Endangered and Threatened Wildlife and Plants; 12-Month Finding for 7 Foreign Species of Elasmobranchs Under the Endangered Species Act

 
CONTENT

Federal Register, Volume 80 Issue 234 (Monday, December 7, 2015)

Federal Register Volume 80, Number 234 (Monday, December 7, 2015)

Proposed Rules

Pages 76067-76115

From the Federal Register Online via the Government Publishing Office www.gpo.gov

FR Doc No: 2015-30660

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Vol. 80

Monday,

No. 234

December 7, 2015

Part II

Department of Commerce

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National Oceanic and Atmospheric Administration

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50 CFR Parts 223 and 224

Endangered and Threatened Wildlife and Plants; 12-Month Finding for 7 Foreign Species of Elasmobranchs Under the Endangered Species Act; Proposed Rule

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DEPARTMENT OF COMMERCE

National Oceanic and Atmospheric Administration

50 CFR Parts 223 and 224

Docket No. 150909839-5839-01

RIN 0648-XE184

Endangered and Threatened Wildlife and Plants; 12-Month Finding for 7 Foreign Species of Elasmobranchs Under the Endangered Species Act

AGENCY: National Marine Fisheries Service (NMFS), National Oceanic and Atmospheric Administration (NOAA), Commerce.

ACTION: Proposed rule; 12-month petition finding; request for comments.

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SUMMARY: We, NMFS, have completed comprehensive status reviews under the Endangered Species Act (ESA) for seven foreign marine elasmobranch species in response to a petition to list those species. These seven species are the daggernose shark (Isogomphodon oxyrhynchus), Brazilian guitarfish (Rhinobatos horkelii), striped smoothhound shark (Mustelus fasciatus), narrownose smoothhound shark (Mustelus schmitti), spiny angel shark (Squatina guggenheim), Argentine angel shark (Squatina argentina), and graytail skate (Bathyraja griseocauda). Based on the best scientific and commercial information available, and after taking into account efforts being made to protect these species, we have determined that the daggernose shark (I. oxyrhynchus), Brazilian guitarfish (R. horkelii), striped smoothhound shark (Mustelus fasciatus), and Argentine angel shark (S. argentina) meet the definition of an endangered species under the ESA. We have determined that the narrownose smoothhound shark (M. schmitti) and spiny angel shark (S. guggenheim) meet the definition of a threatened species under the ESA. Therefore, we propose to list these six species under the ESA. Additionally, we have determined that the graytail skate (B. griseocauda) does not warrant listing under the ESA at this time. We are not proposing to designate critical habitat for any of the species proposed for listing because the geographical areas occupied by these species are entirely outside U.S. jurisdiction, and we have not identified any unoccupied areas within U.S. jurisdiction that are currently essential to the conservation of any of these species. We are soliciting comments on our proposal to list these six foreign marine elasmobranch species.

DATES: Comments on this proposed rule must be received by February 5, 2016. Public hearing requests must be made by January 21, 2016.

ADDRESSES: You may submit comments on this document, identified by NOAA-NMFS-2015-0161, by either of the following methods:

Electronic Submissions: Submit all electronic public comments via the Federal eRulemaking Portal. Go to www.regulations.gov/#!docketDetail;D=NOAA-NMFS-2015-0161. Click the ``Comment Now'' icon, complete the required fields, and enter or attach your comments.

Mail: Submit written comments to NMFS Office of Protected Resources (F/PR3), 1315 East West Highway, Silver Spring, MD 20910, USA.

Instructions: Comments sent by any other method, to any other address or individual, or received after the end of the comment period, may not be considered by NMFS. All comments received are a part of the public record and will generally be posted for public viewing on www.regulations.gov without change. All personally identifying information (e.g., name, address, etc.), confidential business information, or otherwise sensitive information submitted voluntarily by the sender will be publicly accessible. NMFS will accept anonymous comments (enter ``N/A'' in the required fields if you wish to remain anonymous).

You can find the petition, status review report, Federal Register notices, and the list of references electronically on our Web site at http://www.nmfs.noaa.gov/pr/species/petition81.htm.

FOR FURTHER INFORMATION CONTACT: Maggie Miller, NMFS, Office of Protected Resources (OPR), (301) 427-8403 or Chelsey Young, NMFS, OPR, (301) 427-8491.

SUPPLEMENTARY INFORMATION:

Background

On July 15, 2013, we received a petition from WildEarth Guardians to list 81 marine species as threatened or endangered under the Endangered Species Act (ESA). This petition included species from many different taxonomic groups, and we prepared our 90-day findings in batches by taxonomic group. We found that the petitioned actions may be warranted for 27 of the 81 species and announced the initiation of status reviews for each of the 27 species (78 FR 63941, October 25, 2013; 78 FR 66675, November 6, 2013; 78 FR 69376, November 19, 2013; 79 FR 9880, February 21, 2014; and 79 FR 10104, February 24, 2014). This document addresses the findings for 7 of those 27 species: daggernose shark (Isogomphodon oxyrhynchus), Brazilian guitarfish (Rhinobatos horkelii), striped smoothhound shark (Mustelus fasciatus), narrownose smoothhound shark (Mustelus schmitti), spiny angel shark (Squatina guggenheim), Argentine angel shark (Squatina argentina), and graytail skate (Bathyraja griseocauda). The status of, and relevant Federal Register notices for, the other 20 species can be found on our Web site at http://www.nmfs.noaa.gov/pr/species/petition81.htm.

We are responsible for determining whether species are threatened or endangered under the ESA (16 U.S.C. 1531 et seq.). To make this determination, we consider first whether a group of organisms constitutes a ``species'' under the ESA, then whether the status of the species qualifies it for listing as either threatened or endangered. Section 3 of the ESA defines a ``species'' to include ``any subspecies of fish or wildlife or plants, and any distinct population segment of any species of vertebrate fish or wildlife which interbreeds when mature.'' On February 7, 1996, NMFS and the U.S. Fish and Wildlife Service (USFWS; together, the Services) adopted a policy describing what constitutes a distinct population segment (DPS) of a taxonomic species (the DPS Policy; 61 FR 4722). The DPS Policy identified two elements that must be considered when identifying a DPS: (1) The discreteness of the population segment in relation to the remainder of the species (or subspecies) to which it belongs; and (2) the significance of the population segment to the remainder of the species (or subspecies) to which it belongs. As stated in the DPS Policy, Congress expressed its expectation that the Services would exercise authority with regard to DPSs sparingly and only when the biological evidence indicates such action is warranted. Based on the scientific information available we determined that the daggernose shark (I. oxyrhynchus), Brazilian guitarfish (R. horkelii), striped smoothhound shark (M. fasciatus), narrownose smoothhound shark (M. schmitti), spiny angel shark (S. guggenheim), Argentine angel shark (S. argentina), and graytail skate (B. griseocauda) are ``species'' under the ESA. There is nothing in the scientific literature indicating that any of these species should be further divided into subspecies or DPSs.

Section 3 of the ESA defines an endangered species as ``any species which is in danger of extinction throughout all or a significant portion of its range'' and a threatened species as

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one ``which is likely to become an endangered species within the foreseeable future throughout all or a significant portion of its range.'' We interpret an ``endangered species'' to be one that is presently in danger of extinction. A ``threatened species,'' on the other hand, is not presently in danger of extinction, but is likely to become so in the foreseeable future (that is, at a later time). In other words, the primary statutory difference between a threatened and endangered species is the timing of when a species may be in danger of extinction, either presently (endangered) or in the foreseeable future (threatened).

When we consider whether a species might qualify as threatened under the ESA, we must consider the meaning of the term ``foreseeable future.'' It is appropriate to interpret ``foreseeable future'' as the horizon over which predictions about the conservation status of the species can be reasonably relied upon. The foreseeable future considers the life history of the species, habitat characteristics, availability of data, particular threats, ability to predict threats, and the reliability to forecast the effects of these threats and future events on the status of the species under consideration. Because a species may be susceptible to a variety of threats for which different data are available, or which operate across different time scales, the foreseeable future is not necessarily reducible to a particular number of years.

Section 4(a)(1) of the ESA requires us to determine whether any species is endangered or threatened due to any of the following factors: the present or threatened destruction, modification, or curtailment of its habitat or range; overutilization for commercial, recreational, scientific, or educational purposes; disease or predation; the inadequacy of existing regulatory mechanisms; or other natural or manmade factors affecting its continued existence. Under section (4)(b)(1)(A), we are also required to make listing determinations based solely on the best scientific and commercial data available, after conducting a review of the species' status and after taking into account efforts being made by any state or foreign nation to protect the species.

Status Reviews

Status reviews for the petitioned species addressed in this finding were conducted by a contractor for the NMFS Southeast Fisheries Science Center and are available at http://www.nmfs.noaa.gov/pr/species/petition81.htm or on the respective species pages found on the Office of Protected Resources Web site (http://www.nmfs.noaa.gov/pr/species/index.htm). These status reviews compiled information on each species' biology, ecology, life history, and threats from information contained in the petition, our files, a comprehensive literature search, and consultation with experts. The draft status review reports (Casselberry and Carlson 2015 a-g) were submitted to independent peer reviewers and comments and information received from peer reviewers were addressed and incorporated as appropriate before finalizing the draft report. The peer review report is available at http://www.cio.noaa.gov/services_programs/prplans/PRsummaries.html. These status reviews did not include extinction risk analyses for the species; thus, the extinction risk analyses for the seven species are included in this 12-

month finding. In addition to the status review reports, we considered information submitted by the public in response to our petition finding as well as information we compiled to assess the extinction risk of the species to make our determinations.

Extinction Risk Analyses

We considered the best available information and applied professional judgment in evaluating the level of risk faced by each of the seven species. For each extinction risk analysis, we evaluated the species' demographic risks (demographic risk analysis), such as low abundance and productivity, and threats to the species including those related to the factors specified by the ESA section 4(a)(1)(A)-(E) (threats assessment), and then synthesized this information to estimate the extinction risk of the species (risk of extinction).

The demographic risk analysis, mentioned above, is an assessment of the manifestation of past threats that have contributed to the species' current status and informs the consideration of the biological response of the species to present and future threats. For this analysis, we considered the demographic viability factors developed by McElhany et al. (2000). The approach of considering demographic risk factors to help frame the consideration of extinction risk has been used in many of our status reviews, including for Pacific salmonids, Pacific hake, walleye pollock, Pacific cod, Puget Sound rockfishes, Pacific herring, scalloped and great hammerhead sharks, and black abalone (see http://www.nmfs.noaa.gov/pr/species/ for links to these reviews). In this approach, the collective condition of individual populations is considered at the species level according to four demographic viability factors: Abundance, growth rate/productivity, spatial structure/

connectivity, and diversity. These viability factors reflect concepts that are well-founded in conservation biology and that individually and collectively provide strong indicators of extinction risk.

In conducting the threats assessment, we identified and summarized the section 4(a)(1) factors that are currently operating on the species and their likely impact on the biological status of the species. We also looked for future threats (where the impact on the species has yet to be manifested) and considered the reliability to which we could forecast the effects of these threats and future events on the status of these species.

Using the findings from the demographic risk analysis and threats assessment, we evaluated the overall extinction risk of the species. Because species-specific information (such as current abundance) is sparse, qualitative ``reference levels'' of risk were used to describe extinction risk. The definitions of the qualitative ``reference levels'' of extinction risk were as follows: ``Low Risk''--a species is at a low risk of extinction if it exhibits a trajectory indicating that it is unlikely to be at a moderate level of extinction risk in the foreseeable future (see description of ``Moderate Risk'' below). A species may be at low risk of extinction due to its present demographics (i.e., stable or increasing trends in abundance/population growth, spatial structure and connectivity, and/or diversity) with projected threats likely to have insignificant impacts on these demographic trends; ``Moderate Risk''--a species is at moderate risk of extinction if it exhibits a trajectory indicating that it will more likely than not be at a high level of extinction risk in the foreseeable future (see description of ``High Risk'' below). A species may be at moderate risk of extinction due to its present demographics (i.e., declining trends in abundance/population growth, spatial structure and connectivity, and/or diversity and resilience) and/or projected threats and its likely response to those threats; ``High Risk''--a species is at high risk of extinction when it is at or near a level of abundance, spatial structure and connectivity, and/or diversity that place its persistence in question. The demographics of the species may be strongly influenced by stochastic or depensatory processes. Similarly, a species may be at high risk of extinction if it faces clear and present threats (e.g., confinement to a small geographic area; imminent destruction,

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modification, or curtailment of its habitat; or disease epidemic) that are likely to create such imminent demographic risks.

Below we summarize information from the status review reports and information we compiled on the seven foreign marine elasmobranch species, analyze extinction risk of each species, assess protective efforts to determine if they are adequate to mitigate existing threats to each species, and propose determinations based on the status of each of the seven foreign marine elasmobranch species.

Daggernose Shark (Isogomphodon oxyrhynchus)

Species Description

The daggernose shark (Isogomphodon oxyrhynchus) is the only species in the genus Isogomphodon, in the family Carcharhinidae (Compagno 1988). It has a uniform gray or gray-brown color and white underside (Compagno 1984; Compagno 1988; Grace 2001), and is identified by its prominent, elongated snout. The pectoral fins of the species are very large and paddle-shaped (Compagno 1984; Compagno 1988; Grace 2001).

