in juvenile
striped smoothhounds in these coastal waters of around 99 percent over
this same period. Considering adult female striped smoothhounds follow
a spring migration into these same coastal areas for pupping purposes,
and, thus, are also susceptible to these artisanal fisheries, the
significant declines in neonate and juvenile abundance likely
correspond to declines in the number of reproductively active females
in the population as well, as overutilization of the species through
the direct removal of young striped smoothhound shark recruits.
Although CPUE data are lacking from other parts of the species'
range, with catches of striped smoothhound characterized as sporadic
and rare in Uruguay and Argentina, respectively, survey data suggest
that the migratory population has also experienced similar declines.
Based on trawl survey data collected from along the Bonaerensean
District of northern Argentina and Uruguay, the population of striped
smoothhounds suffered an estimated 96 percent decline in biomass
between 1994 and 1999. No other information on abundance or trends was
available from this portion of the species' range. However, considering
the species was of naturally low abundance prior to exploitation, and
fishing pressure has historically been high (particularly on neonates
in nursery areas and juvenile and adults on the inner shelf, including
on both the resident and migratory populations) with no indications
that this pressure has ceased, it is likely that the species has
continued to suffer declines throughout its range.
Growth Rate/Productivity
Very little information is known about the life history of M.
fasciatus. Age and growth studies are unavailable for the species, and
there is conflicting information reported from the literature regarding
the species' size at birth and size at maturity from Rio Grande do Sul,
Brazil. Estimates of size at maturity range from 119 to 130 cm TL for
males and 121 to 135 cm TL for females, with the smaller and more
recent size estimates a possible compensatory response to fishing
mortality. Size at birth ranges from 35 to 48 cm TL. The species is
generally thought to have low fecundity, with a long gestation time (~1
year) and an average of only 8 pups per litter. These reproductive
characteristics suggest the species has relatively low productivity,
similar to other elasmobranch species, which has likely hindered its
ability to quickly rebound from threats that decrease its abundance
(such as overutilization).
Spatial Structure/Connectivity
The striped smoothhound has a very restricted coastal range of only
1,500 km. On the Plataforma Sul off southern Brazil, there is thought
to be a permanent, year-round resident population. Vooren and Klippel
(2005b) note that the area occupied by this population represents one
third of the species' total range, and that the conservation of this
resident population is integral to the conservation of the taxon as a
whole, indicating the relative importance of this population to the
species' survival. However, there is also thought to be a migratory
population that is present on the Plataforma Sul in the winter that
returns to Uruguay and
[[Page 76084]]
Argentina in the summer concurrent with changes in water temperature.
No information exists on the connectivity between the resident and
winter migrant M. fasciatus populations found on the Plataforma Sul;
however, based on the significant decline of the population off the
Buenos Aires Province, it seems likely that the increased fishing
pressure on the migratory population while they winter on the
Plataforma Sul may be negatively impacting the populations found in
other parts of the species' range.
Diversity
The loss of diversity can increase a species' extinction risk
through decreasing a species' capability of responding to episodic or
changing environmental conditions. This can occur through a significant
change or loss of variation in life history characteristics (such as
reproductive fitness and fecundity), morphology, behavior, or other
genetic characteristics. Although it is unknown if M. fasciatus has
experienced a loss of diversity, high fishing pressure on neonates and
reproductively active adults in coastal waters has negatively affected
recruitment rates of neonates into the population, resulting in a
significant depletion of the resident population on the Plataforma Sul.
This reduction of the important resident population in Brazil, combined
with the likely small populations elsewhere throughout its range,
suggest the species may be at an increased risk of random genetic drift
and could experience the fixing of recessive detrimental genes,
reducing the overall fitness of the species.
Threats Assessment
The primary threat to striped smoothhounds is overutilization in
commercial fisheries. Although not targeted in any fisheries throughout
its range, due to its presumed naturally low abundance, striped
smoothhounds are caught as part of the multispecies smoothhound
fisheries and as bycatch in fisheries for other species such as drums,
flounders, and mullets. While adult striped smoothhounds were once
commonly caught as bycatch in the 1970s and 1980s in Brazil, albeit in
low numbers, they are now considered rare in commercial catches.
Additionally, intensive fishing by gillnet and trawl fisheries in
shallow coastal areas where juveniles and neonates occur results in
constant fishing pressure on the species before it reaches maturity,
negatively affecting recruitment of neonates into the population. In
fact, the historical data on the abundance of newborns in coastal
waters provide strong evidence that a 95 percent reduction in annual
production of neonates occurred from 1984 to 2005 as a result of
constant fishing pressure in important coastal nursery areas. Adult
striped smoothhounds are also susceptible to these fisheries during
their spring migration into these same coastal areas for pupping, and
are at risk of being caught as bycatch by the industrial gillnet and
trawl fleets operating on the inner shelf throughout the rest of year.
In fact, the level of fishing mortality on the migratory wintering
population on the Plataforma Sul may have led to the observed declines
in the striped smoothhound population found off the coast of northern
Argentina. Thus, the intense fishing effort by the commercial and
artisanal fisheries on the Plataforma Sul appear to be negatively
affecting the reproductive capacity and growth of the population
throughout its range.
In 2004, the species was listed on Brazil's endangered species
list, which effectively prohibited the capture of this species. As of
2014, the species was classified as ``critically endangered'' on this
list. Although the species is not identified as one of 12 species of
concern under Brazil's FAO NPOA-sharks, the plan calls for fishing
closures in areas of <20 m deep that would provide protection to
neonates and juveniles, as well as other closures to protect adult
aggregations. In Uruguay, the striped smoothhound is listed as a
species of high priority on its FAO NPOA-sharks (Domingo et al. 2008);
however, as mentioned previously, the implementation and effectiveness
of the recommendations outlined in both the Brazilian and Uruguayan
plans remain uncertain, with the best available information indicating
that current regulatory measures in both countries are inadequate to
protect the species from further overutilization.
Given the continued and significant fishing effort by the
industrial trawl fleet and artisanal gillnet on the Plataforma Sul,
contributing to the fishing mortality of the resident population as
well as the wintering migratory population, and inadequacy of existing
regulatory measures to control the exploitation of the marine resources
throughout the species' range, the best available information suggests
that overutilization of the species by industrial and artisanal
fisheries is a threat significantly contributing to its risk of
extinction.
Risk of Extinction
Although there is significant uncertainty regarding the current
status of the species, the best available information indicates that
the species has suffered significant declines throughout its range due
to overutilization in industrial and artisanal fisheries. The species'
very restricted coastal range, with data to suggest it has undergone a
decline of over 90 percent in one third of this range, combined with
its present rarity throughout the rest of its range, make it
particularly susceptible to local extirpations and significantly
increases its risk of extinction from environmental and anthropogenic
perturbations or catastrophic events. With no indication that abundance
trends have stabilized or reversed in recent years, nor any indication
that regulatory measures have been implemented or are adequately
enforced to protect the Plataforma Sul neonates in important nursery
areas, the local reproducing adult population, or the migratory
population from unsustainable fishing mortality levels, it is likely
that the species continues to suffer from population declines. Based on
the species' demographic risks, these severely depleted populations are
likely to be strongly influenced by stochastic or depensatory processes
without adequate protection. This vulnerability is further exacerbated
by the present threats of overutilization and inadequacy of existing
regulatory measures that continue to contribute to the decline of the
existing populations, compromising the species' long-term viability.
Therefore, based on the best available information and the above
analysis, we conclude that M. fasciatus is presently at a high risk of
extinction throughout its range.
Protective Efforts
With the exception of the recommendations within Brazil and
Uruguay's FAO NPOA-sharks, we were unable to find any other information
on protective efforts for the conservation of striped smoothhound
sharks in Brazil, Uruguay, or Argentina that would potentially alter
the extinction risk for the species. We seek additional information on
other conservation efforts in our public comment process (see below).
Proposed Determination
Based on the best available scientific and commercial information
as presented in the status review report and this finding, we find that
the striped smoothhound is presently in danger of extinction throughout
its range. We assessed the ESA section 4(a)(1) factors and conclude
that the species faces ongoing threats from overutilization and
inadequacy of existing regulatory
[[Page 76085]]
mechanisms throughout its range. The species' natural biological
vulnerability to overexploitation and present demographic risks (e.g.,
significantly reduced and declining abundance levels, decreases in
neonate production and recruitment, low productivity, restricted range
with likely small and/or isolated populations at an increased risk of
random genetic drift) are currently exacerbating the negative effects
of the aforementioned threats, placing this species in danger of
extinction. We also found no evidence of protective efforts for the
conservation of striped smoothhound that would reduce the level of
extinction risk faced by the species or otherwise alter its current
status. We therefore propose to list the striped smoothhound shark as
an endangered species.
Narrownose Smoothhound Shark (Mustelus schmitti)
Species Description
The narrownose smoothhound shark has a slender body, similar in
form to other triakids, and a short head (Compagno 1984; Rosa and Gadig
2010). The species has large eyes and a snout that is bluntly angular
(Compagno 1984) with a narrow internostril distance (Rosa and Gadig
2010). Like M. fasciatus, labial folds are present on the mouth and are
longer on the upper jaw than on the lower jaw (Compagno 1984; Heemstra
1997; Rosa and Gadig 2010). Narrownose smoothhounds are grey with
numerous small white spots on their dorsal side and solid white
coloration on their ventral side (Compagno 1984; Heemstra 1997). The
trailing edges of both dorsal fins have exposed ceratotrichia (slender
soft or stiff filaments of an elastic protein that superficially
resembles keratin), a distinctive characteristic for the species (Rosa
and Gadig 2010). The pectoral and pelvic fins are both relatively
small, (Compagno 1984) and the ventral lobe of the caudal fin is poorly
developed (Heemstra 1997).
Range and Habitat Use
The narrownose smoothhound is found in the southwestern Atlantic
from southern Brazil to southern Argentina between 22[deg] S. and
47[deg]45' S. (Belleggia et al. 2012). Rio de Janeiro, Brazil, is the
northernmost limit of the species' range (Oddone et al. 2007) and
R[iacute]a Deseado, Argentina is the southernmost limit (Chiaramonte
and Pettovello 2000). Narrownose smoothhound occurs at depths up to 120
m in Argentina and has been captured as deep as 195 m in Brazil
(Belleggia et al. 2012). In Argentinian waters, narrownose smoothhound
is found in waters with surface temperatures of 8 [deg]C-11.7 [deg]C
and bottom temperatures of 5.5 [deg]C-11 [deg]C (Menni 1985;
Chiaramonte and Pettovello 2000) and salinity that is generally 22.4
practical salinity units (psu) and higher (Molina and Cazorla 2011).
Like striped smoothhounds, a portion of the narrownose smoothhound
population is migratory. In the winter, juveniles, adults, and gravid
females migrate north into Brazilian waters and remain there from April
to November (Haimovici 1997; Vooren 1997; Oddone et al. 2005; Massa et
al. 2006). This migration is thought to be triggered by cold water
moving north into their Argentinian range (Haimovici 1997). Water
temperatures in the wintering grounds are usually between 12 [deg]C and
20 [deg]C (Massa et al. 2006). In the spring, summer, and autumn
(December to April) narrownose smoothhounds are most common in waters
off Uruguay (Vooren 1997; Oddone et al. 2005) and Argentina, with
highest abundance in Argentinian waters noted off Buenos Aires Province
and northern Patagonia (Molina and Cazorla 2011).
Diet and Feeding
Olivier et al. (1968) first characterized the diet of the
narrownose smoothhound as carcinophagous (i.e., eats crabs and other
crustaceans), benthic infaunal (i.e., eats animals that live in the
substrate), and ichthiophagous (i.e., eats fish). The narrownose
smoothhound is an opportunistic predator that generally feeds on
epifaunal benthic organisms and the diet appears to vary geographically
and ontogenetically (Capitoli et al. 1995). For example, in R[iacute]o
de la Plata and El Rinc[oacute]n, Argentina, the diet is generally
dominated by crustaceans, fishes, and polychaetes; however, as
narrownose smoothhounds increase in body size, the consumption of
polychaetes declines and is replaced by more fishes and crustaceans.
The shift to crustaceans occurs around 60 cm TL, while narrownose
smoothhounds around 85 cm TL feed primarily on fish (Belleggia et al.
2012). Temporal and ontogenetic variations in diet were also found for
M. schmitti in Anegada Bay, Argentina, where neonates are more
specialized feeders and predominantly consume decapods, and adults more
commonly consume polychaetes, decapods, bivalves, and occasionally
cephalopods (Molina and Carzorla 2011). Smaller scale diet studies in
Argentina also found the diet to be dominated by epifaunal benthic
organisms, including decapod crabs, fishes, isopods, and polychaetes,
and, to a lesser extent, some teleosts and cephalopods (Chiaramonte and
Pettovello 2000; Van der Molen and Caille 2001).
Growth and Reproduction
The narrownose smoothhound has an estimated lifespan of 20.8 and
24.7 years for males and females, respectively (Hozbor et al. 2010). In
general, narrownose smoothhound females grow faster and grow to a
larger size than males (Chiaramonte and Pettovello 2000; Sidders et al.
2005; Segura and Milessi 2009). Maximum recorded size for M. schmitti
is 110 cm TL, with a modal TL in Brazil of 60 cm for males and 72 cm
for females ((Massa et al. 2006; Molina and Cazorla 2011). Size at
maturity varies throughout the narrownose smoothhound's range, with
estimates for male size at 50 percent maturity ranging from 55 cm TL to
59 cm TL and for females ranging from 56 to 72 cm TL (Chiaramonte and
Pettovello 2000; Oddone et al. 2005; Segura and Milessi 2009; Colautti
et al. 2010). Age at first breeding in Brazil is 4 years for females
and 3 years for males, while it is 6.5 years for females and 5.7 years
for males in Argentina (Casselberry and Carlson 2015d).
Narrownose smoothhound sharks are non-placental and reported to be
yolk-sac viviparous (Hamlett et al. 2005; Gal[iacute]ndez et al. 2010).
Their reproductive cycle is annual with a gestation of 11 months
followed by immediate ovulation and mating (Chiaramonte and Pettovello
2000). In the spring, females move inshore to pup and mate, and then
migrate offshore in late summer to early autumn (Colautti et al. 2010).
Reproduction occurs at different times, ranging from late November in
northern Argentina to mid-December at the southern extent of its range
(Molina and Cazorla 2011). Litter size varies between 2 and 14 pups
(Massa et al. 2006), with an average litter size of around 4 to 5 pups
(Sidders et al. 2005; Gal[iacute]ndez et al. 2010). Litter size
increases significantly with maternal length (Oddone et al. 2005;
Cort[eacute]s 2007), but larger females do not produce larger offspring
(Sidders et al. 2005). Nursery grounds for the narrownose smoothhound
shark in Argentina (based on higher abundance of neonates and juveniles
within these areas) are found in the El Rinc[oacute]n area (including
Bah[iacute]a Blanca and Anegada Bay) and the R[iacute]o de la Plata
(including Samboromb[oacute]n Bay) (Chiaramonte and Pettovello 2000;
Molina and Cazorla 2011).
[[Page 76086]]
Genetics and Population Structure
In terms of population structure, only one genetics study has been
conducted to determine if multiple stocks occur throughout the species'
range (Pereya et al. 2010). Results of this study indicate that M.
schmitti comprises a single demographic unit in the R[iacute]o de la
Plata area and its maritime front (area separating Uruguay and
Argentina), suggesting high connectivity and genetic homogeneity over
this geographic range (Perey et al. 2010). The authors attribute this
genetic homogeneity to the likely high dispersal and migration rates of
the species (based on tagging studies of related species M. antarcticus
and M. lenticulatis; Francis 1988) and lack of obvious dispersal
barriers in the study area. The study also found that nucleotide
diversity in M. schmitti was lower than that reported for other
elasmobranchs. These results may indicate that narrownose smoothhound
experienced a genetic bottleneck, recent expansion, or selection, which
potentially occurred during the Pleistocene Era (Pereyra et al. 2010).
Demography
The annual population growth rate for narrownose smoothhound in
Brazil was calculated to be 1.058 between 1980 and 1994 (Massa et al.
2006). More recently, using life history parameters from individuals
collected off Mar del Plata, Argentina, Cort[eacute]s (2007) determined
the intrinsic rate of increase (r) for narrownose smoothhound to be
0.175 per year when the population is not subject to exploitation
(lower 95 percent confidence limit = 0.030; upper 95 percent confidence
limit = 0.314). Because of this relatively high intrinsic rate of
increase, Cort[eacute]s (2007) concluded that narrownose smoothhound
could withstand higher levels of exploitation than other coastal sharks
in the Buenos Aires coastal region, with sustainable exploitation rates
equivalent to an annual removal rate of about 10 percent of the
population. Natural mortality rates of the species ranged from 0.139 to
0.412 (Cort[eacute]s 2007). These demographic parameters place
narrownose smoothhound toward the faster growing end of the ``fast-
slow'' continuum of population parameters calculated by Cort[eacute]s
(2002), which means this species generally has a higher potential to
recover from exploitation.
Historical and Current Distribution and Population Abundance
The narrownose smoothhound is the most abundant and widely
distributed triakid in the Argentine Sea (Van der Molen and Caille
2001), with densities off Rio de la Plata as high as 44 t/nm\2\ in 1994
(Cousseau et al. 1998). Throughout the rest of the Argentine-Uruguayan
Common Fishing Zone (AUCFZ) [an area that extends 200 nm off the coast
from the border of Uruguay and Brazil to just south of Necochea,
Argentina)] densities of narrownose smoothhounds ranged between 1 and
10 t/nm\2\, with some areas supporting densities as high as 22 t/nm\2\
(Cousseau et al. 1998). Based on data from research surveys conducted
in the spring in Argentine maritime waters (covering coastal Buenos
Aires and waters off Uruguay from 35[deg] S.-41[deg] S.), abundance of
M. schmitti in this area increased from 82,000 t in 1978 to 184,302 t
in 1994. In 1999, M. schmitti abundance on the continental shelf and
slope from 34[deg] S.-48[deg] S. was estimated to be 191,722 t
(Argentina FAO NPOA-sharks 2009). Although recent abundance estimates
could not be found, Massa et al. (2006), citing unpublished data,
indicate that between 1998 and 2002, biomass of the species declined by
22 percent in main fishing areas along the coast of Buenos Aires
Province (Argentina) and the Bonaerensean region (Uruguay) and national
landings in Argentina decreased by 30 percent. By 2003, abundance of M.
schmitti (between 35[deg] S.-41[deg] S.) had fallen to 88,500 t
(Argentina FAO NPOA-sharks 2009). Declines in abundance continued to be
seen in Argentine waters through 2005 (Massa and Hozbor 2008).
Similarly, in Brazil, based on CPUE data, abundance of the winter
migrant population of M. schmitti is estimated to have declined by 85
percent between 1985 and 1994 (Miranda and Vooren 2003), and Massa et
al. (2006) note that a small local breeding population that was
relatively common in the 1980s in southern Brazil has seemingly been
extirpated from the area.
Summary of Factors Affecting Narrownose Smoothhound (Mustelus schmitti)
We reviewed the best available information regarding historical,
current, and potential threats to the narrownose smoothhound shark. We
find that the main threat to this species is overutilization for
commercial purposes. We consider the severity of this threat to be
reduced by the species' natural biological ability to withstand higher
levels of exploitation. However, we find that historical and present
levels of utilization have exceeded the species' biological capacity to
quickly recover from exploitation, and have subsequently led to
significant declines in abundance. We also find that current regulatory
measures are inadequate to protect the species from further
overutilization. Hence, we identify these factors as additional threats
contributing to the species' risk of extinction. We summarize
information regarding these threats and their interactions below
according to the factors specified in section 4(a)(1) of the ESA.
Available information does not indicate that habitat destruction or
modification, disease, predation or other natural or manmade factors
are operative threats on these species; therefore, we do not discuss
these factors further in this finding. See Casselbury and Carlson
(2015d) for discussion of these ESA section 4(a)(1) threat categories.
Overutilization for Commercial, Recreational, Scientific, or
Educational Purposes
The primary threat to the narrownose smoothhound is overutilization
in commercial and artisanal fisheries as the species is intensely
fished throughout its entire range, including within its nursery
grounds. In Argentina, M. schmitti is considered the most important
elasmobranch in Argentine fisheries, making up 9-12 percent of the
total landings from coastal fleets (Gal[iacute]ndez et al. 2010), and
is the most heavily exploited shark species in artisanal fisheries. As
bycatch in Argentine commercial bottom trawls, narrownose smoothhounds
comprise around 20 percent of the coastal harvest from these fisheries
(Colautti et al. 2010). In the 1990s, fishing for the species increased
in the directed industrial shark fisheries (Massa et al. 2004a), with
the narrownose smoothhound being the main shark caught in the Argentine
Sea (based on an extracted biomass of 10,200 t for that time period),
and the second most consumed domestic fish (Van der Molen et al. 1998;
Chiaramonte 1998). Between 1981 and 1991, commercial catches of M.
schmitti ranged from 5,000 t-8,000 t, with peak landings of 13,000 t in
1988 (Cousseau and Perrotta 2000 cited in Massa et al. 2004a; FAO
Global Capture Production Database). From 1992 to 1997, total catch of
narrownose smoothhound remained fairly stable, hovering between 6,000 t
and 8,000 t (Massa et al. 2004a), whereas the number of Argentine
fishing vessels catching M. schmitti increased from 216 to 298 (Massa
and Hozbor 2003). This increase in vessels and associated fishing
pressure on the species consequently led to significant declines in the
abundance of the species off the Argentine coast over this time period.
Specifically, between 1992 and 1998, CPUE declined by 50 percent for
the fishing fleet comprised of small-sized
[[Page 76087]]
vessels (<20 m) operating on the Argentine shelf, whereas the larger
vessels (>20 m) that fished in deeper waters saw a decrease in CPUE of
78 percent (Massa and Hozbor 2003). The larger fishing vessels also
reported a decrease in the mean length of landed narrownose
smoothhounds, from 59 cm in 1994 to 55 cm in 1999, a size smaller than
estimated size at 50 percent maturity (Colautti et al. 2010). The
decline in biomass and CPUE of the species, as well as the decrease in
the average size of narrownose smoothhounds in the landings, all point
to evidence of the significant historical overutilization of the
species off the Argentine coast. In 2003, reported landings of
narrownose smoothhound in Argentine ports reached 7,899 t, which
exceeded the recommended maximum catch limit of 7,200 t for that year
(Massa et al. 2004b), but between 2003 and 2007, mean values of CPUE of
the species steadily increased, from 37.72 kg/h in 2003 to 42.3 kg/h in
2007 (Perez et al. 2011). However, Perez et al. (2011) cautions that
the increase in CPUE does not necessarily reflect an increase in
abundance of the species. Rather the CPUE increase appears to be
influenced by greater accessibility to the species (with the data
indicating an increase in directed fishing effort for M. schmitti or a
greater overlap of the species with other targeted species) (Perez et
al. 2011).
In the artisanal fisheries in Argentina, the narrownose smoothhound
is a highly targeted shark, particularly in the coastal areas between
36[deg] S. and 41[deg] S. latitudes. In Anegada Bay, a known nursery
area for the shark, the smoothhound artisanal fishing season used to
operate from October 15 to December 15, with fishermen exclusively
using bottom gillnets to catch the sharks. In 2004, M. schmitti
comprised 96 percent of artisanal landings from Anegada Bay; however,
due to the selectivity of the artisanal gillnet sizes, only 1.8 percent
of the fish captured were juveniles and 36.8 percent corresponded to
pre-adults or young adults (Colautti et al. 2010). The catches ranged
in size from 52-75 cm TL, which is generally below the recommended size
for sustainable exploitation of this species (Cort[eacute]s 2007),
although size at maturity in Anegada Bay has been estimated at 61 cm
for males and 64 cm for females (Colautti et al. 2010). Since 2008, the
smoothhound fishery in this bay has been closed as an additional level
of protection for the species; however, Colautti et al. (2010) note
that extensive coastal commercial fishing still occurs year-round in
the surrounding El Rinc[oacute]n area in the southwest Buenos Aires
province, which contains a number of nursery habitats for the species
in addition to Anegada Bay. Because trawl nets are the predominant
commercial gear used throughout the El Rinc[oacute]n area, a high
proportion of the narrownose smoothhound catch in the coastal
commercial fisheries are juveniles (Cousseau et al. 1998; Massa et al.
2004a; Pereyra et al. 2008; Molina and Cazorla 2011). In addition,
catches from this area comprise a significant proportion of the total
Argentinian narrownose smoothhound landings, with El Rinc[oacute]n
landings making up 37-53 percent of the national total of M. schmitti
landings from 2003 to 2008 (Colautti et al. 2010). Colautti et al.
