Introduction
The Chondrichthyes fishes (sharks, rays, and chimeras) comprise a vertebrate group with long evolutionary and ecological histories, belonging to about 1263 known living species (Compagno, Reference Compagno1984a, Reference Compagno1984b; Compagno, Reference Compagno2001; Compagno et al., Reference Compagno, Dando and Fowler2005; Ebert et al., Reference Ebert, Fowler and Compagno2013; Last et al., Reference Last, White, Carvalho, Séret, Stehmann and Naylor2016; Weigmann, Reference Weigmann2016; Ebert et al., Reference Ebert, Dando and Fowler2021). Despite such high ecological and morphological diversity and the pivotal role of meso and top predators in aquatic (mainly marine) ecosystems (Heithaus et al., Reference Heithaus, Dunn, Farabaugh, Lester, Madin, Meekan, Papastamatiou, Roff, Vaudo, Wirsing, Carrier, Simpfendorfer, Heithaus and Yopak2022), there are a few faunistic and diversity studies on a regional basis aiming to assess population parameters and build conservation and fisheries management public policies. The Brazilian Chondrichthyes fauna is recognizably rich and diverse, owing to the presence of numerous freshwater ray species belonging to the Potamotrygonidae family, as well as many marine members found along the country's coastline and Exclusive Economic Zone, totalling at least 211 species, consisting of 94 sharks, 104 rays, and eight chimeras (Gadig and Rosa, Reference Gadig, Rosa, Kotas, Vizuete, Santos, Baggio, Salge and Barreto2023). These numbers rank Brazil as seventh concerning Chondrichthyes biodiversity worldwide, highlighted by the fact that this diversity is distributed in only one ocean, the Atlantic, unlike other countries that have many of their territories bathed by more than one ocean (Gadig and Rosa, Reference Gadig, Rosa, Kotas, Vizuete, Santos, Baggio, Salge and Barreto2023).
Due to Brazil's extensive aquatic environment areas (i.e. watersheds and coastal/marine zones), knowledge concerning the local Chondrichthyes fauna is constantly being updated, with several species not yet described and others currently undergoing the description process (Gadig and Rosa, Reference Gadig, Rosa, Kotas, Vizuete, Santos, Baggio, Salge and Barreto2023). The country, however, still lacks a broad enough diagnosis, mainly concerning faunal surveys on a regional scale, in order to subsidize biogeographical studies and meet increasingly urgent demands for the establishment of public policies that act in favour of the management and conservation of this group's biodiversity, such as state-level extinction risk assessments. Adequate knowledge on the faunal elements that make up local diversities allows for Chondrichthyes life cycle-associated studies (habitat use, feeding, reproduction, age, and growth), all of which are considered knowledge gaps for the group in Brazil (Kotas et al., Reference Gales, Parsons, Biesack, Ready, Siccha-Ramirez, Rosa, Rosa, Rotundo, Bills, Rodrigues, Rodrigues-Filho, Mcdowell and Sales2023), as well as assessments on their exploitation (historical capture and effort series, mortality, and demography). These studies compose the information mosaic to be employed in Chondrichthyes management, use, and conservation efforts.
In this regard, some memorable studies have left their mark on Espírito Santo chondrofauna history. Ruschi (Reference Ruschi1965), for example, listed 47 cartilaginous fish species in the state. After four decades, a taxonomic list of Chondrichthyes species occurring in Brazil was published, with Espírito Santo listed among the states that make up the central coast (Lessa et al., Reference Lessa, Santana, Rincón, Gadig and El-Deir1999), which now presents a slightly known chondrofauna. Over the following decades, some studies, even if not focused on Chondrichthyes, have compiled important records, contributing to knowledge on this group in Espírito Santo (e.g. Nunan and Senna, Reference Nunan, Senna, Costa, Martins and Olavo2007; Pinheiro et al., Reference Pinheiro, Mazzei, Moura, Amado-Filho, Carvalho Filho, Braga, Costa, Ferreira, Ferreira, Floeter, Francini-Filho, Gasparini, Macieira, Martins, Olavo, Pimental, Rocha, Sazima, Simon, Teixeira, Xavier and Joyeux2015).