Range and Habitat Use

The daggernose shark occurs in the central western Atlantic Ocean and Caribbean Sea and has been reported along the coasts of Venezuela, Trinidad, Guyana, Suriname, French Guiana, and northern Brazil (Lessa et al. 2006a). The Brazilian range includes the states of Amapaacute, Paraacute, and Maranhatildeo, with Tubaratildeo Bay in Maranhatildeo 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 degC to 31.5 degC 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 Marajoacute 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 Corteacutes (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 (micro1) was 10.7 years and the expected number of replacements (R0) was 1.05. Lessa et al. (2010) estimated annual population growth to be r = -0.048 under natural mortality rates (of 0.28 using the Hoenig (1984) method and 0.378 using the Pauly (1980) method), and a generation time of 9 years. If fishing mortality rates were incorporated, the annual population growth was estimated to be r = -0.074, with a generation time of 8.4 years (Lessa et al. 2010). These demographic parameters place daggernose sharks towards the slow growing end of the ``fast-

slow'' continuum of population parameters calculated for 38 species of sharks by Corteacutes (2002), which means this species generally has a low potential to recover from exploitation.

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Historical and Current Distribution and Population Abundance

In Brazil, daggernose sharks were historically found in the states of Amapaacute, Paraacute, and Maranhatildeo, and were first formally recorded in surveys from the 1960s in the state of Maranhatildeo (Lessa 1986). In 1999, daggernose sharks were documented as occurring in two Marine Conservation Areas in northern Brazil, the Parque Nacional Cabo Orange in Amapaacute, and the Reentracircncias Maranhenses in Maranhatildeo (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 Braganccedila fish market in northern Brazil (State of Paraacute), 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 Maranhatildeo 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 Cervigoacuten 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 Paraacute, 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 Maranhatildeo 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 Paraacute (Lessa et al. 2010) or Maranhatildeo (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 Amapaacute and Paraacute), 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 Maranhatildeo 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; Ministeacuterio 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 (Ministeacuterio do Meio Ambiente/Instituto Brasileiro do Meio Ambiente e dos

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Recursos Naturais Renovaacuteveis (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 Espeacutecies da Fauna Ameaccediladas de Extinccedilatildeo--Peixes e Invertebrados Aquaacuteticos'' (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 Reentracircncias 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 Maranhatildeo, 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 Reentracircncias 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

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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

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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 Paraacute, and was caught in large numbers by the artisanal gillnet fisheries operating on the Maranhatildeo 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 Amapaacute and Paraacute) and Northwest region (which includes the States of Maranhatildeo 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

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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 degC, while in the summer, individuals are found in average water temperatures of 26 degC (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 28deg and 34deg 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 (28deg36' S.) to Arroio Chuiacute (33deg45' S.). In historical bottom trawl surveys between latitudes 28deg00' S. and 34deg30' S., R. horkelii was common across the Plataforma Sul south of latitude 29deg40' 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 Chuiacute and Solidatildeo (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 (34deg S.-43deg 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.

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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 28deg S.-34deg 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 28deg S.-30deg 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 (16 degC 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 Solidatildeo 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

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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) 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 36deg S. and 41deg 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 (Corteacutes 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 Rincoacuten 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 Rincoacuten 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 Rincoacuten 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 Rincoacuten 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 Rincoacuten 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, Corteacutes (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,

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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 Lamoacutenaca 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, Riacutea Deseado (~40 km; 47deg45' S.; 65deg55' 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 Riacutea Deseado waters in the late spring and stay until late summer (Chiaramonte and Pettovello 2000). Anegada Bay (39deg50'51'' S. to 40deg43'08'' S. and 62deg28'44'' W. to 62deg03'00'' 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 Rincoacuten 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 Comisioacuten Teacutecnica Mixta del Frente Mariacutetimo (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

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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. Ndeg 5/11, Res. Ndeg 5/02), and in 2012, the CTMFM set a species-specific total permissible catch limit for narrownose smoothhound at 4,500 t (Res. Ndeg 11/13, Res. Ndeg 9/12). This catch limit remained at this level until 2015, when it was reduced to 3,500 t (Res Ndeg 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 Ndeg 445). As described in previous species assessments, an Annex 1 listing prohibits the catch of the species except for scientific purposes, which requires a special license from IBAMA. There is also a prohibition of trawl fishing within three nautical miles from the coast of southern Brazil, although the enforcement of this prohibition has been noted as difficult (Chiaramonte and Vooren 2007). In addition, the species is still susceptible to being caught as bycatch in the legally permitted coastal gillnet fisheries and offshore trawl and gillnet fisheries and vulnerable to the associated bycatch mortality (Lessa and Vooren 2007). Additionally, unlike the striped smoothhound, the narrownose smoothhound is listed as one of the 12 species of concern under Brazil's FAO NPOA-sharks and would also benefit from the proposed fishing closures and other management measures outlined in the plan. However, as mentioned previously, the plan was only just approved as of December 2014, and will not be fully implemented for another 5 years. Thus, the implementation and effectiveness of the recommendations outlined in the plan remain uncertain, with the best available information indicating that current regulatory measures in Brazil to protect vulnerable species are poorly enforced.

Extinction Risk

The best available information provides multiple lines of evidence indicating that the M. schmitti currently faces a moderate risk of extinction. Below, we present the demographic risk analysis, threats assessment, and overall risk of extinction for the narrownose smoothhound shark.

Demographic Risk Analysis

Abundance

There is limited information available regarding quantitative abundance estimates of narrownose smoothhound throughout its range. However, biomass estimates as well as trends in commercial landings and CPUE data can provide some insight into the abundance of the species. The narrownose smoothhound is the most abundant and widely distributed triakid in the Argentine Sea. In Argentina, the narrownose smoothhound is mainly landed by the commercial fleet operating in the Buenos Aires coastal region, and represents up to 14.5 percent of landings (Carozza et al. 2001 cited in Massa et al. 2004b). Between 1992 and 1997, landings of the species in Argentina were fairly stable, on the order of 6,000-8,000 t; however, CPUE values decreased by upwards of 78 percent during this time period, indicating a likely decline in the abundance of the species. From 1998 to 2002, biomass of M. schmitti reportedly declined in the main fishing areas along the coast of Buenos Aires Province and the surrounding region by approximately 22 percent (Massa et al. 2006). National landings also decreased in Argentina by 30 percent during this same time period and have continued to decline based on FAO landings data through 2013. It is important to note that the decrease in landings is not due to falling market values as M. schmitti continues to fetch a high price in the Argentine domestic market (Massa et al. 2004b). In 2003, the spring time abundance of M. schmitti from coastal Buenos Aires and Uruguay (between 34deg S.-

41deg S.) was estimated to be 88,500 t, which represents a 50 percent and 39 percent decline from estimated values in 1994 and 1999, respectively (Massa et al. 2004a). Additionally, based on estimates calculated in 2007, size at maturity of the species has chronologically decreased since the 1970s, a strong indication of overutilization of the species and declining abundance.

In Uruguay, there is conflicting information regarding the trend in catches of M. schmitti. Landings of smoothhounds in Uruguay are aggregated at the genus level because catch is often reported by common name and the same common name is used for multiple species. Thus, identifying the true species composition of shark catches in Uruguay is problematic. According to Domingo et al. (2008), landings of smoothhounds in Uruguay (primarily M. schmitti) increased dramatically between 1999 and 2000, reaching 1,300 tons, and then steadily declined to approximately 850 tons by 2005. Based on landings data reported to the FAO, catches of M. schmitti have continued to decline, with only 194 t reported in 2013. However, without corresponding effort information, it is unclear if the decrease in landings is a result of decreases in abundance in the species.

In Brazil, M. schmitti occurs as winter migrants on the Plataforma Sul and is caught by the trawl and oceanic gillnet fleets operating on the continental shelf. Based on CPUE data from these fleets, the wintering population has likely suffered significant declines in abundance. The CPUE values from both the single and pair trawl fisheries showed an increase from the mid 1970s to the late 1980s; however, after 1987, CPUE values for both fleets decreased rapidly, and in 1994, these CPUE values showed an approximate 85 percent abundance decline of M. schmitti from 1985 values (Miranda and Vooren 2003). Massa et al. (2006) also cites

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unpublished data that indicate the likely extirpation of a local breeding population of narrownose smoothhound in Brazil as a result of fishing in inshore pupping and nursery areas. Although no further information was given regarding this population, survey and fisheries data suggest significant declines in newborn M. schmitti from a local nursery area off the coast of Rio Grande do Sul. Once abundant in the 1980s in the coastal waters off Casino Beach, Rio Grande do Sul, neonates of this local population have since seemingly disappeared, with data that show an absence of individuals from artisanal beach nets in 2003 and coastal trawl surveys in 2005 (Vooren et al. 2005b). This absence of neonates, compared to data from the 1980s, is likely a sign of decline of this population and may even suggest a potential extirpation.

Overall, best available information suggests the species is likely in decline in parts of its Argentine and Uruguayan range, and has experienced a significant decrease in abundance in its winter migrant population in Brazil. Although present abundance estimates are unknown, the significant declines in both CPUE and landings of the species throughout its range, as well as the chronological reduction of the species' average size (based on landings data) and size of maturity, suggest overexploitation of the species and a declining abundance trend. Targeting of the species will continue, given its demand in the market and importance in both the artisanal and commercial fisheries in the region and, combined with the high fishing pressure in the species' nursery areas, the species may continue to experience population declines throughout its range, with abundance levels that will likely contribute significantly to its extinction risk in the foreseeable future.

Growth Rate/Productivity

The narrownose smoothhound has an estimated lifespan of 20.8 years and 24.7 years for males and females, respectively, with a maximum recorded size of 110 cm TL. Information regarding size and age of maturity estimates vary throughout the species' range, but the most recent estimate from Hozbor et al. (2010) suggests an age at maturity of 4 years for both sexes. Although M. schmitti has an annual reproductive cycle with a lengthy gestation period (11 months) and an average of only 4-5 pups per litter, the species' intrinsic rate of population increase is relatively high, at 0.175 per year. Natural mortality rates ranged from 0.139 to 0.412 (Corteacutes 2007). These estimates indicate that M. schmitti has a higher potential to recover from exploitation compared to other coastal sharks, and could withstand annual removal rates of up to approximately 10 percent of the population. However, based on confirmed chronological reductions in both average size (from landings data) and total length at maturity in the species, it is apparent that removal rates of the species have been exceeding the 10 percent sustainable removal rate. The reduction in mean size and size at maturity is particularly concerning due to the positive relationship between maternal length and litter size (i.e., litter size increases significantly with maternal length) in which a decrease in maximum size has the potential to reduce the species' reproductive output. As such, these reductions likely compromise the species' growth rate and productivity, and consequently, hinder its ability to recover from exploitation.

Spatial Structure/Connectivity

Very limited information is available regarding spatial structure and connectivity of M. schmitti populations. Tagging studies of related species M. antarcticus and M. lenticulatis found that they have high dispersal capacities (Francis 1988), but no such studies have been conducted specifically for M. schmitti. If narrownose smoothhound populations are connected, then the significant fishing pressure on the migratory population while they winter on the Plataforma Sul may be negatively impacting the populations found in other parts of the species' range (perhaps contributing to the observed declines off Argentina and Uruguay). However, based on the available data, there is not enough information to identify critical populations or determine whether the rates of dispersal among populations, metapopulations, or habitat patches are posing a risk of extinction.

Diversity

The loss of diversity can increase a species' extinction risk through decreasing a species' capability of responding to episodic or changing environmental conditions. This can occur through a significant change or loss of variation in life history characteristics (such as reproductive fitness and fecundity), morphology, behavior, or other genetic characteristics. In terms of population structure, only one genetics study has been conducted to determine if multiple stocks occur throughout the species' range (Pereya et al. 2010). Results of this study indicate that M. schmitti comprises a single demographic unit in the Riacuteo de la Plata area and its maritime front (area separating Uruguay and Argentina), with no distinct population structure found between or within the Riacuteo de la Plata, the Atlantic coast or its outer shelf. These findings indicate high connectivity and suggest genetic homogeneity over this geographic range, which is attributed to the likely high dispersal and migration rates of the species (Pereya et al. 2010). However, a lack of genetic structure can also result from many other factors, including large effective population sizes and/or the presence of shared ancestral polymorphisms due to recent population divergence.

In addition to genetic homogeneity, the study found that nucleotide diversity in M. schmitti was lower than that reported for other elasmobranchs. These results may indicate that narrownose smoothhound experienced a genetic bottleneck, recent expansion, or selection, which potentially occurred during the Pleistocene Era (Pereyra et al. 2010). However, it is difficult to unambiguously discern between evidence for natural selection and demographic population expansion. Overall, the low genetic diversity values found for the species and evidence that fishing pressure may have already altered the genetic characteristics of the population (i.e., smaller average size and size at maturity, which in turn can alter reproductive fitness and fecundity) raise considerable concern over the species' status. This information indicates that M. schmtti may be at an increased risk of inbreeding depression or random genetic drift, and could experience the fixing of recessive detrimental genes, reducing the overall fitness of the species.

Threats Assessment

The primary threat to narrownose smoothhounds is overutilization in commercial and artisanal fisheries, with the species both targeted and bycaught throughout its range. In Argentina, M. schmitti is considered the most important elasmobranch for Argentine fisheries; however, data suggest that the majority of narrownose smoothhounds caught by Argentine fishermen are juveniles (e.g. up to 81.7 percent of the landings in 2002), indicating significant fishing pressure in important nursery areas. Declines in both CPUE and biomass of M. schmitti in Argentina occurred throughout the 1990s and early 2000s; however, mean values of CPUE have shown a slight upward trend from 2003-2007. However, as noted previously, these values should be interpreted with caution as they could

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be the result of increased directed fishing pressure on M. schmitti or an increase in overlap of fishing vessels in areas where M. schmitti has higher concentrations. Further, the chronological reduction in mean size and size of sexual maturity since the 1970s indicates overfishing of the species, suggesting exploitation rates are higher than what the species can presently sustain.