(2010) suggests that this heavy coastal commercial fishing pressure on
narrownose smoothhounds in the El Rinc[oacute]n area, especially in the
nursery areas of the species, is not only leading to overfishing of the
sharks in the region but is also contributing to a potential loss of
genetic diversity, as individuals with the highest growth rate are
preferentially removed from the population during fishing operations.
Declines in the biomass of the species have already been reported from
the El Rinc[oacute]n area, with estimates of up to 50 percent between
1994 and 2003 (Colautti et al. 2010).
In Uruguay, landings of smoothhounds (primarily M. schmitti, but
also M. fasciatus and M. canis) increased dramatically between 1999 and
2000, reaching 1,300 t, and then began to steadily decline, reaching
approximately 850 t by 2005 (Domingo et al. 2008). According to data
reported to the FAO, these estimates may be underestimated as the
landings from Uruguay show peaks of 2,156 t and 3,212 t of narrownose
smoothhound in 1998 and 1999, respectively (FAO Global Capture
Production Database). True species composition of shark catches in
Uruguay can be difficult because catch is often reported by common name
and the same common name is used for multiple species (Nion 1999).
However, similar to the Domingo et al. (2008) estimates, the FAO
landings also decreased after 2001, with 892 t estimated in 2005. By
2009, the narrownose smoothhound was considered overfished in the
coastal regions of Uruguay (Defeo et al. 2009).
In the AUCFZ, narrownose smoothhounds are the most heavily
exploited shark (Segura and Milessi 2009). Though maximum permitted
catch limits in the AUCFZ are set by both countries (Argentina and
Uruguay), population declines have been seen throughout this portion of
the narrownose smoothhound's range, mostly due to increased fishing
effort on juveniles of the population (Colautti et al. 2010; Molina and
Cazorla 2011). For example, samples taken in the port of Mar del Plata,
where the largest percentage of the species is landed, indicate that in
2001, nearly half of M. schmitti landings consisted of juveniles, with
the average size of the landings estimated at 61.5 cm TL (Izzo and Rico
2003 cited in Massa et al. 2004b). In 2002, the percentage of juveniles
landed increased to 81.7 percent, and the average size of the
narrownose smoothhound sharks in the landings decreased to 52.5 cm TL
(Izzo and Rico 2004 cited in Massa et al. 2004b), a value below the
size at maturity of the species (i.e., 55 to 60 cm TL). In other words,
this level of utilization of the species, including the apparent
removal of larger individuals from the population, led to a decrease in
the average size of narrownose smoothhound sharks in landings, with the
majority of the landings comprised of immature individuals. As litter
sizes are correlated with maternal length, this removal of larger
individuals from the population may significantly reduce the
reproductive output of the species. Additionally, focusing fishing
effort on primarily juveniles of the population can also have
significant negative effects on recruitment (Vooren 1997) and may lead
to further declines in the species. In fact, landings of the species in
the AUFCZ have decreased in recent years, from 4,480 t in 2010 to 2,921
t in 2014, a decline in catch of around 35 percent (CTMFM 2015). In
addition, the estimated size at maturity of narrownose smoothhounds in
the AUCFZ has chronologically decreased since the 1970s, which is also
indicative of overutilization of the species in this area.
Specifically, in 1978, the size at maturity for males and females was
estimated to be 60 cm and 62 cm TL, respectively (Menni et al. 1986).
In 1997, Diaz de Astarloa et al. (1997) calculated size of maturity
using data from a 1993 winter coastal fishing cruise to be 54.9 and
60.5 cm TL for males and females, respectively. Similarly, estimates
calculated in 1998 determined the size at maturity to be 57.6 cm for
males and 59.9 cm for females (Cousseau et al. 1998). More recently,
Cort[eacute]s (2007) estimated the total size of maturity of the
species to be 56.04 cm TL, which is lower than estimates in previous
studies (Menni et al. 1986; Diaz de Astarloa et al. 1997; Cousseau et
al. 1998) and is consistent with a declining population trend. Finally,
[[Page 76088]]
since 2008, total landings of M. schmitti reported by Argentina and
Uruguay to the FAO have decreased by over 57 percent and 63 percent,
respectively, although no corresponding effort information is
available. Despite the multiple indicators of overutilization of the
species, in 2013, Argentina landed a total of 4,379 t of M. schmitti
and Uruguay landed 194 t (FAO Global Capture Production Database),
suggesting the species is still considered valuable catch and bycatch
in these countries.
In Brazil, M. schmitti occurs as winter migrants on the Plataforma
Sul off Rio Grande do Sul and, similar to R. horkelli and M. fasciatus,
is caught by the trawl and oceanic gillnet fleets operating on the
continental shelf. From 1975 to 1997, M. schmitti was one of two
species that made up the majority of demersal shark landings in the
port of Rio Grande (the other being the school shark, Galeorhinus
galeus; Miranda and Vooren 2003). Targeted fishing for the species is
thought to have increased from the mid 1970s through the 1980s, as
evidenced by the near tripling of CPUE values of M. schmitti in the
single trawl fleet, from 2.48 t/trip in 1975 to 7.31 t/trip in 1987
(Miranda and Vooren 2003). Likewise, the CPUE of M. schmitti by pair
trawls from 1975 to 1987 reflected a similar trend, increasing from
0.35 t/trip to 2 t/trip (Miranda and Vooren 2003). However, CPUE values
for both fleets decreased rapidly after 1987, with values in 1994 (1 t/
trip for single trawl and 0.3 t/trip for pair trawl) indicating an
approximate 85 percent decline in abundance of M. schmitti from 1985
numbers (Miranda and Vooren 2003). Despite the decline, M. schmitti was
still being landed at the port of Rio Grande from April to October in
1994 and 1995 by single trawl and oceanic gillnet fleets, with peak
CPUE from these fleets corresponding with the seasonal occurrence of
the species on the Plataforma Sul.
Similar to the trends seen in the striped smoothhound within the
coastal waters off southern Brazil, neonates of M. schmitti have also
declined in abundance, a likely result of the intense coastal
commercial and artisanal fishing along the Brazilian coast (see
additional discussion of these fisheries in the assessments for
Brazilian guitarfish and striped smoothhound). As mentioned previously,
these coastal fisheries primarily use beach seines, gillnet and trawl
gear in the nearshore locations off Rio Grande do Sul, habitat for
narrownose smoothhound neonates and juveniles. Consequently, neonate M.
schmitti populations that were once abundant in the 1980s have since
seemingly disappeared, with data that show an absence of neonate
individuals from artisanal beach net catches in 2003 and coastal trawl
surveys conducted in 2005 (Vooren et al. 2005b). Further, Massa et al.
(2006) report that a small local population of narrownose smoothhounds
that was known to give birth in south Brazil in November and remain
through February may have been extirpated, but additional information
to confirm this potential extirpation is unavailable.
As discussed in both the Brazilian guitarfish and striped
smoothhound assessments, fishing by the industrial and artisanal fleets
continues to occur at high efforts on the Plataforma Sul, and
especially within the important coastal nursery and inner shelf
habitats for the species (which overlap with both R. horkelli and M.
fasciatus). This heavy fishing pressure may have led to the apparent
extirpation of the local breeding population of narrownose smoothhound
in southern Brazil (Massa et al. 2006 citing Vooren and Lam[oacute]naca
unpublished data) and is likely contributing to the fishing mortality
of the wintering migratory population. Based on the trends from
available fisheries data (see R. horkelli and M. fasciatus
assessments), it is unlikely that the industrial and artisanal fishing
on the Plataforma Sul, and particularly off the coast of Rio Grande do
Sul within narrownose smoothhound habitat, will decrease in the
foreseeable future, indicating that overutilization (in the form of
bycatch mortality) will continue to be a threat to the species leading
to further declines in the wintering migratory population.
Inadequacy of Existing Regulatory Mechanisms
In Argentina, there are few regulations in place to protect
narrownose smoothhound nursery habitat. For example, R[iacute]a Deseado
(~40 km; 47[deg]45' S.; 65[deg]55' W.), the southernmost limit of the
narrownose smoothhound's range, is designated as a nature preserve and
protects the local population from fishery-related mortality
(Chiaramonte and Pettovello 2000). It has been identified as a nursery
area, where breeding adults, neonates, and juveniles enter R[iacute]a
Deseado waters in the late spring and stay until late summer
(Chiaramonte and Pettovello 2000). Anegada Bay (39[deg]50'51'' S. to
40[deg]43'08'' S. and 62[deg]28'44'' W. to 62[deg]03'00'' W.),
Argentina, another known narrownose smoothhound nursery area, is also
protected from fishing operations. The bay was previously designated as
a multiple use zone reserve in 2000, which did little to protect the M.
schmitti population from fishing mortality as a smoothhound fishery
operated within the bay waters. However, in 2004 and 2008, fishing was
banned in the bay due to concern over the conservation of the bay's
natural resources, and since 2008, the smoothhound fishery in Anegada
Bay has remained closed (Colautti et al. 2010). However, as Anegada Bay
is surrounded by the larger El Rinc[oacute]n area, which also includes
a number of other nursery habitats for the species and is open to
fishing, it is unclear how effective the protections in Anegada Bay
will be in decreasing the extinction risk of the species from
overutilization. While these specific areas provide important
protection for the species during critical life stages, they comprise a
very small portion of the species' range and it is unclear to what
extent the species relies on these small nursery areas for recruitment
to the population.
In Uruguay, regulations that likely contribute to decreasing the
fishery-related mortality of the species include a summer trawling ban
in 25 m to 50 m depths between La Paloma and Chuy and specific fishery
area closures in the spring, summer, and autumn on the Uruguayan
continental shelf, designated to protect juvenile hake (Merluccius
hubbsi) but which also correspond with high use areas of the narrownose
smoothhound population (Pereyra et al. 2008).
Both Argentina and Uruguay list the narrownose smoothhound as a
high priority species within their respective FAO NPOA-sharks (Domingo
et al. 2008; Argentina FAO NPOA-sharks 2009). These plans, as stated
previously, set goals to collect the necessary information on its
priority species in order to conduct abundance assessments, increase
research and improve management of the species, review current fishing
licenses, and promote public awareness to release captured individuals.
However, no updated results from the goals and priorities of these
plans could be found. As such, the implementation and overall
effectiveness of these plans at decreasing the threats to the
narrownose smoothhound remains highly uncertain.
In the AUCFZ, the area where current fisheries information
indicates narrownose smoothhounds may likely be most abundant and
heavily targeted, the Comisi[oacute]n T[eacute]cnica Mixta del Frente
Mar[iacute]timo (CTMFM) is in charge of managing fish stocks and does
so through the implementation of catch limits and fishery closures. For
example, every year, the CTMFM implements a prohibition against
[[Page 76089]]
demersal trawling in an area that covers a large section of the common
fishing zone, extending across the continental shelf, in order to
protect vulnerable chondrichthyans from fishery-related mortality. This
prohibition, which is usually in place between November and March,
helps to decrease fishery-related mortality of the narrownose
smoothhound shark during at least part of the year. The CTMFM also
establishes additional area closures to trawling gear throughout the
year in the AUCFZ, including within the Rio de la Plata (where
historical estimates of narrownose smoothhound were as high as 44 t/
nm\2\; Cousseau et al. 1998), in order to protect whitemouth croaker
(Micropogonias furnieri) and juvenile hake from overexploitation by the
fisheries. As these areas correspond with high use by the narrownose
smoothhound population, the trawling bans will also directly help to
protect the narrownose smoothhound from additional fishery-related
mortality.
In terms of the direct management of M. schmitti sharks, from 2002
to 2010, the CTMFM has set the total permissible catch limit for all
Mustelus spp. at 4,850 t. In 2011, this limit was lowered to 4,000 t
(Res. N[deg] 5/11, Res. N[deg] 5/02), and in 2012, the CTMFM set a
species-specific total permissible catch limit for narrownose
smoothhound at 4,500 t (Res. N[deg] 11/13, Res. N[deg] 9/12). This
catch limit remained at this level until 2015, when it was reduced to
3,500 t (Res N[deg] 6/15). However, despite these maximum allowable
catch levels for Mustelus spp. that have been set since 2002, McCormack
et al. (2007) reports that elasmobranch quotas and size regulations are
largely ignored in Argentina and poorly enforced. This may explain why
population declines continued to occur in this part of the species'
range even after regulations were implemented to sustainably manage the
species. Due to a lack of abundance data since 2003, it is unclear
whether the catch limits for Mustelus spp. have positively affected the
population since 2002, though it is worth noting that since 2010,
catches of M. schmitti in the AUFCZ have been below the total allowable
levels and on a decline (CTMFM 2015). However, perhaps the recent
decline in M. schmitti landings prompted the reduction in catch limits
in 2015.
In Brazil, the narrownose smoothhound is listed on Annex 1 of
Brazil's endangered species list and classified as critically
endangered (Directive N[deg] 445). As described in previous species
assessments, an Annex 1 listing prohibits the catch of the species
except for scientific purposes, which requires a special license from
IBAMA. There is also a prohibition of trawl fishing within three
nautical miles from the coast of southern Brazil, although the
enforcement of this prohibition has been noted as difficult
(Chiaramonte and Vooren 2007). In addition, the species is still
susceptible to being caught as bycatch in the legally permitted coastal
gillnet fisheries and offshore trawl and gillnet fisheries and
vulnerable to the associated bycatch mortality (Lessa and Vooren 2007).
Additionally, unlike the striped smoothhound, the narrownose
smoothhound is listed as one of the 12 species of concern under
Brazil's FAO NPOA-sharks and would also benefit from the proposed
fishing closures and other management measures outlined in the plan.
However, as mentioned previously, the plan was only just approved as of
December 2014, and will not be fully implemented for another 5 years.
Thus, the implementation and effectiveness of the recommendations
outlined in the plan remain uncertain, with the best available
information indicating that current regulatory measures in Brazil to
protect vulnerable species are poorly enforced.
Extinction Risk
The best available information provides multiple lines of evidence
indicating that the M. schmitti currently faces a moderate risk of
extinction. Below, we present the demographic risk analysis, threats
assessment, and overall risk of extinction for the narrownose
smoothhound shark.
Demographic Risk Analysis
Abundance
There is limited information available regarding quantitative
abundance estimates of narrownose smoothhound throughout its range.
However, biomass estimates as well as trends in commercial landings and
CPUE data can provide some insight into the abundance of the species.
The narrownose smoothhound is the most abundant and widely distributed
triakid in the Argentine Sea. In Argentina, the narrownose smoothhound
is mainly landed by the commercial fleet operating in the Buenos Aires
coastal region, and represents up to 14.5 percent of landings (Carozza
et al. 2001 cited in Massa et al. 2004b). Between 1992 and 1997,
landings of the species in Argentina were fairly stable, on the order
of 6,000-8,000 t; however, CPUE values decreased by upwards of 78
percent during this time period, indicating a likely decline in the
abundance of the species. From 1998 to 2002, biomass of M. schmitti
reportedly declined in the main fishing areas along the coast of Buenos
Aires Province and the surrounding region by approximately 22 percent
(Massa et al. 2006). National landings also decreased in Argentina by
30 percent during this same time period and have continued to decline
based on FAO landings data through 2013. It is important to note that
the decrease in landings is not due to falling market values as M.
schmitti continues to fetch a high price in the Argentine domestic
market (Massa et al. 2004b). In 2003, the spring time abundance of M.
schmitti from coastal Buenos Aires and Uruguay (between 34[deg] S.-
41[deg] S.) was estimated to be 88,500 t, which represents a 50 percent
and 39 percent decline from estimated values in 1994 and 1999,
respectively (Massa et al. 2004a). Additionally, based on estimates
calculated in 2007, size at maturity of the species has chronologically
decreased since the 1970s, a strong indication of overutilization of
the species and declining abundance.
In Uruguay, there is conflicting information regarding the trend in
catches of M. schmitti. Landings of smoothhounds in Uruguay are
aggregated at the genus level because catch is often reported by common
name and the same common name is used for multiple species. Thus,
identifying the true species composition of shark catches in Uruguay is
problematic. According to Domingo et al. (2008), landings of
smoothhounds in Uruguay (primarily M. schmitti) increased dramatically
between 1999 and 2000, reaching 1,300 tons, and then steadily declined
to approximately 850 tons by 2005. Based on landings data reported to
the FAO, catches of M. schmitti have continued to decline, with only
194 t reported in 2013. However, without corresponding effort
information, it is unclear if the decrease in landings is a result of
decreases in abundance in the species.
In Brazil, M. schmitti occurs as winter migrants on the Plataforma
Sul and is caught by the trawl and oceanic gillnet fleets operating on
the continental shelf. Based on CPUE data from these fleets, the
wintering population has likely suffered significant declines in
abundance. The CPUE values from both the single and pair trawl
fisheries showed an increase from the mid 1970s to the late 1980s;
however, after 1987, CPUE values for both fleets decreased rapidly, and
in 1994, these CPUE values showed an approximate 85 percent abundance
decline of M. schmitti from 1985 values (Miranda and Vooren 2003).
Massa et al. (2006) also cites
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unpublished data that indicate the likely extirpation of a local
breeding population of narrownose smoothhound in Brazil as a result of
fishing in inshore pupping and nursery areas. Although no further
information was given regarding this population, survey and fisheries
data suggest significant declines in newborn M. schmitti from a local
nursery area off the coast of Rio Grande do Sul. Once abundant in the
1980s in the coastal waters off Casino Beach, Rio Grande do Sul,
neonates of this local population have since seemingly disappeared,
with data that show an absence of individuals from artisanal beach nets
in 2003 and coastal trawl surveys in 2005 (Vooren et al. 2005b). This
absence of neonates, compared to data from the 1980s, is likely a sign
of decline of this population and may even suggest a potential
extirpation.
Overall, best available information suggests the species is likely
in decline in parts of its Argentine and Uruguayan range, and has
experienced a significant decrease in abundance in its winter migrant
population in Brazil. Although present abundance estimates are unknown,
the significant declines in both CPUE and landings of the species
throughout its range, as well as the chronological reduction of the
species' average size (based on landings data) and size of maturity,
suggest overexploitation of the species and a declining abundance
trend. Targeting of the species will continue, given its demand in the
market and importance in both the artisanal and commercial fisheries in
the region and, combined with the high fishing pressure in the species'
nursery areas, the species may continue to experience population
declines throughout its range, with abundance levels that will likely
contribute significantly to its extinction risk in the foreseeable
future.
Growth Rate/Productivity
The narrownose smoothhound has an estimated lifespan of 20.8 years
and 24.7 years for males and females, respectively, with a maximum
recorded size of 110 cm TL. Information regarding size and age of
maturity estimates vary throughout the species' range, but the most
recent estimate from Hozbor et al. (2010) suggests an age at maturity
of 4 years for both sexes. Although M. schmitti has an annual
reproductive cycle with a lengthy gestation period (11 months) and an
average of only 4-5 pups per litter, the species' intrinsic rate of
population increase is relatively high, at 0.175 per year. Natural
mortality rates ranged from 0.139 to 0.412 (Cort[eacute]s 2007). These
estimates indicate that M. schmitti has a higher potential to recover
from exploitation compared to other coastal sharks, and could withstand
annual removal rates of up to approximately 10 percent of the
population. However, based on confirmed chronological reductions in
both average size (from landings data) and total length at maturity in
the species, it is apparent that removal rates of the species have been
exceeding the 10 percent sustainable removal rate. The reduction in
mean size and size at maturity is particularly concerning due to the
positive relationship between maternal length and litter size (i.e.,
litter size increases significantly with maternal length) in which a
decrease in maximum size has the potential to reduce the species'
reproductive output. As such, these reductions likely compromise the
species' growth rate and productivity, and consequently, hinder its
ability to recover from exploitation.
Spatial Structure/Connectivity
Very limited information is available regarding spatial structure
and connectivity of M. schmitti populations. Tagging studies of related
species M. antarcticus and M. lenticulatis found that they have high
dispersal capacities (Francis 1988), but no such studies have been
conducted specifically for M. schmitti. If narrownose smoothhound
populations are connected, then the significant fishing pressure on the
migratory population while they winter on the Plataforma Sul may be
negatively impacting the populations found in other parts of the
species' range (perhaps contributing to the observed declines off
Argentina and Uruguay). However, based on the available data, there is
not enough information to identify critical populations or determine
whether the rates of dispersal among populations, metapopulations, or
habitat patches are posing a risk of extinction.
Diversity
The loss of diversity can increase a species' extinction risk
through decreasing a species' capability of responding to episodic or
changing environmental conditions. This can occur through a significant
change or loss of variation in life history characteristics (such as
reproductive fitness and fecundity), morphology, behavior, or other
genetic characteristics. In terms of population structure, only one
genetics study has been conducted to determine if multiple stocks occur
throughout the species' range (Pereya et al. 2010). Results of this
study indicate that M. schmitti comprises a single demographic unit in
the R[iacute]o de la Plata area and its maritime front (area separating
Uruguay and Argentina), with no distinct population structure found
between or within the R[iacute]o de la Plata, the Atlantic coast or its
outer shelf. These findings indicate high connectivity and suggest
genetic homogeneity over this geographic range, which is attributed to
the likely high dispersal and migration rates of the species (Pereya et
al. 2010). However, a lack of genetic structure can also result from
many other factors, including large effective population sizes and/or
the presence of shared ancestral polymorphisms due to recent population
divergence.
In addition to genetic homogeneity, the study found that nucleotide
diversity in M. schmitti was lower than that reported for other
elasmobranchs. These results may indicate that narrownose smoothhound
experienced a genetic bottleneck, recent expansion, or selection, which
potentially occurred during the Pleistocene Era (Pereyra et al. 2010).
However, it is difficult to unambiguously discern between evidence for
natural selection and demographic population expansion. Overall, the
low genetic diversity values found for the species and evidence that
fishing pressure may have already altered the genetic characteristics
of the population (i.e., smaller average size and size at maturity,
which in turn can alter reproductive fitness and fecundity) raise
considerable concern over the species' status. This information
indicates that M. schmtti may be at an increased risk of inbreeding
depression or random genetic drift, and could experience the fixing of
recessive detrimental genes, reducing the overall fitness of the
species.
Threats Assessment
The primary threat to narrownose smoothhounds is overutilization in
commercial and artisanal fisheries, with the species both targeted and
bycaught throughout its range. In Argentina, M. schmitti is considered
the most important elasmobranch for Argentine fisheries; however, data
suggest that the majority of narrownose smoothhounds caught by
Argentine fishermen are juveniles (e.g. up to 81.7 percent of the
landings in 2002), indicating significant fishing pressure in important
nursery areas. Declines in both CPUE and biomass of M. schmitti in
Argentina occurred throughout the 1990s and early 2000s; however, mean
values of CPUE have shown a slight upward trend from 2003-2007.
However, as noted previously, these values should be interpreted with
caution as they could
[[Page 76091]]
be the result of increased directed fishing pressure on M. schmitti or
an increase in overlap of fishing vessels in areas where M. schmitti
has higher concentrations. Further, the chronological reduction in mean
size and size of sexual maturity since the 1970s indicates overfishing
of the species, suggesting exploitation rates are higher than what the
species can presently sustain.
In the AUCFZ, where M. schmitti is most heavily exploited, fishing
regulations currently set total permissible catch of M. schmitti at
3,500 t (which is a reduction from the 4,500 t limit that was in place
since 2012). Additionally, trawling is banned within 5 nm of the coast,
which coincides with the pupping and breeding areas of the species.
While there is no information to indicate whether these regulatory
mechanisms are positively affecting the status of the narrownose
smoothhound, particularly since species-specific catch limits for M.
schmitti have only been implemented since 2012, these regulations may
help reduce fishing pressure in this important part of the species'
range. Since 2010, catches of M. schmitti in the AUFCZ have been below
the total allowable levels (for Mustelus spp. and M. schmitti) and on a
decline; however, it should be noted that despite total allowable
catch, minimum sizes, and annual quotas in place for many elasmobranchs
in Argentina, they are largely ignored and poorly enforced (McCormack
et al. 2007).
In Uruguay, narrownose smoothhounds are both targeted in artisanal
fisheries and caught as bycatch. Despite the difficulties in
identifying species composition of shark catches and discrepancies in
catch information, data indicate landings of M. schmitti have declined
in Uruguay, and in 2009, the species was classified as overfished in
coastal regions of Uruguay and considered a high priority under the
country's FAO NPOA-sharks.
In southern Brazil, the intensive fishing effort on the Plataforma
Sul has likely led to overutilization, and consequently, significant
declines in the winter migrant population of M. schmitti and potential
extirpation of a local breeding population. Bottom trawl fishery CPUE
data provide evidence that abundance of the winter migrant population
of M. schmitti decreased by 85 percent due to intensive fishing effort
from 1985 onwards. The absence of neonates from coastal waters, where
they were once abundant in the 1980s, also suggest that intense fishing
effort, especially in important nursery areas, has led to significant
declines in local populations and potential extirpation of a small
population of Brazilian migrants that was known to give birth in south
Brazil in November and remain through February (Massa et al. 2006).
