ARTISANALLY LANDED ELASMOBRANCHS ALONG THE COAST OF RIO DE JANEIRO, BRAZIL

Nathan Lagares Franco Araujo1,2, Catarina Amorim Lopes1,2,3, Vanessa Bettcher Brito2,3, Luciano Neves dos Santos2, Márcio Luiz Vargas Barbosa-Filho4, César Rogério Leal do Amaral5, Salvatore Siciliano6,7, Rachel Ann Hauser-Davis1,7* *corresponding author: rachel.hauser.davis@gmail.com; rachel.davis@ ioc.fi ocruz.br 1Laboratório de Avaliação e Promoção da Saúde Ambiental, Instituto Oswaldo Cruz/Fiocruz, Av. Brasil, 4.365, Manguinhos, Rio de Janeiro, RJ, 21040-360, Brazil. 2Laboratório de Ictiologia Teórica e Aplicada, Instituto de Biociências, Universidade Federal do Estado do Rio de Janeiro, Avenida Pasteur, 458, Urca, Rio de Janeiro, RJ, 22290-255, Brazil. 3Programa de Pós-graduação em Ecologia e Evolução, Universidade Estadual do Rio de Janeiro, Rua São Francisco Xavier, 524, Maracanã, 20550-900, Rio de Janeiro, RJ, Brazil 4Programa de Pós-graduaç ão em Etnobiologia e Conservaç ão da Natureza, Universidade Federal Rural de Pernambuco, Campus Dois Irmãos, Recife, 52171-900, PE, Brazil 5Laboratório de Diagnósticos por DNA, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, São Francisco Xavier, 524, Maracanã, Rio de Janeiro, RJ, 20550-013, Brazil 6Laboratório de Biodiversidade, Instituto Oswaldo Cruz, Fiocruz, Pavilhão Mourisco Sala 18, Manguinhos, Rio de Janeiro, RJ 21040-900 Brazil 7Grupo de Estudos de Mamíferos Marinhos da Região dos Lagos (GEMM-Lagos), Rua São José 1.260, Praia Seca, Araruama, RJ 28970-000 Brazil


INTRODUCTION
Brazil is home to approximately one million registered artisanal fi shers, which contribute to over 50% of the total fi sh produced in the country (Vasconcellos et al. 2007). However, data concerning artisanal fi sheries are poor (Kaliloski & Vasconcellos 2012;Previero & Gasalla 2018), making it diffi cult to identify and assess the eff ectiveness of conservation management actions (Costa et al., 2018). Elasmobranchs in particular are extremely vulnerable to artisanal fishery (Lack & Sant 2009;Bornatowski et al. 2014), either targeted or captured as bycatch (Molina & Cooke 2012;Ferrette et al. 2019), as they are long lived organisms displaying slow growth rates, delayed maturation, long gestation, and small litters (Stevens et al. 2000;Dulvy et al. 2014). Approximately 25% of this class has been reported as threatened with extinction by the International Union for Conservation of Nature (IUCN)  and, 47% of these are classifi ed by the IUCN as data defi cient, indicating absence of minimal information to be evaluated (Mace et al. 2008;Dulvy et al. 2014).
In many countries, shark and ray meat are viewed as a low-quality food item and, thus, marketed under generic designations not directly linked to these animals, in order to overcome consumer resistance (Vannuccini 1999;Bornatowski et al. 2013Bornatowski et al. , 2015Dent & Clarke 2015). This is the case in Brazil, where shark and ray meat are sold as caç ão fi llets (Bornatowski et al. 2018). The lack of consumer knowledge regarding caç ão meat and what it really consists in has increasingly led to overfi shing due to attractive shark and ray meat prices ( Bornatowski et al. 2018) and is of signifi cant ecological concern, as these animals play an important role in maintaining ecosystem equilibrium and health (Heupel et al. 2014). In this scenario, due to both targeted and non-targeted fi sheries, Brazilian fi sheries have reached critical levels for several elasmobranch species (Bornatowski et al. 2018) and 33% of all elasmobranchs are categorized as threatened, while 36% are considered data defi cient (Instituto Chico Mendes de Conservação da Biodiversidade 2018), overcoming the global rate of threatened species. Most pelagic shark populations are currently depleted in Brazil while coastal species data are very poor (Bornatowski et al. 2018).
