Endangered and Threatened Wildlife and Plants; 12-Month Finding for 7 Foreign Species of Elasmobranchs Under the Endangered Species Act
Federal RegisterDec 7, 2015
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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.
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
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,
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 Amapá, Pará, and Maranhão, with Tubarão Bay in Maranhão 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 °C to 31.5 °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 Marajó 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 Cortés (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 (µ
1
) was 10.7 years and the expected number of replacements (R
0
) 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 Cortés (2002), which means this species generally has a low potential to recover from exploitation.
Historical and Current Distribution and Population Abundance
In Brazil, daggernose sharks were historically found in the states of Amapá, Pará, and Maranhão, and were first formally recorded in surveys from the 1960s in the state of Maranhão (Lessa 1986). In 1999, daggernose sharks were documented as occurring in two Marine Conservation Areas in northern Brazil, the Parque Nacional Cabo Orange in Amapá, and the Reentrâncias Maranhenses in Maranhão (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 Bragança fish market in northern Brazil (State of Pará), 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 Maranhão 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 Cervigón 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 Pará, 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 Maranhão 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 Pará (Lessa
et al.
2010) or Maranhão (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 Amapá and Pará), 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 Maranhão 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; Ministério 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 (Ministério do Meio Ambiente/Instituto Brasileiro do Meio Ambiente e dos
Recursos Naturais Renováveis (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 Espécies da Fauna Ameaçadas de Extinção—Peixes e Invertebrados Aquáticos” (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 Reentrâncias 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 Maranhão, 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 Reentrâncias 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
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
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 Pará, and was caught in large numbers by the artisanal gillnet fisheries operating on the Maranhão 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 Amapá and Pará) and Northwest region (which includes the States of Maranhão 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
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 °C, while in the summer, individuals are found in average water temperatures of 26 °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° and 34° 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°36′ S.) to Arroio Chuí (33°45′ S.). In historical bottom trawl surveys between latitudes 28°00′ S. and 34°30′ S.,
R. horkelii
was common across the Plataforma Sul south of latitude 29°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 Chuí and Solidão (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° S.-43° 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.
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° S.-34° 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° S.-30° 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 São 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
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 Gestão 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 São 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 Cananéia-Iguape-Peruíbe (São Paulo; 234,000 hectares), PARNA do Superagui (Parana; 33,988 hectares), REBIO do Arvoredo (Santa Catarina; 17,600 hectares) and RESEX Marinha do Pirjubaé (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
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° S. and 34° S. in southern Brazil, and it is scarce elsewhere. On the northern Argentine continental shelf, between 34° S. and 43° 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
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° S. and 34° 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° S.-30° 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 São 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).
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 Bahía 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 Chuí 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 Chuí 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 °C-15 °C for juveniles during winter months, and >16 °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 Solidão 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
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 Bahía 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 Mendonça 1996; Vooren and Klippel 2005b). Striped
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 Chuí 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 Chuí 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 Mendonça 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
(Dirección Nacional de Recursos Acuáticos (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
(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° S. and 34° 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
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
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° S. and 47°45′ S. (Belleggia
et al.
2012). Rio de Janeiro, Brazil, is the northernmost limit of the species' range (Oddone
et al.
2007) and Ría 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 °C-11.7 °C and bottom temperatures of 5.5 °C-11 °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 °C and 20 °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 Río de la Plata and El Rincón, 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; Galíndez
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; Galíndez
et al.
2010). Litter size increases significantly with maternal length (Oddone
et al.
2005; Cortés 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 Rincón area (including Bahía Blanca and Anegada Bay) and the Río de la Plata (including Samborombón Bay) (Chiaramonte and Pettovello 2000; Molina and Cazorla 2011).
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 Río 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, Cortés (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, Cortés (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 (Cortés 2007). These demographic parameters place narrownose smoothhound toward the faster growing end of the “fast-slow” continuum of population parameters calculated by Cortés (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° S.-41° 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° S.-48° 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° S.-41° 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 (Galíndez
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
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° S. and 41° 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 (Cortés 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 Rincón 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 Rincón 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 Rincón 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 Rincón 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 Rincón 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, Cortés (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,
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 Lamónaca 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, Ría Deseado (~40 km; 47°45′ S.; 65°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 Ría Deseado waters in the late spring and stay until late summer (Chiaramonte and Pettovello 2000). Anegada Bay (39°50′51″ S. to 40°43′08″ S. and 62°28′44″ W. to 62°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 Rincón 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 Comisión Técnica Mixta del Frente Marítimo (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
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° 5/11, Res. N° 5/02), and in 2012, the CTMFM set a species-specific total permissible catch limit for narrownose smoothhound at 4,500 t (Res. N° 11/13, Res. N° 9/12). This catch limit remained at this level until 2015, when it was reduced to 3,500 t (Res N° 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° 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 th
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