In the AUCFZ, where M. schmitti is most heavily exploited, fishing regulations currently set total permissible catch of M. schmitti at 3,500 t (which is a reduction from the 4,500 t limit that was in place since 2012). Additionally, trawling is banned within 5 nm of the coast, which coincides with the pupping and breeding areas of the species. While there is no information to indicate whether these regulatory mechanisms are positively affecting the status of the narrownose smoothhound, particularly since species-specific catch limits for M. schmitti have only been implemented since 2012, these regulations may help reduce fishing pressure in this important part of the species' range. Since 2010, catches of M. schmitti in the AUFCZ have been below the total allowable levels (for Mustelus spp. and M. schmitti) and on a decline; however, it should be noted that despite total allowable catch, minimum sizes, and annual quotas in place for many elasmobranchs in Argentina, they are largely ignored and poorly enforced (McCormack et al. 2007).

In Uruguay, narrownose smoothhounds are both targeted in artisanal fisheries and caught as bycatch. Despite the difficulties in identifying species composition of shark catches and discrepancies in catch information, data indicate landings of M. schmitti have declined in Uruguay, and in 2009, the species was classified as overfished in coastal regions of Uruguay and considered a high priority under the country's FAO NPOA-sharks.

In southern Brazil, the intensive fishing effort on the Plataforma Sul has likely led to overutilization, and consequently, significant declines in the winter migrant population of M. schmitti and potential extirpation of a local breeding population. Bottom trawl fishery CPUE data provide evidence that abundance of the winter migrant population of M. schmitti decreased by 85 percent due to intensive fishing effort from 1985 onwards. The absence of neonates from coastal waters, where they were once abundant in the 1980s, also suggest that intense fishing effort, especially in important nursery areas, has led to significant declines in local populations and potential extirpation of a small population of Brazilian migrants that was known to give birth in south Brazil in November and remain through February (Massa et al. 2006). Since 2004, the species has been listed on Brazil's endangered species list, which prohibits fishers from catching this species. The species is also listed as one of 12 species of concern under Brazil's FAO NPOA-

sharks, which calls for fishing closures in areas of -\1\ with a theoretical maximum size (Linfin) of 94.7 cm TL. Length and age at first maturity is estimated to be 72 cm TL and 4 years, respectively (Vooren and Klippel 2005a).

In terms of reproduction, the spiny angel shark has only one functional ovary (Vooren and da Silva 1991), with the maturation of ovarian follicles lasting about 2 years before ovulation, followed by gestation (Colonello et al. 2007). The female reproductive cycle is thought to be triennial (Colonello et al. 2007), with a gestation period that likely lasts 12 months (Colonello et al. 2007). Gestation begins in the summer (January-February) and pupping occurs the following spring (November-December) (Sunye and Vooren 1997). Gestation is divided into two stages: Uterine gestation and cloacal gestation. Early gestation (January-April) occurs only in the uteri, which contains recently ovulated eggs and embryos up to 25 mm TL (Sunye and Vooren 1997). During mid-term gestation and parturition (June-November) the uteri undergo a physical reconfiguration, causing the uteri and cloaca to form a heart-shaped chamber where the embryos develop (Sunye and Vooren 1997). According to Sunye and Vooren (1997), because this uterine-cloacal chamber is open to the external environment through a cloacal vent, this anatomical configuration is thought to be the reason why Squatina species are observed easily aborting embryos during capture or handling.

Pupping occurs during the spring and summer months (September-

March) in depths less than 20 m (Vooren 1997; Miranda and Vooren 2003). Litter sizes for the species range between 2 and 8 pups (Colonello et al. 2007; Vooren and Klippel 2005a). For spiny angel sharks in Argentina, Colonello et al. (2007) estimated an average of 4.07 pups per litter, with fecundity increasing with female length. In contrast, Vooren and Klippel (2005a) note that spiny angel sharks in southern Brazil frequently have 5 or 6 pups per litter, with the number of pups unrelated to female length. However, given the 3-year reproductive cycle, the range in pup estimates for spiny angel sharks results in a very low annual fecundity for the species (e.g., between 0.67 and 2.67 pups per year) (Colonello et al. 2007; Vooren and Klippel 2005a). After pupping, juveniles of the species will remain in the shallow waters for one year before migrating out to the continental shelf (Vooren and da Silva 1991; Vooren 1997; Vooren and Klippel 2005a). In terms of known juvenile habitat, the area of Rio Grande do Sul between 31deg50' S. and 33deg30' S. at depths less than 20 m is considered a nursery area for spiny angel sharks (Vooren and Klippel 2005a).

Genetics and Population Structure

Recently, Garcia et al. (2015) examined the population structure of the spiny angel shark in the middle of its range, in and around the Rio de la Plata estuary. Using mitochondrial DNA (which is maternally-

inherited DNA), the authors found that individuals from the outer estuary, surrounding coastal sites, and the outer shelf of the southwestern Atlantic showed no evidence of population genetic structuring. However, examination of nuclear recombinant DNA genes (which are biparentally-inherited) indicated that there was a remarkably high level of population genetic structure between the outer shelf spiny angel sharks and the coastal and outer estuarine angel sharks. In other words, the samples of spiny angel shark from the outer shelf represent an isolated group from the samples of spiny angel shark from the coastal and outer estuarine sites. Additionally, mitochondrial DNA indicated that the number of immigrant females per generation from the outer shelf to the Atlantic coast was much lower (2.8 individuals per generation) than the number of immigrant females per generation between the other populations (with estimates ranging from 12.8-46.9 individuals). All analyses revealed very low values of haplotype and nucleotide diversity from the recombinant DNA genes. Based on the low level of genetic diversity detected in S. guggenheim, Garcia et al. (2015) suggest the species has either undergone a long-term population decline or experienced a population bottleneck and recent expansion. Either scenario suggests a vulnerability to overexploitation, given the species' longevity and low reproductive potential. However, additional genetic studies are needed to better understand these patterns (Garcia et al. 2015).

Demography

Information on natural mortality rates or the intrinsic rate of population increase of the spiny angel shark is currently unavailable.

Historical and Current Distribution and Population Abundance

In northern Argentina, spiny angel sharks are considered to be a eurythermic coastal shelf species with highest abundances on the outer coastal shelf between depths of 28.9 m and 49.6 m (Jaureguizar et al. 2006). In the Rio de la Plata estuary, Argentina, spiny angel sharks were present most frequently in the deepest estuarine zone (12.6 m-16 m) with salinities between 25 and 34 psu. They are not considered a

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permanent resident of the estuary, with abundances higher in the summer than during the spring and fall (Jaureguizar et al. 2003).

In the AUCFZ, spiny angel shark distribution appears to be influenced by temperature, with clear avoidance of water temperatures below 5 degC and above 20 degC (Voumlgler et al. 2008). Specifically, Voumlgler et al. (2008) found that spiny angel sharks concentrate in water temperatures between 13.2 degC and 18.5 degC in the spring and between 7.0 degC and 15.0 degC in the fall. They prefer salinities between 33.4 and 33.5, with avoidance of salinities below 33.0 and above 34.0. Additionally, a strong association was found between spiny angel shark presence and thermal horizontal fronts, which indicates that temperature is the principal environmental variable that influences distribution (Voumlgler et al. 2008). In Rio de la Plata, in the AUCFZ, spiny angel shark densities are particularly high along the Uruguayan coast in the spring, which is thought to be related to the presence of higher salinity waters on the Uruguayan coast than the Argentine coast during this season (Colonello et al. 2007).

In southern Brazil, spiny angel sharks are considered a resident species (Vooren 1997). From 1980-1984 spiny angel sharks were common year round on the southern shelf (at depths between 10 m and 100 m) from Solidatildeo to Chuiacute, with some areas recording CPUE densities as high as 50 kg/h (Vooren and Klippel 2005a). According to Vooren and Klippel (2005a), a portion of the S. guggenheim population makes seasonal migrations across the continental shelf, which is related to the 3-year reproductive cycle of the species (i.e., one third of adult females in the population will migrate per year to give birth). Specifically, this inshore migration is into depths between 10 m and 40 m and occurs in the spring and summer (September-March) for pupping and likely mating purposes (as adults of both sexes conduct this migration in addition to pregnant females) (Vooren 1997; Miranda and Vooren 2003). As mentioned previously, newborns remain in these shallow waters (28 m in length), which focus effort on the inner and outer continental shelf (habitat for larger juveniles and adults of the species), experienced declines in CPUE of angel sharks of around 44 and 50 percent, respectively (Massa and Hozbor 2003).

Current fishing pressure remains high on the spiny angel shark in Argentinian waters. In fact, recent landings of angel sharks, and just from the AUCFZ portion of the species' Argentinian range, suggest total Argentinian landings have likely been of similar magnitude as those totals reported in the 1990s (CTMFM 2015). In 2010, total landings in the AUCFZ amounted to 3,763 t and were over 3,000 t in 2011. In 2012, landings were 2,736 t and by 2013 and 2014 dropped to below 2,300 t (CTMFM 2015). Although landings have remained high in recent years, they also appear to be on a declining trend. Given that catch levels in the 1990s, which resulted in declines of up to 58 percent in the species' abundance, remained at similar levels in 2010 and 2011, suggests that the decrease in landings may likely be a result of a declining spiny angel shark population as opposed to a decrease in fishing effort. In fact, since 2006, the total number of vessels in Argentina's fishing fleet has remained fairly stable (OECD 2014), and, as of June 2014, there were 635 vessels authorized to operate in the AUCFZ, with more than half of these vessels identified as trawlers (CTMFM 2015). Additionally, of the 635 vessels, around 20 percent identified as coastal vessels, suggesting that fishing pressure and associated fishery-related mortality will continue to be a threat to all life stages of the species into the foreseeable future.

In Uruguay, spiny angel sharks are captured by industrial trawling fleets in coastal and offshore waters (Voumlgler et al. 2008). They are bycatch species in bottom longline, estuarine gillnet, and some trawl fisheries, but they are also targeted in oceanic gillnet and bottom trawl fisheries (Domingo et al. 2008). The Uruguayan artisanal and industrial trawling fleets primarily operate at depths between 10 m and 200 m, which covers the entire depth range of the spiny angel shark. Annual catches of angel sharks in Uruguay were less than 100 t from 1977 to 1996 and ranged between 200 t and 400 t between 1997 and 2005, with the majority likely spiny angel sharks (Domingo et al. 2008). Currently, Uruguay has a fishing fleet of 62 vessels operating within the AUFCZ, with Uruguayan vessels responsible for around 5.6-7.5 percent of the total angel shark landings from this area from 2010 to 2013. In 2014, this proportion sharply increased to 18.4 percent as did the total number of landings (from 26 t in 2012 to 142 t and 158 t in 2013 and 2014, respectively) indicating a potential increasing trend in the exploitation of the spiny angel shark by Uruguayan fishing vessels.

In southern Brazil, spiny angel sharks have been heavily fished by industrial trawlers and gillnet fleets for the past few decades (Haimovici 1998; Voumlgler et al. 2008). In fact, mean annual landings of all angel sharks (of which the majority were likely S. guggenheim) were over 2000 t from 1985 to 1994, with a peak of 2,296 t in 1993. Given the depth and distribution of S. guggenheim on the Plataforma Sul, (which likely extends from 200 m (Klippel et al. 2005). The removal of primarily juveniles from a population can have significant negative impacts on recruitment, especially for a species with a 3-year reproductive cycle. And, in fact, in a 2005 bottom trawl survey conducted in the coastal waters of the Plataforma Sul between Torres and Chuiacute, only neonate spiny angel sharks were caught, despite the fact that both juveniles and adults would be expected within the trawled depth range (7 m-20 m) (Vooren et al. 2005b). The CPUE of S. guggenheim was also low compared to historical estimates, with an estimate of only 0.18 kg/h (Vooren et al. 2005b).

Despite the decreases observed in spiny angel shark abundance on the Plataforma Sul, fishing effort remains high. Additionally, all life stages of spiny angel sharks are susceptible to the industrial shelf fisheries as the fleets operate year round covering the entire depth distribution of the species. In fact, in 2002, it was estimated that the fishing effort of the industrial trawl fleet from Rio Grande do Sul and Santa Catarina (the two largest fishing fleets operating on the Plataforma Sul) trawled around 141,000 km\2\, corresponding to approximately 50 percent of the land area of the state of Rio Grande do Sul (Klippel et al. 2005). Hypothetically, if the area swept by each trawl vessel was different, the 100,907 km\2\ of the Plataforma Sul would be completely swept every 9 months (Klippel et al. 2005). When considering the number of gillnet vessels, nets, and the total length of these nets operating on the Plataforma Sul, it was estimated that the length of these gillnets (combined) would equate to around 8,250 km, which corresponds to approximately the entire length of the Brazilian coast (Klippel et al. 2005). In 2002, a total of 892 t of angel sharks were landed, with 62 percent landed in Santa Catarina and 38 percent in the Rio Grande do Sul. The oceanic gillnet fleet was responsible for most of the landings (42 percent), followed by double-

rig trawl fleet (25 percent), and the coastal gillnet, pair, and single trawl fleets, which each contributed about 10 percent of the landings (Klippel et al. 2005). These fleets, which historically contributed to the decline in S. guggenheim on the Plataforma Sul, remain active today.