A constant that determines the diffi culty of social and ecological fi shing activity management in Brazil is the lack of specifi c monitoring for each fi shing sector, both large and small (artisanal) scale, in the long term, as, although fi shery statistics are achieved regionally by some states, most of the country lacks this specifi city. However, eff ective governance between conservation and fi sheries can only be eff ective by fi lling in the gaps in fi sheries data (Kolding et al., 2010). In Brazil, the latest version of the National Fisheries and Aquaculture Statistical Bulletin (Instituto Chico Mendes de Conservação da Biodiversidade, 2011) illustrates the main problem faced by sector managers, of data discontinuity, since this government document has not been updated for eight years. At the state level, the Rio de Janeiro Institute of Fisheries Foundation issues an annual report on Fisheries and Aquaculture where, in addition to unspecifi c fi sh categorization, a combination of large and scale small data is noted, making it very diffi cult, for example, to discern which species are vulnerable to what types of fi sheries, leading to signifi cant data defi ciency, especially with regard to artisanal fi shing.
However, no recent evaluation of artisanally landed sharks and rays are available for many artisanal fi sheries regions, such as those located in the metropolitan region of Rio de Janeiro, and the Região dos Lagos region, which comprises over 1500 registered artisanal fi shers from at least eight cities (Saquarema, Maricá, Araruama, Iguaba Grande, São Pedro da Aldeia, Cabo Frio, Búzios and Arraial do Cabo) (FIPERJ 2015).
In this context, this study aimed to assess artisanally landed sharks and rays along the coast of Rio de Janeiro, RJ, Brazil through fi sheries monitoring, fi sher interviews and photographs taken by the fi shers and the researchers.

MATERIAL AND METHODS
The state of Rio de Janeiro (22° 54' 13'' S, 43° 12' 35'' W), is located in southeastern Brazil, occupying the 4 th place in terms of economy and 3 rd in population size in the national ranking (IBGE, 2019), extremely important in a socio-economic context.
A total of 28 artisanal fisher colonies are distributed throughout the state of Rio de Janeiro, from São Francisco do Itabapoana to Paraty (FIPERJ, 2019), with the main fi shing ports located at Niterói, São Gonçalo, Cabo Frio and Angra dos Reis.
Samplings were carried out at two artisanal fi shing unions and one fi sher association located in Rio de Janeiro, namely the Z-13 fi shing colony/union, in Copacabana (22 ° 59 '10 "S,43 ° 11' 19" W), in the metropolitan Rio de Janeiro area, the Associação de Pesca de Tamoios (Tamoios Fishers Association), located in the Pontal de Santo Antônio, in Cabo Frio (22° 35' 55.0'' S, 41° 59' 40.9'' W), on the Southeastern coast of the state, and the Z-7 fi shing colony/union, at Itaipu (22º53'14"S,43º22'48"W), in Niterói ( Figure 1). Located in the central region of the state, artisanal fi sher colonies Z-13 and Z-7, at Copacabana and Itaipu, respectively, operate in fishing areas that undergo strong infl uences from Guanabara Bay, an eutrophic estuarine environment, mainly in the regions most associated with oceanic waters. On the other hand, the Associação de Pesca de Tamoios, in Cabo Frio is located in an area characterized by a signifi cant upwelling phenomenon, where deep South Atlantic Central Waters rise continuously, resulting in a high abundance of nectonic species, making this area one of the most productive fi shing areas in the state of Rio de Janeiro (Valentin, 2001).
No standardized sampling eff ort was carried out in this study, due to logistic reasons. All specimens were caught within the fi shing spectrum of the respective sites, no further that 15 km from the fi shing colonies.
Samples from the Z-7 Itaipu colony, which consists of 130 associated fi shers, were obtained from January to July 2016, comprising 10 visits at random. Initial visits by the researchers to this colony enabled the development of both a close relation with the fi shers and elasmobranch landings, so, in the absence of the research team, fi shers would send photographs of elasmobranchs whenever these animals were landed. Elasmobranch landing data for Itaipu were obtained from Brito (2016). Concerning Tamoios, periodic visits were made every three months to the Associação de Pesca de Tamoios, from 2017 to 2018. At Tamoios, landing assessments were always performed by the research team, through sample collections and photographic records, without the aid of local fi shermen.
Data collection at the Z-13 colony was carried out from September 2018 to September 2019. Observations and species identifi cation through the scientifi c literature (Gomes et al. 2010) were performed through frequent visits to the colony, of at least 3 times a week, according to sea conditions, obtaining photographic records and/or tissue samples of the sampled animals. In the absence of the research team, fi shers would send photographs of elasmobranchs whenever these animals were landed.