Since 2004, the species has been listed on Brazil's endangered species
list, which prohibits fishers from catching this species. The species
is also listed as one of 12 species of concern under Brazil's FAO NPOA-
sharks, which calls for fishing closures in areas of <20 m deep that
would provide protection to neonates and juveniles, as well as other
closures to protect adult aggregations; however, the implementation and
effectiveness of the recommendations outlined in the plan remain
uncertain, with the best available information indicating that current
regulatory measures in Brazil to protect vulnerable species are poorly
enforced, particularly in artisanal fisheries.
Based on the best available information, it is evident that M.
schmitti is heavily exploited and has likely experienced population
declines throughout its range as a result of historical and continued
overutilization of the species. In limited parts of the species' range,
regulatory mechanisms are seemingly adequate to control for
overutilization, such as the closures of important nursery areas in
Argentina which protect neonates and juveniles from fishing mortality.
However, throughout large portions of the species' range, particularly
in areas where the species is most heavily exploited, it is evident
that regulatory mechanisms are not adequately protecting the species
from further decline. For example, in the AUCFZ, continued population
declines have been seen in this part of the species' range through 2005
(Massa and Hozbor 2008), despite annual maximum allowable catches for
Mustelus spp. since 2002. Additionally, while CPUE values in Argentina
have shown a slight upward trend from 2003-2007, the cause of this
trend is uncertain and may actually reflect increased direct and
indirect fishing effort on M. schmitti. While species-specific catch
limits were implemented for M. schmitti in 2012, it is unclear if these
levels are adequate to prevent further declines in the species.
Although corresponding effort data are unavailable, since 2008,
landings of M. schmitti reported by Argentina and Uruguay to the FAO
have decreased by over 50 percent. Since 2010, catches in the AUFCZ
have been below the total allowable catch levels and also on a decline,
which may suggest reducing fishing pressure on the species or evidence
that catch regulations are potentially being followed. However,
McCormack et al. (2007) note that quotas and size regulations are
largely ignored and lack enforcement in Argentina. Additionally, since
2006, the total number of vessels in Argentina's fishing fleet has
remained fairly stable (OECD 2014), potentially indicating that fishing
effort has not decreased substantially in recent years. As such, the
decreasing landings, even below total allowable catch limits, may
indicate a continued decline in the abundance of the species. Overall,
based on the best available information, we find that existing
regulatory measures throughout the most heavily exploited areas of the
species' range are inadequate to protect the species from
overutilization, which is the main threat significantly contributing to
the extinction risk of M. schmitti.
Risk of Extinction
While there is considerable uncertainty regarding the species'
current abundance, the best available information indicates that the
species has experienced population declines of significant magnitude
throughout its range. Most concerning is the evidence to suggest M.
schmitti has undergone a chronological decline in average size (based
on landings data) and mean size of maturity, as shown in studies from
the 1970s through 2007 (Massa et al. 2004a; Cort[eacute]s 2007). Not
surprisingly, this decreasing trend corresponds to an increase of
fishing operations and provides evidence of the negative impact of
historical and current exploitation rates and associated fishing
mortality on the biological status of the species. Because of the
positive relationship between maternal length and litter size for the
species, a decrease in the average size of the population has the
potential to reduce the species' reproductive output. Furthermore, a
decrease in average size below the species' mean size of maturity can
hasten the reduction of biomass and increase the risk of local
extinction (Baum and Myers 2004 cited in Massa et al. 2004b). Although
the species' relatively high intrinsic rate of population increase and
ability to withstand moderate levels of exploitation up to 10 percent
of the total population provides the narrownose smoothhound shark with
some protection from extinction, and is likely the reason why the
species remains the most abundant houndshark in the Argentine Sea, the
aforementioned decreases in average size and size at maturity as well
as population size suggest the species is being exploited at a level
exceeding what it can sustain. Thus, based on the best available
[[Page 76092]]
information, we conclude that the species is currently at a moderate
risk of extinction due to declining trends in abundance and population
growth/productivity, which are unlikely to reverse in the foreseeable
future because of the continued overutilization of the species in
commercial and artisanal fisheries and inadequacy of existing
regulatory measures to control this level of exploitation.
Protective Efforts
With the exception of the recommendations within the FAO NPOA-
sharks discussed above, we were unable to find any other information on
protective efforts for the conservation of narrownose smoothhound in
Argentina, Uruguay, or Brazil that would potentially alter the
extinction risk for the species. We seek additional information on
other conservation efforts in our public comment process (see below).
Proposed Determination
Based on the best available scientific and commercial information
as presented in the status review report and this finding, we find that
the narrownose smoothhound is not presently in danger of extinction
throughout its range, but likely to become so in the foreseeable
future. We assessed the ESA section 4(a)(1) factors and conclude that
the species faces ongoing threats from overutilization and inadequacy
of existing regulatory mechanisms throughout its range. Due to the
species' relatively fast population growth rate (for elasmobranchs) and
likely high historical abundance, it can withstand moderate rates of
exploitation. However, based on the declining trends in the species'
abundance, its low genetic diversity, the observed decreases in average
size of the species in catches as well as the decreases in size at
maturity in areas where it is most heavily exploited, best available
data suggest that the fishing mortality rate is higher than what the
species can sustain. Although the species' present level of abundance
does not appear to be at such a low level to trigger the onset of
depensatory processes, the species' observed downward trend is unlikely
to reverse in the foreseeable future as a result of continued
overutilization. We therefore conclude that the species is on a
trajectory indicating that it will more likely than not be at risk of
extinction in the foreseeable future. We also found no evidence of
protective efforts for the conservation of narrownose smoothhound that
would reduce the level of extinction risk faced by the species. We
therefore propose to list the narrownose smoothhound as a threatened
species.
Angel Sharks
Angel sharks are members of the family Squatinidae. Both the spiny
angel shark (Squatina guggenheim) and Argentine angel shark (Squatina
argentina), two of the elasmobranchs considered for listing in this
finding, can be found in the Southwestern Atlantic Ocean from southern
Brazil to Argentina. The taxonomy of angel sharks of the southwestern
Atlantic Ocean has been a source of ongoing controversy (Vooren and
Chiaramonte 2006). Due to similar morphological characteristics, S.
argentina, S. guggenheim, S. occulta, and S. punctata have been
variously synonymized with each other (Compagno 2005; Vooren and
Chiaramonte 2006; de Carvalho 2012). Currently, S. punctata is
considered a junior synonym of S. guggenheim (Vooren and da Silva 1991;
de Carvalho et al. 2012; Vaz and Carvalho 2013). Extensive studies of
the morphotypes that occur in southern Brazil and the southwestern
Atlantic concluded that S. argentina, S. guggenheim, and S. occulta are
three different species that can be distinguished by morphological
differences as well as life history characteristics, such as
differences in reproductive patterns, overall size, and depth and
temperature preference (Vooren and da Silva 1991; Vaz and Carvalho
2013). An analysis of molecular systematics of angel sharks confirms
the validity of S. guggenheim and S. occulta as separate species
(Stelbrink et al. 2010).
Spiny Angel Shark (Squatina guggenheim)
Species Description
The spiny angel shark (S. guggenheim) can be distinguished from its
sympatric species by the presence of a median row of spines or
tubercles on its dorsal side (Vooren and da Silva 1991; Milessi et al.
2001; Sch[auml]fer et al. 2012; Vaz and Carvalho 2013). There are 30-35
spines, which are short, conical, and slightly recurved, between the
head and the first dorsal fin. As females mature, their dorsal spines
become less distinct and take the form of flattened tubercles, whereas
juveniles less than 35 cm TL of both sexes have spines flanked on each
side by a diffuse row of smaller spines (Vooren and da Silva 1991).
Adult males have small spines on the outermost tips of the dorsal
surface of their pectoral fins that are inclined towards the shark's
midline. The outer edges of the pectoral fins are straight and the
posterior corners are located nearer to the origin of the pelvic fin
than to the outer corner of the pelvic fins (Vooren and da Silva 1991).
The dorsal skin is light to dark brown with several white or creamy-
white to yellowish large, rounded blotches that are variable in size
and symmetrically distributed on the entire dorsal surface (Vaz and
Carvalho 2013).
Range and Habitat Use
The spiny angel shark is found in the southwestern Atlantic Ocean
from Esp[iacute]rito Santo, Brazil, to Rawson, Argentina (Milessi et
al. 2001; V[ouml]gler et al. 2003; Awruch et al. 2008). It is a
primarily coastal, bottom dwelling angel shark (Chiaramonte and Vooren
2007; Crespi-Abril 2013). Spiny angel sharks prefer depths between 10 m
and 80 m, but have been reported as deep as 150 m off Argentina
(Cousseau 1973; Chiaramonte and Vooren 2007), and occur in temperatures
between 10 [deg]C and 22 [deg]C (Vooren and da Silva 1991). The species
lives in muddy or sandy bottom substrates and is relatively inactive
during the day. This nocturnal activity makes the spiny angel shark
more vulnerable to gillnet fisheries, which tend to operate at night
(Vooren and Klippel 2005a).
Diet and Feeding
Spiny angel sharks are thought to be sit-and-wait predators, lying
motionless on the bottom until prey passes closely overhead. The prey
is then grasped by an upward bite (Vooren and da Silva 1991). Based on
diet studies, the spiny angel shark appears to prefer bony fishes but
will also feed on crustaceans, molluscs, and polychaetes (V[ouml]gler
et al. 2003; Colonello 2005; V[ouml]gler et al. 2009). In the AUCFZ, a
study of spiny angel shark trophic ecology found that, numerically,
bony fish made up the vast majority of the diet, at 89.7 percent
(V[ouml]gler et al. 2003). Crustaceans (4.8 percent), molluscs (4.4
percent), and polychaetes (0.46 percent) made up the remaining portions
(V[ouml]gler et al. 2003). Spiny angel sharks consumed both pelagic and
demersal fishes including Engraulis anchoita, Cynoscion guatucupa,
Patagonotothen ramsayi, Notothenia longipes, and Merluccius hubbsi. The
crustaceans consumed were primarily shrimps (Penaeidae), while the
squid Illex argentinus was the only species of mollusc consumed
(V[ouml]gler et al. 2003, 2009).
Although ontogenetic and seasonal differences in diet have been
observed for the species (V[ouml]gler et al. 2003; Colonello 2005;
V[ouml]gler et al. 2009), bony fish remain the primary prey item for
all size classes and during all
[[Page 76093]]
seasons, and, generally, as size of the spiny angel shark increases so
does its trophic level. Ranging from a minimum trophic level of 3.69
for the smallest length group of spiny angel shark (23-60 cm) to a
maximum trophic level of 4.40 for the largest length group (81-91 cm),
the entire population of spiny angel sharks in the AUFCZ was estimated
to have a trophic level of 3.90 (V[ouml]gler et al. 2003; 2009). For
comparison, in aquatic environments, trophic levels tend to range from
2 (for species that are lower on the food chain, such as herbivores and
detritivores) to 5.5 (for predators of marine mammals, such as the
polar bear and killer whale) (Pauly et al. 2014).
Growth and Reproduction
Very few age and growth studies on the spiny angel shark could be
found. In terms of length frequency distributions of spiny angel
sharks, individuals caught in the San Mat[iacute]as Gulf, Argentina
showed a modal peak of 75-90 cm TL for males and 80-95 cm TL for
females, with no evidence of size dimorphism (Awruch et al. 2008). The
largest recorded animals were 95 cm TL for both sexes (Awruch et al.
2008). Length at 50 percent maturity for males was reached at 76 cm TL
and for females at 73 cm TL (Awruch et al. 2008).
Studies of spiny angel sharks farther north, in Rio de la Plata and
El Rinc[oacute]n, Argentina, found that males from El Rinc[oacute]n at
a given length were significantly heavier than males from Rio de la
Plata, while females showed no significant differences in the length-
weight relationship (Colonello et al. 2007). Both sexes grew larger in
El Rinc[oacute]n than in Rio de la Plata (Colonello et al. 2007); but,
length at 50 percent maturity in males was not significantly different
between El Rinc[oacute]n and Rio de la Plata (75 cm TL and 72.45 cm TL,
respectively). However, length at 50 percent maturity was significantly
different between study areas for females, with estimates of 71.34 cm
TL in Rio de la Plata and 77.01 cm TL in El Rinc[oacute]n (Colonello et
al. 2007).
In southern Brazil, spiny angel sharks reach a maximum length of 92
cm TL and age of 12 years (Vooren and Klippel 2005a). According to the
characteristics for the S. guggenheim population presented in Vooren
and Klippel (2005a), the relative growth rate (k) of the species from
the von Bertalanffy growth equation is 0.275 year-\1\ with a
theoretical maximum size (L[infin]) of 94.7 cm TL. Length
and age at first maturity is estimated to be 72 cm TL and 4 years,
respectively (Vooren and Klippel 2005a).
In terms of reproduction, the spiny angel shark has only one
functional ovary (Vooren and da Silva 1991), with the maturation of
ovarian follicles lasting about 2 years before ovulation, followed by
gestation (Colonello et al. 2007). The female reproductive cycle is
thought to be triennial (Colonello et al. 2007), with a gestation
period that likely lasts 12 months (Colonello et al. 2007). Gestation
begins in the summer (January-February) and pupping occurs the
following spring (November-December) (Sunye and Vooren 1997). Gestation
is divided into two stages: Uterine gestation and cloacal gestation.
Early gestation (January-April) occurs only in the uteri, which
contains recently ovulated eggs and embryos up to 25 mm TL (Sunye and
Vooren 1997). During mid-term gestation and parturition (June-November)
the uteri undergo a physical reconfiguration, causing the uteri and
cloaca to form a heart-shaped chamber where the embryos develop (Sunye
and Vooren 1997). According to Sunye and Vooren (1997), because this
uterine-cloacal chamber is open to the external environment through a
cloacal vent, this anatomical configuration is thought to be the reason
why Squatina species are observed easily aborting embryos during
capture or handling.
Pupping occurs during the spring and summer months (September-
March) in depths less than 20 m (Vooren 1997; Miranda and Vooren 2003).
Litter sizes for the species range between 2 and 8 pups (Colonello et
al. 2007; Vooren and Klippel 2005a). For spiny angel sharks in
Argentina, Colonello et al. (2007) estimated an average of 4.07 pups
per litter, with fecundity increasing with female length. In contrast,
Vooren and Klippel (2005a) note that spiny angel sharks in southern
Brazil frequently have 5 or 6 pups per litter, with the number of pups
unrelated to female length. However, given the 3-year reproductive
cycle, the range in pup estimates for spiny angel sharks results in a
very low annual fecundity for the species (e.g., between 0.67 and 2.67
pups per year) (Colonello et al. 2007; Vooren and Klippel 2005a). After
pupping, juveniles of the species will remain in the shallow waters for
one year before migrating out to the continental shelf (Vooren and da
Silva 1991; Vooren 1997; Vooren and Klippel 2005a). In terms of known
juvenile habitat, the area of Rio Grande do Sul between 31[deg]50' S.
and 33[deg]30' S. at depths less than 20 m is considered a nursery area
for spiny angel sharks (Vooren and Klippel 2005a).
Genetics and Population Structure
Recently, Garcia et al. (2015) examined the population structure of
the spiny angel shark in the middle of its range, in and around the Rio
de la Plata estuary. Using mitochondrial DNA (which is maternally-
inherited DNA), the authors found that individuals from the outer
estuary, surrounding coastal sites, and the outer shelf of the
southwestern Atlantic showed no evidence of population genetic
structuring. However, examination of nuclear recombinant DNA genes
(which are biparentally-inherited) indicated that there was a
remarkably high level of population genetic structure between the outer
shelf spiny angel sharks and the coastal and outer estuarine angel
sharks. In other words, the samples of spiny angel shark from the outer
shelf represent an isolated group from the samples of spiny angel shark
from the coastal and outer estuarine sites. Additionally, mitochondrial
DNA indicated that the number of immigrant females per generation from
the outer shelf to the Atlantic coast was much lower (2.8 individuals
per generation) than the number of immigrant females per generation
between the other populations (with estimates ranging from 12.8-46.9
individuals). All analyses revealed very low values of haplotype and
nucleotide diversity from the recombinant DNA genes. Based on the low
level of genetic diversity detected in S. guggenheim, Garcia et al.
(2015) suggest the species has either undergone a long-term population
decline or experienced a population bottleneck and recent expansion.
Either scenario suggests a vulnerability to overexploitation, given the
species' longevity and low reproductive potential. However, additional
genetic studies are needed to better understand these patterns (Garcia
et al. 2015).
Demography
Information on natural mortality rates or the intrinsic rate of
population increase of the spiny angel shark is currently unavailable.
Historical and Current Distribution and Population Abundance
In northern Argentina, spiny angel sharks are considered to be a
eurythermic coastal shelf species with highest abundances on the outer
coastal shelf between depths of 28.9 m and 49.6 m (Jaureguizar et al.
2006). In the Rio de la Plata estuary, Argentina, spiny angel sharks
were present most frequently in the deepest estuarine zone (12.6 m-16
m) with salinities between 25 and 34 psu. They are not considered a
[[Page 76094]]
permanent resident of the estuary, with abundances higher in the summer
than during the spring and fall (Jaureguizar et al. 2003).
In the AUCFZ, spiny angel shark distribution appears to be
influenced by temperature, with clear avoidance of water temperatures
below 5 [deg]C and above 20 [deg]C (V[ouml]gler et al. 2008).
Specifically, V[ouml]gler et al. (2008) found that spiny angel sharks
concentrate in water temperatures between 13.2 [deg]C and 18.5 [deg]C
in the spring and between 7.0 [deg]C and 15.0 [deg]C in the fall. They
prefer salinities between 33.4 and 33.5, with avoidance of salinities
below 33.0 and above 34.0. Additionally, a strong association was found
between spiny angel shark presence and thermal horizontal fronts, which
indicates that temperature is the principal environmental variable that
influences distribution (V[ouml]gler et al. 2008). In Rio de la Plata,
in the AUCFZ, spiny angel shark densities are particularly high along
the Uruguayan coast in the spring, which is thought to be related to
the presence of higher salinity waters on the Uruguayan coast than the
Argentine coast during this season (Colonello et al. 2007).
In southern Brazil, spiny angel sharks are considered a resident
species (Vooren 1997). From 1980-1984 spiny angel sharks were common
year round on the southern shelf (at depths between 10 m and 100 m)
from Solid[atilde]o to Chu[iacute], with some areas recording CPUE
densities as high as 50 kg/h (Vooren and Klippel 2005a). According to
Vooren and Klippel (2005a), a portion of the S. guggenheim population
makes seasonal migrations across the continental shelf, which is
related to the 3-year reproductive cycle of the species (i.e., one
third of adult females in the population will migrate per year to give
birth). Specifically, this inshore migration is into depths between 10
m and 40 m and occurs in the spring and summer (September-March) for
pupping and likely mating purposes (as adults of both sexes conduct
this migration in addition to pregnant females) (Vooren 1997; Miranda
and Vooren 2003). As mentioned previously, newborns remain in these
shallow waters (<20 m) for the first year of their life before
migrating to deeper waters on the continental shelf. The other, larger
portion of the population, which is not moving seasonally and includes
both juveniles and adults of both sexes, are most abundant in depths of
40 m to 60 m year-round (Vooren and Klippel 2005a). In fact, research
surveys off of Ubatuba, S[atilde]o Paulo, Brazil caught spiny angel
sharks in shallow sampling stations around 20 m deep, but found that
they were most abundant near 50 m depths (Rocha et al. 1998).
In general, very few abundance estimates are available for the
species. According to Chiaramonte and Vooren (2007), the spiny angel
shark is likely composed of smaller, localized populations throughout
its range. In Argentinian waters, fishery surveys and commercial data
provide limited indication of abundance and trends in this part of the
species' range. In 1993, for example, the abundance of spiny angel
sharks in the San Mat[iacute]as Gulf, Argentina (southern Argentina)
was estimated to be 192.53 t (Argentina FAO NPOA-sharks 2009); however,
the San Mat[iacute]as Gulf makes up a very small portion (approximately
9.6 percent) of the spiny angel shark's range and no recent abundance
estimates could be found. Surveys of the continental shelf in northern
Argentina (between 34[deg] S. and 41[deg] S.; approximately 20 percent
of the species' range), conducted during the spring when abundance of
spiny angel sharks is highest, provided estimates of mean biomass
density of 0.518 t/nm\2\ in 1981, 1.305 t/nm\2\ in 1995, and 0.394 t/
nm\2\ in 1999 (Jaureguizar et al. 2006). Catch rates of the species
were also fairly high based on data from trawl research surveys
conducted in this same area from October 1997 to June 1998, especially
during the inshore spring/summer migration months (September to March).
Specifically, CPUE ranged from 25 sharks/30 min of trawling in March to
80 sharks/30 min of trawling in October (Vogler et al. 2008). A later
study, conducted from 2000-2003 and in the same area, also recorded
high densities of the species during the spring months (November-
December) with estimates of 750 to <1500 kg/km\2\ (equivalent to 2.58-
5.15 t/nm\2\) (Colonello et al. 2007). However, based on fishery-
independent data collected during research surveys conducted in the
winter of 1993 and 2004, and spring of 1994, 1999, 2003, and 2005,
Massa and Hozbor (2008) observed a decrease in the biomass of S.
guggenheim, mainly between the winter seasons of 1993 and 2004. Trends
in biomass for the spring time cruises were less clear, with decreases
estimated between 1994 and 1999 and between 2003 and 2005, and
increases between 1999 and 2003 (Massa and Hozbor 2008). Declines were
also observed in the CPUE of fishing fleets operating on the
Argentinian shelf, particularly for the smaller-sized vessels (<28 m)
that fish in shallower waters on the shelf and would most likely
interact with spiny angel sharks. These vessels saw declines of up to
58 percent in CPUE of Squatina spp. (of which spiny angel sharks are
thought to comprise the majority) between the years of 1992 and 1998
(Massa and Hozbor 2003). In the spring of 2003, the estimated biomass
of spiny angel sharks for all of coastal Argentina was 23,600 t (Massa
et al. 2004b). Information about effort was not provided and more
recent abundance or biomass estimates could not be found.
In Brazil, there are no biomass estimates for the species and most
of the fisheries data for angel sharks is grouped into a general
Squatina spp. category; however, spiny angel sharks are thought to
comprise the majority of the group (Vooren and da Silva 1991; Cousseau
and Figueroa 2001; Vooren and Klippel 2005a). Off Rio Grande do Sul
(between 35[deg] S. and 28[deg] S.), where spiny angel sharks are
primarily exploited in Brazil, mean annual landings of all angel sharks
were over 2000 t from 1985 to 1994 but fell to 607 t by 1997. In 1995,
mortality rates of S. guggenheim exceeded population growth rates
leading to an annual population decline rate of 16 percent (Vooren and
Klippel 2005a citing Vieira 1996). Based on CPUE data from fisheries
operating in this area, the population of S. guggenheim is estimated to
have declined by 85 percent between 1986 and 2002 (Vooren and Klippel
2005a). Catches of angel sharks have continued to decline; however,
landings of both S. guggenheim and S. occulta have been prohibited in
Brazil since 2004, and this could explain why catches have declined.
Summary of Factors Affecting the Spiny Angel Shark
We reviewed the best available information regarding historical,
current, and potential threats to the spiny angel shark. We find that
the main threat to this species is overutilization for commercial
purposes. We consider the severity of this threat to be somewhat
reduced by the species' relatively high abundance in the southern
portions of its range; however, its demographic characteristics
(including very low productivity, limited connectivity, and low genetic
diversity) increase the susceptibility of the species to depletion and,
with the continued fishing pressure on the species, places it at an
increased risk of extinction. We summarize information regarding these
threats and their interactions below according to the factors specified
in section 4(a)(1) of the ESA. Available information does not indicate
that habitat destruction or curtailment, disease, predation or other
natural or manmade factors are
[[Page 76095]]
operative threats on these species; therefore, we do not discuss these
factors further in this finding. See Casselbury and Carlson (2015e) for
discussion of these ESA section 4(a)(1) threat categories.