The coastline of the state of Espírito Santo comprises about 411 km, with a series of geomorphological features, such as continental shees presenting varying widths, submerged mountain ranges, coastal and oceanic islands, and deep slopes, which diversify the marine environments under its jurisdiction (Albino et al., Reference Albino, Neto, Oliveira, Klein and Short2016). However, although these heterogeneous coastal and marine environments exhibit high biodiversity potential, basic faunal Chondrichthyes composition studies, as well as knowledge on their distribution and biological aspects, are still lacking for the region. As Espírito Santo is one of the priority areas for Chondrichthyes biological inventories and abundance monitoring (Lessa et al., Reference Lessa, Santana, Rincón, Gadig and El-Deir1999), this is clearly paramount.
Understanding the diversity of Chondrichthyes is, in fact, of strategic importance under an ecosystem approach, as these animals occupy predator or meso-predator niches (Heithaus et al., Reference Heithaus, Dunn, Farabaugh, Lester, Madin, Meekan, Papastamatiou, Roff, Vaudo, Wirsing, Carrier, Simpfendorfer, Heithaus and Yopak2022) and exhibit certain biological characteristics that make them highly susceptible to mortality by unnatural factors, such as fisheries and habitat degradation (Dulvy et al., Reference Dulvy, Pacoureau, Rigby, Pollom, Jabado, Ebert, Finucci, Pollock, Cheok, Derrick, Herman, Samantha-Sherman, VanderWright, Lawson, Walls, Carlson, Charvet, Bineesh, Fernando, Ralph and Simpfendorfer2021). Therefore, this study aims to present a comprehensive and revised list of shark and ray species recorded so far for the state of Espírito Santo, Southeastern Brazil, based on species records from museums, bibliographic reviews, and fisheries monitoring.
Material and methods
The present study was carried out in the state of Espírito Santo, which is located in the southeast region of Brazil, bordering the state of Bahia to the north and Rio de Janeiro to
the south, between geographic coordinates 18°20’45.8”S/ 39°40’49.6”W and 21°18’04”S/ 40°57’24”W (Figure 1). Espírito Santo is a coastal state, and covers an area of approximately 411 km (Albino et al., Reference Albino, Neto, Oliveira, Klein and Short2016), and also includes the oceanic islands of Trindade and Martim Vaz in its territory.
Figure 1. Map of Espírito Santo state, Brazil, indicating municipalities with onboard monitoring to the north (area with dots) and municipalities with onboard monitoring and fisheries landing monitoring to the south (area with lines).
The data used for the preparation of the list of Chondrichthyes species in Espírito Santo was based on three main sources:
1) Local specimens deposited in scientific collections, namely the Professor Mello Leitão Biology Museum (MBML), the National Museum of Rio de Janeiro (MNRJ), the Zoology Museum at the University of São Paulo (MZUSP), the Ichthyological Collections belonging to the Federal University of Espírito Santo (CIUFES) and the Department of Zoology at the State University of Rio de Janeiro (DZ-UERJ), and the Fish Collection belonging to the Ecology and Socio-Environmental Development Nucleus at the Federal University of Rio de Janeiro (NPM).
2) A literature data review carried out by consulting articles, monographs, dissertations, theses, technical reports, books, and book chapters, alongside online databases and exchanges with researchers, abstracts released at scientific and occasional events, and any other documents that indicate elasmobranch occurrences in the state of Espírito Santo. This search was initially carried out through traditional species survey references that indicated the occurrence of elasmobranchs in the state (i.e. Ruschi, Reference Ruschi1965; Lessa et al., Reference Lessa, Santana, Rincón, Gadig and El-Deir1999; Revizee documents). Subsequently, we searched the curriculum of researchers who monitored fisheries or sampled fish, as well as looking for references from these documents to look for older references that had not appeared in the searches to try to go back historically to who had made the first record of a elasmobranch in the state. The bibliographic material underwent a critical data evaluation considering the current nomenclature and obvious mistakes and/or uncertainties in the identification or capture location.