Furthermore, as previously discussed in the other species assessments, these fleets operate at high efforts on the Plataforma Sul and especially within important coastal nursery and inner shelf habitats for the species. Although landings of the species are currently prohibited, the fleets' extensive operations will continue to contribute to the fishing mortality of all life stages of

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the species as the spiny angel shark likely has high discard mortality rates based on rates estimated for similar angel shark species. For example, the at-vessel mortality rate reported for the African angelshark (S. africana) is 60 percent in prawn trawlers (Fennessy 1994) and 67 percent in protective shark gillnets (Shelmerdine and Cliff 2006). For the Australian angel shark (S. australis), mortality rate estimates of 25 percent and 34 percent have been reported for sharks caught in gillnets (Reid and Krogh 1992; Braccini et al. 2012). These two angel shark species have similar life history traits and ecology, including: Reproductive characteristics (ovoviviparous and produce small litters; Compagno 1984; Rowling et al. 2010), maturity and maximum sizes (Compagno 1984), depth distribution (continental shelf and upper slope), behavior, and diet (mainly teleosts; Shelmerddine and Cliff 2006; Rowling et al. 2010). Given the general similarities, it seems reasonable to infer similar discard survival rates for the spiny angel shark from these other two Squatina species. As such, given the sensitive life history traits of the spiny angel shark as well as the evidence of significant population declines, an assumed 60 percent at-vessel mortality rate in trawl fisheries and 25-

67 percent mortality in gillnets is likely to significantly contribute to the overutilization of the species and increase its extinction risk.

These industrial trawl and gillnet fleets currently participate in nationally important fisheries and, as such, the threat they pose to S. guggenheim is unlikely to decrease in the foreseeable future. In fact, in the oceanic drift gillnet fishery, the fishery responsible for the highest landings of angel sharks, the main fish species targeted (Umbrina canosai, Cynoscion guatucupa, and Micropogonias furnieri) represented around 12.8 percent of the total national marine fish landings in 2011 for all of Brazil. Micropogonias furnieri is the second most landed fish nationally, and U. canosai is the seventh most landed. Based on the above information, the significant level of fishing effort and associated fishing mortality, especially of juvenile angel sharks, likely caused and will continue to cause substantial declines in the spiny angel shark population.

Inadequacy of Existing Regulatory Mechanisms

In the AUCFZ, the area comprising around one quarter of the species' range, and where survey data suggest the species is likely at highest concentration (Jaureguizar et al. 2006; Colonello et al. 2007; Massa and Hozbor 2008; Vogler et al. 2008), spiny angel sharks are commercially exploited. Similar to the narrownose smoothhound, the CTMFM manages this exploitation through the implementation of catch limits and fishery closures. As stated previously, the CTMFM implements an annual prohibition against demersal trawling in a large section of the AUCFZ, extending across the continental shelf, in order to protect vulnerable chondrichthyans from fishery-related mortality. The CTMFM also establishes additional area closures to trawling gear throughout the year in the AUCFZ to protect other species, with these closures also indirectly protecting spiny angel sharks from further fishery-

related mortality from trawl gear. In terms of the direct management of spiny angel sharks, since 2012, the CTMFM has set a total permissible catch limit for all Squatina spp. at 2,600 t (Res. Ndeg 8/14, Res. Ndeg 10/13, Res. Ndeg 10/12). In November 2012, this limit was met and landings of Squatina spp. were banned for the month of December (Res. Ndeg 13/12). In 2013, an additional reserve of 400 t was proposed to be allowed if the 2,600 t limit was reached; however, total landings had decreased from the previous year to 2,103 t (CTMFM 2015). In 2014 a 10 percent increase in total allowable catch was allowed to be added to the limit if the CTMFM saw fit (Res. Ndeg 10/13, Res. Ndeg 8/14); but this was unnecessary as landings amounted to only 2,281 t (CTMFM 2015). In 2015, the CTMFM kept the same limit that was implemented in 2014 (2,600 t with an allowance of 10 percent increase; Res. Ndeg 07/15). Although McCormack et al. (2007) report that elasmobranch quotas and size regulations are largely ignored in Argentina and poorly enforced, Squatina landings have been below the maximum catch limit in recent years, providing evidence that regulations are potentially being followed. However, without effort information, it is unclear whether these regulations and the corresponding decreases in landings can be attributed to adequate control of the exploitation of the species or rather reflects the lower abundance of the species from declining populations, or more likely a combination of the two scenarios.

In Uruguay, regulations that likely contribute to decreasing the fishery-related mortality of the species include a summer trawling ban in 25 m to 50 m depths between La Paloma and Chuy and specific fishery area closures in the spring, summer, and autumn on the Uruguayan continental shelf, designated to protect juvenile hake (Merluccius hubbsi) (Pereyra et al. 2008). Although the depth distribution of the spiny angel shark in Uruguayan waters is unresolved, in southern Brazilian waters, the species was previously common year-round at depths between 10 m and 100 m. Specifically, adults were frequently found in waters between 40 m and 100 m during the autumn and winter and between 10 m and 40 m in the spring and summer; and both adults and juveniles were abundant in depths of 40 m-60 m year-round (Vooren 1997; Miranda and Vooren 2003; Vooren and Klippel 2005a). In northern Argentina, spiny angel sharks displayed highest abundances on the outer coastal shelf between 29 m and 50 m depths (Jaureguizar et al. 2006). Using the above depth distribution in areas just north and south of Uruguay as a proxy for the species' depth distribution in Uruguayan waters, it is likely that the proposed fishery closures and trawling bans will provide some level of protection from fishery-related mortality, especially during the species' spring/summer migration to shallower waters for pupping and potentially mating purposes.

The spiny angel shark is also listed as a species of high priority in Uruguay's FAO NPOA-sharks (Domingo et al. 2008). The plan, as stated previously, has set goals to collect the necessary information on its priority species in order to conduct abundance assessments, review current fishing licenses, and promote public awareness to release captured individuals. However, no updated results from the goals and priorities of this plan could be found.

In Brazil, the spiny angel shark is listed on Annex 1 of Brazil's endangered species list and classified as critically endangered (Directive Ndeg 445). As described in previous species accounts, an Annex 1 listing prohibits the catch of the species except for scientific purposes, which requires a special license from IBAMA. There is also a prohibition of trawl fishing within three nautical miles from the coast of southern Brazil, although the enforcement of this prohibition has been noted as difficult (Chiaramonte and Vooren 2007). In addition, the species is still susceptible to being caught as bycatch in the legally permitted coastal gillnet fisheries and offshore trawl and gillnet fisheries and vulnerable to the associated bycatch mortality (Lessa and Vooren 2007). The spiny angelshark is also listed as one of the 12 species of concern under Brazil's FAO NPOA-sharks and would benefit from the proposed fishing closures and other

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management measures outlined in the plan. This includes the fishing moratorium and marketing ban, which is proposed to be in effect until there is scientific evidence that supports population recovery of the spiny angel shark. It also suggests that a fishing exclusion area be established in the coastal zone (specifically over a large region of the coast of Rio Grande do Sul at depths of 20 m) to protect important nursery grounds for the species. However, as mentioned previously, the plan was only just approved as of December 2014 and will not be fully implemented for another 5 years. Thus, the implementation and effectiveness of the recommendations outlined in the plan remain uncertain, with the best available information indicating that current regulatory measures in Brazil to protect vulnerable species are poorly enforced.

Extinction Risk

The best available information provides multiple lines of evidence indicating that the S. guggenheim currently faces a moderate risk of extinction. Below, we present the demographic risk analysis, threats assessment, and the overall risk of extinction for the spiny angel shark.

Demographic Risk Analysis

Abundance

Spiny angel sharks are likely the most abundant angel shark species from southern Brazil to Argentina; however, current quantitative estimates of abundance of the species throughout its range are unavailable. In Argentina, the abundance of spiny angel sharks in the San Matiacuteas Gulf (which comprises around 9.6 percent of the species' range) was estimated to be 192.53 t in 1993. In 2003, the estimated biomass of spiny angel sharks for all of coastal Argentina was 23,600 t. No other population estimates have been calculated for the species. Additionally, between 1981 and 2004, catch rates and density estimates for areas off the Argentine continental shelf have been variable; however, fishing fleets reported declines of up to 58 percent in CPUE between 1992 and 1998.

In Brazil, quantitative information, in the form of CPUE and landings data for the fishing fleets operating on the Plataforma Sul, is available for all angel shark species, of which S. guggenheim likely comprises a majority. These data provide insight into trends in abundance of the spiny angel shark in roughly 20 percent of its range. Based on a comparison of the CPUE estimates of angel sharks caught on the Plataforma Sul in both the single and pair trawl fishing fleets over the time periods of 1980-1988 and 1997-2002, the population of S. guggenheim off southern Brazil has declined by around 85 percent since 1985 (Miranda and Vooren 2003; Vooren and Klippel 2005a). More recent landings data from the Santa Catarina oceanic gillnet fishery, covering the years 2001-2010, show a peak in angel shark landings in 2004 of 340 mt before significantly dropping, with only 2.6 mt landed in 2010. However, in 2004, landings of S. guggenheim along with S. occulta were prohibited and, as such, the decline in landings data after 2004 may be a reflection of this prohibition.

Based on the commercial fishery information, it is likely that spiny angel sharks have experienced varying levels of population decline throughout its range. In the northern half of the species' range (off Brazil), the best available information indicates the species has undergone rather substantial population declines, with evidence of negative population growth rates that led to significant decreases in the overall abundance of the species to the point where catch rates and observations of spiny angel sharks are extremely low. Off Uruguay and Argentina, where reported biomass estimates suggest the species was and is likely still most concentrated, the higher abundance levels may explain why the magnitude of population decline is estimated to be smaller in this portion of the species' range. Therefore, while the species may not be of such low abundance such that it is currently at risk of extinction, given the high exploitation of the species throughout its range and subsequent population decline in the northern half, coupled with the species' low productivity, abundance levels will likely continue to decline through the foreseeable future to the point where it may be a significant contributing factor to the species' overall extinction risk.

Growth Rate/Productivity

There is minimal information on the growth rate and productivity of the species. Based on the estimated von Bertalanffy growth parameters, the spiny angel shark exhibits rather fast growth rates for a shark species (with a growth coefficient (k) of 0.275/year; Vooren and Klippel 2005a). Fast growth rates help protect species from extinction by allowing species to attain larger sizes at earlier ages, protecting it from predation, and also allowing species to attain sexual maturity sooner, thereby contributing to population growth. The fast growth rates of the spiny angel shark likely led to the species being the most common angel shark found in the southwest Atlantic. However, despite its fast growth rates, the spiny angel shark has a significantly lengthy reproductive cycle of 3 years, with a litter size ranging between 2 and 8 pups and an average of around 4-5 pups/litter. This translates to an annual fecundity between 0.67 and 2.67 pups per year. Spiny angel sharks are also thought to have cloacal gestation during the latter half of pregnancy, which is thought to be the reason why Squatina species are observed easily aborting embryos during capture or handling. Given the already low annual fecundity of the species, any further loss of embryos would significantly decrease their already low reproductive output. Overall, these reproductive characteristics suggest the species has relatively low productivity, similar to other elasmobranch species, which may hinder the species' ability to quickly rebound from threats that decrease its abundance (such as overutilization) and render the spiny angel shark more vulnerable to extinction in the face of other demographic risks and threats.

Spatial Structure/Connectivity

The spiny angel shark has a widespread range in the southwest Atlantic but is thought to be comprised of smaller, more localized populations (Chiaramonte and Vooren 2007); however, information to support this is currently unavailable. Information on the connectivity among S. guggenheim populations throughout its range is limited. The populations occurring on the Plataforma Sul, off southern Brazil, are assumed to carry out their entire lifecycle within the same area. This behavior indicates that these populations maintain population growth by recruiting within each area without producing a necessary excess of recruits with the potential to migrate to other areas (Vooren and Klippel 2005a). As a result, S. guggenheim populations on the Plataforma Sul likely have limited movement and dispersal migration between neighboring populations, with migrants having no impact on the short term abundance of a population. Based on genetic studies, there is also evidence of limited connectivity between populations found in other parts of the species' range. For example, genetic analyses of individuals found around the Rio de la Plata estuary indicate a high level of population genetic structure between the spiny angel sharks that occur on the outer shelf and those that are found in the outer estuarine and coastal waters (with very few immigrants between these

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populations) (Garcia et al. 2015). In other words, the evidence of limited inter-population exchange observed in the species reduces the recovery potential for the depleted and small local populations found throughout the range, and may increase the risk of local extirpations, possibly leading to complete extinction.

Diversity

A recent genetic analysis using maternally-inherited mitochondrial DNA markers from spiny angel sharks in and around the Rio de la Plata Estuary (approximately mid point of the species' range) found no evidence of population genetic structuring (Garcia et al. 2015). However, analyses using biparentally-inherited nuclear recombinant DNA genes indicated that there was a remarkably high level of population genetic structure between spiny angel sharks found on outer shelf and those in the coastal and outer estuarine areas (Garcia et al. 2015). The combination of low haplotype and high nucleotide diversity can be indicative of a transient bottleneck in the ancestral population, or an admixture of samples from small, geographically subdivided populations, with the genetic patterns of exchange potentially explained by sex-

biased behavior or long term shifts in spatial and temporal environmental variables leading to current displacements (Garcia et al. 2015). However, overall, the low levels of genetic diversity in spiny angel shark populations suggest a vulnerability to overexploitation in the southwestern Atlantic Ocean (Garcia et al. 2015) and will likely render the spiny angel shark more susceptible to extinction in the face of other demographic risks and threats.

Threats Assessment

The primary threat to S. guggenheim is overutilization in artisanal and commercial fisheries. The vast majority of fisheries information on angel sharks is generally reported as ``Squatina spp'' throughout Brazil, Uruguay, and Argentina; however, spiny angel sharks are thought to be the most abundant angel shark species from southern Brazil to Argentina and, therefore, likely comprise the majority of the Squatina species that are landed.