Overutilization for Commercial, Recreational, Scientific, or
Educational Purposes
The primary threat to spiny angel sharks is overutilization in
commercial and artisanal fisheries as the species is heavily fished
throughout its entire range, including within its nursery grounds. As
noted previously, the vast majority of fisheries information available
on angel sharks from Argentina, Uruguay, and Brazil is reported as
Squatina spp., which includes S. guggenheim, S. argentina, and S.
occulta. All information in this section that refers to angel sharks
includes multiple angel shark species, whereas information specific to
S. guggenheim will specifically reference spiny angel sharks.
In Argentina, there is no directed fishery for angel sharks, but
they are captured in multispecies artisanal shark fisheries and are
considered a valuable bycatch species (Chiaramonte 1998; Bornatowski et
al. 2011). The spiny angel shark, in particular, is commercially
exploited in local fisheries that occur in the San Mat[iacute]as Gulf,
Argentina (Perier et al. 2011), which comprises around 10 percent of
its range. The species is also commercially exploited by the fisheries
operating in the AUFCZ, which, based on survey data, overlaps with
areas of higher concentration of the species (Jaureguizar et al. 2006;
Colonello et al. 2007; Massa and Hozbor 2008; V[ouml]gler et al. 2008)
and comprises around 25 percent of the species' range. Angel sharks are
widely consumed as fresh product called pollo de mar (chicken of the
sea) and as dried and salted product called bacalao argentino
(Argentine cod) (Chiaramonte 1998), and in 2007, angel shark export
revenue in Argentina totaled $2,732,274 U.S. dollars (Argentina FAO
NPOA-sharks 2009).
In Argentina, in the 1990s, angel sharks were considered
commercially important bycatch, particularly in the Necochea school
shark (Galeorhinus galeus) gillnet fishery. During the 1980s, the
school shark became an important resource for coastal fisheries, and by
the 1990s, it was the main shark fishery in the Southwest Atlantic
(Chiaramonte 1998). As the school shark was traditionally fished using
gillnets, the fishery also landed significant amounts of demersal angel
sharks (S. guggenheim and S. argentina), the majority of which were
gravid females (Chiaramonte 1998). Angel sharks (likely comprised
primarily of S. guggenheim) became the second most important fish in
the Necochea artisanal gillnet fishery (Chiaramonte 1998). In fact,
total declared landings of angel sharks in Argentina between 1992 and
1996 steadily rose from 1,358.6 mt to 4,281.1 mt with the majority (66
to 75 percent) of the landings attributed to coastal fishing vessels
(Chiaramonte 1998). Massa and Hozbor (2003) report even higher landings
figures for the years of 1992 to 1995, with landings over 3,500 mt and
totaling more than 14,5000 t for that time period. From 1996 to 1998,
annual landings of angel sharks reached over 4,000 mt (Massa and Hozbor
2003). Although landings of angel sharks were relatively high and
fairly stable throughout the 1990s, there were corresponding decreases
in CPUE, signifying a decline in the abundance of angel sharks that can
likely be attributed to overutilization of S. guggenheim. According to
Massa and Hozbor (2003), the small coastal vessels (<20 m in length),
which were responsible for the majority of angel shark landings, saw
CPUE decline from 12 kg/hour in 1992 to around 5 kg/hour by 1998, a
decrease of around 58 percent. The larger fishing vessels (of 20 m-28 m
in length and >28 m in length), which focus effort on the inner and
outer continental shelf (habitat for larger juveniles and adults of the
species), experienced declines in CPUE of angel sharks of around 44 and
50 percent, respectively (Massa and Hozbor 2003).
Current fishing pressure remains high on the spiny angel shark in
Argentinian waters. In fact, recent landings of angel sharks, and just
from the AUCFZ portion of the species' Argentinian range, suggest total
Argentinian landings have likely been of similar magnitude as those
totals reported in the 1990s (CTMFM 2015). In 2010, total landings in
the AUCFZ amounted to 3,763 t and were over 3,000 t in 2011. In 2012,
landings were 2,736 t and by 2013 and 2014 dropped to below 2,300 t
(CTMFM 2015). Although landings have remained high in recent years,
they also appear to be on a declining trend. Given that catch levels in
the 1990s, which resulted in declines of up to 58 percent in the
species' abundance, remained at similar levels in 2010 and 2011,
suggests that the decrease in landings may likely be a result of a
declining spiny angel shark population as opposed to a decrease in
fishing effort. In fact, since 2006, the total number of vessels in
Argentina's fishing fleet has remained fairly stable (OECD 2014), and,
as of June 2014, there were 635 vessels authorized to operate in the
AUCFZ, with more than half of these vessels identified as trawlers
(CTMFM 2015). Additionally, of the 635 vessels, around 20 percent
identified as coastal vessels, suggesting that fishing pressure and
associated fishery-related mortality will continue to be a threat to
all life stages of the species into the foreseeable future.
In Uruguay, spiny angel sharks are captured by industrial trawling
fleets in coastal and offshore waters (V[ouml]gler et al. 2008). They
are bycatch species in bottom longline, estuarine gillnet, and some
trawl fisheries, but they are also targeted in oceanic gillnet and
bottom trawl fisheries (Domingo et al. 2008). The Uruguayan artisanal
and industrial trawling fleets primarily operate at depths between 10 m
and 200 m, which covers the entire depth range of the spiny angel
shark. Annual catches of angel sharks in Uruguay were less than 100 t
from 1977 to 1996 and ranged between 200 t and 400 t between 1997 and
2005, with the majority likely spiny angel sharks (Domingo et al.
2008). Currently, Uruguay has a fishing fleet of 62 vessels operating
within the AUFCZ, with Uruguayan vessels responsible for around 5.6-7.5
percent of the total angel shark landings from this area from 2010 to
2013. In 2014, this proportion sharply increased to 18.4 percent as did
the total number of landings (from 26 t in 2012 to 142 t and 158 t in
2013 and 2014, respectively) indicating a potential increasing trend in
the exploitation of the spiny angel shark by Uruguayan fishing vessels.
In southern Brazil, spiny angel sharks have been heavily fished by
industrial trawlers and gillnet fleets for the past few decades
(Haimovici 1998; V[ouml]gler et al. 2008). In fact, mean annual
landings of all angel sharks (of which the majority were likely S.
guggenheim) were over 2000 t from 1985 to 1994, with a peak of 2,296 t
in 1993. Given the depth and distribution of S. guggenheim on the
Plataforma Sul, (which likely extends from <10 m to up to 150 m depths
based on species accounts in Argentina; Cousseau 1973; Vooren and da
Silva 1991; Chiaramonte and Vooren 2007), it is highly susceptible to
being caught by the various types of industrial fleets operating on the
continental shelf, including the pair trawl fleet, which primarily
operates off the coast and on the inner continental shelf (up to depths
of 100 m), and the simple trawl fleet, which primarily focuses the
outer continental shelf (in depths of 50 m to <200 m) (Vooren et al.
2005 a; Klippel et al. 2005). Although S. guggenheim did not appear to
be a species of interest
[[Page 76096]]
in the mid-1970s, this started to change by the early 1980s. For
example, in the simple trawl fleet, which operated out of Rio Grande in
depths of 50 m-100 m and engaged in multi-species fisheries directed
towards bony fishes (Klippel et al. 2005; Vooren and Klippel 2005a),
the proportion of angel sharks (S. guggenheim and S. occulata) in the
landings steadily rose from 1975 to 1986. From 1975-1979, the
proportion of angel sharks in the landings data was estimated to be 3.5
percent (range: 2.6-4.1 percent) and for the period covering 1980-1986,
this had increased to 6.2 percent (range: 5.3-7.2 percent) (Vooren and
Klippel 2005a). Although the simple trawl fleet did not specifically
target Squatina spp., the increase of angel sharks in landings suggests
a greater interest in the species and indicates that it was
incidentally caught and retained during regular fishing operations
(Vooren and Klippel 2005a). In 1987, the proportion of angel sharks in
the landings reached a peak of 9.5 percent, which Vooren and Klippel
(2005a) suggest may be evidence of a directed fishery for the species
in the simple trawl fleet. However, after 1987, the angel shark
proportion in the landings significantly decreased, dropping to 5.4
percent in 1990 and 0.5 percent by 2001 (Vooren and Klippel 2005a). The
CPUE of angel sharks (S. guggenheim and S. occulata) by the simple
trawl fleets also decreased over this time period, from an average of
2.75 t/trip (range: 2.59-3.02 t/trip) from 1980-1988 to 0.41 t/trip
(range: 0.26-0.62 t/trip) over the years 1997-2002. This 85 percent
decrease in CPUE of the species suggests that the declining trend in
the landings data was likely indicative of overexploitation that led to
a decline in the species' abundance in the fishing area where these
fleets operate (Vooren and Klippel 2005a). Additionally, given that
CPUE of angel sharks (S. guggenheim and S. occulata) in the Rio Grande
pair trawl fleet also declined over this time period, the decrease in
abundance of angel sharks was likely widespread over the continental
shelf. In the pair trawl fleet, CPUE decreased from 0.94 t/trip (range:
0.34-1.39 t/trip) to 0.12 t/trip (range: 0.08-0.17 t/trip) between the
periods of 1980-1988 and 1997-2002, a decline of 87 percent (Vooren and
Klippel 2005a). In 1995, it was estimated that the fishing mortality
rate of S. guggenheim had exceeded its population growth rate,
resulting in an annual rate of population decline of 16 percent (Vooren
and Klippel 2005a citing Vieira 1996). Based on the above data, as well
as data from fishery research surveys, Vooren and Klippel (2005a)
estimate that the S. guggenheim population on the Plataforma Sul
decreased by around 85 percent between 1986 and 2002, with the decline
occurring simultaneously with the increase in fishing effort and caused
by overexploitation of the species.
However, spiny angel sharks are not only at risk of fishing
mortality from the industrial trawl fleets operating on the Plataforma
Sul, but also from the commercial oceanic gillnet fisheries which began
expanding in the 1990s. As the trawl fleets saw catches start to
decline, due to the overexploitation of the marine resources, many
trawlers began converting their boats to gillnet vessels in the early
1990s. These vessels would fish at depths of up to 300 m, with the
oceanic bottom gillnet fishermen specifically targeting sharks and,
based on CPUE data, potentially Squatina species (Miranda and Vooren
2003). The number of gillnet vessels as well as fishing effort
increased throughout the 1990s, with annual landings of angel sharks by
the oceanic gillnet fleet of more than 800 t between the years 1992 to
1998 (Klippel et al. 2005). Mazzoleni and Schwingel (1999; cited by
Klippel et al. 2005) report that landings of the three angel shark
species (S. guggenheim, S. occulta and S. argentina) were common in the
Santa Catarina bottom gillnet fleet operating on the Plataforma Sul
between 1994 and 1999. However, from 1999 to 2002, annual landings of
angel sharks had dropped in half (Klippel et al. 2005). The CPUE of the
fleet also decreased, from a maximum of 4.3 t/trip in 1992 to values
that varied between 0.5 t/trip and 1 t/trip in the following years
(from 1994-2002; Klippel et al. 2005).
Likely contributing to the decreases in CPUE seen in both the
industrial trawl and gillnet fleets is the fact that the majority of
landings from these fisheries consist of juvenile angel sharks which,
after spending their first year in depths <20 m, migrate out over the
continental shelf (see Historical and Current Distribution and
Population Abundance section). In an examination of landings at the
Port of Rio Grande between June 2002 and July 2003, Klippel et al.
(2005) found that around 70-85 percent of the spiny angel sharks were
juveniles (TL <72 cm). The proportion of juveniles was highest in the
landings from the double-rig trawl fleet, which is to be expected as
the fleet primarily operates in depths <50 m (Klippel et al. 2005).
However, the proportion of juveniles was still high, around 70 percent,
in the landings of the bottom gillnet, pair, and single trawl fleets,
which operate from the coast to depths >200 m (Klippel et al. 2005).
The removal of primarily juveniles from a population can have
significant negative impacts on recruitment, especially for a species
with a 3-year reproductive cycle. And, in fact, in a 2005 bottom trawl
survey conducted in the coastal waters of the Plataforma Sul between
Torres and Chu[iacute], only neonate spiny angel sharks were caught,
despite the fact that both juveniles and adults would be expected
within the trawled depth range (7 m-20 m) (Vooren et al. 2005b). The
CPUE of S. guggenheim was also low compared to historical estimates,
with an estimate of only 0.18 kg/h (Vooren et al. 2005b).
Despite the decreases observed in spiny angel shark abundance on
the Plataforma Sul, fishing effort remains high. Additionally, all life
stages of spiny angel sharks are susceptible to the industrial shelf
fisheries as the fleets operate year round covering the entire depth
distribution of the species. In fact, in 2002, it was estimated that
the fishing effort of the industrial trawl fleet from Rio Grande do Sul
and Santa Catarina (the two largest fishing fleets operating on the
Plataforma Sul) trawled around 141,000 km\2\, corresponding to
approximately 50 percent of the land area of the state of Rio Grande do
Sul (Klippel et al. 2005). Hypothetically, if the area swept by each
trawl vessel was different, the 100,907 km\2\ of the Plataforma Sul
would be completely swept every 9 months (Klippel et al. 2005). When
considering the number of gillnet vessels, nets, and the total length
of these nets operating on the Plataforma Sul, it was estimated that
the length of these gillnets (combined) would equate to around 8,250
km, which corresponds to approximately the entire length of the
Brazilian coast (Klippel et al. 2005). In 2002, a total of 892 t of
angel sharks were landed, with 62 percent landed in Santa Catarina and
38 percent in the Rio Grande do Sul. The oceanic gillnet fleet was
responsible for most of the landings (42 percent), followed by double-
rig trawl fleet (25 percent), and the coastal gillnet, pair, and single
trawl fleets, which each contributed about 10 percent of the landings
(Klippel et al. 2005). These fleets, which historically contributed to
the decline in S. guggenheim on the Plataforma Sul, remain active
today.
Furthermore, as previously discussed in the other species
assessments, these fleets operate at high efforts on the Plataforma Sul
and especially within important coastal nursery and inner shelf
habitats for the species. Although landings of the species are
currently prohibited, the fleets' extensive operations will continue to
contribute to the fishing mortality of all life stages of
[[Page 76097]]
the species as the spiny angel shark likely has high discard mortality
rates based on rates estimated for similar angel shark species. For
example, the at-vessel mortality rate reported for the African
angelshark (S. africana) is 60 percent in prawn trawlers (Fennessy
1994) and 67 percent in protective shark gillnets (Shelmerdine and
Cliff 2006). For the Australian angel shark (S. australis), mortality
rate estimates of 25 percent and 34 percent have been reported for
sharks caught in gillnets (Reid and Krogh 1992; Braccini et al. 2012).
These two angel shark species have similar life history traits and
ecology, including: Reproductive characteristics (ovoviviparous and
produce small litters; Compagno 1984; Rowling et al. 2010), maturity
and maximum sizes (Compagno 1984), depth distribution (continental
shelf and upper slope), behavior, and diet (mainly teleosts;
Shelmerddine and Cliff 2006; Rowling et al. 2010). Given the general
similarities, it seems reasonable to infer similar discard survival
rates for the spiny angel shark from these other two Squatina species.
As such, given the sensitive life history traits of the spiny angel
shark as well as the evidence of significant population declines, an
assumed 60 percent at-vessel mortality rate in trawl fisheries and 25-
67 percent mortality in gillnets is likely to significantly contribute
to the overutilization of the species and increase its extinction risk.
These industrial trawl and gillnet fleets currently participate in
nationally important fisheries and, as such, the threat they pose to S.
guggenheim is unlikely to decrease in the foreseeable future. In fact,
in the oceanic drift gillnet fishery, the fishery responsible for the
highest landings of angel sharks, the main fish species targeted
(Umbrina canosai, Cynoscion guatucupa, and Micropogonias furnieri)
represented around 12.8 percent of the total national marine fish
landings in 2011 for all of Brazil. Micropogonias furnieri is the
second most landed fish nationally, and U. canosai is the seventh most
landed. Based on the above information, the significant level of
fishing effort and associated fishing mortality, especially of juvenile
angel sharks, likely caused and will continue to cause substantial
declines in the spiny angel shark population.
Inadequacy of Existing Regulatory Mechanisms
In the AUCFZ, the area comprising around one quarter of the
species' range, and where survey data suggest the species is likely at
highest concentration (Jaureguizar et al. 2006; Colonello et al. 2007;
Massa and Hozbor 2008; Vogler et al. 2008), spiny angel sharks are
commercially exploited. Similar to the narrownose smoothhound, the
CTMFM manages this exploitation through the implementation of catch
limits and fishery closures. As stated previously, the CTMFM implements
an annual prohibition against demersal trawling in a large section of
the AUCFZ, extending across the continental shelf, in order to protect
vulnerable chondrichthyans from fishery-related mortality. The CTMFM
also establishes additional area closures to trawling gear throughout
the year in the AUCFZ to protect other species, with these closures
also indirectly protecting spiny angel sharks from further fishery-
related mortality from trawl gear. In terms of the direct management of
spiny angel sharks, since 2012, the CTMFM has set a total permissible
catch limit for all Squatina spp. at 2,600 t (Res. N[deg] 8/14, Res.
N[deg] 10/13, Res. N[deg] 10/12). In November 2012, this limit was met
and landings of Squatina spp. were banned for the month of December
(Res. N[deg] 13/12). In 2013, an additional reserve of 400 t was
proposed to be allowed if the 2,600 t limit was reached; however, total
landings had decreased from the previous year to 2,103 t (CTMFM 2015).
In 2014 a 10 percent increase in total allowable catch was allowed to
be added to the limit if the CTMFM saw fit (Res. N[deg] 10/13, Res.
N[deg] 8/14); but this was unnecessary as landings amounted to only
2,281 t (CTMFM 2015). In 2015, the CTMFM kept the same limit that was
implemented in 2014 (2,600 t with an allowance of 10 percent increase;
Res. N[deg] 07/15). Although McCormack et al. (2007) report that
elasmobranch quotas and size regulations are largely ignored in
Argentina and poorly enforced, Squatina landings have been below the
maximum catch limit in recent years, providing evidence that
regulations are potentially being followed. However, without effort
information, it is unclear whether these regulations and the
corresponding decreases in landings can be attributed to adequate
control of the exploitation of the species or rather reflects the lower
abundance of the species from declining populations, or more likely a
combination of the two scenarios.
In Uruguay, regulations that likely contribute to decreasing the
fishery-related mortality of the species include a summer trawling ban
in 25 m to 50 m depths between La Paloma and Chuy and specific fishery
area closures in the spring, summer, and autumn on the Uruguayan
continental shelf, designated to protect juvenile hake (Merluccius
hubbsi) (Pereyra et al. 2008). Although the depth distribution of the
spiny angel shark in Uruguayan waters is unresolved, in southern
Brazilian waters, the species was previously common year-round at
depths between 10 m and 100 m. Specifically, adults were frequently
found in waters between 40 m and 100 m during the autumn and winter and
between 10 m and 40 m in the spring and summer; and both adults and
juveniles were abundant in depths of 40 m-60 m year-round (Vooren 1997;
Miranda and Vooren 2003; Vooren and Klippel 2005a). In northern
Argentina, spiny angel sharks displayed highest abundances on the outer
coastal shelf between 29 m and 50 m depths (Jaureguizar et al. 2006).
Using the above depth distribution in areas just north and south of
Uruguay as a proxy for the species' depth distribution in Uruguayan
waters, it is likely that the proposed fishery closures and trawling
bans will provide some level of protection from fishery-related
mortality, especially during the species' spring/summer migration to
shallower waters for pupping and potentially mating purposes.
The spiny angel shark is also listed as a species of high priority
in Uruguay's FAO NPOA-sharks (Domingo et al. 2008). The plan, as stated
previously, has set goals to collect the necessary information on its
priority species in order to conduct abundance assessments, review
current fishing licenses, and promote public awareness to release
captured individuals. However, no updated results from the goals and
priorities of this plan could be found.
In Brazil, the spiny angel shark is listed on Annex 1 of Brazil's
endangered species list and classified as critically endangered
(Directive N[deg] 445). As described in previous species accounts, an
Annex 1 listing prohibits the catch of the species except for
scientific purposes, which requires a special license from IBAMA. There
is also a prohibition of trawl fishing within three nautical miles from
the coast of southern Brazil, although the enforcement of this
prohibition has been noted as difficult (Chiaramonte and Vooren 2007).
In addition, the species is still susceptible to being caught as
bycatch in the legally permitted coastal gillnet fisheries and offshore
trawl and gillnet fisheries and vulnerable to the associated bycatch
mortality (Lessa and Vooren 2007). The spiny angelshark is also listed
as one of the 12 species of concern under Brazil's FAO NPOA-sharks and
would benefit from the proposed fishing closures and other
[[Page 76098]]
management measures outlined in the plan. This includes the fishing
moratorium and marketing ban, which is proposed to be in effect until
there is scientific evidence that supports population recovery of the
spiny angel shark. It also suggests that a fishing exclusion area be
established in the coastal zone (specifically over a large region of
the coast of Rio Grande do Sul at depths of 20 m) to protect important
nursery grounds for the species. However, as mentioned previously, the
plan was only just approved as of December 2014 and will not be fully
implemented for another 5 years. Thus, the implementation and
effectiveness of the recommendations outlined in the plan remain
uncertain, with the best available information indicating that current
regulatory measures in Brazil to protect vulnerable species are poorly
enforced.
Extinction Risk
The best available information provides multiple lines of evidence
indicating that the S. guggenheim currently faces a moderate risk of
extinction. Below, we present the demographic risk analysis, threats
assessment, and the overall risk of extinction for the spiny angel
shark.
Demographic Risk Analysis
Abundance
Spiny angel sharks are likely the most abundant angel shark species
from southern Brazil to Argentina; however, current quantitative
estimates of abundance of the species throughout its range are
unavailable. In Argentina, the abundance of spiny angel sharks in the
San Mat[iacute]as Gulf (which comprises around 9.6 percent of the
species' range) was estimated to be 192.53 t in 1993. In 2003, the
estimated biomass of spiny angel sharks for all of coastal Argentina
was 23,600 t. No other population estimates have been calculated for
the species. Additionally, between 1981 and 2004, catch rates and
density estimates for areas off the Argentine continental shelf have
been variable; however, fishing fleets reported declines of up to 58
percent in CPUE between 1992 and 1998.
In Brazil, quantitative information, in the form of CPUE and
landings data for the fishing fleets operating on the Plataforma Sul,
is available for all angel shark species, of which S. guggenheim likely
comprises a majority. These data provide insight into trends in
abundance of the spiny angel shark in roughly 20 percent of its range.
Based on a comparison of the CPUE estimates of angel sharks caught on
the Plataforma Sul in both the single and pair trawl fishing fleets
over the time periods of 1980-1988 and 1997-2002, the population of S.
guggenheim off southern Brazil has declined by around 85 percent since
1985 (Miranda and Vooren 2003; Vooren and Klippel 2005a). More recent
landings data from the Santa Catarina oceanic gillnet fishery, covering
the years 2001-2010, show a peak in angel shark landings in 2004 of 340
mt before significantly dropping, with only 2.6 mt landed in 2010.
However, in 2004, landings of S. guggenheim along with S. occulta were
prohibited and, as such, the decline in landings data after 2004 may be
a reflection of this prohibition.
Based on the commercial fishery information, it is likely that
spiny angel sharks have experienced varying levels of population
decline throughout its range. In the northern half of the species'
range (off Brazil), the best available information indicates the
species has undergone rather substantial population declines, with
evidence of negative population growth rates that led to significant
decreases in the overall abundance of the species to the point where
catch rates and observations of spiny angel sharks are extremely low.
Off Uruguay and Argentina, where reported biomass estimates suggest the
species was and is likely still most concentrated, the higher abundance
levels may explain why the magnitude of population decline is estimated
to be smaller in this portion of the species' range. Therefore, while
the species may not be of such low abundance such that it is currently
at risk of extinction, given the high exploitation of the species
throughout its range and subsequent population decline in the northern
half, coupled with the species' low productivity, abundance levels will
likely continue to decline through the foreseeable future to the point
where it may be a significant contributing factor to the species'
overall extinction risk.
Growth Rate/Productivity
There is minimal information on the growth rate and productivity of
the species. Based on the estimated von Bertalanffy growth parameters,
the spiny angel shark exhibits rather fast growth rates for a shark
species (with a growth coefficient (k) of 0.275/year; Vooren and
Klippel 2005a). Fast growth rates help protect species from extinction
by allowing species to attain larger sizes at earlier ages, protecting
it from predation, and also allowing species to attain sexual maturity
sooner, thereby contributing to population growth. The fast growth
rates of the spiny angel shark likely led to the species being the most
common angel shark found in the southwest Atlantic. However, despite
its fast growth rates, the spiny angel shark has a significantly
lengthy reproductive cycle of 3 years, with a litter size ranging
between 2 and 8 pups and an average of around 4-5 pups/litter. This
translates to an annual fecundity between 0.67 and 2.67 pups per year.
Spiny angel sharks are also thought to have cloacal gestation during
the latter half of pregnancy, which is thought to be the reason why
Squatina species are observed easily aborting embryos during capture or
handling. Given the already low annual fecundity of the species, any
further loss of embryos would significantly decrease their already low
reproductive output. Overall, these reproductive characteristics
suggest the species has relatively low productivity, similar to other
elasmobranch species, which may hinder the species' ability to quickly
rebound from threats that decrease its abundance (such as
overutilization) and render the spiny angel shark more vulnerable to
extinction in the face of other demographic risks and threats.