The same fi shing gear, gillnets, was used in all three regions. Only the amount of cloths and mesh size diff er among the fi shing colonies. All nets had an average height of two meters. At Copacabana, 50 mm mesh gillnets are used for bottom and mid-column fi shing, with about 8 cloths per boat, resulting in about 400 to 500m nets for each boat. At Tamoios, a mesh size between 40 and 45mm is used, with varying amounts of cloths according to boat size, of about 100m each, reaching up to 10 cloths in a single boat. At Itaipu, gillnets with mesh sizes varying from 40 to 80 mm are used for mid-column and bottom fi shing. No information on net lengths are available for this colony. All elasmobranchs were captured as by-catch, due to the non-selectivity of the fi shing methodology, even at diff erent depths.

RESULTS
A total of twenty-three species from twelve families were identified at all sample sites. Data concerning the Order, Family, popular names, global and national Conservation States, and geographic distribution of the artisanally landed elasmobranchs   are presented in Table 1, while data concerning elasmobranch individuals landed at three artisanal fi shing colonies in the state of Rio de Janeiro, Brazil, from 2016 to 2019 are presented in Table 2.
Frequency data for each elasmobranch species landed at the Tamoios, Z-7 and Z-13 artisanal colonies is displayed in Figure 2. It is important to note that no standardized sampling eff ort was carried out in this study, so no frequency proportion extrapolation in possible for the analyzed areas.

DISCUSSION
The present study reports a preliminary assessment carried out during three years regarding artisanal fishing elasmobranch landing at three locations throughout the coast of Rio de Janeiro. Although the Associação de Pesca de Tamoios, in Cabo Frio is home to the previously described upwelling phenomenon, the highest richness concerning oceanic elasmobranchs was recorded at the Z-13 colony, in Copacabana, located in the metropolitan region of Rio de Janeiro. This sampling site is a part of Guanabara Bay, and the results presented herein reinforce the signifi cant biodiversity of the bay and the importance of its recovery for elasmobranch management and conservation strategies.
In addition, many specimens belonging to diff erent species sampled from this site (Sphyrna zygaena, Sphyrna lewini, Carcharinus brevipinna, Isurus oxyrinchus and Galeocerdo cuvier) were juvenile (Araujo, pers. obs.), while three spinner shark females (Carcharinus brevipinna) with mature oocytes were also noted (Araujo, pers. obs.), indicating that this may be a strategic reproduction and juvenile settlement site for several of the landed species. This is further supported by the record of six females of Rhizoprionodon lalandii, a coastal species, containing embryos and/or oocytes, as well as the high presence of juvenile hammerhead sharks (Sphyrna lewini), indicating potential development area (Motta et al., 2005). It is noteworthy both Itaipu and Copacabana are inserted in the estuarine Guanabara Bay, while Tamoios is located the São João River, both a strong indication of an elasmobranch breeding area, as reported by Plumlee et al. (2018) and Parsons and Hoff mayer (2007). In addition to species that are more commonly caught by gillnets, more pelagic and cosmopolitan species such as Tiger (Galeocerdo cuvier) and Mako (Isurus oxyrinchus) sharks were also caught by the same fishing methodology, all juveniles, once again indicating potential elasmobranch breeding and development areas.
In its most recent report, the Rio de Janeiro Institute for Fisheries Foundation (FIPERJ) reported that, in 2016, the species identifi ed as cação-frango (Sharpnose shark, Rhizoprionodon sp.) was the most representative species regarding total landings, with a production of 5,212,8 kg, followed by cação-anjo (angel shark, Squatina sp.), at 2,661.5 kg and, fi nally, cação-martelo (hammerhead shark, Sphyrna sp.), totaling 1,004kgs (Fundação Instituto de Pesca do Estado do Rio de Janeiro 2016). However, the data reported herein cannot be quantitatively compared to FIPERJ data, as FIPERJ provides mixed and generalized information containing artisanal, semiindustrial and industrial fi shing data, where artisanal fi shing represents only a portion of the catch. In addition, the diff erent range of fi shing fl eets should also be taken into account, as a limiting factor for the habitat range of certain species, such as hammerhead sharks and angelfi sh, due to depths and distance from the shore. It is also noteworthy that FIPERJ accounts for the weight of a certain species and data per individual, which may overestimate the data, as an adult fi sh may weigh more than 10 juvenile individuals.