In Argentina, although the species is not directly targeted, they are caught incidentally in multispecies artisanal shark fisheries and are considered a valuable bycatch species (Chiaramonte 1998; Bornatowski et al. 2011). Fishery-independent research surveys have recorded relatively high densities of the species on the Argentinian shelf; however, based on CPUE data, the population saw declines of up to 58 percent in the late 1990s. Although exploitation of the species in the AUCFZ, where the species appears to be at highest concentration, has been managed since 2012 with area closures and catch limits, the lack of recent abundance estimates or trends hinders an evaluation of the adequacy of current regulatory measures in preventing the overutilization of the species from this portion of its range. It is important to note that landings prior to 2012 from this area were on the same order of magnitude as those reported for all of Argentina and which subsequently led to the declines observed in the late 1990s. Landings have since decreased since the implementation of the catch limits, and appear to be on a declining trend; however, the number of fishing vessels authorized to operate in the AUCFZ has remained fairly stable, potentially indicating that fishing effort has not decreased substantially in recent years. In other words, the recent declining trend in landings, even below total allowable catch limits, may indicate decreasing abundance of the species in this part of its range.

In Uruguay, spiny angel sharks are both targeted and caught as bycatch by industrial trawling fleets in coastal and offshore waters (Voumlgler et al. 2008; Domingo et al. 2008). All life stages of the species are exploited as the fleets operate over the entire depth range of the species (between 10 m and 200 m). Abundance and trends of the species within this region are unknown; however, declines in populations just north and south of this region have been observed, with the species listed as high priority in Uruguay's FAO NPOA-sharks. Additionally, landings of angel sharks by Uruguayan vessels in the AUCFZ have increased in both number and proportion of total angel shark landings in the AUCFZ, indicating a potential increase in fishing effort of this vulnerable species.

In Brazil, spiny angel sharks have been heavily exploited by industrial trawlers and gillnet fleets since the 1980s (Haimovici 1998; Voumlgler et al. 2008). In southern Brazil, angel shark landings are recorded in industrial single trawl, pair trawl, oceanic bottom gillnet, and coastal artisanal fisheries. These industrial and coastal artisanal fleets operate year round in depths that span 500 m) (Perez and Pezzuto 2006 cited in Perez et al. 2009). Brazilian trawlers concentrated their activities on the shelf break (at 100-200 m) while chartered gillnet vessels concentrated their efforts in deeper areas of the upper slope (at 300-400 m). As a result of this expansion of fishing activities into deeper waters, deep-water monkfish (Lophius gastrophysus) was the first fishing resource that proved abundant enough to sustain profitable deepwater fishing operations off southern Brazil, and thus a targeted fishery developed for the species. In 2001, a total of 7,094 t of monkfish were landed, mostly by national double-rig trawlers (58 percent) and foreign chartered gillnetters (36 percent) operating in a fishing area that extended along the southern Brazilian slope, from 21deg S. to 34deg S. and within the 100-600 m isobaths (Perez et al. 2005). Monkfish biomass also happened to be concentrated between 125 m and 350 m depths, which overlaps with the principal depth distribution of the Argentine angel shark (120 m-320 m). As a result, Argentine angel sharks were reported as a significant bycatch species in the monkfish gillnet fishery. In fact, Perez and Warhlich (2005) noted that S. argentina was one of the most retained bycatch species in the monkfish gillnet fishery, with bycatch estimated at 1.052 per 100 nets in 2001 (total 8,698 individuals). This fishing regime that contributed to the significant bycatch of Argentine angel shark continued operating at high levels through most of the following year (2002), with monkfish landings of 5,129 t (Perez et al. 2009). The numerous incidental catches produced by monkfish gillnetting suggests that the development of this fishery off southern Brazil substantially increased the levels of fishery-related mortality in the S. argentina population and potentially introduced adverse effects in the recruitment process (i.e., recruitment overfishing), especially considering that the species' reproductive cycle may exceed 1 year (Cousseau and Perrota 1998 cited in Perez and Warhlich 2005). In fact, research bottom trawl surveys of the outer shelf and upper slope from Cape Santa Marta Grande to Chuiacute (the main habitat of Argentine angel sharks) found decreases in both the CPUE and frequency of occurrence of Argentine angel sharks during the winter and fall seasons between the years 1986/87 and 2001/02. Specifically, these surveys detected declines of 75 and 96 percent in S. argentina CPUE (kg/hour) and frequency of occurrence, respectively, during the winter months, and declines of 97 and 63 percent, respectively, during the fall surveys. These declines confirm that the abundance of S. argentina in southern Brazil decreased by roughly 80 percent from its original level as a result of recruitment overfishing, primarily due to the bottom gillnet fishery (Vooren and Lamoacutenaca 2002; Vooren and Klippel 2005a).

In 2003, the fishery regime changed, as the foreign chartered vessels abandoned Brazilian waters as a result of conflicts with national trawlers (Perez et al. 2009). Since then, exploitation has been maintained mostly by double-rig trawlers along with a few vessels of the national fleet transformed to fish with the new gillnet technology (Wahrlich et al. 2004 cited in Perez et al. 2009). Landings of monkfish decreased by roughly 50 percent from 2002 to 2003, and have remained stable around 2,500 t ever since (Perez et al. 2009). The large reduction in monkfish biomass after 2002 (and the stabilization at biologically insecure levels thereafter) is largely attributed to the fact that landed catches have been systematically higher than maximum recommended catches (Perez, 2007a; Anon 2007 cited in Perez et al. 2009). In 2004, the monkfish fishery was declared overexploited, with subsequent biomass assessments lacking any signs of recovery for the monkfish stock (Perez et al. 2009). Given the significant bycatch of Argentine angel sharks in the monkfish fishery in 2001, and the subsequent 80 percent decline in the angel shark population by 2002, the continued intense exploitation by the monkfish fishery within the Argentine angel shark habitat likely contributed to further abundance declines of S. argentina after 2002. This is especially probable considering the fact that the fishery operates on the outer and upper slope areas of the continental shelf, where the Argentine angel shark reproduces and likely carries out its entire lifecycle. Thus, the significant increase in fishing effort on the outer shelf and slope areas, particularly by the monkfish fishery, likely impacted all life stages of the species, resulting in recruitment overfishing and, ultimately, overutilization of the species leading to a significant population decline.

Argentine angel sharks are still likely susceptible to fishing pressure in the monkfish fishery, as the fishery is still operational today. Recent landings of monkfish for years 2009, 2010, and 2011 were 2,744 mt, 2,592 mt and 2,616 mt, respectively (IBAMA 2011). While this is a large reduction from peak landings in 2001 of 7,094 mt, Argentine angel sharks of all life stages are likely still bycaught by this fishery, which may limit the species from recovering from its initial 80 percent population decline, especially considering the species' low productivity. In addition, the Argentine angel shark likely has high discard mortality rates based on rates estimated for similar angel shark species (see spiny angel shark--Threats Assessment). Given general similarities between the Argentine angel shark and other Squatina species, it seems reasonable to infer similar discard survival rates for the Argentine angel shark (i.e., ~60 percent at-vessel

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mortality rate in trawl fisheries and ~25-67 percent mortality in gillnets).

Thus, while the bottom gillnet fishery specifically targeting monkfish has been restricted in terms of overall effort, with only the national trawl fleet continuing to operate on the upper slope (Perez et al. 2009), the threat of overutilization remains. However, the monkfish fishery is not the only fishery presently operating within the Argentine angel shark habitat. There are a number of oceanic bottom gillnet fisheries targeting other species (e.g., Umbrina canosai, Cynoscion guatucupa, and Micropogonias furnieri) that currently operate on the shelf and slope at depths of up to 300 m. In fact, due to their effort and fishing area of operation, these oceanic bottom gillnet fisheries now land the majority of angel sharks in Brazil (Klippel et al. 2005). As described in the spiny angel shark assessment, fishing effort (both by trawl and gillnet fleets) on the Plataforma Sul remains high and poorly regulated, and therefore, the susceptibility of the species' to fishery-related mortality also remains high. As such, given the best available information and the above analysis, we conclude that overutilization is a factor that is significantly contributing to the extinction risk of the species.

Inadequacy of Existing Regulatory Mechanisms

In Argentina, catches of angel sharks are regulated through annual catch limits and fisheries closures. Since 2013, Squatina landings have been below the maximum catch limit in recent years, providing evidence that regulations are potentially being followed. However, without effort information, it is unclear whether these regulations are adequately controlling the exploitation of angel sharks and given that Argentine angel sharks are particularly rare in Argentina, the degree to which these regulations are decreasing the threat of overutilization of the species in this portion of its range is uncertain.

In Uruguay, the Argentine angel shark is listed as a species of high priority in the country's FAO NPOA-sharks (Domingo et al. 2008). The plan, as stated previously, has set goals to collect the necessary information on its priority species in order to conduct abundance assessments, review current fishing licenses, and promote public awareness to release captured individuals. However, no updated results from the goals and priorities of this plan could be found.

Like the spiny angel shark, and other species described previously in this proposed rule, the Argentine angel shark was listed as ``critically endangered'' under Annex I of Brazil's endangered species list in 2004. As described in previous species assessments, an Annex 1 listing prohibits the catch of the species except for scientific purposes, which requires a special license from IBAMA. There is also a prohibition of trawl fishing within three nautical miles from the coast of southern Brazil, although enforcement of this prohibition has been noted as difficult (Chiaramonte and Vooren 2007), and moreover, the ban only covers depths of -1 with a theoretical maximum size (Linfin) of 169.9 cm TL and an estimated size-at-birth (L0) of 6.1 cm. Arkhipkin et al. (2008), using samples collected only off the Falkland Islands, reported a lower growth rate (k) of 0.02 year-1, with a maximum theoretical size (Linfin) of 313.4 cm total length. Growth rates of graytail skate begin around 5.6 cm/year for the first 9 years of life and decline to 4.3 cm/year between 14 and 20 years old (Arkhipkin et al. 2008). In comparison, a study of caudal thorn band counts and vertebral centra ring counts found that the most accurate von Bertalanffy growth parameters came from the vertebral centra with the relative growth rate (k) based on vertebrae centra to be 0.033 year-1 with a theoretical maximum size (Linfin) of 219.7 cm total length (Gallagher 2000). However, based on observed size data, these parameters still slightly underestimate growth (Gallagher 2000).

Little is known about the reproduction of the graytail skate (Saacutenchez and Mabragantildea 2002) and available age and growth studies from the same region provide conflicting estimates for length and age at maturity. For example, in the Falkland Islands, Gallagher (2000) estimated a total length at 50 percent maturity of 120.7 cm for both sexes, with males and females maturing after 17.6 and 24.8 years respectively. Arkhipkin et al. (2008) estimated a total length at 50 percent maturity to be 108.2 cm for females and 94.5 cm for males, with age at maturity of 14 years for males and 17.8 years for females. Based on commercial fleet observer and research cruise data collected around the Falkland Islands, males reached 50 percent maturity at a disc width of 76-77 cm (Agnew et al. 2000; Wakeford et al. 2005). A Falkland Islands study of graytail skate suggests that graytail skate females may spawn year-round with a weak spawning peak in the spring and summer months observed (Arkhipkin et al. 2008). Around the Falkland Islands, the spawning grounds of the graytail skate can be found northwest of the islands in deep waters, close to the edge of the continental shelf between 200 and 300 m deep (Arkhipkin et al. 2008) and in waters south of 51deg latitude (Dr. Andreas Winter, Falkland Islands Fisheries Stock Assessment Scientist, personal communication 2015). Based on catches of the smallest skates, it is thought that hatchlings have disc widths between 9 cm and 12 cm (Brickle et al. 2003; Arkhipkin et al. 2008).

Genetics and Population Structure

Studies examining the genetics of the species or information on its population structure could not be found.

Demography

Little is known about the population growth and natural mortality of the graytail skate. However, based on the life history parameters described previously, like other elasmobranchs, the graytail skate is a K-selected species with slow growth rates and late age at maturity, which is indicative of low productivity (Gallagher 2000; Buumlcker 2006; Arkhipkin et al. 2008).

Historical and Current Distribution and Population Abundance

Graytail skate occur on the continental shelf and slope in the southwestern Atlantic Ocean, south of 34deg S. and in the southeastern Pacific Ocean, south of 39deg S. (Figueroa et al. 1999; Saacuteez and Lamilla 2004). In the Falkland Islands, graytail skate are caught in cool, deep waters on the slopes of the continental shelf break, making them more common to the west of the islands (Agnew et al. 1999; Arkhipkin et al. 2008; Arkhipkin et al. 2012). Outside the Falkland Islands, on the Patagonian shelf, they are more commonly found on the northwestern outer shelf and northern shelf and slope (Figueroa et al. 1999; Arkhipkin et al. 2012). In Argentina, graytail skate are found on the continental shelf and slope around Argentina south of 37deg S. and 41deg S. respectively (McCormack et al. 2007), where they exhibit strict stenothermic and stenohaline behavior. In other words, the species appears to tolerate very narrow ranges of temperature and salinity (Figueroa et al. 1999), with catch data that suggest that the species occurs at water temperatures below 6 degC (Menni and Lopez 1984; Colonello and Massa 2004) and salinity above 33.9 psu (Colonello and Massa 2004).

Throughout their range, graytail skates are found at depths between 106 m and 1,010 m, but have been caught as shallow as 77 m in Argentine waters (Buumlcker 2006). Graytail skate are typically most common at depths below 300 m (Bigelow and Schroeder 1965; Menni and Lopez 1984; Brickle et al. 2003; Laptikhovsky et al. 2005; Wakeford et al. 2005; Arkhipkin et al. 2008; Arkhipkin et al. 2012). However, in Argentina, the highest density of graytail skate catches was reported at depths of 120 m on the Argentina platform between 45deg S. and 41deg S. during the late winter and early spring months (Colonello and Massa, 2004). As graytail skates mature, they display an ontogenetic shift in depth preference (Arkhipkin et al. 2008). For example, in Falkland Islands waters, hatchlings occupy nursery grounds of approximately 300 m-350 m depth, but transition to deeper waters of 400 m-600 m as juveniles (Arkhipkin et al. 2008). At 20 cm-30 cm DW, some individuals migrate up to shallower depths of 200 m-400 m, while others move into water deeper than 600 m (Arkhipkin et al. 2008). Skates 80 cm-90 cm DW or larger occur most commonly at depths of 400 m-600 m (Arkhipkin et al. 2008). Despite these depth changes, studies around the Falkland Islands have shown little evidence of large spatial or temporal movements, which could indicate that graytail skates carry out their entire life cycle within the waters where they hatch (Agnew et al. 2000; Wakeford et al. 2005; Winter et al. unpublished).