Spatial Structure/Connectivity
The spiny angel shark has a widespread range in the southwest
Atlantic but is thought to be comprised of smaller, more localized
populations (Chiaramonte and Vooren 2007); however, information to
support this is currently unavailable. Information on the connectivity
among S. guggenheim populations throughout its range is limited. The
populations occurring on the Plataforma Sul, off southern Brazil, are
assumed to carry out their entire lifecycle within the same area. This
behavior indicates that these populations maintain population growth by
recruiting within each area without producing a necessary excess of
recruits with the potential to migrate to other areas (Vooren and
Klippel 2005a). As a result, S. guggenheim populations on the
Plataforma Sul likely have limited movement and dispersal migration
between neighboring populations, with migrants having no impact on the
short term abundance of a population. Based on genetic studies, there
is also evidence of limited connectivity between populations found in
other parts of the species' range. For example, genetic analyses of
individuals found around the Rio de la Plata estuary indicate a high
level of population genetic structure between the spiny angel sharks
that occur on the outer shelf and those that are found in the outer
estuarine and coastal waters (with very few immigrants between these
[[Page 76099]]
populations) (Garcia et al. 2015). In other words, the evidence of
limited inter-population exchange observed in the species reduces the
recovery potential for the depleted and small local populations found
throughout the range, and may increase the risk of local extirpations,
possibly leading to complete extinction.
Diversity
A recent genetic analysis using maternally-inherited mitochondrial
DNA markers from spiny angel sharks in and around the Rio de la Plata
Estuary (approximately mid point of the species' range) found no
evidence of population genetic structuring (Garcia et al. 2015).
However, analyses using biparentally-inherited nuclear recombinant DNA
genes indicated that there was a remarkably high level of population
genetic structure between spiny angel sharks found on outer shelf and
those in the coastal and outer estuarine areas (Garcia et al. 2015).
The combination of low haplotype and high nucleotide diversity can be
indicative of a transient bottleneck in the ancestral population, or an
admixture of samples from small, geographically subdivided populations,
with the genetic patterns of exchange potentially explained by sex-
biased behavior or long term shifts in spatial and temporal
environmental variables leading to current displacements (Garcia et al.
2015). However, overall, the low levels of genetic diversity in spiny
angel shark populations suggest a vulnerability to overexploitation in
the southwestern Atlantic Ocean (Garcia et al. 2015) and will likely
render the spiny angel shark more susceptible to extinction in the face
of other demographic risks and threats.
Threats Assessment
The primary threat to S. guggenheim is overutilization in artisanal
and commercial fisheries. The vast majority of fisheries information on
angel sharks is generally reported as ``Squatina spp'' throughout
Brazil, Uruguay, and Argentina; however, spiny angel sharks are thought
to be the most abundant angel shark species from southern Brazil to
Argentina and, therefore, likely comprise the majority of the Squatina
species that are landed.
In Argentina, although the species is not directly targeted, they
are caught incidentally in multispecies artisanal shark fisheries and
are considered a valuable bycatch species (Chiaramonte 1998;
Bornatowski et al. 2011). Fishery-independent research surveys have
recorded relatively high densities of the species on the Argentinian
shelf; however, based on CPUE data, the population saw declines of up
to 58 percent in the late 1990s. Although exploitation of the species
in the AUCFZ, where the species appears to be at highest concentration,
has been managed since 2012 with area closures and catch limits, the
lack of recent abundance estimates or trends hinders an evaluation of
the adequacy of current regulatory measures in preventing the
overutilization of the species from this portion of its range. It is
important to note that landings prior to 2012 from this area were on
the same order of magnitude as those reported for all of Argentina and
which subsequently led to the declines observed in the late 1990s.
Landings have since decreased since the implementation of the catch
limits, and appear to be on a declining trend; however, the number of
fishing vessels authorized to operate in the AUCFZ has remained fairly
stable, potentially indicating that fishing effort has not decreased
substantially in recent years. In other words, the recent declining
trend in landings, even below total allowable catch limits, may
indicate decreasing abundance of the species in this part of its range.
In Uruguay, spiny angel sharks are both targeted and caught as
bycatch by industrial trawling fleets in coastal and offshore waters
(V[ouml]gler et al. 2008; Domingo et al. 2008). All life stages of the
species are exploited as the fleets operate over the entire depth range
of the species (between 10 m and 200 m). Abundance and trends of the
species within this region are unknown; however, declines in
populations just north and south of this region have been observed,
with the species listed as high priority in Uruguay's FAO NPOA-sharks.
Additionally, landings of angel sharks by Uruguayan vessels in the
AUCFZ have increased in both number and proportion of total angel shark
landings in the AUCFZ, indicating a potential increase in fishing
effort of this vulnerable species.
In Brazil, spiny angel sharks have been heavily exploited by
industrial trawlers and gillnet fleets since the 1980s (Haimovici 1998;
V[ouml]gler et al. 2008). In southern Brazil, angel shark landings are
recorded in industrial single trawl, pair trawl, oceanic bottom
gillnet, and coastal artisanal fisheries. These industrial and coastal
artisanal fleets operate year round in depths that span <20 m to 300 m,
including during the sharks' reproductive seasonal migrations, and
hence capture all life stages of spiny angel sharks (Vooren and Klippel
2005a). The impact of this fishing pressure and effort led to observed
declines in S. guggenheim (around 85 percent), with fishing mortality
rates exceeding population growth rates and resulting in an annual rate
of population decline of 16 percent for spiny angel sharks in the mid
1990s (Vorren and Klippel 2005a). Although many trawlers began
converting their boats to gillnet vessels in the early 1990s (due to
decreases in catch), the threat of overutilization remains as the
oceanic bottom gillnet fishermen also fish at depths of up to 300 m and
now land the majority of angel sharks, of which 70-85 percent are
juveniles (Klippel et al. 2005). Although spiny angel sharks have been
a prohibited species since 2004, the fishing effort (both by trawl and
gillnet fleets) on the Plataforma Sul remains high and poorly
regulated, and, therefore, the susceptibility of the species' to
fishery-related mortality also remains high. The industrial gillnet and
trawl fleets, which contributed to the historical decline in the
population off southern Brazil, are active today and participate in
nationally important fisheries. Given the percentage of juveniles
caught by these fisheries coupled with the assumed discard mortality
rates, the continued operations of these fleets will likely have
significant negative impacts on S. guggenheim recruitment to the
population, especially for a species with a 3-year reproductive cycle.
The present level of fishing effort by the artisanal and industrial
fisheries on Brazil's continental shelf will continue to lead to
declines in the spiny angel shark population and, hence, contribute to
the extinction risk of the species.
Risk of Extinction
There is significant uncertainty regarding the current abundance of
the species throughout its entire range. While the Brazilian
populations have experienced substantial declines and remain at risk
from overutilization by fisheries, the same cannot be concluded with
certainty for the populations farther south in the species' range.
Based on the available data, the populations off Uruguay and Argentina
have likely experienced moderate declines, with recent landings and
vessel data potentially indicating a decreasing trend in abundance and
stable or increasing trend in fishing effort. The significant
demographic risks to the species (e.g., extremely low fecundity,
declining population growth rate, and limited connectivity), the
decline and subsequent rarity of the species in an area that comprises
around half of its range, and the evidence of continued and heavy
fishing pressure on the species throughout its entire range, place the
species on a trajectory indicating that it will more likely than
[[Page 76100]]
not be at a high level of extinction risk in the foreseeable future.
Therefore, based on the best available information and the above
analysis, we conclude that S. guggenheim is presently at a moderate
risk of extinction throughout its range.
Protective Efforts
With the exception of the recommendations within the FAO NPOA-
sharks discussed above, we were unable to find any other information on
protective efforts for the conservation of spiny angel sharks in
Argentina, Uruguay, or Brazil that would potentially alter the
extinction risk for the species. We seek additional information on
other conservation efforts in our public comment process (see below).
Proposed Determination
Based on the best available scientific and commercial information
as presented in the status review report and this finding, we find that
the spiny angel shark is not presently in danger of extinction
throughout its range but likely to become so in the foreseeable future.
We assessed the ESA section 4(a)(1) factors and conclude that the
species faces ongoing threats from overutilization and inadequacy of
existing regulatory mechanisms throughout its range. Due to the
species' relatively fast growth rate (for elasmobranchs) and high
biomass in the southern portion of its range, the species has not yet
declined to abundance levels that would likely trigger the onset of
depensatory processes. However, the species' demographic risks
(including very low fecundity, low genetic diversity, and connectivity)
coupled with the significant reduction in the population from the
northern portion of its range, greatly increases the species'
vulnerability to extinction from environmental variation or
anthropogenic perturbations. Furthermore, given the evidence of
decreasing landings despite stable (or even increasing) fishing effort,
we find that the level of exploitation in the area where spiny angel
sharks are currently most concentrated is likely contributing to
unsustainable fishing mortality rates. We therefore conclude that the
species is on a trajectory indicating that it will more likely than not
be at risk of extinction in the foreseeable future. We also found no
evidence of protective efforts for the conservation of spiny angel
sharks that would reduce the level of extinction risk faced by the
species. We therefore propose to list the spiny angel shark as a
threatened species.
Argentine Angel Shark (Squatina argentina)
Species Description
In addition to the spiny angel shark, the Argentine angel shark was
petitioned for listing under the ESA. The Argentine angel shark occurs
in the Southwest Atlantic and can be distinguished from its sympatric
species by its coloration, dental formula, neurocranial features,
dorsal surface denticle pattern, and pectoral fin shape. Unlike S.
guggenheim, the Argentine angel shark lacks a dorsal midline of
morphologically distinct denticles (Vaz and Carvalho 2013). Dermal
denticles densely cover the entire dorsal surface, except for the
posterior margins of unpaired fins and the anterior apex of the
pectoral fins. The pectoral fins are large, twice as long as they are
wide, with the anterior margins strongly convex, creating a visible
``shoulder'' area at the base of the head (Vaz and Carvalho 2013). The
dorsal coloration is dark to purplish brown with small, round, white
spots symmetrically distributed across the entire dorsal surface
(Vooren and da Silva 1991; Milessi et al. 2001; Vaz and Carvalho 2013).
Small individuals are creamy white over the entire ventral surface,
while larger animals develop dark beige on the central region of the
head, margins of the pectoral fins, origin of the pelvic fins, and the
posterior region of the trunk (Vaz and Carvalho 2013). Unlike S.
guggenheim and S. occulta, female Argentine angel sharks have two
functional ovaries, which can also serve as an identifying feature
(Vooren and da Silva 1991).
Range and Habitat Use
While there is some conflicting information regarding the range of
Argentine angel shark, it is clear that they have a restricted range in
the Southwest Atlantic, and are present in southern Brazil (from Rio de
Janeiro southward), Uruguay, and at least the northern part of
Argentina (i.e., Buenos Aires). Argentine angel sharks live on muddy or
sandy bottom substrates on the continental shelf and slope at depths
between 100 m and 400 m, with a principal depth range of 120 m-320 m
(Cousseau 1973; Vooren and da Silva 1991; Vooren and Klippel 2005a).
Angel sharks are active mostly at night, and show limited movement and
dispersal migration between neighboring populations, with migrants
having no impact on the short term abundance of a population (Vooren
and Klippel 2005a).
Diet and Feeding
Like the spiny angel shark, the Argentine angel shark is thought to
be a sit-and-wait predator, lying motionless on the bottom until prey
passes closely overhead. The prey is then grasped by an upward bite
(Vooren and da Silva 1991). There is limited information regarding the
Argentine angel shark diet. In a study that analyzed stomach contents
of 53 individuals, results showed that fish made up 68.33 percent of
the diet, and crustaceans and molluscs made up 15 percent and 1.6
percent of the diet, respectively (Cousseau 1973). The rest of the diet
contained unidentifiable remains. The most common fish species was
Cynoscion striatus, while the shrimp Artemesia longinaris and
Hymenopenaeus mulleri were the most common crustaceans, and Loligo
brasiliensis was the most common mollusc (Cousseau 1973). Argentine
angel sharks are also thought to occasionally consume the short-finned
squid (Illex argentinus) (dos Santos and Haimovici 2000).
Growth and Reproduction
Little is known about the growth and reproduction of the Argentine
angel shark. Their maximum total length is estimated at 138 cm with a
size at sexual maturity of 120 cm TL; however, age at first maturity
and size at birth are unknown (Vooren and da Silva 1991; Vooren and
Klippel 2005a). Gravid females and neonates are rarely found, so little
is known about the reproductive characteristics of the species.
Gestation is lecithotrophic (developing embryos depend on yolk for
nutrition) (Vooren 1997) and litter size ranges from 7-11 pups (most
commonly 9 or 10 pups) (Vooren and Klippel 2005a). Like S. occulta and
S. guggenheim, the Argentine angel shark may have cloacal gestation
during the latter half of pregnancy (Vooren and Klippel 2005a). Based
on the location and capture of two neonates of 35 cm and 37 cm TL in
Santa Catarina, Brazil, it is assumed that Argentine angel sharks
reproduce on the slope of the southern Brazilian continental shelf
(Vooren and Klippel 2005a). Additionally, the Bahia Engano in coastal
Patagonia is thought to serve as a nursery area for the Argentine angel
shark (Van der Molen et al. 1998).
Genetics and Population Structure
Studies examining the genetics of the species or information on its
population structure could not be found.
Demography
Information regarding natural mortality rates or the intrinsic rate
of
[[Page 76101]]
population increase of the Argentine angel shark is currently unknown.
Historical and Current Distribution and Population Abundance
As previously described, there is conflicting information regarding
the range of the Argentine angel shark, and the species' distribution
is poorly defined. While there are no specific population abundance
estimates for Argentine angel sharks, they are considered to be the
least common species of angel shark found in the southwestern Atlantic,
particularly in Argentina (Vooren and Klippel 2005a). According to one
paper, Argentine angel sharks occur in highest densities (from 1 to
11.4 t/nm\2\) along the Uruguayan coast in the AUCFZ, where salinities
are higher than the Argentine coast (D[iacute]az de Astarloa et al.
1997). However, this paper refers to all Squatina species as Argentine
angel sharks and, based on the distribution of S. guggenheim (see
species assessment; Colonello et al. 2007), the authors have likely
misidentified spiny angel sharks as Argentine angel sharks.
In Brazil, Argentine angel sharks of all life stages are most
abundant between Rio Grande and Chu[iacute] in Rio Grande do Sul, with
no evidence of abundant populations outside of this area (Vooren and
Klippel 2005a; Vooren and Chiaramonte 2006). Specifically, the outer
shelf and upper slope of the southern Brazilian continental shelf,
south of latitude 32 [deg]S., are important habitat areas for S.
argentina. However, based on fishery independent research surveys from
1986-2002, the abundances of both the Argentine angel shark and the
hidden angel shark (S. occulta) within this area have declined by
approximately 80 percent (Vooren and Klippel 2005a).
Summary of Factors Affecting the Argentine Angel Shark
We reviewed the best available information regarding historical,
current, and potential threats to the Argentine angel shark species. We
find that the main threat to this species is overutilization for
commercial purposes. We consider the severity of this threat to be
exacerbated by the species' natural biological vulnerability to
overexploitation, which has led to significant declines in abundance of
the species. We find current regulatory measures inadequate to protect
the species from further overutilization. Hence, we identify these
factors as additional threats contributing to the species' risk of
extinction. We summarize information regarding these threats and their
interactions below according to the factors specified in section
4(a)(1) of the ESA. Available information does not indicate that
habitat destruction or modification, disease, predation or other
natural or manmade factors are operative threats on these species;
therefore, we do not discuss these factors further in this finding. See
Casselbury and Carlson (2015f) for discussion of these ESA section
4(a)(1) threat categories.
Overutilization for Commercial, Recreational, Scientific or Educational
Purposes
The primary threat to S. argentina is overutilization by commercial
fisheries, particularly the trawl and bottom gillnet fisheries in
Brazil, where the species is likely most concentrated. As mentioned
previously, the vast majority of fisheries information on angel sharks
is documented as ``Squatina spp'' throughout Brazil, Uruguay, and
Argentina; however, the Argentine angel shark is the rarest Squatina
species in the region. Additionally, incorrect species identification
of angel sharks is a problem that persists in the AUCFZ, particularly
in Argentine landings (Milessi et al. 2001); therefore, determining the
magnitude of threats currently acting specifically on S. argentina is
challenging. However, some information, including fisheries effort,
catch and landings data, provides insight into the current status of
Argentine angel shark, as described below.
As discussed in the spiny angel shark assessment, angel sharks, in
general, have been historically caught in the multispecies artisanal
shark fisheries and considered valuable bycatch species in Argentina
(see spiny angel shark: Overutilization section). However, the
Argentine angel shark is considered relatively rare in Argentina (Menni
et al. 1984 cited in Vooren and Klippel 2005a), with S. guggenheim
comprising the majority of the catch (Massa et al. 2004b). From 1981-
1982, Otero et al. (1982) noted the low density of S. argentina off the
Buenos Aires coast and estimated an annual biomass of only 4,050 t. In
the 1990s, angel sharks became commercially important bycatch,
particularly in the Necochea school shark (Galeorhinus galeus) gillnet
fishery, and were a prevalent bycatch species in the Patagonian coastal
trawl fisheries. According to 1993-1996 observer data from the
Patagonian fishery, Argentine angel sharks were bycaught with medium
frequency, particularly in the San Matias Gulf and Bahia Engano. By
1993, declared landings of S. argentina were on the same order of
magnitude as the total biomass of the population estimated from the
early 1980s, at 3,974.7 mt, and landings remained near this level in
1994 at 3,621.8 mt (Chiaramonte 1998). However, by 1998, CPUE values
indicated that the level of fishing mortality on the Squatina shark
populations was leading to declines in abundance of angel sharks.
Specifically, Massa and Hozbor (2003) estimated that CPUE of angel
sharks declined by 58 percent between 1992 and 1998 for vessels
operating on the Argentine shelf, and since 1998, landings of Squatina
species have been on a decline (Massa et al. 2004b).
In Uruguay, Argentine angel sharks are targeted in the Atlantic
gillnet fishery and bottom trawl fisheries. They are also caught as
bycatch in bottom longline, estuarine gillnet, and bottom trawl
fisheries (Domingo et al. 2008). Both artisanal and industrial trawl
fleets operate at depths between 10 m and 200 m in Uruguay, which
overlap with the principal depth range of S. argentina. Annual catches
of all angel sharks in Uruguay have increased over time, with less than
100 t landed from 1977 to 1996 and increasing to between 200 t and 400
t from 1997 to 2005. In 2012, catches for Squatina spp. exceeded the
set catch limit in the AUCFZ (2,600 t), resulting in the closure of the
fishery for the following month. However, similar to catch composition
reported in Argentina, it is likely that the majority of these reported
angel shark landings are spiny angel sharks rather than Argentine angel
sharks (Domingo et al. 2008).
In Brazil, Argentine angel sharks are most abundant between Rio
Grande and Chu[iacute] in Rio Grande do Sul, off southern Brazil
(Vooren and Klippel 2005a; Vooren and Chiaramonte 2006); however, they
are the least captured Squatina species in Brazilian fisheries (Perez
and Wahlrich 2005). In general, angel shark landings are recorded in
single trawl, pair trawl, oceanic gillnet, and coastal artisanal
fisheries. Historically, angel sharks were fished on the Brazilian
shelf by double rig trawlers down to 140 m depths, with S. guggenheim
comprising the majority of the catch (Haimovici 1998).
As catch rates of shelf resources decreased, and international
markets for traditionally discarded or poorly known species expanded,
deep-water demersal fishing operations off southern Brazil (from
20[deg] S.-34[deg] S.) increased in the early 1990s (Valentini et al.
1991; Haimovici 1998) and greatly accelerated after 1999. This was
largely a result of shrimp and groundfish trawlers expanding their
fishing grounds towards the previously unexploited resources of
[[Page 76102]]
the outer shelf and slope (Valentim et al. 2007; Perez and Wahrlich
2005), but also reflected the increasing number of gillnet vessels
operating on the outer shelf. In fact, in the early 1990s, in response
to a decline in trawl catch of marine resources, many trawlers began
converting their boats to gillnet vessels. These vessels would fish at
depths of up to 300 m, with the oceanic bottom gillnet fisheries
specifically targeting sharks and, based on CPUE data, potentially
Squatina species (Miranda and Vooren 2003). The number of gillnet
vessels as well as fishing effort increased throughout the 1990s, with
annual landings of angel sharks by the oceanic gillnet fleet of more
than 800 t between the years 1992 to 1998. Landings of the three angel
shark species (S. guggenheim, S. occulta and S. argentina) were
especially common in the Santa Catarina bottom gillnet fleet operating
on the Plataforma Sul between 1994 and 1999 (Mazzoleni and Schwingel
1999; cited by Klippel et al. 2005). However, in the following years,
from 1999 to 2002, annual landings of angel sharks dropped in half and
the CPUE of the bottom gillnet fleet also decreased, from a maximum of
4.3 t/trip in 1992 to values that varied between 0.5 t/trip and 1 t/
trip in the years 1994-2002 (Klippel et al. 2005).
As the regional Brazilian fleets gradually occupied slope grounds
in the 1990s, they were joined by foreign fleets chartered by national
companies as part of a deep-water fishing development program promoted
by Brazilian authorities (Perez et al. 2003). This program was
implemented in 2000, with chartered vessels operating at depths of 200
m to 900 m in the Brazilian EEZ, using traps, longlines, gillnets, and
trawl nets (Perez and Pezzuto 2006 cited in Perez et al. 2009).
Together, both national and foreign trawlers concentrated their efforts
in the southern and southeastern sectors of the Brazilian coast,
exploiting three discrete bathymetric strata: shelf break (100-250 m),
upper slope (250-500 m), and lower slope (> 500 m) (Perez and Pezzuto
2006 cited in Perez et al. 2009). Brazilian trawlers concentrated their
activities on the shelf break (at 100-200 m) while chartered gillnet
vessels concentrated their efforts in deeper areas of the upper slope
(at 300-400 m). As a result of this expansion of fishing activities
into deeper waters, deep-water monkfish (Lophius gastrophysus) was the
first fishing resource that proved abundant enough to sustain
profitable deepwater fishing operations off southern Brazil, and thus a
targeted fishery developed for the species. In 2001, a total of 7,094 t
of monkfish were landed, mostly by national double-rig trawlers (58
percent) and foreign chartered gillnetters (36 percent) operating in a
fishing area that extended along the southern Brazilian slope, from
21[deg] S. to 34[deg] S. and within the 100-600 m isobaths (Perez et
al. 2005). Monkfish biomass also happened to be concentrated between
125 m and 350 m depths, which overlaps with the principal depth
distribution of the Argentine angel shark (120 m-320 m). As a result,
Argentine angel sharks were reported as a significant bycatch species
in the monkfish gillnet fishery. In fact, Perez and Warhlich (2005)
noted that S. argentina was one of the most retained bycatch species in
the monkfish gillnet fishery, with bycatch estimated at 1.052 per 100
nets in 2001 (total 8,698 individuals). This fishing regime that
contributed to the significant bycatch of Argentine angel shark
continued operating at high levels through most of the following year
(2002), with monkfish landings of 5,129 t (Perez et al. 2009). The
numerous incidental catches produced by monkfish gillnetting suggests
that the development of this fishery off southern Brazil substantially
increased the levels of fishery-related mortality in the S. argentina
population and potentially introduced adverse effects in the
recruitment process (i.e., recruitment overfishing), especially
considering that the species' reproductive cycle may exceed 1 year
(Cousseau and Perrota 1998 cited in Perez and Warhlich 2005). In fact,
research bottom trawl surveys of the outer shelf and upper slope from
Cape Santa Marta Grande to Chu[iacute] (the main habitat of Argentine
angel sharks) found decreases in both the CPUE and frequency of
occurrence of Argentine angel sharks during the winter and fall seasons
between the years 1986/87 and 2001/02. Specifically, these surveys
detected declines of 75 and 96 percent in S. argentina CPUE (kg/hour)
and frequency of occurrence, respectively, during the winter months,
and declines of 97 and 63 percent, respectively, during the fall
surveys. These declines confirm that the abundance of S. argentina in
southern Brazil decreased by roughly 80 percent from its original level
as a result of recruitment overfishing, primarily due to the bottom
gillnet fishery (Vooren and Lam[oacute]naca 2002; Vooren and Klippel
2005a).