3) Sampling at fisheries landings and fisheries monitoring onboard commercial vessels: (1) Between October 2016 and January 2023, 33 fisheries landings monitoring and 33 onboard fisheries monitoring in southern Espírito Santo (Marataízes, Itapemirim, Piúma, Anchieta and Guarapari municipalities) of surface gillnet, surface longline, bottom trawling and beach hauling fishing were made; (2) Observations of 12 onboard fisheries monitoring in bottom gillnet fishing vessels were carried out monthly between April 2018 and March 2019 in northern Espírito Santo (Conceição da Barra, São Mateus, and Linhares municipalities). Elasmobranchs were identified at the lowest taxonomic level possible in the field or at the laboratory for specimens that were difficult to identify in the field. The species were identified based on Bigelow and Schroeder (Reference Bigelow and Schroeder1948, Reference Bigelow and Schroeder1953 – for general sharks and rays); Figueiredo (Reference Figueiredo1977 – for southeast Brazilian sharks and rays); Garrick (Reference Garrick1982 - Carcharhinus spp. Blainville, Reference Blainville1816); Compagno (Reference Compagno1984a, Reference Compagno1984b – general sharks); Gadig (Reference Gadig2001 - Brazilian sharks); Gomes et al. (Reference Gomes, Signori, Gadig and Santos2010 - southeast Brazilian sharks and rays); Rosa and Gadig (Reference Rosa and Gadig2010 - Brazilian Mustelus spp. Linck, Reference Linck1790); Last et al. (Reference Last, White, Carvalho, Séret, Stehmann and Naylor2016 - general rays); Soares et al. (Reference Soares, Gomes and Carvalho2016 – Scyliorhinidae); Viana et al. (Reference Viana, Carvalho and Gomes2016 – for Squalus spp. Linnaeus, Reference Linnaeus1758).
Sampling was conducted under the approval of the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio, license #14258/5). In most cases, animal welfare laws, guidelines or policies were not applicable because no live fish was sampled or collected, with the specimens being sold to the public by fishermen.
Extinction risks were established at both the Brazilian and global levels, with the former employing the Brazilian Chondrichthyes Species Assessment (ICMBio, 2016) and, for endangered species, the most recent legislation that recognizes the National List of Endangered Species (Ministério do Meio Ambiente (GM/MMA), 2022), while the latter considered the International Union for the Conservation of Nature (IUCN) Threat Status Assessment (2022).
To establish a relationship between the most abundant orders, families, and genera, we made a bar graph with the R Program (version 4.3.3) (R Core Team, 2024) and the ggplot2 package (Wickham, Reference Wickham2016). For a better understanding of which orders were represented, illustrative images were taken from the website Phylopic.org (Keesey, Reference Keesey2024) and included in the chart using the Adobe Photoshop 2020 program. To construct the pie donut chart containing the classification of species extinction risks at a national and global level, we used, for shaping the graph, in addition to the previous program and package, the webr package (Moon, Reference Moon2020).
Results
The data obtained in our assessment indicated 10 orders, 28 families, 42 genera, and 79 species of elasmobranchs occurring on the coast of Espírito Santo, totalling 51 sharks and 28 rays (Table 1). The richest group was noted as the Carcharhiniformes order, comprising 29 species, 18 of them belonging to the Carcharhinidae family, five Sphyrnidae, three Triakidae, and three Scyliorhinidae. The Myliobatiformes order was the second most representative, consisting of 15 species, namely Dasyatidae (5), Myliobatidae (3), Mobulidae (3), Gymnuridae (2), and Aetobatidae (1) (Figure 2). Among the main sources of species records, the highlight was the review of literature data with 68 species, followed by landing and boarding sampling with 34 species and finally specimens collected in museums with 26 species (Table 1).