Concerning species vulnerability, Squatina occulta and Squatina guggenheim, are classifi ed as critically endangered and endangered, respectively, according to the IUCN. In addition, Squatina guggenheim, was reported as reaching critically low levels and populational declines during the 1990s (Boeckman & Vooren, 1997;Vooren 1997;Lessa et al. 1999), indicating significant vulnerability for this species. In turn, all six hammerhead shark species distributed along the Brazilian coast are currently nationally listed as threatened (Instituto Chico Mendes de Conservação da Biodiversidade 2018). Given that the present study identifi ed several Squatina guggenheim, Sphyrna lewini and Sphyrna zygaena individuals, it is clear that environmental education actions, measures to avoid the capture of this species or release actions alongside fi shers at these locations are required, in order to sensitize them to the inherent impact of capturing these species and avoid further damage.
A signifi cant amount of landed elasmobranch species is unidentifi ed, or identifi ed solely by their common names by the fi shers, which also change according to fi shery region (FIPERJ, 2016). For example, many unidentifi ed species may belong to the cação category, the Brazilian generic name for most shark species, representing a signifi cant amount of the 3.1 tons landed in 2016 for which no scientifi c identifi cation was carried out. The same is probably true for rays, as these animals are distributed into categories with popular names such as raia-manteiga (stingrays) (about 1 ton) or raia-pintada (spotted rays) (3 tons) (FIPERJ, 2016). Thus, many species may be easily confused, making it diffi cult to create an elasmobranch management plan, and species identifi cation is paramount. In addition, it is important to note the signifi cant elasmobranch role as a fi shing resource in Brazil, attributed to the current market incentive for the consumption of shark meat, due to, mainly, low costs, leading to social and economic, BOLETIM DO LABORATÓRIO DE HIDROBIOLOGIA, 30:51-53. 2020 as well as ecological, concerns (Bornatowski et al. 2018).
Rio de Janeiro extractive marine fisheries represent about 2.5% of total shark landings caught per year in Brazil (Ministério da Pesca e Aquicultura 2014). However, in 2010 alone, in the Southwest Atlantic region, about 33% more sharks were fi shed in reality compared to lower fi gures reported by Southwest Atlantic governments to the Food and Agriculture Organization of the United Nations (FAO), attributed to artisanal, illegal and discarded fi sheries (Pauly & Zeller, 2016). Allied to the lack of knowledge on the commercial and artisanal exploitation of these animals, the lack of information on the occurrence of shark species makes it diffi cult to employ conservation strategies aiming at the preservation and management of this resource. One way to circumvent the reported diffi culties is the scientifi c monitoring of the artisanal fi shermen colonies and performing a scientifi c approach towards the ecological knowledge of these fi shermen, which, besides contributing to landing monitoring, enables taxonomic, physiological and genetic elasmobranch studies, furthering knowledge concerning the population ecology and geographical distribution of the group. In recent years, several studies have been conducted in Brazil addressing these issues (Palmeira et al. 2013;Barbosa-Filho et al. 2014, 2016Bornatowski et al. 2015;Gemaque et al. 2017;Feitosa et al. 2018), denoting the relevance of information of this nature to the management and conservation of this threatened zoological group. Dulvy et al. (2014) estimated that about a quarter of the world's shark and ray species are threatened by overfi shing, and although the state of Rio de Janeiro is fl agged as one of the world's priority shark conservation areas (Lucifora et al. 2011), the results presented herein indicate high amounts of threatened species being caught as by-catch. From an ecosystem perspective, it is well known that the presence of top predators and mesopredators as trophic regulators is essential for the functioning of ecosystem interaction webs (Stevens et al. 2000). Thus, declines in shark and ray population stocks may lead detrimental eff ects on marine communities (Myers et al. 2007;Bornatowski et al. 2014). The main documented phenomenon implies in the deregulation of lower trophic level maintenance exerted by top predator pressure, known as the topdown eff ect, thus aff ecting not only the ecosystem in question, but also the fi shing industry itself (Ferretti et al. 2010).
In this regard, it is important to take into account the presence of keystone species. Keystone species are defined as species which "have an extremely high impact on a particular ecosystem relative to its population, and are also critical for the overall structure and function of an ecosystem, and infl uence which other types of organisms make up that ecosystem" (Humphries et al., 2017). Six keystone elasmobranch species have been previously observed throughout the Southeastern coast of Brazil (Bornatowski et al. 2014), and the present study reports four of them, namely Galeocerdo cuvier, Sphyrna lewini, S. zygaena and Zapteryx brevirostris, further indicating the importance of future assessments concerning elasmobranch fi sheries monitoring in Brazil. In addition, due to the continuity of oceanographic conditions between the Brazilian Southeast and South, it is probable that the species reported herein display an extended ecosystem importance to the South, implicating in further social and economic concerns.