In 2003, the fishery regime changed, as the foreign chartered
vessels abandoned Brazilian waters as a result of conflicts with
national trawlers (Perez et al. 2009). Since then, exploitation has
been maintained mostly by double-rig trawlers along with a few vessels
of the national fleet transformed to fish with the new gillnet
technology (Wahrlich et al. 2004 cited in Perez et al. 2009). Landings
of monkfish decreased by roughly 50 percent from 2002 to 2003, and have
remained stable around 2,500 t ever since (Perez et al. 2009). The
large reduction in monkfish biomass after 2002 (and the stabilization
at biologically insecure levels thereafter) is largely attributed to
the fact that landed catches have been systematically higher than
maximum recommended catches (Perez, 2007a; Anon 2007 cited in Perez et
al. 2009). In 2004, the monkfish fishery was declared overexploited,
with subsequent biomass assessments lacking any signs of recovery for
the monkfish stock (Perez et al. 2009). Given the significant bycatch
of Argentine angel sharks in the monkfish fishery in 2001, and the
subsequent 80 percent decline in the angel shark population by 2002,
the continued intense exploitation by the monkfish fishery within the
Argentine angel shark habitat likely contributed to further abundance
declines of S. argentina after 2002. This is especially probable
considering the fact that the fishery operates on the outer and upper
slope areas of the continental shelf, where the Argentine angel shark
reproduces and likely carries out its entire lifecycle. Thus, the
significant increase in fishing effort on the outer shelf and slope
areas, particularly by the monkfish fishery, likely impacted all life
stages of the species, resulting in recruitment overfishing and,
ultimately, overutilization of the species leading to a significant
population decline.
Argentine angel sharks are still likely susceptible to fishing
pressure in the monkfish fishery, as the fishery is still operational
today. Recent landings of monkfish for years 2009, 2010, and 2011 were
2,744 mt, 2,592 mt and 2,616 mt, respectively (IBAMA 2011). While this
is a large reduction from peak landings in 2001 of 7,094 mt, Argentine
angel sharks of all life stages are likely still bycaught by this
fishery, which may limit the species from recovering from its initial
80 percent population decline, especially considering the species' low
productivity. In addition, the Argentine angel shark likely has high
discard mortality rates based on rates estimated for similar angel
shark species (see spiny angel shark--Threats Assessment). Given
general similarities between the Argentine angel shark and other
Squatina species, it seems reasonable to infer similar discard survival
rates for the Argentine angel shark (i.e., ~60 percent at-vessel
[[Page 76103]]
mortality rate in trawl fisheries and ~25-67 percent mortality in
gillnets).
Thus, while the bottom gillnet fishery specifically targeting
monkfish has been restricted in terms of overall effort, with only the
national trawl fleet continuing to operate on the upper slope (Perez et
al. 2009), the threat of overutilization remains. However, the monkfish
fishery is not the only fishery presently operating within the
Argentine angel shark habitat. There are a number of oceanic bottom
gillnet fisheries targeting other species (e.g., Umbrina canosai,
Cynoscion guatucupa, and Micropogonias furnieri) that currently operate
on the shelf and slope at depths of up to 300 m. In fact, due to their
effort and fishing area of operation, these oceanic bottom gillnet
fisheries now land the majority of angel sharks in Brazil (Klippel et
al. 2005). As described in the spiny angel shark assessment, fishing
effort (both by trawl and gillnet fleets) on the Plataforma Sul remains
high and poorly regulated, and therefore, the susceptibility of the
species' to fishery-related mortality also remains high. As such, given
the best available information and the above analysis, we conclude that
overutilization is a factor that is significantly contributing to the
extinction risk of the species.
Inadequacy of Existing Regulatory Mechanisms
In Argentina, catches of angel sharks are regulated through annual
catch limits and fisheries closures. Since 2013, Squatina landings have
been below the maximum catch limit in recent years, providing evidence
that regulations are potentially being followed. However, without
effort information, it is unclear whether these regulations are
adequately controlling the exploitation of angel sharks and given that
Argentine angel sharks are particularly rare in Argentina, the degree
to which these regulations are decreasing the threat of overutilization
of the species in this portion of its range is uncertain.
In Uruguay, the Argentine angel shark is listed as a species of
high priority in the country's FAO NPOA-sharks (Domingo et al. 2008).
The plan, as stated previously, has set goals to collect the necessary
information on its priority species in order to conduct abundance
assessments, review current fishing licenses, and promote public
awareness to release captured individuals. However, no updated results
from the goals and priorities of this plan could be found.
Like the spiny angel shark, and other species described previously
in this proposed rule, the Argentine angel shark was listed as
``critically endangered'' under Annex I of Brazil's endangered species
list in 2004. As described in previous species assessments, an Annex 1
listing prohibits the catch of the species except for scientific
purposes, which requires a special license from IBAMA. There is also a
prohibition of trawl fishing within three nautical miles from the coast
of southern Brazil, although enforcement of this prohibition has been
noted as difficult (Chiaramonte and Vooren 2007), and moreover, the ban
only covers depths of <10 m, which does little to provide any
protection to the Argentine angel shark given its principal depth
distribution of 120-320 m. As described in previous species
assessments, Brazil has a FAO NPOA-sharks; however, the Argentine angel
shark is not considered one of the 12 species of concern.
Finally, there are some regulatory mechanisms in place for the
monkfish fishery in Brazil, which operates in the primary habitat of
the Argentine angel shark and has been a significant source of bycatch-
related mortality for the species. In mid-2002, government regulations
were implemented to prohibit foreign gillnetters from operating south
of 21[deg]S (to the southern extent of Brazil's EEZ), which roughly
encompasses the entirety of the Argentine angel shark's Brazilian
range. This regulation effectively terminated foreign chartered gillnet
operations off Brazil and left a national fleet of 5 licensed units to
continue the fishery (Perez et al. 2009). However, despite this
reduction of the monkfish fishery fleet, uncontrolled exploitation
continued and the stock was declared overexploited in 2004. It was not
until 2005 that a management plan for the monkfish fishery was
eventually developed, which included the implementation of 100 percent
observer coverage for monitoring the fishery, logbooks, and a
recommendation to ban fishing shallower than 250 m (Perez et al. 2009).
However, the principal depth range of S. argentina exceeds the 250 m
restriction, thus this recommendation only theoretically protects a
portion of the species' depth range. In 2008, catch limits of 1,500 t
per year were imposed for the monkfish gillnet fishery, as well as
bycatch limits of certain species; however, though the catch limits
should help reduce overall fishing effort, the species is still
susceptible to bycatch-related mortality in the fishery.
Overall, regulatory mechanisms for the monkfish fishery,
particularly the ban of chartered foreign gillnets from 21[deg] S. to
the southern extent of Brazil's EEZ, which were responsible for
catching a total of 157,656 monkfish (compared to a total of only
16,697 monkfish landed by all gears of the national fleet) from 2000-
2007, and recent catch limits of 1,500 tons for the gillnet fishery,
have likely reduced the level of fishing pressure and subsequent
mortality of Argentine angel sharks. However, the fact that enforcement
of management rules for the monkfish fishery has been poor, with no
evident signs of recovery for this overexploited resource (Perez et al.
2009), may indicate that the regulations outlined in the management
plan for the monkfish are inadequate to control for indirect
overutilization of Argentine angel sharks. Given that the conservation
status of the Argentine angel shark likely relies heavily upon the
success of the management plan for the southern Brazil gillnet monkfish
fishery (Vooren and Chiaramonte 2006) and that the monkfish fishery is
still operational throughout the species' Brazilian range via the
national fleet, with reportedly poor enforcement of management rules,
the fishery is likely still exerting fishing pressure and contributing
to the overutilization of the already at-risk S. argentina population.
This continued exploitation is concerning for a species that has
already undergone such significant declines in a critical portion of
its range, with no indication of a reversal of this trend. As such, we
conclude that existing regulatory mechanisms to control for
overutilization of the Argentine angel shark are inadequate,
particularly in Brazil, where the species is most heavily concentrated
and utilized.
Extinction Risk
Demographic Risk Analysis
Abundance
Estimates of population abundance specifically for Argentine angel
shark (Squatina argentina) throughout its range are not available.
However, some qualitative information as well as density and biomass
estimates are available from parts of the species' range. Compared to
congeners S. guggenheim and S. occulta, the Argentine angel shark is
the rarest species of angel shark found in the southwestern Atlantic,
particularly in Argentina. Biomass of S. argentina in Argentina was
estimated to be 40,000 mt in 1998, although there is high uncertainty
with this estimate. In Brazil, this species is reportedly most abundant
between Rio Grande and Chu[iacute] in Rio Grande do Sul, with no
evidence of abundant populations outside this region. Based on fishery-
independent
[[Page 76104]]
surveys conducted from 1986-2002, abundance of Argentine angel shark
declined by approximately 80 percent on the outer shelf and upper slope
of the Plataforma Sul, which is where the highest concentrations of the
species is located. Due to uncertainties regarding the range and
distribution of the species, as well as identification issues between
S. argentina and other Squatina spp. in the region, the current
abundance of the species cannot be determined at this time. However,
given the intense year-round fishing pressure from trawl and gillnet
fisheries within the very restricted range of this rare species,
combined with the species' presumed low reproductive output, it is
likely that S. argentina is experiencing continued population declines
throughout its range, which is significantly contributing to its
extinction risk.
Growth Rate/Productivity
There is limited information regarding the growth and reproduction
of the Argentine angel shark, and information on natural mortality
rates or the potential intrinsic rate of population increase for the
species is unavailable. The species has an estimated maximum total
length of 138 cm with a size at sexual maturity of 120 cm TL, which
means the species must grow to approximately 87 percent of its maximum
size before reaching sexual maturity. Gravid females and neonates are
rarely found, so little is known about the gestation and birth of this
species; however, litter sizes range from 7-11 pups (with 9-10 pups
being common) and their reproductive cycle is reportedly at least
biennial (Vooren and Chiaramonte 2006). These reproductive
characteristics suggest the species has relatively low productivity,
similar to other elasmobranch species, which has likely hindered its
ability to quickly rebound from threats that decrease its abundance
(such as overutilization) and renders the species more vulnerable to
extinction. In addition, similar to its congener S. guggenheim, S.
argentina is thought to have cloacal gestation during the latter half
of pregnancy, which increases the likelihood that the species will
abort pups upon capture and significantly decreases their already low
reproductive output.
Spatial Structure/Connectivity
The Argentine angel shark has a very restricted range, from Santa
Catarina, Brazil to northern Argentina (i.e., Buenos Aires). Currently,
there is no evidence of abundant populations outside of southern
Brazil. Argentine angel sharks are sedentary, territorial, and assumed
to carry out their entire lifecycles within the same area. This
indicates that populations of the species maintain population growth by
recruiting within each area without producing a necessary excess of
recruits with the potential to migrate to other areas (Vooren and
Klippel 2005a). As a result, S. argentina populations reportedly have
limited movement and dispersal migration between neighboring
populations, with migrants having no impact on the short term abundance
of a population. This limited inter-population exchange reduces the
recovery potential for the depleted and small local populations and may
increase the risk of local extirpations, possibly leading to complete
extinction. Given the lack of evidence of abundant populations outside
of southern Brazil, and the limited connectivity between the
populations of southern Brazil and populations elsewhere throughout the
species' range, conservation of the southern Brazilian populations of
S. argentina is likely critical for the conservation of the taxon as a
whole. Thus, based on the available information, low dispersal rates
among populations of S. argentina poses a significant risk of
extinction to the species.
Diversity
The loss of diversity can increase a species' extinction risk
through decreasing a species' capability of responding to episodic or
changing environmental conditions. This can occur through a significant
change or loss of variation in life history characteristics (such as
reproductive fitness and fecundity), morphology, behavior, or other
genetic characteristics. Although it is unknown if S. argentina has
experienced a loss of diversity, the significant decline estimated for
the population in southern Brazil, as well as the likely small
populations elsewhere throughout its range, and limited connectivity of
these populations, suggest the species may be at an increased risk of
inbreeding depression or random genetic drift and could experience the
fixing of recessive detrimental genes, reducing the overall fitness of
the species.
Threats Assessment
The primary threat to S. argentina is overutilization by commercial
fisheries, with particular vulnerability to trawl and bottom gillnet
fisheries. As previously mentioned, the vast majority of fisheries
information on angel sharks is documented as ``Squatina spp''
throughout Brazil, Uruguay, and Argentina; therefore, determining the
magnitude of threats currently acting specifically on S. argentina is
challenging. However, there are some landings and CPUE data for S.
argentina, which suggest the historical and continued level of fishing
pressure has led to significant observed declines in the species.
Historically, angel sharks, including S. argentina, were caught in
multispecies artisanal shark fisheries and considered a valuable
bycatch species. In Argentina, in the 1990s, angel sharks were
considered commercially important bycatch, particularly in the Necochea
school shark (Galeorhinus galeus) gillnet fishery, and between 1992 and
1998, landings of angel sharks in Argentina were fairly stable.
However, declines in CPUE over this time period (of up to 58 percent)
were recorded for vessels operating on the Argentine shelf, indicating
a level of fishing mortality on the angel shark population that was
leading to declines in abundance, and since 1998, landings have been on
a decline (Massa et al. 2004b). In Uruguay, catches of angel sharks
(Squatina spp) have actually been on an increasing trend since the
1970s, and exceeded the catch limit imposed in the AUCFZ for 2012
(2,600 mt). However, in both Argentina and Uruguay, Argentine angel
sharks are relatively rare, with the majority of angel shark landings
comprised of S. guggenheim. As such, it is unclear whether
overutilization is significantly contributing to the species'
extinction risk in this portion of its range.
Off southern Brazil, angel sharks have been and continue to be
heavily exploited by the trawl and gillnet fisheries (see the S.
guggenheim assessment for more details). This heavy exploitation has
led to observed declines in the abundance of S. argentina on the
Plataforma Sul as a result of recruitment overfishing (primarily by the
bottom gillnet fishery targeting monkfish). Given the natural rarity
and low productivity of the species, these declines (of up to 80
percent) have placed the Argentine angel shark at an increased risk of
extinction from stochastic and depensatory processes. In addition, it
is likely that the population of Argentine angel shark has continued to
decline (from the 80 percent estimate in 2002) as a result of the
continued exploitation of the species by the monkfish gillnet fishery
that continued unabated until 2004, and the present fishing pressure by
the reduced monkfish fishery and the other oceanic gillnet fisheries
operating within the species' habitat. Further, few existing
regulations appear adequate to
[[Page 76105]]
control the overutilization of S. argentina. In the monkfish fishery,
which catches significant amounts of Argentine angel shark as byatch, a
management plan was implemented in 2005. Though the monkfish fishery
has been significantly reduced in terms of overall effort through catch
limits and fisheries restrictions, enforcement of management rules has
been poor with no evident signs of recovery for this overexploited
resource (Perez et al. 2009). Additionally, in 2004, the Argentine
angel shark was classified as ``critically endangered'' on Brazil's
endangered species list, which effectively prohibited the catch of this
species. However, for the most part, there is reportedly minimal
control of the fisheries operating on the Plataforma Sul, and this
regulation does not address the threat of bycatch-related mortality of
the species. Additionally, although landings of the species are
currently prohibited, the fleets' extensive operations will continue to
contribute to the fishing mortality of all life stages of the species
as the Argentine angel shark likely has high discard mortality rates
based on rates estimated for similar angel shark species (see spiny
angel shark--Threats Assessment). Thus, given general similarities
between the Argentine angel shark and other Squatina species, it seems
reasonable to infer similar discard survival rates for the Argentine
angel shark from these other Squatina species. As such, given the
sensitive life history traits of the Argentine angel shark as well as
the evidence of significant population declines, an assumed 60 percent
at-vessel mortality rate in trawl fisheries and 25-67 percent mortality
in gillnets is likely to significantly contribute to the
overutilization of the species and increase its extinction risk.
Overall, it is likely that S. argentina has suffered significant
population declines throughout its restricted range as a result of
historical and continued overutilization of the species from direct and
indirect fishing pressure. Given the reduction of the species'
critically important southern Brazilian population of at least 80
percent, combined with inadequate regulatory mechanisms in this part of
the species' range to control the high level of fishing pressure on the
species, we conclude that overutilization is significantly contributing
to the species' risk of extinction.
Risk of Extinction
Although there is significant uncertainty regarding the current
abundance of the species, it appears that the Argentine angel shark is
relatively rare outside of southern Brazil, where small, isolated
populations have experienced substantial declines and remain at risk
from overutilization by fisheries targeting deep-water monkfish. Best
available information indicates the species has experienced at least an
80 percent reduction of its critically important southern Brazil
population as a result of intense year-round fishing pressure, and will
continue to decline without adequate protection from overutilization.
Given the species' restricted range and present rarity throughout the
range, combined with its limited movement and dispersal between
populations and low reproductive output, S. argentina is likely
strongly influenced by stochastic or depensatory processes. This
vulnerability is further exacerbated by the present threats of
overutilization and inadequacy of existing regulatory measures that are
and will continue to significantly contribute to the decline of the
existing populations (based on its demographic risks), compromising the
species' long-term viability. Therefore, based on the best available
information and the above analysis, we conclude that S. argentina is
presently at a high risk of extinction throughout its range.
Protective Efforts
Aside from the management goals outlined in the previously
described FAO NPOA-sharks in Uruguay, we could not find any additional
information regarding protective efforts for the Argentine angel shark.
Proposed Determination
Based on the best available scientific and commercial information
as presented in the status review report and this finding, we find that
the Argentine angel shark is presently at risk of extinction throughout
all of its range. We assessed the ESA section 4(a)(1) factors and
conclude that the species faces ongoing threats from overutilization
and inadequacy of existing regulatory mechanisms throughout its range.
The species' present rarity and restricted range, combined with the its
natural biological vulnerability to overexploitation and demographic
risks (e.g., low and declining abundance, low productivity, likely
small and/or isolated populations at an increased risk of random
genetic drift, and limited dispersal capabilities) are exacerbating the
negative effects of the aforementioned threats, placing this species in
danger of extinction. We also found no evidence of protective efforts
for the conservation of Argentine angel shark that would reduce the
level of extinction risk faced by the species or otherwise alter its
current status. We therefore propose to list the Argentine angel shark
as an endangered species.
Graytail Skate (Bathyraja griseocauda)
Species Description
The graytail skate, Bathyraja griseocauda, is a member of the genus
Bathyraja, the most speciose genus of the family Arhynchobatidae
(McCormack et al. 2007). Physical features of the graytail skate
include a disc that is rhomboidal in shape (Bizikov et al. 2004),
brownish in color with traces of darker spots or rings on its dorsal
surface, and white or yellow coloring on the ventral side (Norman 1937;
Bigelow and Schroeder 1965). The posterior margins of the pelvic and
pectoral fins are dusky, and the tail is grayish brown in color (Norman
1937), with the underside covered in dark spots (Bizikov et al. 2004).
The dorsal surface is covered in numerous small spinules, but the tip
of the snout and axils of the pectoral fins lack spinules (Bigelow and
Schroeder 1965). There are 18-20 strong median spines on the tail that
begin above the origin of the pelvic fins and extend to the first
dorsal fin (Norman 1937; Springer 1971; Bizikov et al. 2004). Males
have alar thorns, curved spines on the outer part of their pectoral
fins, arranged in rows with 5-7 thorns per row (Bizikov et al. 2004).
Range and Habitat Use
The graytail skate occurs in Southwest Atlantic waters off the
coasts of Argentina, Uruguay, Chile, and the Falkland Islands, and in
the Southeast Pacific off of Chile (S[aacute]ez and Lamilla 2004). They
have been caught at latitudes as far north as 39[deg] S. in the Pacific
Ocean and 34[deg] S. in the Atlantic Ocean, and as far south as 60[deg]
S. in the Southern Ocean on the Antarctic shelf (Bigelow and Schroeder
1965; Figueroa et al. 1999; S[aacute]ez and Lamilla 2004). A few
individuals have been captured on the Antarctic continental shelf,
around the Antarctic Peninsula. There are also unconfirmed records of
graytail skate in the Southern Ocean in Prydz Bay, Antarctica (GBIF
2013). If these records are validated, this would extend the range of
the skate beyond the southwest Atlantic Ocean and eastern Pacific.
Diet and Feeding
Various studies on graytail skate diet indicate they are
opportunistic predators that consume a variety of prey items, but
primarily favor fish. The most extensive study of the diet and feeding
[[Page 76106]]
habits of the graytail skate caught around the Falkland Islands found
that skates smaller than 50 cm (DW) preyed mostly on benthic gammarid
amphipods and isopods, such as Serolis spp., whereas skates larger than
50 cm DW preyed increasingly on fishes (Brickle et al. 2003).
Subsequent studies off the Falkland Islands have confirmed this
ontogenetic diet shift (Laptikhovsky et al. 2005). In adult graytail
skate, fish can make up more than 40 percent of the diet
(S[aacute]nchez and Mabraga[ntilde]a 2002). Off the coast of Argentina,
the graytail skate did not consume crustaceans (S[aacute]nchez and
Mabraga[ntilde]a 2002), which contrasts with data from the Falkland
Islands.
Growth and Reproduction
Graytail skates have a lifespan of approximately 28 years, with a
maximum observed disc width of 130 cm and a maximum weight of 30.4 kg
(Arkhipkin et al. 2008; Wakeford et al. 2005). Based on vertebral band
counts from samples collected from along the coast of Argentina,
B[uuml]cker (2006) calculated the relative growth rate (k) from the von
Bertalanffy growth equation to be 0.064 year-1 with a
theoretical maximum size (L[infin]) of 169.9 cm TL and an
estimated size-at-birth (L0) of 6.1 cm. Arkhipkin et al. (2008), using
samples collected only off the Falkland Islands, reported a lower
growth rate (k) of 0.02 year-1, with a maximum theoretical
size (L[infin]) of 313.4 cm total length. Growth rates of
graytail skate begin around 5.6 cm/year for the first 9 years of life
and decline to 4.3 cm/year between 14 and 20 years old (Arkhipkin et
al. 2008). In comparison, a study of caudal thorn band counts and
vertebral centra ring counts found that the most accurate von
Bertalanffy growth parameters came from the vertebral centra with the
relative growth rate (k) based on vertebrae centra to be 0.033
year-1 with a theoretical maximum size (L[infin])
of 219.7 cm total length (Gallagher 2000). However, based on observed
size data, these parameters still slightly underestimate growth
(Gallagher 2000).
Little is known about the reproduction of the graytail skate
(S[aacute]nchez and Mabraga[ntilde]a 2002) and available age and growth
studies from the same region provide conflicting estimates for length
and age at maturity. For example, in the Falkland Islands, Gallagher
(2000) estimated a total length at 50 percent maturity of 120.7 cm for
both sexes, with males and females maturing after 17.6 and 24.8 years
respectively. Arkhipkin et al. (2008) estimated a total length at 50
percent maturity to be 108.2 cm for females and 94.5 cm for males, with
age at maturity of 14 years for males and 17.8 years for females. Based
on commercial fleet observer and research cruise data collected around
the Falkland Islands, males reached 50 percent maturity at a disc width
of 76-77 cm (Agnew et al. 2000; Wakeford et al. 2005). A Falkland
Islands study of graytail skate suggests that graytail skate females
may spawn year-round with a weak spawning peak in the spring and summer
months observed (Arkhipkin et al. 2008). Around the Falkland Islands,
the spawning grounds of the graytail skate can be found northwest of
the islands in deep waters, close to the edge of the continental shelf
between 200 and 300 m deep (Arkhipkin et al. 2008) and in waters south
of 51[deg] latitude (Dr. Andreas Winter, Falkland Islands Fisheries
Stock Assessment Scientist, personal communication 2015). Based on
catches of the smallest skates, it is thought that hatchlings have disc
widths between 9 cm and 12 cm (Brickle et al. 2003; Arkhipkin et al.
2008).
Genetics and Population Structure
Studies examining the genetics of the species or information on its
population structure could not be found.
Demography
Little is known about the population growth and natural mortality
of the graytail skate. However, based on the life history parameters
described previously, like other elasmobranchs, the graytail skate is a
K-selected species with slow growth rates and late age at maturity,
which is indicative of low productivity (Gallagher 2000; B[uuml]cker
2006; Arkhipkin et al. 2008).
Historical and Current Distribution and Population Abundance
Graytail skate occur on the continental shelf and slope in the
southwestern Atlantic Ocean, south of 34[deg] S. and in the
southeastern Pacific Ocean, south of 39[deg] S. (Figueroa et al. 1999;
S[aacute]ez and Lamilla 2004). In the Falkland Islands, graytail skate
are caught in cool, deep waters on the slopes of the continental shelf
break, making them more common to the west of the islands (Agnew et al.