Table 1. Checklist of Chondrichthyes species known in Espírito Santo, Brazil
Types of evidence: Li, Literature; Mu, Museum (species recorded in ichthyological collections); Co, Collected. CR, Critically Endangered; EN, Endangered; VU, Vulnerable; NT, Near Threatened; LC, Least Concern; DD, Data Deficient; NE, Not Evaluated; BR, national assessment; IUCN, IUCN red list assessment.
Figure 2. Count of families, genus and species of Chondrichthyes orders recorded in Espírito Santo state, Brazil.
A first record for the Brazilian large-eyed stingray, Hypanus marianae (Gomes et al., Reference Gomes, Rosa and Gadig2000), was observed for Espírito Santo (Figure 3). A total of 43 specimens were identified during the onboard monitoring, 10 females and 33 males, with disc widths between 25.5 and 36 cm, captured with bottom gillnets at depths ranging from 16 to 49.8 m.
Figure 3. Male specimen of Hypanus marianae measuring 35 cm disc width and captured in December, 2018 northern Espírito Santo state, Brazil.
According to the Brazilian risk of extinction categorization, 42 species are listed as threatened, with 17 as Vulnerable, seven as Endangered, and 18 as Critically Endangered. When considering the global categorization, 52 species are listed as threatened, with 20 categorized as Vulnerable, 21 as Endangered, and 11 as Critically Endangered (Figure 4).
Figure 4. Extinction risk categories according to A national assessment and B IUCN red lists. CR: Critically Endangered; EN: Endangered; VU: Vulnerable; NT: Near Threatened; LC: Least Concern; DD: Data Deficient; NE: Not Evaluated.
Discussion
This study aimed to carry out a Chondrichthyes survey for the state of Espírito Santo through local specimens deposited in scientific collections, a literature review, and samples disembarked and shipped from various fisheries along the state's coast. As a detailed biodiversity investigation was proposed, all bibliographic material underwent a critical evaluation to precisely define the fauna attributed to the state. In addition, some exclusions of species previously recorded for Espírito Santo were conducted, detailed below.
Species belonging to the Holocephali subclass (chimeras) were not reported for Espírito Santo, as most of the data compiled herein indicate that records for this subclass are based on more accessible marine environments (pelagic zones and shallower areas) and consider that the representatives of this group inhabit deeper regions. However, Costa et al. (Reference Costa, Martins, Silva, Braga and Haimovici2000), in a demersal survey carried out by the REVIZEE Program, cite a Chimaera sp. Linnaeus, Reference Linnaeus1758 record for the central coast, although they do not indicate the sampling location (campaign carried out between 11° and 22° South) within a wide area involving the states of Bahia, Espírito Santo, and Rio de Janeiro. Studies in environments other than those routinely sampled by fisheries, such as slopes and deeper zones, therefore, display high potential for validating the occurrence of Chimaera sp. or that of other chimera species in the state of Espírito Santo.
Some large oceanic sharks, Hexanchus griseus (Bonaterre, 1788), Lamna nasus, Odontaspis noronhai Maul, Reference Maul1955, and Carcharhinus altimus (Springer, Reference Springer1950), cited by Amorim and Arfelli (Reference Amorim and Arfelli1992), were also not included in the list, as their capture locations were also not reported, and the study covered a wide area beyond the limits of the state of Espírito Santo. It is possible that these species occur or have occurred in the past in Espírito Santo, but the lack of capture location precision associated with the low number of sampled individuals from these species led us to not include them in the state's fauna list. On the other hand, the occurrence of Carcharhinus brachyurus (Günther, Reference Günther1870), Alopias vulpinus (Bonaterre, 1788), Carcharhinus signatus (Poey, Reference Poey1868), and Sphyrna mokarran (Rüppell, 1837) cited by Amorim and Arfelli (Reference Amorim and Arfelli1992) in the state of Espírito Santo was confirmed during the data collection carried out in the present study.