Range-wide abundance estimates for graytail skate are not available; however, biomass estimates exist for the populations off the Falkland Islands and Argentina. In the Falkland Islands, graytail skate were part of the fish assemblage of both the southern and northern skate and ray stocks. They were particularly abundant south of the islands, making them dominant in catches of the southern skate and ray assemblage. However, due to declining CPUEs of the southern stock, especially for graytail skate, the southern rajid fishery was closed in 1996 (Agnew et al. 1999; Agnew et al. 2000; Wakeford et al. 2005). Current biomass estimates from this area could not be found. North of

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the Falkland Islands, declines in the CPUE of graytail skate were also observed between 1992 and 2001 (Wakeford et al. 2005); however, based on recent biomass estimates, the population appears to have recovered and stabilized. Specifically, analysis of 2010 fishery survey cruise data resulted in an estimated biomass of graytail skate of 7,232 t, which is consistent with the earlier biomass estimates for the species from the 1990s (Falkland Islands Government 2011). As this biomass estimate is just for the graytail skate population north of the Falkland Islands, it is likely a significant underestimation of the total biomass for the entire Falkland Islands population, especially considering the southern stock, which was historically more abundant, has been protected from targeted fishing since 1996.

In 2002, Saacutenchez and Mabragantildea (2002) estimated the population abundance of the graytail skate on the continental Argentine shelf between 48deg S. and 55deg S. to be 259,210 individuals, or 2,431.98 t. This estimate was calculated prior to the apparent recovery of the graytail skate in the Falkland Islands and also corresponds to when CPUE of the graytail skate was at its minimum in the Falkland Islands (Wakeford et al. 2005). As such, it could be assumed that biomass has since increased on the shelf; however, with no recent abundance estimates available, the trends within this portion of the species' range cannot be determined with certainty.

Farther north on the Argentine shelf, between 45deg S. and 41deg S., the biomass of graytail skate was estimated to be 503 t in 2004, but had a large confidence interval (2,237 t), with an average density of the species of 0.05 t/nm\2\ (Colonello and Massa 2004). More recent estimates or trends in population abundance or biomass levels for graytail skate are not available.

There is very little information pertaining to the presence of graytail skate in Uruguayan and Chilean waters. No information on commercial, recreational, or research catches of graytail skate is available from Uruguay. Likewise, there is no estimate of abundance from this area. In Chile, graytail skate are found south of 41deg S. and at depths of 137 m to 595 m (McCormack et al. 2007). In 1995, Saez and Lamilla (2004) caught 42 graytail skate between March and December at 350 m depth approximately 20 miles from Punta Galera; however, no other information is available on scientific or commercial catch distribution or population abundance from this area.

Summary of Factors Affecting the Graytail Skate

We reviewed the best available information regarding historical, current, and potential threats to the graytail skate species. We find that the main threat to this species is overutilization for commercial purposes; however, we consider the severity of this threat to be greatly reduced by the regulatory mechanisms in place in the Falkland Islands, where the species was historically most heavily exploited. Thus, we find that historical and present levels of utilization are not exceeding the species' biological capacity to sustain current levels of exploitation. We also find that current regulatory measures are adequate to protect the species from further overutilization. Additionally, available information does not indicate that habitat destruction or modification, disease, predation or other natural or manmade factors are operative threats on these species. We summarize information regarding these factors and their interactions below according to section 4(a)(1) of the ESA. See Casselbury and Carlson (2015g) for a more detailed discussion of these factors.

Present or Threatened Destruction, Modification, or Curtailment of Habitat or Range

Trawl fisheries occur throughout the graytail skate's range. Studies show that the interaction of bottom trawling gears with bottom substrate can have negative effects on benthic fish habitat (Valdemarsen et al. 2007). These impacts are often the most serious on hard substrates with organisms that grow up from the bottom, such as corals and sponges, but alterations to soft substrates have also been seen. The trawl doors on bottom otter trawls often cause the most damage to the ocean bottom, but other parts of trawling gear, such as weights, sweeps, and bridles that contact the bottom can also be damaging. Intense fishing disturbance from trawling has reduced the abundance of several benthic species (Valdemarsen et al. 2007); however, there is no specific information available that indicates this habitat modification has had a direct effect on the abundance of the graytail skate, or is specifically responsible for the curtailment of its habitat or range.

Overutilization for Commercial, Recreational, Scientific, or Educational Purposes

Information available on the harvest of the graytail skate indicates that they are most heavily exploited in the Falkland Islands multispecies skate and ray fishery by foreign fleets (Agnew et al. 1999; Falkland Islands Government 2005-2013). Prior to the 1990s, catches from the Falkland Islands were mainly attributed to Spanish vessels fishing in a mixed groundfish fishery, with rajid catches of less than 1,500 t per year (Wakeford et al. 2005). However, in 1989, Korean vessels began to specifically target rajids in this fishery using demersal trawls, and by 1991 catches of skates and rays rose to more than 7,000 t/year (Wakeford et al. 2005). Subsequently, two rather distinct rajid fisheries developed within the Falkland Islands: a southern rajid fishery that fished in a small area south of the Falkland Islands (a ray ``hot spot;'' Agnew et al. 2000), and a northern rajid fishery that operated in a more extensive area to the north of the Falkland Islands (primarily on the slope between 200 m-400 m depths; Wakeford et al. 2005). In the 1990s, the graytail skate was the most important species caught in the Falkland Islands multispecies rajid fisheries based on catch weight, and was estimated to make up approximately 58 percent of the catch in the southern rajid fishery and 39 percent of the catch in the northern rajid fishery between 1993 and 1995 (Agnew et al. 1999; Bizikov et al. 2004). However, with this heavy exploitation on the skate populations by Korean fleets (which were responsible for 88 percent of the directed rajid catch between 1990 and 1997; Agnew et al. 2000), the proportional catches of graytail skate declined in all areas that were fished. This decline was particularly precipitous in the southern batoid aggregation area, where graytail skate spawn (A. Winter, pers. comm. 2015) and had previously comprised the majority of the catch (Agnew et al. 1999). Agnew et al. (2000) calculated that total mortality rates (fishing mortality rates + natural mortality rates) in the northern and southern areas were significantly higher than what could be sustained by the batoid assemblage, particularly graytail skates. Specifically, the authors estimated that graytail skates could sustain total mortality rates of less than 0.3/year; however, the total mortality rate in the northern area from 1991-1995 was on the order of 0.42/year and in the southern area was 0.61/year (Agnew et al. 2000). Consequently, significant declines in CPUE were observed between 1990 and 1997. A steep 58 percent decline was noted in the southern rajid fishery from 1993 to 1996, which was attributed to the decline in graytail skate abundance

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(Agnew et al. 1999, 2000) and declines ranging from 44 to 65 percent were observed for the northern rajid fishery from 1990-1996 (Agnew et al. 2000). For catches of graytail skate, Wakeford et al. (2005) estimated a decline in CPUE of around 70 percent between 1992 and 2001 in the northern rajid fishery, and observer data indicate CPUE of graytail skate continued to decline through 2007 (Winter et al. unpublished). Catches of graytail skate also showed a reduction in average disc width. From 1993-1995, average disc width declined from 52.18 cm to 31.91 cm (Agnew et al. 2000), and based on observer data collected from the Falkland Islands Inner Conservation and Management Zone (located between 49deg S.-54deg S. and 64deg W.-54deg W.), the majority of graytail skate catches in the commercial trawl fishery from 1997-2006 were still relatively small skates with modal disc widths between 25 cm and 40 cm (Arkhipkin et al. 2008). Additionally, about 54 percent of the catches were female skates with disc widths between 10 cm and 80 cm, and the majority were under the estimated size at 50 percent maturity (Arkhipkin et al. 2008).

As a result of the marked declines in CPUE, particularly for the entire southern batoid aggregation, which was presumed to be driven by declines in graytail skate (Agnew et al. 1999, 2000; Wakeford et al. 2005), the southern ray fishery was closed in 1996 and separate skate target trawling licenses and catch limits (of around 3,000 t through the late 1990s) were imposed in the northern ray fishery. Following the implementation of these catch limits, which equated to between 6.5 and 7.6 percent of the estimated pre-exploitation biomass, the northern rajid stock appeared to stabilize by 2000 (Agnew et al. 2000). In fact, based on a stock assessment of the northern skate stock, with updated data through 2014, estimated biomass of the entire stock has gradually and consistently increased since 1996, from a low of 13,641 t in 1989 (95 percent CI: 10,591-24,214), which marked the start of heavy exploitation, to a recent peak high of 34,558 t in 2014 (90 percent CI: 27,284-59,806) (Fisheries Committee 2015). In addition, CPUE of the northern stock has been gradually increasing over the years (Agnew et al. 2000; Falkland Islands Fisheries Committee 2015) whereas targeting of skate and ray species in the Falkland Islands has been decreasing, with a large portion (almost half) of the skate catch now taken as bycatch under finfish licenses (Falkland Islands Government 2014). In fact, the most recent data from the fishery show that in 2014 total skate catch amounted to 5,543.2 t, with 53 percent of this total representing targeted skate catch (Fisheries Committee 2015). Furthermore, even with the proportional increase in bycaught skates and decrease in targeted skate catch, the total skate catch for the fishery appears sustainable as it falls below the Maximum Sustainable Yield (MSY) estimate, which is the theoretical largest catch that can be taken from a stock. Based on the latest stock assessment of the northern skate assemblage, MSY is estimated to be 6,048 t (95 percent CI: 6,198-46,811), which is approximately 8 percent higher than the 2014 total skate catch (Fisheries Committee 2015).

In terms of the graytail skate, despite the reported historical reductions in CPUE, B. griseocauda remains one of the most abundant species caught in the Falkland Islands multispecies skate fishery (Agnew et al. 1999; Arkhipkin et al. 2008; Falkland Islands Government 2005, 2006, 2007, 2008, 2010, 2011, 2012) and presently makes up between 11 percent and 18 percent of the skate trawl catch and bycatch identified by observers (Agnew et al. 2000; Falkland Islands Government 2010, 2011, 2012, 2014). Recent data from the Falkland Islands Government (2012) also indicate that the modal disc width of graytail skate catches has increased to 63 cm in 2012. The increase in modal disc width could be indicative of population recovery for graytail skates in recent years. This is supported by the fact that in 2010, fishery-independent surveys conducted to estimate skate biomass in the northern area of the Falkland Islands (the area that generally yields the highest skate catches by the targeted skate fishery) confirm that total skate biomass, and particularly the predominant skate species, including graytail skate, have remained stable in recent years. Using CPUE as an index of abundance, an analysis incorporating more recent data from 1994 to 2013 revealed that B. griseocauda was in decline until about 2007, with a decrease in CPUE from 120.1 kg/hr in 1994 to 22.6 kg/hr in 2007 (Winter et al. unpublished). However, CPUE has since increased to an estimated 70.1 kg/hr in 2013, similar to levels observed in 1997-2001, with abundance continuing on a positive trend (Winter et al. unpublished). Furthermore, given that these estimates are only for graytail skate in the northern area of the Falkland Islands, it is likely that the total abundance of the Falkland Islands population is significantly higher and has recovered even more so due to the complete ban on commercial skate fishing in the southern batoid aggregation area, where the spawning grounds of the species are mostly located (A. Winter, pers. comm. 2015).

Given the evidence of increasing CPUE and biomass of the northern skate assemblage, skate catch estimates that are below MSY, stable biomass estimates of graytail skate, and increasing abundance and sizes of graytail skates in catches, the current fishing effort and level of exploitation of skates in general, and graytail skate in particular, in the Falkland Islands appears to be sustainable (Falkland Islands Government 2014). In other words, overutilization of the species in this portion of its range is not a threat that is contributing significantly to its risk of extinction.

In Argentina, an active commercial elasmobranch fishery, which exploits sharks, skates, and rays, has shown an increasing trend in both catches and number of vessels reporting skate and ray landings since the early 1990s. Historically, skates and rays were mainly discarded as fisheries bycatch, but are now landed as both target and non-target catch (Chiaramonte 1998; Massa and Hozbor 2003). Specifically, catches have increased from 183 t in 1991 to 13,265 t in 2000, and vessels reporting landings have increased from 69 in 1992 to 377 in 1998 (Saacutenchez and Mabragantildea 2002; Massa and Hozbor 2003). From 1994-1998, Massa and Hozbor (2003) estimated a decline of around 36 percent in the CPUE of large fishing vessels (>28 m in length) for all skates and rays on the Argentine shelf between 34 and 48deg S.; however, the data are not species-specific and deep-water skates, like the graytail skate, are generally not monitored despite the fact that they are under fishing pressure (Massa et al. 2004b). Additionally, the CPUE of skates and rays for smaller fishing vessels (with lengths -1 in Argentinean waters (i.e., low), and 0.02 year-1 to 0.033 year-1 in the Falkland Islands (i.e., very low). Graytail skates are long-lived species, with an estimated lifespan of approximately 28 years, and a maximum disc width of 130 cm. Although age and growth studies from skates in the same region provide conflicting estimates for length and age at maturity, with age of maturity estimates ranging from 14-17.6 years for males and 17.8-24.8 years for females, all estimates indicate a very late age of maturity. While there is some evidence to suggest that graytail skates may reproduce year-round, overall, these reproductive characteristics suggest the species has relatively low productivity, similar to other elasmobranch species, which may hinder its ability to quickly rebound from threats that decrease its abundance (such as overutilization) and render the species more vulnerable to extinction in the face of other demographic risks and threats. Additionally, the observed decrease in the species' mean disc width in catches from 1993-1995 and 1997-2006 (to sizes that ranged between 25 cm and 40 cm) likely portended a declining growth rate for the species. This is because changes in metrics, such as average size, can significantly impact other important life history functions, like fecundity or even natural mortality rates (Audzijonyte et al. 2015), that affect the instantaneous per capita growth rate of a species. However, since 2006, data from the Falkland Islands Government show an increase in size of the modal disc width of graytail skate catches, with the most recent size estimate of 63 cm in 2012, likely indicating that the population is recovering and that growth rate is no longer declining.