1999; Arkhipkin et al. 2008; Arkhipkin et al. 2012). Outside the
Falkland Islands, on the Patagonian shelf, they are more commonly found
on the northwestern outer shelf and northern shelf and slope (Figueroa
et al. 1999; Arkhipkin et al. 2012). In Argentina, graytail skate are
found on the continental shelf and slope around Argentina south of
37[deg] S. and 41[deg] S. respectively (McCormack et al. 2007), where
they exhibit strict stenothermic and stenohaline behavior. In other
words, the species appears to tolerate very narrow ranges of
temperature and salinity (Figueroa et al. 1999), with catch data that
suggest that the species occurs at water temperatures below 6 [deg]C
(Menni and Lopez 1984; Colonello and Massa 2004) and salinity above
33.9 psu (Colonello and Massa 2004).
Throughout their range, graytail skates are found at depths between
106 m and 1,010 m, but have been caught as shallow as 77 m in Argentine
waters (B[uuml]cker 2006). Graytail skate are typically most common at
depths below 300 m (Bigelow and Schroeder 1965; Menni and Lopez 1984;
Brickle et al. 2003; Laptikhovsky et al. 2005; Wakeford et al. 2005;
Arkhipkin et al. 2008; Arkhipkin et al. 2012). However, in Argentina,
the highest density of graytail skate catches was reported at depths of
120 m on the Argentina platform between 45[deg] S. and 41[deg] S.
during the late winter and early spring months (Colonello and Massa,
2004). As graytail skates mature, they display an ontogenetic shift in
depth preference (Arkhipkin et al. 2008). For example, in Falkland
Islands waters, hatchlings occupy nursery grounds of approximately 300
m-350 m depth, but transition to deeper waters of 400 m-600 m as
juveniles (Arkhipkin et al. 2008). At 20 cm-30 cm DW, some individuals
migrate up to shallower depths of 200 m-400 m, while others move into
water deeper than 600 m (Arkhipkin et al. 2008). Skates 80 cm-90 cm DW
or larger occur most commonly at depths of 400 m-600 m (Arkhipkin et
al. 2008). Despite these depth changes, studies around the Falkland
Islands have shown little evidence of large spatial or temporal
movements, which could indicate that graytail skates carry out their
entire life cycle within the waters where they hatch (Agnew et al.
2000; Wakeford et al. 2005; Winter et al. unpublished).
Range-wide abundance estimates for graytail skate are not
available; however, biomass estimates exist for the populations off the
Falkland Islands and Argentina. In the Falkland Islands, graytail skate
were part of the fish assemblage of both the southern and northern
skate and ray stocks. They were particularly abundant south of the
islands, making them dominant in catches of the southern skate and ray
assemblage. However, due to declining CPUEs of the southern stock,
especially for graytail skate, the southern rajid fishery was closed in
1996 (Agnew et al. 1999; Agnew et al. 2000; Wakeford et al. 2005).
Current biomass estimates from this area could not be found. North of
[[Page 76107]]
the Falkland Islands, declines in the CPUE of graytail skate were also
observed between 1992 and 2001 (Wakeford et al. 2005); however, based
on recent biomass estimates, the population appears to have recovered
and stabilized. Specifically, analysis of 2010 fishery survey cruise
data resulted in an estimated biomass of graytail skate of 7,232 t,
which is consistent with the earlier biomass estimates for the species
from the 1990s (Falkland Islands Government 2011). As this biomass
estimate is just for the graytail skate population north of the
Falkland Islands, it is likely a significant underestimation of the
total biomass for the entire Falkland Islands population, especially
considering the southern stock, which was historically more abundant,
has been protected from targeted fishing since 1996.
In 2002, S[aacute]nchez and Mabraga[ntilde]a (2002) estimated the
population abundance of the graytail skate on the continental Argentine
shelf between 48[deg] S. and 55[deg] S. to be 259,210 individuals, or
2,431.98 t. This estimate was calculated prior to the apparent recovery
of the graytail skate in the Falkland Islands and also corresponds to
when CPUE of the graytail skate was at its minimum in the Falkland
Islands (Wakeford et al. 2005). As such, it could be assumed that
biomass has since increased on the shelf; however, with no recent
abundance estimates available, the trends within this portion of the
species' range cannot be determined with certainty.
Farther north on the Argentine shelf, between 45[deg] S. and
41[deg] S., the biomass of graytail skate was estimated to be 503 t in
2004, but had a large confidence interval (2,237
t), with an average density of the species of 0.05 t/nm\2\ (Colonello
and Massa 2004). More recent estimates or trends in population
abundance or biomass levels for graytail skate are not available.
There is very little information pertaining to the presence of
graytail skate in Uruguayan and Chilean waters. No information on
commercial, recreational, or research catches of graytail skate is
available from Uruguay. Likewise, there is no estimate of abundance
from this area. In Chile, graytail skate are found south of 41[deg] S.
and at depths of 137 m to 595 m (McCormack et al. 2007). In 1995, Saez
and Lamilla (2004) caught 42 graytail skate between March and December
at 350 m depth approximately 20 miles from Punta Galera; however, no
other information is available on scientific or commercial catch
distribution or population abundance from this area.
Summary of Factors Affecting the Graytail Skate
We reviewed the best available information regarding historical,
current, and potential threats to the graytail skate species. We find
that the main threat to this species is overutilization for commercial
purposes; however, we consider the severity of this threat to be
greatly reduced by the regulatory mechanisms in place in the Falkland
Islands, where the species was historically most heavily exploited.
Thus, we find that historical and present levels of utilization are not
exceeding the species' biological capacity to sustain current levels of
exploitation. We also find that current regulatory measures are
adequate to protect the species from further overutilization.
Additionally, available information does not indicate that habitat
destruction or modification, disease, predation or other natural or
manmade factors are operative threats on these species. We summarize
information regarding these factors and their interactions below
according to section 4(a)(1) of the ESA. See Casselbury and Carlson
(2015g) for a more detailed discussion of these factors.
Present or Threatened Destruction, Modification, or Curtailment of
Habitat or Range
Trawl fisheries occur throughout the graytail skate's range.
Studies show that the interaction of bottom trawling gears with bottom
substrate can have negative effects on benthic fish habitat
(Valdemarsen et al. 2007). These impacts are often the most serious on
hard substrates with organisms that grow up from the bottom, such as
corals and sponges, but alterations to soft substrates have also been
seen. The trawl doors on bottom otter trawls often cause the most
damage to the ocean bottom, but other parts of trawling gear, such as
weights, sweeps, and bridles that contact the bottom can also be
damaging. Intense fishing disturbance from trawling has reduced the
abundance of several benthic species (Valdemarsen et al. 2007);
however, there is no specific information available that indicates this
habitat modification has had a direct effect on the abundance of the
graytail skate, or is specifically responsible for the curtailment of
its habitat or range.
Overutilization for Commercial, Recreational, Scientific, or
Educational Purposes
Information available on the harvest of the graytail skate
indicates that they are most heavily exploited in the Falkland Islands
multispecies skate and ray fishery by foreign fleets (Agnew et al.
1999; Falkland Islands Government 2005-2013). Prior to the 1990s,
catches from the Falkland Islands were mainly attributed to Spanish
vessels fishing in a mixed groundfish fishery, with rajid catches of
less than 1,500 t per year (Wakeford et al. 2005). However, in 1989,
Korean vessels began to specifically target rajids in this fishery
using demersal trawls, and by 1991 catches of skates and rays rose to
more than 7,000 t/year (Wakeford et al. 2005). Subsequently, two rather
distinct rajid fisheries developed within the Falkland Islands: a
southern rajid fishery that fished in a small area south of the
Falkland Islands (a ray ``hot spot;'' Agnew et al. 2000), and a
northern rajid fishery that operated in a more extensive area to the
north of the Falkland Islands (primarily on the slope between 200 m-400
m depths; Wakeford et al. 2005). In the 1990s, the graytail skate was
the most important species caught in the Falkland Islands multispecies
rajid fisheries based on catch weight, and was estimated to make up
approximately 58 percent of the catch in the southern rajid fishery and
39 percent of the catch in the northern rajid fishery between 1993 and
1995 (Agnew et al. 1999; Bizikov et al. 2004). However, with this heavy
exploitation on the skate populations by Korean fleets (which were
responsible for 88 percent of the directed rajid catch between 1990 and
1997; Agnew et al. 2000), the proportional catches of graytail skate
declined in all areas that were fished. This decline was particularly
precipitous in the southern batoid aggregation area, where graytail
skate spawn (A. Winter, pers. comm. 2015) and had previously comprised
the majority of the catch (Agnew et al. 1999). Agnew et al. (2000)
calculated that total mortality rates (fishing mortality rates +
natural mortality rates) in the northern and southern areas were
significantly higher than what could be sustained by the batoid
assemblage, particularly graytail skates. Specifically, the authors
estimated that graytail skates could sustain total mortality rates of
less than 0.3/year; however, the total mortality rate in the northern
area from 1991-1995 was on the order of 0.42/year and in the southern
area was 0.61/year (Agnew et al. 2000). Consequently, significant
declines in CPUE were observed between 1990 and 1997. A steep 58
percent decline was noted in the southern rajid fishery from 1993 to
1996, which was attributed to the decline in graytail skate abundance
[[Page 76108]]
(Agnew et al. 1999, 2000) and declines ranging from 44 to 65 percent
were observed for the northern rajid fishery from 1990-1996 (Agnew et
al. 2000). For catches of graytail skate, Wakeford et al. (2005)
estimated a decline in CPUE of around 70 percent between 1992 and 2001
in the northern rajid fishery, and observer data indicate CPUE of
graytail skate continued to decline through 2007 (Winter et al.
unpublished). Catches of graytail skate also showed a reduction in
average disc width. From 1993-1995, average disc width declined from
52.18 cm to 31.91 cm (Agnew et al. 2000), and based on observer data
collected from the Falkland Islands Inner Conservation and Management
Zone (located between 49[deg] S.-54[deg] S. and 64[deg] W.-54[deg] W.),
the majority of graytail skate catches in the commercial trawl fishery
from 1997-2006 were still relatively small skates with modal disc
widths between 25 cm and 40 cm (Arkhipkin et al. 2008). Additionally,
about 54 percent of the catches were female skates with disc widths
between 10 cm and 80 cm, and the majority were under the estimated size
at 50 percent maturity (Arkhipkin et al. 2008).
As a result of the marked declines in CPUE, particularly for the
entire southern batoid aggregation, which was presumed to be driven by
declines in graytail skate (Agnew et al. 1999, 2000; Wakeford et al.
2005), the southern ray fishery was closed in 1996 and separate skate
target trawling licenses and catch limits (of around 3,000 t through
the late 1990s) were imposed in the northern ray fishery. Following the
implementation of these catch limits, which equated to between 6.5 and
7.6 percent of the estimated pre-exploitation biomass, the northern
rajid stock appeared to stabilize by 2000 (Agnew et al. 2000). In fact,
based on a stock assessment of the northern skate stock, with updated
data through 2014, estimated biomass of the entire stock has gradually
and consistently increased since 1996, from a low of 13,641 t in 1989
(95 percent CI: 10,591-24,214), which marked the start of heavy
exploitation, to a recent peak high of 34,558 t in 2014 (90 percent CI:
27,284-59,806) (Fisheries Committee 2015). In addition, CPUE of the
northern stock has been gradually increasing over the years (Agnew et
al. 2000; Falkland Islands Fisheries Committee 2015) whereas targeting
of skate and ray species in the Falkland Islands has been decreasing,
with a large portion (almost half) of the skate catch now taken as
bycatch under finfish licenses (Falkland Islands Government 2014). In
fact, the most recent data from the fishery show that in 2014 total
skate catch amounted to 5,543.2 t, with 53 percent of this total
representing targeted skate catch (Fisheries Committee 2015).
Furthermore, even with the proportional increase in bycaught skates and
decrease in targeted skate catch, the total skate catch for the fishery
appears sustainable as it falls below the Maximum Sustainable Yield
(MSY) estimate, which is the theoretical largest catch that can be
taken from a stock. Based on the latest stock assessment of the
northern skate assemblage, MSY is estimated to be 6,048 t (95 percent
CI: 6,198-46,811), which is approximately 8 percent higher than the
2014 total skate catch (Fisheries Committee 2015).
In terms of the graytail skate, despite the reported historical
reductions in CPUE, B. griseocauda remains one of the most abundant
species caught in the Falkland Islands multispecies skate fishery
(Agnew et al. 1999; Arkhipkin et al. 2008; Falkland Islands Government
2005, 2006, 2007, 2008, 2010, 2011, 2012) and presently makes up
between 11 percent and 18 percent of the skate trawl catch and bycatch
identified by observers (Agnew et al. 2000; Falkland Islands Government
2010, 2011, 2012, 2014). Recent data from the Falkland Islands
Government (2012) also indicate that the modal disc width of graytail
skate catches has increased to 63 cm in 2012. The increase in modal
disc width could be indicative of population recovery for graytail
skates in recent years. This is supported by the fact that in 2010,
fishery-independent surveys conducted to estimate skate biomass in the
northern area of the Falkland Islands (the area that generally yields
the highest skate catches by the targeted skate fishery) confirm that
total skate biomass, and particularly the predominant skate species,
including graytail skate, have remained stable in recent years. Using
CPUE as an index of abundance, an analysis incorporating more recent
data from 1994 to 2013 revealed that B. griseocauda was in decline
until about 2007, with a decrease in CPUE from 120.1 kg/hr in 1994 to
22.6 kg/hr in 2007 (Winter et al. unpublished). However, CPUE has since
increased to an estimated 70.1 kg/hr in 2013, similar to levels
observed in 1997-2001, with abundance continuing on a positive trend
(Winter et al. unpublished). Furthermore, given that these estimates
are only for graytail skate in the northern area of the Falkland
Islands, it is likely that the total abundance of the Falkland Islands
population is significantly higher and has recovered even more so due
to the complete ban on commercial skate fishing in the southern batoid
aggregation area, where the spawning grounds of the species are mostly
located (A. Winter, pers. comm. 2015).
Given the evidence of increasing CPUE and biomass of the northern
skate assemblage, skate catch estimates that are below MSY, stable
biomass estimates of graytail skate, and increasing abundance and sizes
of graytail skates in catches, the current fishing effort and level of
exploitation of skates in general, and graytail skate in particular, in
the Falkland Islands appears to be sustainable (Falkland Islands
Government 2014). In other words, overutilization of the species in
this portion of its range is not a threat that is contributing
significantly to its risk of extinction.
In Argentina, an active commercial elasmobranch fishery, which
exploits sharks, skates, and rays, has shown an increasing trend in
both catches and number of vessels reporting skate and ray landings
since the early 1990s. Historically, skates and rays were mainly
discarded as fisheries bycatch, but are now landed as both target and
non-target catch (Chiaramonte 1998; Massa and Hozbor 2003).
Specifically, catches have increased from 183 t in 1991 to 13,265 t in
2000, and vessels reporting landings have increased from 69 in 1992 to
377 in 1998 (S[aacute]nchez and Mabraga[ntilde]a 2002; Massa and Hozbor
2003). From 1994-1998, Massa and Hozbor (2003) estimated a decline of
around 36 percent in the CPUE of large fishing vessels (>28 m in
length) for all skates and rays on the Argentine shelf between 34 and
48[deg] S.; however, the data are not species-specific and deep-water
skates, like the graytail skate, are generally not monitored despite
the fact that they are under fishing pressure (Massa et al. 2004b).
Additionally, the CPUE of skates and rays for smaller fishing vessels
(with lengths <28 m) did not show similar declines; rather, CPUE for
these vessels on the Argentine shelf remained fairly stable from 1994-
1998 (Massa and Hozbor 2003).
Along the Patagonian shelf, the graytail skate has also been
observed as bycatch in the scallop (Zygochlamys patagonica) fishery.
This Patagonian scallop fishery primarily operates along the 100 m
isobath, between 36[deg]43' S and 48[deg]30' S, and uses non-selective
bottom otter trawls (Schejter et al. 2012). In a research study
examining the bycatch composition from this fishery, the graytail skate
occurred in 6.8 percent of the sampled fishing sites (n=177) (Schejter
et al. 2012); however, no information on abundance of the species
within those sites was provided. Overall, the limited abundance data as
[[Page 76109]]
well as the lack of species-specific information and trends data makes
it difficult to determine the magnitude of utilization that may be
occurring specifically for B. griseocauda in this part of its
Argentinian range, and whether this level of utilization is
contributing significantly to the species' extinction risk.
Similarly, little information is available on the exploitation of
the graytail skate in Chilean waters. There is a directed skate fishery
off Chile that primarily targets the yellownose skate (Zearaja
chilensis), and although information on the depth at which the fishery
operates could not be found, Z. chilensis lives at depths between 28 m
and 435 m. This depth range overlaps with the shallower half of the
graytail skate's depth range (Kyne et al. 2007) and thus this fishery
may also incidentally catch graytail skates. Since 1979, declines in Z.
chilensis catches have been reported, and it is suspected that other
skate species, including the graytail skate, have also been affected
(McCormack et al. 2007); however, graytail skate comprise less than 5
percent of the skate landings in this fishery (McCormack et al. 2007).
As such, the impact of this fishery on graytail skate abundance and
overall extinction risk is likely to be minimal.
Disease or Predation
At this time, there is no available information regarding diseases
or predators of the species. As such, there is no evidence to indicate
that these factors are a threat to the graytail skate.
Inadequacy of Existing Regulatory Mechanisms
In the Falkland Islands, there are numerous management measures in
place that provide for the protection of graytail skate from
overutilization. The Falkland Islands multispecies fishery, where
graytail skate is presumably most heavily exploited, is rigorously
managed through fishing effort controls. In order to protect the
southern batoid aggregation area that displayed marked declines in CPUE
in the early 1990s (Agnew et al. 1999), the Falkland Islands government
implemented a number of management measures to ensure long-term
sustainability of the rajid fishery, including: (1) The placement of
observers on vessels to identify batoids to species and collect other
biological data to inform fisheries management; (2) the development of
specific skate and ray fishery seasons and licenses to better regulate
the catch of rajids; and (3) the implementation and continuation of a
prohibition on trawling for skates and rays south of 51[deg] S, which
effectively closed the southern ray fishery. Before the prohibition,
graytail skate were particularly abundant south of the islands, where
its spawning grounds are mostly located (A. Winter, pers. comm. 2015),
and made up a significant portion of the catch from this area. Thus,
this measure helps protect not only a large segment of the population
from further depletion in an area where they were historically most
concentrated, but also important life history behavior required for the
survival of the species (Agnew et al. 2000). In addition to the closure
of the southern ray fishery via the trawl prohibition, catch limits
were also imposed for the northern rajid fishery in 1996. Since then,
the northern batoid stock has seen a gradual increase in both CPUE and
biomass, with total catches lower than MSY, suggesting regulatory
measures are adequate in providing for the sustainable exploitation of
the northern skate assemblage in Falkland waters. Data also suggest
that these regulatory measures have allowed for the recovery of the
graytail skate population, as indicated by the increasing CPUE and
sizes of graytail skate in recent catches. As such, the Fisheries
Committee, which advises the Falkland Islands Fisheries Department,
recommended maintaining the skate target catch at the current level of
effort allocation for the 2016 fishing year as these limits are
effective at maintaining a sustainable multispecies fishery and appear
adequate to protect the graytail skate from extinction.
In Argentina, the graytail skate is covered under the country's FAO
NPOA-sharks; however, it is not considered a priority species. Several
sources have noted that Argentina does little to actively protect
elasmobranchs, particularly skates and rays, in its waters (Massa and
Hozbor 2003; Massa et al. 2004b, McCormack et al. 2007). Though total
allowable catch, minimum sizes, and annual quotas are in place for many
elasmobranchs in Argentina, they are largely ignored and poorly
enforced (McCormack et al. 2007). In 2013, El Instituto Nacional de
Investigaci[oacute]n y Desarrollo Pesquero (INIDEP) set the recommended
total allowable catch for all skates and rays at 9,000 t and a landing
limit for skates and rays was set at no more than 30 percent of the
catch. However, due to the lack of information regarding the status of
the graytail skate in Argentina, there is no indication that existing
regulatory mechanisms are inadequate in controlling threats to the
species or are contributing significantly to the species' risk of
extinction.
In Uruguay, the graytail skate is considered a species of high
priority under Uruguay's FAO NPOA-sharks, which outlines plans to:
investigate the species' age, growth, reproduction, diet, distribution,
and habitat use in Uruguayan waters; generate a time series for catch
and effort of the skate in fisheries; conduct an abundance assessment;
establish measures to review current fishing licenses for graytail
skate and determine possible modifications to the licenses; and
finally, prohibit new fishing permits. However, aside from the species'
presence in Uruguayan waters, there is a significant lack of
information regarding the status of graytail skate in Uruguay; thus,
there is no indication that existing regulatory mechanisms are
inadequate in controlling threats to the species in this portion of its
range, or are contributing significantly to its risk of extinction.
In Chile, there are little to no regulations for the protection of
graytail skate; however, the exploitation of the species in Chilean
waters is minimal. While there are regulations pertaining to other
fisheries in Chilean waters that overlap the graytail skate's range, it
is unknown how these regulations affect the status of graytail skate.
Based on the available information, there is no indication that
existing regulatory mechanisms are inadequate in controlling threats to
the species in this portion of its range, or are contributing
significantly to its risk of extinction.
Other Natural or Manmade Factors Affecting the Species
Besides the information already discussed above in the other factor
sections, no additional information was found regarding threats to the
species that would fall under this category. As such, there is no
evidence to indicate that this factor is a threat to the graytail
skate.
Extinction Risk
Demographic Risk Analysis
Abundance
Although range-wide abundance estimates for graytail skate are
unavailable; biomass estimates and trends exist for the areas where the
species was historically and is currently most abundant. In the
Falkland Islands, graytail skate represented a dominant part of the
southern rajid assemblage in the mid-1990s and comprised around 39
percent of the northern rajid catch. Due to heavy fishing pressure
contributing to unsustainable mortality rates, significant declines in
the CPUE of the species were observed between 1992 and 2007 indicating
a likely reduction in population abundance. However,
[[Page 76110]]
since the decline, CPUE (as an index of abundance of graytail skate)
from north of the Falkland Islands has been increasing, already
reaching levels observed in 1997-2001, with biomass of the species in
2010 estimated to be 7,232 t, consistent with biomass estimates from
the early 1990s. Additionally, the graytail skate remains one of the
most abundant species caught in the Falkland Islands multispecies skate
fishery. Therefore, while the species likely experienced historical
declines in abundance as a result of heavy exploitation in the early
1990s, the available information on biomass estimates and trends
between the 1990s and 2014 indicate that the population is potentially
stabilized and even recovering. Therefore, the species' present level
of abundance is unlikely to pose a demographic risk to the species.
Furthermore, there is no other abundance information or trend data from
the rest of the species' range to indicate that the species' present
abundance level is contributing significantly to its risk of
extinction.
Growth Rate/Productivity
Relative growth rates (k) of graytail skates were estimated to be
0.064 year-1 in Argentinean waters (i.e., low), and 0.02
year-1 to 0.033 year-1 in the Falkland Islands
(i.e., very low). Graytail skates are long-lived species, with an
estimated lifespan of approximately 28 years, and a maximum disc width
of 130 cm. Although age and growth studies from skates in the same
region provide conflicting estimates for length and age at maturity,
with age of maturity estimates ranging from 14-17.6 years for males and
17.8-24.8 years for females, all estimates indicate a very late age of
maturity. While there is some evidence to suggest that graytail skates
may reproduce year-round, overall, these reproductive characteristics
suggest the species has relatively low productivity, similar to other
elasmobranch species, which may hinder its ability to quickly rebound
from threats that decrease its abundance (such as overutilization) and
render the species more vulnerable to extinction in the face of other
demographic risks and threats. Additionally, the observed decrease in
the species' mean disc width in catches from 1993-1995 and 1997-2006
(to sizes that ranged between 25 cm and 40 cm) likely portended a
declining growth rate for the species. This is because changes in
metrics, such as average size, can significantly impact other important
life history functions, like fecundity or even natural mortality rates
(Audzijonyte et al. 2015), that affect the instantaneous per capita
growth rate of a species. However, since 2006, data from the Falkland
Islands Government show an increase in size of the modal disc width of
graytail skate catches, with the most recent size estimate of 63 cm in
2012, likely indicating that the population is recovering and that
growth rate is no longer declining.
Spatial Structure/Connectivity
Based on trends in commercial fisheries data from the Falkland
Islands and Argentina, Wakeford et al. (2005) concluded that graytail
skates have limited spatial and temporal movements and, therefore, may
likely exist as localized populations. Limited inter-population
exchange reduces the recovery potential for depleted and small local
populations and may increase the risk of local extirpations, possibly
leading to complete extinction. However, no other information is
available regarding spatial structure or connectivity of graytail skate
populations throughout its range, and there is no evidence to suggest
this demographic risk is presently significantly contributing to the
graytail skate's risk of extinction.
Diversity
The loss of diversity can increase a species' extinction risk
through decreasing a species' capability of responding to episodic or
changing environmental conditions. This can occur through a significant
change or loss of variation in life history characteristics (such as
reproductive fitness and fecundity), morphology, behavior, or other
genetic characteristics. Currently, there is no information regarding
the graytail skates' diversity throughout its range, thus we can not
conclude whether its present level of diversity is contributing to its
extinction risk.
Threats Assessment
The best available information indicates that graytail skates are
most heavily exploited in the Falkland Islands multispecies skate and
ray fishery by foreign fleets and likely suffered significant declines
in abundance due to overexploitation in the early 1990s. However, since
1996, the area of operation of the Falkland Islands rajid fishery has
been significantly restricted (to an area north of the Islands) with
imposed catch limits to manage the northern batoid stock assemblage
(which includes graytail skates) within this area. As a result of these
management measures, there has been a gradual increase in CPUE and
biomass of the northern batoid stock assemblage. As for graytail skates
specifically, they remain one of the most abundant species caught in
the Falkland Islands multispecies skate fishery. Recent data from the
Falkland Islands Government shows an increasing trend in the CPUE of
the species as well as in the the modal disc width of graytail skate
catches, with the latest estimate of 63 cm DW in 2012. While 63 cm is
still below the size of sexual maturity (i.e., 75 cm) it is a marked
improvement from the modal disc widths between 1993 and 2006 (after
heavy exploitation), which ranged between 25 cm and 40 cm, and
indicates potential recovery of the population. Additionally, since the
early 2000s, there has been a general decreasing trend in the targeting
of skate and ray species in the Falkland Islands, with most species now
taken as bycatch in the finfish fishery. Furthermore, total skate catch
in recent years has remained below MSY, indicating that current catch
and effort of the skate and ray fishery are likely sustainable. Based
on the above information, it is clear that existing regulatory
measures, including current catch limits and trawling closures, are
adequate to protect the graytail skate in the Falkland Islands from
extinction.
In Argentina, there is an active commercial elasmobranch fishery,
which exploits sharks, skates, and rays, and it has shown an increasing
trend in both catches and number of vessels reporting skate and ray
landings (Massa and Hozbor 2003). However, based on the lack of
species-specific information from the region, it is highly uncertain if
present levels of utilization of skates and rays are a threat that is
contributing significantly to the extinction risk of the graytail
skate.
In Chile, a directed skate fishery that primarily targets Zearaja
chilensis in areas where graytail skate may also occur has reported
declines in catch since 1979. It is suspected that other skate species,
including the graytail skate, have also been affected. However, there
are no available data that indicate a decline in graytail skate
abundance or catch, and given that the species comprises less than 5
percent of the total skate landings in this fishery, it is unlikely
that this fishery is significantly contributing to the extinction risk
of the graytail skate.
Overall, while the species likely experienced historical declines
in abundance during the 1990s due to exploitation by the Falkland
Islands multispecies rajid fisheries, the available biomass estimates
and trends over the past decade, including gradual increases in the
CPUE and biomass of
[[Page 76111]]
the northern batoid stock and specifically the graytail skate in recent
years, as well as an increasing trend in graytail modal disc width
size, indicate the population is potentially stable and possibly moving
towards recovery. This is likely a result of rigorous regulations
implemented by the Falkland Islands government to sustainably manage
the rajid fishery by reducing fishing effort, accomplished by setting
catch limits in the northern rajid fishery and closing the southern
rajid fishery area, where graytail skates likely spawn and were
historically most heavily exploited. It should be noted that while this
closure helps to protect the Falkland Islands population, due to
uncertainty surrounding the connectivity of graytail skate populations,
these regulations may not provide protection to skate populations found
outside of Falkland waters. However, based on the available
information, it appears that the Falkland Islands is where the species
is most concentrated, and, hence, the protection of this population
from extinction is likely critical for the survival of the species.
Outside of the Falkland Islands, the minimal available information on
the species does not indicate that present levels of utilization or any
other factors are contributing significantly to the extinction risk of
the species.
Risk of Extinction
While the species' demographic characteristics increase its
inherent vulnerability to depletion, and likely contributed to past
population declines of varying magnitudes, the best available
information suggests these risks have decreased due to the adequate
control of exploitation of the species. In the Falkland Islands, where
the species was most heavily exploited and is likely presently most
concentrated, abundance estimates and trends from the 1990s to 2013,
and increases in the species' mean disc width, suggest potential
stabilization and even recovery of the population. The continued
rigorous management and monitoring of the fishery appears adequate in
protecting the species from levels of overutilization that would
increase its extinction risk. Despite fishing pressure in other parts
of the species' range (e.g., Chile and Argentina) and evidence of it
being taken as bycatch in various fisheries, graytail skates are not
monitored and we have no other information (e.g., catch rates,
abundance trends, or any other species-specific data) to indicate that
present levels of utilization or any other factors are significantly
contributing to the species' risk of extinction. Thus, considering the
above information and analysis, we conclude that B. griseocauda is at a
low risk of extinction throughout its range, and as such, does not
warrant listing as a threatened or endangered species throughout its
range.
Significant Portion of Its Range Analysis
Because our range-wide analysis for the species leads us to
conclude that the species is not threatened or endangered throughout
its range, under the final Significant Portion of Its Range (SPR)
policy announced in July 2014, we must go on to consider whether the
species may have a higher risk of extinction in a significant portion
of its range (79 FR 37577; July 1, 2014).
The final policy explains that it is necessary to fully evaluate a
portion for potential listing under the ``significant portion of its
range'' authority only if 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 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 (Id. 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.''). 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.
After a review of the best available information, we identified the
Falkland Islands as likely constituting a ``significant'' portion of
the graytail skate range. Under the policy, a portion of a species'
range is significant if, without that portion, the species would have
an increased vulnerability to threats to the point that the overall
species would be in danger of extinction or likely to become so in the
foreseeable future. As mentioned previously, the historical and current
fisheries data indicate that graytail skate are likely most
concentrated in Falkland waters. Graytail skate have also been
identified and caught elsewhere throughout its range, such as north of
the Falkland Islands on the Argentinian shelf between 45[deg] S. and
41[deg] S., and on the Pacific coast off Chile (south of 41[deg] S.);
however, based on trends in commercial fisheries data from the Falkland
Islands and Argentina, Wakeford et al. (2005) concluded that graytail
skates have limited spatial and temporal movements and, therefore, may
likely exist as localized or isolated populations. If we assume the
Falkland Islands population is isolated from the populations of
graytail skate elsewhere throughout its range, then, technically, loss
of this population would not directly affect the abundance of the other
remaining populations. However, loss of this population could
significantly increase the extinction risk of the species as a whole,
as only small, fragmented, and isolated populations of the species
(based on the best available abundance information--see the Historical
and Current Distribution and Population Abundance and Demographic Risk
Analysis sections above) would remain, making them more vulnerable to
catastrophic events and environmental or anthropogenic perturbations.
Limited inter-population exchange also reduces the recovery potential
for these small local populations and increases the risk of local
extirpations and overall complete extinction.
Under the policy, if we believe the Falkland Islands population may
constitute a ``significant'' portion of the range, then we must either
evaluate the extinction risk of this population first to determine
whether it is threatened or endangered in that portion or determine
[[Page 76112]]
if this portion is, in fact, ``significant.'' Ultimately, of course,
both tests have to be met to qualify the species for listing. Given the
extremely limited amount of information on the species outside of its
Falkland Islands range, it is difficult to conduct a more definitive
analysis to determine whether or not this portion does, in fact,
constitute a ``significant'' portion of the range of the graytail
skate. Additionally, there is no information to suggest that any other
portion may be significant. However, even if we were to assume that the
Falklands Islands population does constitute a ``significant'' portion
of the graytail skate range, based on the information and analysis in
the previous extinction risk section, there are no identified threats
concentrated in this portion that are significantly contributing to the
species' risk of extinction. In fact, the most recent available
information indicate that existing regulatory measures are adequate in
protecting the graytail skate in the Falkland Islands from extinction,
with graytail skate abundance on a positive trend and exhibiting signs
of population recovery based on both CPUE and size data. Thus, under
the policy, the preliminary determination that a portion of the
species' range may be both significant and endangered or threatened has
not been met. Therefore, listing is not warranted under the SPR policy.
Proposed Determination
Based on the best available scientific and commercial information
as presented in the status review report and this finding, we find that
the graytail skate is not presently in danger of extinction throughout
all or a significant portion of its range, nor is it likely to become
so in the foreseeable future. We summarize the factors supporting this
conclusion as follows: (1) Although there is no formal estimate of the
current population size and historical declines in biomass have been
observed, current biomass estimates from the Falkland Islands, where
the species is likely most concentrated, suggest the population is
stable and CPUE trends indicate abundance is increasing; (2) a
reduction in mean disc width of the Falkland Islands population
occurred in the late 1990s and early 2000s as a result of intensive
fishing pressure; however, recent evidence suggests an increase in
modal disc width, which is likely indicative of population recovery;
(3) while an identified threat to the species was historical
overutilization in the Falkland Islands commercial fisheries,
subsequent fishery closures in the southern rajid fishery and catch
limits in the northern rajid fishery of the Falkland Islands have
contributed to a significant reduction of fishing pressure on the
species, leading to increases in the abundance of the population and
providing for sustainable fishing of the northern Falkland Islands
rajid assemblage; (4) targeting of skates and rays in the Falkland
Islands, where the species was most heavily exploited, has been on a
decreasing trend since the early 2000s; (5) there is no evidence that
destruction of habitat, disease or predation are factors contributing
to an increased risk of extinction for the species; and (6) the
continual implementation of rigorous monitoring and fishery management
measures in the Falkland Islands appears effective in addressing the
most important threat to the species (overharvest) now and into the
foreseeable future. Based on these findings, we conclude that the
graytail skate is not presently in danger of extinction throughout all
or a significant portion of its range, nor is it likely to become so
within the foreseeable future. Accordingly, the graytail skate does not
meet the definition of a threatened or endangered species and therefore
does not warrant listing as threatened or endangered at this time.
Effects of Listing
Conservation measures provided for species listed as endangered or
threatened under the ESA include recovery actions (16 U.S.C. 1533(f));
concurrent designation of critical habitat, if prudent and determinable
(16 U.S.C. 1533(a)(3)(A)); Federal agency requirements to consult with
NMFS under section 7 of the ESA to ensure their actions do not
jeopardize the species or result in adverse modification or destruction
of critical habitat should it be designated (16 U.S.C. 1536); and
prohibitions on taking for endangered species (16 U.S.C. 1538).
Recognition of the species' plight through listing promotes
conservation actions by Federal and state agencies, foreign entities,
private groups, and individuals. The main effects of the proposed
endangered listings are prohibitions on take, including export and
import.
Identifying Section 7 Conference and Consultation Requirements
Section 7(a)(2) (16 U.S.C. 1536(a)(2)) of the ESA and NMFS/USFWS
regulations require Federal agencies to consult with us to ensure that
activities they authorize, fund, or carry out are not likely to
jeopardize the continued existence of listed species or destroy or
adversely modify critical habitat. Section 7(a)(4) (16 U.S.C.
1536(a)(4)) of the ESA and NMFS/USFWS regulations also require Federal
agencies to confer with us on actions likely to jeopardize the
continued existence of species proposed for listing, or that result in
the destruction or adverse modification of proposed critical habitat of
those species. It is unlikely that the listing of these species under
the ESA will increase the number of section 7 consultations, because
these species occur outside of the United States and are unlikely to be
affected by Federal actions.
Critical Habitat
Critical habitat is defined in section 3 of the ESA (16 U.S.C.
1532(5)) as: (1) The specific areas within the geographical area
occupied by a species, at the time it is listed in accordance with the
ESA, on which are found those physical or biological features (a)
essential to the conservation of the species and (b) that may require
special management considerations or protection; and (2) specific areas
outside the geographical area occupied by a species at the time it is
listed upon a determination that such areas are essential for the
conservation of the species. ``Conservation'' means the use of all
methods and procedures needed to bring the species to the point at
which listing under the ESA is no longer necessary. Section 4(a)(3)(A)
of the ESA (16 U.S.C. 1533(a)(3)(A)) requires that, to the extent
prudent and determinable, critical habitat be designated concurrently
with the listing of a species. However, critical habitat shall not be
designated in foreign countries or other areas outside U.S.
jurisdiction (50 CFR 424.12(h)).
The best available scientific and commercial data as discussed
above identify the geographical areas occupied by Isogomphodon
oxyrhynchus, Rhinobatos horkelii, Mustelus fasciatus, M. schmitti,
Squatina guggenheim and S. argentina as being entirely outside U.S.
jurisdiction, so we cannot designate critical habitat for these
species.
We can designate critical habitat in areas in the United States
currently unoccupied by the species, if the area(s) are determined by
the Secretary to be essential for the conservation of the species.
Regulations at 50 CFR 424.12(e) specify that we shall designate as
critical habitat areas outside the geographical range presently
occupied by the species only when the designation limited to its
present range would be inadequate to ensure the conservation of the
species. The best available scientific and commercial information on
these species does not indicate that U.S. waters provide any
[[Page 76113]]
specific essential biological function for any of the species proposed
for listing. Therefore, based on the available information, we do not
intend to designate critical habitat for Isogomphodon oxyrhynchus,
Rhinobatos horkelii, Mustelus fasciatus, M. schmitti, Squatina
guggenheim or S. argentina.
Identification of Those Activities That Would Constitute a Violation of
Section 9 of the ESA
On July 1, 1994, NMFS and FWS published a policy (59 FR 34272) that
requires us to identify, to the maximum extent practicable at the time
a species is listed, those activities that would or would not
constitute a violation of section 9 of the ESA.
Because we are proposing to list Isogomphodon oxyrhynchus,
Rhinobatos horkelii, Mustelus fasciatus and Squatina argentina as
endangered, all of the prohibitions of section 9(a)(1) of the ESA will
apply to these species. These include prohibitions on the import,
export, use in foreign commerce, or ``take'' of the species. These
prohibitions apply to all persons subject to the jurisdiction of the
United States, including in the United States, its territorial sea, or
on the high seas. Take is defined as ``to harass, harm, pursue, hunt,
shoot, wound, kill, trap, capture, or collect, or to attempt to engage
in any such conduct.'' The intent of this policy is to increase public
awareness of the effects of this listing on proposed and ongoing
activities within the species' range. Activities that we believe could
result in a violation of section 9 prohibitions for these species
include, but are not limited to, the following:
(1) Possessing, delivering, transporting, or shipping any
individual or part (dead or alive) taken in violation of section
9(a)(1);
(2) Delivering, receiving, carrying, transporting, or shipping in
interstate or foreign commerce any individual or part, in the course of
a commercial activity;
(3) Selling or offering for sale in interstate commerce any part,
except antique articles at least 100 years old;
(4) Importing or exporting these species or any part of these
species.
We emphasize that whether a violation results from a particular
activity is entirely dependent upon the facts and circumstances of each
incident. Further, an activity not listed may in fact constitute a
violation.
Identification of Those Activities That Would Not Constitute a
Violation of Section 9 of the ESA
We will identify, to the extent known at the time of the final
rule, specific activities that will not be considered likely to result
in a violation of section 9 of the ESA. Although not binding, we are
considering the following actions, depending on the circumstances, as
not being prohibited by ESA section 9:
(1) Take authorized by, and carried out in accordance with the
terms and conditions of, an ESA section 10(a)(1)(A) permit issued by
NMFS for purposes of scientific research or the enhancement of the
propagation or survival of the species;
(2) Continued possession of parts that were in possession at the
time of listing. Such parts may be non-commercially exported or
imported; however, the importer or exporter must be able to provide
evidence to show that the parts meet the criteria of ESA section
9(b)(1) (i.e., held in a controlled environment at the time of listing,
in a non-commercial activity).
Protective Regulations Under Section 4(d) of the ESA
We are proposing to list Mustelus fasciatus and Squatina guggenheim
as threatened species. In the case of threatened species, ESA section
4(d) leaves it to the Secretary's discretion whether, and to what
extent, to extend the section 9(a) ``take'' prohibitions to the
species, and authorizes us to issue regulations necessary and advisable
for the conservation of the species. Thus, we have flexibility under
section 4(d) to tailor protective regulations, taking into account the
effectiveness of available conservation measures. The 4(d) protective
regulations may prohibit, with respect to threatened species, some or
all of the acts which section 9(a) of the ESA prohibits with respect to
endangered species. These 9(a) prohibitions apply to all individuals,
organizations, and agencies subject to U.S. jurisdiction. We will
consider extending some or all potential protective regulations
pursuant to section 4(d) for the proposed threatened species. We seek
public comment on potential 4(d) protective regulations (see below).
Public Comments Solicited
To ensure that any final action resulting from this proposed rule
will be as accurate and effective as possible, we are soliciting
comments and information from the public, other concerned governmental
agencies, the scientific community, industry, and any other interested
parties on information in the status review and proposed rule. Comments
are encouraged on these proposals (See DATES and ADDRESSES). We must
base our final determination on the best available scientific and
commercial information when making listing determinations. We cannot,
for example, consider the economic effects of a listing determination.
Final promulgation of any regulation(s) on these species' listing
proposals will take into consideration the comments and any additional
information we receive, and such communications may lead to a final
regulation that differs from this proposal or result in a withdrawal of
this listing proposal. We particularly seek:
(1) Information concerning the threats to any of the six species
proposed for listing;
(2) Taxonomic information on any of these species;
(3) Biological information (life history, genetics, population
connectivity, etc.) on any of these species;
(4) Efforts being made to protect any of these species throughout
their current ranges;
(5) Information on the commercial trade of any of these species;
(6) Historical and current distribution and abundance and trends
for any of these species;
(7) Current or planned activities within the range of these species
and their possible impact on these species; and,
(8) Information relevant to potential ESA section 4(d) protective
regulations for any of the proposed threatened species.
We request that all information be accompanied by: (1) Supporting
documentation, such as maps, bibliographic references, or reprints of
pertinent publications; and (2) the submitter's name, address, and any
association, institution, or business that the person represents.
Role of Peer Review
In December 2004, the Office of Management and Budget (OMB) issued
a Final Information Quality Bulletin for Peer Review establishing a
minimum peer review standard. Similarly, a joint NMFS/FWS policy (59 FR
34270; July 1, 1994) requires us to solicit independent expert review
from qualified specialists, concurrent with the public comment period.
The intent of the peer review policy is to ensure that listings are
based on the best scientific and commercial data available. We
solicited peer review comments on the species' status review reports
(Casselbury and Carlson 2015a-
[[Page 76114]]
g) from 22 scientists from the academic and scientific community that
were either familiar with the species or had expertise in elasmobranch
biology, ecology, or conservation. We received comments from nine
scientists and incorporated those comments into the status review
reports and this proposed rule. Their comments on the status reviews
are also summarized in the peer review report available at http://www.cio.noaa.gov/services_programs/prplans/PRsummaries.html.
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), we have concluded that ESA listing actions are not subject to
the environmental assessment requirements of the National Environmental
Policy Act (NEPA) (See NOAA Administrative Order 216-6).
Executive Order 12866, Regulatory Flexibility Act, and Paperwork
Reduction Act
As noted in the Conference Report on the 1982 amendments to the
ESA, economic impacts cannot be considered when assessing the status of
a species. Therefore, the economic analysis requirements of the
Regulatory Flexibility Act are not applicable to the listing process.
In addition, this proposed rule is exempt from review under Executive
Order 12866. This proposed rule does not contain a collection-of-
information requirement for the purposes of the Paperwork Reduction
Act.
Executive Order 13132, Federalism
In accordance with E.O. 13132, we determined that this proposed
rule does not have significant Federalism effects and that a Federalism
assessment is not required. In keeping with the intent of the
Administration and Congress to provide continuing and meaningful
dialogue on issues of mutual state and Federal interest, this proposed
rule will be given to the relevant governmental agencies in the
countries in which the species occurs, and they will be invited to
comment. We will confer with the U.S. Department of State to ensure
appropriate notice is given to foreign nations within the range of all
three species. As the process continues, we intend to continue engaging
in informal and formal contacts with the U.S. State Department, giving
careful consideration to all written and oral comments received.
List of Subjects
50 CFR Part 223
Endangered and threatened species, Exports, Imports,
Transportation.
50 CFR Part 224
Endangered and threatened species, Exports, Imports,
Transportation.
Dated: November 30, 2015.
Samuel D. Rauch, III,
Deputy Assistant Administrator for Regulatory Programs, National Marine
Fisheries Service.
For the reasons set out in the preamble, 50 CFR parts 223 and 224
are proposed to be amended as follows:
PART 223--THREATENED MARINE AND ANADROMOUS SPECIES
0
1. The authority citation for part 223 continues to read as follows:
Authority: 16 U.S.C. 1531-1543; subpart B, Sec. 223.201-202
also issued under 16 U.S.C. 1361 et seq.; 16 U.S.C. 5503(d) for
Sec. 223.206(d)(9).
0
2. In Sec. 223.102, amend the table in paragraph (e) by adding new
entries for two species in alphabetical order under the ``Fishes''
table subheading to read as follows:
Sec. 223.102 Enumeration of threatened marine and anadromous species.
* * * * *
(e) * * *
----------------------------------------------------------------------------------------------------------------
Species \1\
-------------------------------------------------------------------- Citation(s) for Critical
Description of listing habitat ESA rules
Common name Scientific name listed entity determination(s)
----------------------------------------------------------------------------------------------------------------
* * * * * * *
----------------------------------------------------------------------------------------------------------------
Fishes
----------------------------------------------------------------------------------------------------------------
* * * * * * *
Shark, spiny angel............ Squatina Entire species.. Federal Register NA NA
guggenheim. citation and
date when
published as a
final rule.
Shark, narrownose smoothhound. Mustelus schmitti Entire species.. Federal Register NA NA
citation and
date when
published as a
final rule.
* * * * * * *
----------------------------------------------------------------------------------------------------------------
\1\ Species includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement,
see 61 FR 4722, February 7, 1996), and evolutionarily significant units (ESUs) (for a policy statement, see 56
FR 58612, November 20, 1991).
\2\ Jurisdiction for sea turtles by the Department of Commerce, National Oceanic and Atmospheric Administration,
National Marine Fisheries Service, is limited to turtles while in the water.
[79 FR 20806, Apr. 14, 2014, as amended at 79 FR 38240, July 3, 2014; 79 FR 40015, July 11, 2014; 79 FR 54122,
Sept. 10, 2014; 80 FR 7978, Feb. 13, 2015]
[[Page 76115]]
PART 224--ENDANGERED MARINE AND ANADROMOUS SPECIES
0
3. The authority citation for part 224 continues to read as follows:
Authority: 16 U.S.C. 1531-1543 and 16 U.S.C 1361 et seq.
0
4. In Sec. 224.101, paragraph (h), amend the table by adding new
entries for four species in alphabetical order under the ``Fishes''
table subheading to read as follows:
Sec. 224.101 Enumeration of endangered marine and anadromous species.
* * * * *
(h) * * *
----------------------------------------------------------------------------------------------------------------
Species \1\
-------------------------------------------------------------------- Citation(s) for Critical
Description of listing habitat ESA rules
Common name Scientific name listed entity determination(s)
----------------------------------------------------------------------------------------------------------------
* * * * * * *
----------------------------------------------------------------------------------------------------------------
Fishes
----------------------------------------------------------------------------------------------------------------
* * * * * * *
Guitarfish, Brazilian......... Rhinobatos Entire species.. Federal Register NA NA
horkelii. citation and
date when
published as a
final rule.
Shark, Argentine angel........ Squatina Entire species.. Federal Register NA NA
argentina. citation and
date when
published as a
final rule.
Shark, daggernose............. Isogomphodon Entire species.. Federal Register NA NA
oxyrhynchus. citation and
date when
published as a
final rule.
Shark, striped smoothhound.... Mustelus Entire species.. Federal Register NA NA
fasciatus. citation and
date when
published as a
final rule.
* * * * * * *
----------------------------------------------------------------------------------------------------------------
\1\ Species includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement,
see 61 FR 4722, February 7, 1996), and evolutionarily significant units (ESUs) (for a policy statement, see 56
FR 58612, November 20, 1991).
\2\ Jurisdiction for sea turtles by the Department of Commerce, National Oceanic and Atmospheric Administration,
National Marine Fisheries Service, is limited to turtles while in the water.
[79 FR 20814, Apr. 14, 2014, as amended at 79 FR 31227, June 2, 2014; 79 FR 38241, July 3, 2014; 79 FR 74005,
Dec. 12, 2014; 79 FR 78725, Dec. 31, 2014; 79 FR 68372, Nov. 17, 2014; 80 FR 7978, Feb. 13, 2015; 80 FR 7390,
Feb. 10, 2015]
[FR Doc. 2015-30660 Filed 12-4-15; 8:45 am]
BILLING CODE 3510-22-P