Spatial Structure/Connectivity

Based on trends in commercial fisheries data from the Falkland Islands and Argentina, Wakeford et al. (2005) concluded that graytail skates have limited spatial and temporal movements and, therefore, may likely exist as localized populations. Limited inter-population exchange reduces the recovery potential for depleted and small local populations and may increase the risk of local extirpations, possibly leading to complete extinction. However, no other information is available regarding spatial structure or connectivity of graytail skate populations throughout its range, and there is no evidence to suggest this demographic risk is presently significantly contributing to the graytail skate's risk of extinction.

Diversity

The loss of diversity can increase a species' extinction risk through decreasing a species' capability of responding to episodic or changing environmental conditions. This can occur through a significant change or loss of variation in life history characteristics (such as reproductive fitness and fecundity), morphology, behavior, or other genetic characteristics. Currently, there is no information regarding the graytail skates' diversity throughout its range, thus we can not conclude whether its present level of diversity is contributing to its extinction risk.

Threats Assessment

The best available information indicates that graytail skates are most heavily exploited in the Falkland Islands multispecies skate and ray fishery by foreign fleets and likely suffered significant declines in abundance due to overexploitation in the early 1990s. However, since 1996, the area of operation of the Falkland Islands rajid fishery has been significantly restricted (to an area north of the Islands) with imposed catch limits to manage the northern batoid stock assemblage (which includes graytail skates) within this area. As a result of these management measures, there has been a gradual increase in CPUE and biomass of the northern batoid stock assemblage. As for graytail skates specifically, they remain one of the most abundant species caught in the Falkland Islands multispecies skate fishery. Recent data from the Falkland Islands Government shows an increasing trend in the CPUE of the species as well as in the the modal disc width of graytail skate catches, with the latest estimate of 63 cm DW in 2012. While 63 cm is still below the size of sexual maturity (i.e., 75 cm) it is a marked improvement from the modal disc widths between 1993 and 2006 (after heavy exploitation), which ranged between 25 cm and 40 cm, and indicates potential recovery of the population. Additionally, since the early 2000s, there has been a general decreasing trend in the targeting of skate and ray species in the Falkland Islands, with most species now taken as bycatch in the finfish fishery. Furthermore, total skate catch in recent years has remained below MSY, indicating that current catch and effort of the skate and ray fishery are likely sustainable. Based on the above information, it is clear that existing regulatory measures, including current catch limits and trawling closures, are adequate to protect the graytail skate in the Falkland Islands from extinction.

In Argentina, there is an active commercial elasmobranch fishery, which exploits sharks, skates, and rays, and it has shown an increasing trend in both catches and number of vessels reporting skate and ray landings (Massa and Hozbor 2003). However, based on the lack of species-specific information from the region, it is highly uncertain if present levels of utilization of skates and rays are a threat that is contributing significantly to the extinction risk of the graytail skate.

In Chile, a directed skate fishery that primarily targets Zearaja chilensis in areas where graytail skate may also occur has reported declines in catch since 1979. It is suspected that other skate species, including the graytail skate, have also been affected. However, there are no available data that indicate a decline in graytail skate abundance or catch, and given that the species comprises less than 5 percent of the total skate landings in this fishery, it is unlikely that this fishery is significantly contributing to the extinction risk of the graytail skate.

Overall, while the species likely experienced historical declines in abundance during the 1990s due to exploitation by the Falkland Islands multispecies rajid fisheries, the available biomass estimates and trends over the past decade, including gradual increases in the CPUE and biomass of

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the northern batoid stock and specifically the graytail skate in recent years, as well as an increasing trend in graytail modal disc width size, indicate the population is potentially stable and possibly moving towards recovery. This is likely a result of rigorous regulations implemented by the Falkland Islands government to sustainably manage the rajid fishery by reducing fishing effort, accomplished by setting catch limits in the northern rajid fishery and closing the southern rajid fishery area, where graytail skates likely spawn and were historically most heavily exploited. It should be noted that while this closure helps to protect the Falkland Islands population, due to uncertainty surrounding the connectivity of graytail skate populations, these regulations may not provide protection to skate populations found outside of Falkland waters. However, based on the available information, it appears that the Falkland Islands is where the species is most concentrated, and, hence, the protection of this population from extinction is likely critical for the survival of the species. Outside of the Falkland Islands, the minimal available information on the species does not indicate that present levels of utilization or any other factors are contributing significantly to the extinction risk of the species.

Risk of Extinction

While the species' demographic characteristics increase its inherent vulnerability to depletion, and likely contributed to past population declines of varying magnitudes, the best available information suggests these risks have decreased due to the adequate control of exploitation of the species. In the Falkland Islands, where the species was most heavily exploited and is likely presently most concentrated, abundance estimates and trends from the 1990s to 2013, and increases in the species' mean disc width, suggest potential stabilization and even recovery of the population. The continued rigorous management and monitoring of the fishery appears adequate in protecting the species from levels of overutilization that would increase its extinction risk. Despite fishing pressure in other parts of the species' range (e.g., Chile and Argentina) and evidence of it being taken as bycatch in various fisheries, graytail skates are not monitored and we have no other information (e.g., catch rates, abundance trends, or any other species-specific data) to indicate that present levels of utilization or any other factors are significantly contributing to the species' risk of extinction. Thus, considering the above information and analysis, we conclude that B. griseocauda is at a low risk of extinction throughout its range, and as such, does not warrant listing as a threatened or endangered species throughout its range.

Significant Portion of Its Range Analysis

Because our range-wide analysis for the species leads us to conclude that the species is not threatened or endangered throughout its range, under the final Significant Portion of Its Range (SPR) policy announced in July 2014, we must go on to consider whether the species may have a higher risk of extinction in a significant portion of its range (79 FR 37577; July 1, 2014).

The final policy explains that it is necessary to fully evaluate a portion for potential listing under the ``significant portion of its range'' authority only if information indicates that the members of the species in a particular area are likely both to meet the test for biological significance and to be currently endangered or threatened in that area. Making this preliminary determination triggers a need for further review, but does not prejudge whether the portion actually meets these standards such that the species should be listed:

To identify only those portions that warrant further consideration, we will determine whether there is substantial information indicating that (1) the portions may be significant and (2) the species may be in danger of extinction in those portions or likely to become so within the foreseeable future. We emphasize that answering these questions in the affirmative is not a determination that the species is endangered or threatened throughout a significant portion of its range--rather, it is a step in determining whether a more detailed analysis of the issue is required (79 FR 37586, July 1, 2014).

Thus, the preliminary determination that a portion may be both significant and endangered or threatened merely requires NMFS to engage in a more detailed analysis to determine whether the standards are actually met (Id. at 37587). Unless both are met, listing is not warranted. The policy further explains that, depending on the particular facts of each situation, NMFS may find it is more efficient to address the significance issue first, but in other cases it will make more sense to examine the status of the species in the potentially significant portions first. Whichever question is asked first, an affirmative answer is required to proceed to the second question. Id. (``If we determine that a portion of the range is not ``significant,'' we will not need to determine whether the species is endangered or threatened there; if we determine that the species is not endangered or threatened in a portion of its range, we will not need to determine if that portion was ``significant.''). Thus, if the answer to the first question is negative--whether that regards the significance question or the status question--then the analysis concludes and listing is not warranted.

After a review of the best available information, we identified the Falkland Islands as likely constituting a ``significant'' portion of the graytail skate range. Under the policy, a portion of a species' range is significant if, without that portion, the species would have an increased vulnerability to threats to the point that the overall species would be in danger of extinction or likely to become so in the foreseeable future. As mentioned previously, the historical and current fisheries data indicate that graytail skate are likely most concentrated in Falkland waters. Graytail skate have also been identified and caught elsewhere throughout its range, such as north of the Falkland Islands on the Argentinian shelf between 45deg S. and 41deg S., and on the Pacific coast off Chile (south of 41deg S.); however, based on trends in commercial fisheries data from the Falkland Islands and Argentina, Wakeford et al. (2005) concluded that graytail skates have limited spatial and temporal movements and, therefore, may likely exist as localized or isolated populations. If we assume the Falkland Islands population is isolated from the populations of graytail skate elsewhere throughout its range, then, technically, loss of this population would not directly affect the abundance of the other remaining populations. However, loss of this population could significantly increase the extinction risk of the species as a whole, as only small, fragmented, and isolated populations of the species (based on the best available abundance information--see the Historical and Current Distribution and Population Abundance and Demographic Risk Analysis sections above) would remain, making them more vulnerable to catastrophic events and environmental or anthropogenic perturbations. Limited inter-population exchange also reduces the recovery potential for these small local populations and increases the risk of local extirpations and overall complete extinction.

Under the policy, if we believe the Falkland Islands population may constitute a ``significant'' portion of the range, then we must either evaluate the extinction risk of this population first to determine whether it is threatened or endangered in that portion or determine

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if this portion is, in fact, ``significant.'' Ultimately, of course, both tests have to be met to qualify the species for listing. Given the extremely limited amount of information on the species outside of its Falkland Islands range, it is difficult to conduct a more definitive analysis to determine whether or not this portion does, in fact, constitute a ``significant'' portion of the range of the graytail skate. Additionally, there is no information to suggest that any other portion may be significant. However, even if we were to assume that the Falklands Islands population does constitute a ``significant'' portion of the graytail skate range, based on the information and analysis in the previous extinction risk section, there are no identified threats concentrated in this portion that are significantly contributing to the species' risk of extinction. In fact, the most recent available information indicate that existing regulatory measures are adequate in protecting the graytail skate in the Falkland Islands from extinction, with graytail skate abundance on a positive trend and exhibiting signs of population recovery based on both CPUE and size data. Thus, under the policy, the preliminary determination that a portion of the species' range may be both significant and endangered or threatened has not been met. Therefore, listing is not warranted under the SPR policy.

Proposed Determination

Based on the best available scientific and commercial information as presented in the status review report and this finding, we find that the graytail skate is not presently in danger of extinction throughout all or a significant portion of its range, nor is it likely to become so in the foreseeable future. We summarize the factors supporting this conclusion as follows: (1) Although there is no formal estimate of the current population size and historical declines in biomass have been observed, current biomass estimates from the Falkland Islands, where the species is likely most concentrated, suggest the population is stable and CPUE trends indicate abundance is increasing; (2) a reduction in mean disc width of the Falkland Islands population occurred in the late 1990s and early 2000s as a result of intensive fishing pressure; however, recent evidence suggests an increase in modal disc width, which is likely indicative of population recovery; (3) while an identified threat to the species was historical overutilization in the Falkland Islands commercial fisheries, subsequent fishery closures in the southern rajid fishery and catch limits in the northern rajid fishery of the Falkland Islands have contributed to a significant reduction of fishing pressure on the species, leading to increases in the abundance of the population and providing for sustainable fishing of the northern Falkland Islands rajid assemblage; (4) targeting of skates and rays in the Falkland Islands, where the species was most heavily exploited, has been on a decreasing trend since the early 2000s; (5) there is no evidence that destruction of habitat, disease or predation are factors contributing to an increased risk of extinction for the species; and (6) the continual implementation of rigorous monitoring and fishery management measures in the Falkland Islands appears effective in addressing the most important threat to the species (overharvest) now and into the foreseeable future. Based on these findings, we conclude that the graytail skate is not presently in danger of extinction throughout all or a significant portion of its range, nor is it likely to become so within the foreseeable future. Accordingly, the graytail skate does not meet the definition of a threatened or endangered species and therefore does not warrant listing as threatened or endangered at this time.

Effects of Listing

Conservation measures provided for species listed as endangered or threatened under the ESA include recovery actions (16 U.S.C. 1533(f)); concurrent designation of critical habitat, if prudent and determinable (16 U.S.C. 1533(a)(3)(A)); Federal agency requirements to consult with NMFS under section 7 of the ESA to ensure their actions do not jeopardize the species or result in adverse modification or destruction of critical habitat should it be designated (16 U.S.C. 1536); and prohibitions on taking for endangered species (16 U.S.C. 1538). Recognition of the species' plight through listing promotes conservation actions by Federal and state agencies, foreign entities, private groups, and individuals. The main effects of the proposed endangered listings are prohibitions on take, including export and import.

Identifying Section 7 Conference and Consultation Requirements

Section 7(a)(2) (16 U.S.C. 1536(a)(2)) of the ESA and NMFS/USFWS regulations require Federal agencies to consult with us to ensure that activities they authorize, fund, or carry out are not likely to jeopardize the continued existence of listed species or destroy or adversely modify critical habitat. Section 7(a)(4) (16 U.S.C. 1536(a)(4)) of the ESA and NMFS/USFWS regulations also require Federal agencies to confer with us on actions likely to jeopardize the continued existence of species proposed for listing, or that result in the destruction or adverse modification of proposed critical habitat of those species. It is unlikely that the listing of these species under the ESA will increase the number of section 7 consultations, because these species occur outside of the United States and are unlikely to be affected by Federal actions.

Critical Habitat

Critical habitat is defined in section 3 of the ESA (16 U.S.C. 1532(5)) as: (1) The specific areas within the geographical area occupied by a species, at the time it is listed in accordance with the ESA, on which are found those physical or biological features (a) essential to the conservation of the species and (b) that may require special management considerations or protection; and (2) specific areas outside the geographical area occupied by a species at the time it is listed upon a determination that such areas are essential for the conservation of the species. ``Conservation'' means the use of all methods and procedures needed to bring the species to the point at which listing under the ESA is no longer necessary. Section 4(a)(3)(A) of the ESA (16 U.S.C. 1533(a)(3)(A)) requires that, to the extent prudent and determinable, critical habitat be designated concurrently with the listing of a species. However, critical habitat shall not be designated in foreign countries or other areas outside U.S. jurisdiction (50 CFR 424.12(h)).

The best available scientific and commercial data as discussed above identify the geographical areas occupied by Isogomphodon oxyrhynchus, Rhinobatos horkelii, Mustelus fasciatus, M. schmitti, Squatina guggenheim and S. argentina as being entirely outside U.S. jurisdiction, so we cannot designate critical habitat for these species.

We can designate critical habitat in areas in the United States currently unoccupied by the species, if the area(s) are determined by the Secretary to be essential for the conservation of the species. Regulations at 50 CFR 424.12(e) specify that we shall designate as critical habitat areas outside the geographical range presently occupied by the species only when the designation limited to its present range would be inadequate to ensure the conservation of the species. The best available scientific and commercial information on these species does not indicate that U.S. waters provide any

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specific essential biological function for any of the species proposed for listing. Therefore, based on the available information, we do not intend to designate critical habitat for Isogomphodon oxyrhynchus, Rhinobatos horkelii, Mustelus fasciatus, M. schmitti, Squatina guggenheim or S. argentina.

Identification of Those Activities That Would Constitute a Violation of Section 9 of the ESA

On July 1, 1994, NMFS and FWS published a policy (59 FR 34272) that requires us to identify, to the maximum extent practicable at the time a species is listed, those activities that would or would not constitute a violation of section 9 of the ESA.

Because we are proposing to list Isogomphodon oxyrhynchus, Rhinobatos horkelii, Mustelus fasciatus and Squatina argentina as endangered, all of the prohibitions of section 9(a)(1) of the ESA will apply to these species. These include prohibitions on the import, export, use in foreign commerce, or ``take'' of the species. These prohibitions apply to all persons subject to the jurisdiction of the United States, including in the United States, its territorial sea, or on the high seas. Take is defined as ``to harass, harm, pursue, hunt, shoot, wound, kill, trap, capture, or collect, or to attempt to engage in any such conduct.'' The intent of this policy is to increase public awareness of the effects of this listing on proposed and ongoing activities within the species' range. Activities that we believe could result in a violation of section 9 prohibitions for these species include, but are not limited to, the following:

(1) Possessing, delivering, transporting, or shipping any individual or part (dead or alive) taken in violation of section 9(a)(1);

(2) Delivering, receiving, carrying, transporting, or shipping in interstate or foreign commerce any individual or part, in the course of a commercial activity;

(3) Selling or offering for sale in interstate commerce any part, except antique articles at least 100 years old;

(4) Importing or exporting these species or any part of these species.

We emphasize that whether a violation results from a particular activity is entirely dependent upon the facts and circumstances of each incident. Further, an activity not listed may in fact constitute a violation.

Identification of Those Activities That Would Not Constitute a Violation of Section 9 of the ESA

We will identify, to the extent known at the time of the final rule, specific activities that will not be considered likely to result in a violation of section 9 of the ESA. Although not binding, we are considering the following actions, depending on the circumstances, as not being prohibited by ESA section 9:

(1) Take authorized by, and carried out in accordance with the terms and conditions of, an ESA section 10(a)(1)(A) permit issued by NMFS for purposes of scientific research or the enhancement of the propagation or survival of the species;

(2) Continued possession of parts that were in possession at the time of listing. Such parts may be non-commercially exported or imported; however, the importer or exporter must be able to provide evidence to show that the parts meet the criteria of ESA section 9(b)(1) (i.e., held in a controlled environment at the time of listing, in a non-commercial activity).

Protective Regulations Under Section 4(d) of the ESA

We are proposing to list Mustelus fasciatus and Squatina guggenheim as threatened species. In the case of threatened species, ESA section 4(d) leaves it to the Secretary's discretion whether, and to what extent, to extend the section 9(a) ``take'' prohibitions to the species, and authorizes us to issue regulations necessary and advisable for the conservation of the species. Thus, we have flexibility under section 4(d) to tailor protective regulations, taking into account the effectiveness of available conservation measures. The 4(d) protective regulations may prohibit, with respect to threatened species, some or all of the acts which section 9(a) of the ESA prohibits with respect to endangered species. These 9(a) prohibitions apply to all individuals, organizations, and agencies subject to U.S. jurisdiction. We will consider extending some or all potential protective regulations pursuant to section 4(d) for the proposed threatened species. We seek public comment on potential 4(d) protective regulations (see below).

Public Comments Solicited

To ensure that any final action resulting from this proposed rule will be as accurate and effective as possible, we are soliciting comments and information from the public, other concerned governmental agencies, the scientific community, industry, and any other interested parties on information in the status review and proposed rule. Comments are encouraged on these proposals (See DATES and ADDRESSES). We must base our final determination on the best available scientific and commercial information when making listing determinations. We cannot, for example, consider the economic effects of a listing determination. Final promulgation of any regulation(s) on these species' listing proposals will take into consideration the comments and any additional information we receive, and such communications may lead to a final regulation that differs from this proposal or result in a withdrawal of this listing proposal. We particularly seek:

(1) Information concerning the threats to any of the six species proposed for listing;

(2) Taxonomic information on any of these species;

(3) Biological information (life history, genetics, population connectivity, etc.) on any of these species;

(4) Efforts being made to protect any of these species throughout their current ranges;

(5) Information on the commercial trade of any of these species;

(6) Historical and current distribution and abundance and trends for any of these species;

(7) Current or planned activities within the range of these species and their possible impact on these species; and,

(8) Information relevant to potential ESA section 4(d) protective regulations for any of the proposed threatened species.

We request that all information be accompanied by: (1) Supporting documentation, such as maps, bibliographic references, or reprints of pertinent publications; and (2) the submitter's name, address, and any association, institution, or business that the person represents.

Role of Peer Review

In December 2004, the Office of Management and Budget (OMB) issued a Final Information Quality Bulletin for Peer Review establishing a minimum peer review standard. Similarly, a joint NMFS/FWS policy (59 FR 34270; July 1, 1994) requires us to solicit independent expert review from qualified specialists, concurrent with the public comment period. The intent of the peer review policy is to ensure that listings are based on the best scientific and commercial data available. We solicited peer review comments on the species' status review reports (Casselbury and Carlson 2015a-

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g) from 22 scientists from the academic and scientific community that were either familiar with the species or had expertise in elasmobranch biology, ecology, or conservation. We received comments from nine scientists and incorporated those comments into the status review reports and this proposed rule. Their comments on the status reviews are also summarized in the peer review report available at http://www.cio.noaa.gov/services_programs/prplans/PRsummaries.html.

References

A complete list of the references used in this proposed rule is available upon request (see ADDRESSES).

Classification

National Environmental Policy Act

The 1982 amendments to the ESA, in section 4(b)(1)(A), restrict the information that may be considered when assessing species for listing. Based on this limitation of criteria for a listing decision and the opinion in Pacific Legal Foundation v. Andrus, 675 F. 2d 825 (6th Cir. 1981), we have concluded that ESA listing actions are not subject to the environmental assessment requirements of the National Environmental Policy Act (NEPA) (See NOAA Administrative Order 216-6).

Executive Order 12866, Regulatory Flexibility Act, and Paperwork Reduction Act

As noted in the Conference Report on the 1982 amendments to the ESA, economic impacts cannot be considered when assessing the status of a species. Therefore, the economic analysis requirements of the Regulatory Flexibility Act are not applicable to the listing process. In addition, this proposed rule is exempt from review under Executive Order 12866. This proposed rule does not contain a collection-of-

information requirement for the purposes of the Paperwork Reduction Act.

Executive Order 13132, Federalism

In accordance with E.O. 13132, we determined that this proposed rule does not have significant Federalism effects and that a Federalism assessment is not required. In keeping with the intent of the Administration and Congress to provide continuing and meaningful dialogue on issues of mutual state and Federal interest, this proposed rule will be given to the relevant governmental agencies in the countries in which the species occurs, and they will be invited to comment. We will confer with the U.S. Department of State to ensure appropriate notice is given to foreign nations within the range of all three species. As the process continues, we intend to continue engaging in informal and formal contacts with the U.S. State Department, giving careful consideration to all written and oral comments received.

List of Subjects

50 CFR Part 223

Endangered and threatened species, Exports, Imports, Transportation.

50 CFR Part 224

Endangered and threatened species, Exports, Imports, Transportation.

Dated: November 30, 2015.

Samuel D. Rauch, III,

Deputy Assistant Administrator for Regulatory Programs, National Marine Fisheries Service.

For the reasons set out in the preamble, 50 CFR parts 223 and 224 are proposed to be amended as follows:

PART 223--THREATENED MARINE AND ANADROMOUS SPECIES

0

  1. The authority citation for part 223 continues to read as follows:

    Authority: 16 U.S.C. 1531-1543; subpart B, Sec. 223.201-202 also issued under 16 U.S.C. 1361 et seq.; 16 U.S.C. 5503(d) for Sec. 223.206(d)(9).

    0

  2. In Sec. 223.102, amend the table in paragraph (e) by adding new entries for two species in alphabetical order under the ``Fishes'' table subheading to read as follows:

    Sec. 223.102 Enumeration of threatened marine and anadromous species.

    * * * * *

    (e) * * *

    ----------------------------------------------------------------------------------------------------------------

    Species \1\

    -------------------------------------------------------------------- Citation(s) for Critical

    Description of listing habitat ESA rules

    Common name Scientific name listed entity determination(s)

    ----------------------------------------------------------------------------------------------------------------

    * * * * * * *

    ----------------------------------------------------------------------------------------------------------------

    Fishes

    ----------------------------------------------------------------------------------------------------------------

    * * * * * * *

    Shark, spiny angel............ Squatina Entire species.. Federal Register NA NA

    guggenheim. citation and

    date when

    published as a

    final rule.

    Shark, narrownose smoothhound. Mustelus schmitti Entire species.. Federal Register NA NA

    citation and

    date when

    published as a

    final rule.

    * * * * * * *

    ----------------------------------------------------------------------------------------------------------------

    \1\ Species includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement,

    see 61 FR 4722, February 7, 1996), and evolutionarily significant units (ESUs) (for a policy statement, see 56

    FR 58612, November 20, 1991).

    \2\ Jurisdiction for sea turtles by the Department of Commerce, National Oceanic and Atmospheric Administration,

    National Marine Fisheries Service, is limited to turtles while in the water.

    79 FR 20806, Apr. 14, 2014, as amended at 79 FR 38240, July 3, 2014; 79 FR 40015, July 11, 2014; 79 FR 54122,

    Sept. 10, 2014; 80 FR 7978, Feb. 13, 2015

    Page 76115

    PART 224--ENDANGERED MARINE AND ANADROMOUS SPECIES

    0

  3. The authority citation for part 224 continues to read as follows:

    Authority: 16 U.S.C. 1531-1543 and 16 U.S.C 1361 et seq.

    0

  4. In Sec. 224.101, paragraph (h), amend the table by adding new entries for four species in alphabetical order under the ``Fishes'' table subheading to read as follows:

    Sec. 224.101 Enumeration of endangered marine and anadromous species.

    * * * * *

    (h) * * *

    ----------------------------------------------------------------------------------------------------------------

    Species \1\

    -------------------------------------------------------------------- Citation(s) for Critical

    Description of listing habitat ESA rules

    Common name Scientific name listed entity determination(s)

    ----------------------------------------------------------------------------------------------------------------

    * * * * * * *

    ----------------------------------------------------------------------------------------------------------------

    Fishes

    ----------------------------------------------------------------------------------------------------------------

    * * * * * * *

    Guitarfish, Brazilian......... Rhinobatos Entire species.. Federal Register NA NA

    horkelii. citation and

    date when

    published as a

    final rule.

    Shark, Argentine angel........ Squatina Entire species.. Federal Register NA NA

    argentina. citation and

    date when

    published as a

    final rule.

    Shark, daggernose............. Isogomphodon Entire species.. Federal Register NA NA

    oxyrhynchus. citation and

    date when

    published as a

    final rule.

    Shark, striped smoothhound.... Mustelus Entire species.. Federal Register NA NA

    fasciatus. citation and

    date when

    published as a

    final rule.

    * * * * * * *

    ----------------------------------------------------------------------------------------------------------------

    \1\ Species includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement,

    see 61 FR 4722, February 7, 1996), and evolutionarily significant units (ESUs) (for a policy statement, see 56

    FR 58612, November 20, 1991).

    \2\ Jurisdiction for sea turtles by the Department of Commerce, National Oceanic and Atmospheric Administration,

    National Marine Fisheries Service, is limited to turtles while in the water.

    79 FR 20814, Apr. 14, 2014, as amended at 79 FR 31227, June 2, 2014; 79 FR 38241, July 3, 2014; 79 FR 74005,

    Dec. 12, 2014; 79 FR 78725, Dec. 31, 2014; 79 FR 68372, Nov. 17, 2014; 80 FR 7978, Feb. 13, 2015; 80 FR 7390,

    Feb. 10, 2015

    FR Doc. 2015-30660 Filed 12-4-15; 8:45 am

    BILLING CODE 3510-22-P