In another case, Somniosus pacificus Bigelow, Schroeder, 1944, was previously recorded for Espírito Santo (Nunan and Senna, Reference Nunan, Senna, Costa, Martins and Olavo2007). However, an image analysis identified the species as Somniosus antarcticus Whitley, Reference Whitley1939. This mistake in the identification of S. pacificus for the South Atlantic is also noted elsewhere (De Astarloa et al., Reference De Astarloa, Figueroa, Lucífora, Menni, Prenski and Chiaramonte1999) and was later corrected to S. antarcticus Whitley, Reference Whitley1939 by Yano et al. (Reference Yano, Stevens and Compagno2007).
For a long time, Brazilian specimens belonging to the genus Squalus were classified within species complexes, represented by three groups, namely acanthias (comprising Squalus acanthias Linnaeus, Reference Linnaeus1758, well defined), megalops/cubensis, and blainvillei/mitsukurii (Marques, Reference Marques1999; Gadig, Reference Gadig2001; Gomes et al., Reference Gomes, Signori, Gadig and Santos2010). Viana et al. (Reference Viana, Carvalho and Gomes2016) presented a revisionary study in this area in the western South Atlantic, describing four new species (S. albicaudus, S. bahiensis, S. lobularis, and S. quasimodo), allowing a more precise and exhaustive diagnosis features for the identification of Brazilian representatives. According to distributional data and descriptions carried out by Viana et al. (Reference Viana, Carvalho and Gomes2016), only Squalus albicaudus and S. lobularis were recorded for Espírito Santo, whereas S. mitsukurii Jordan & Snyder, 1903, S. megalops (MacLeay, Reference Macleay1881), S. cubensis Howell Rivero, Reference Howell Rivero1936, and S. blainville (Risso, Reference Risso1827), previously cited as occurring in the state of Espírito Santo (e.g. Ruschi, Reference Ruschi1965; Lessa et al., Reference Lessa, Santana, Rincón, Gadig and El-Deir1999; Martins et al., Reference Martins, Olavo, Costa, Costa, Martins and Olavo2005b; Nunan and Senna, Reference Nunan, Senna, Costa, Martins and Olavo2007), are now no longer part of the Brazilian fauna.
Another three species listed by Ruschi (Reference Ruschi1965) do not match their respective natural geographic areas and were, therefore, not included here, as follows: (1) Potamotrygon motoro (Müller and Henle, Reference Müller and Henle1841), a freshwater ray species occurring in Brazil only in the Amazonas, Mearim, and Parnaíba river basins (Lasso et al., Reference Lasso, Rosa, Sánchez-Duarte, Morales-Betancourt and Agudelo-Córdoba2016). The only evidence of this species is a specimen listed at the Prof. Mello Leitão Biology Museum (MBML-2048), however, with the capture site indicated as in the city of Manaus, in the Brazilian Amazon; (2) Paratrygon ajereba (Müller and Henle, Reference Müller and Henle1841), another freshwater stingray distributed only in the Brazilian Amazon river basin (Lasso et al., Reference Lasso, Rosa, Sánchez-Duarte, Morales-Betancourt and Agudelo-Córdoba2016); and (3) Leucoraja erinacea (Mitchill, Reference Mitchill1825), which displays a restricted geographical distribution on the east coast of Canada and northern USA (Last et al., Reference Last, White, Carvalho, Séret, Stehmann and Naylor2016). Ruschi (Reference Ruschi1965) also recorded Squatina squatina (Linnaeus, Reference Linnaeus1758), a restricted species from the Mediterranean Sea and Northwest African continent (Morey et al., Reference Morey, Barker, Hood, Gordon, Bartolí, Meyers, Ellis, Sharp, Jimenez-Alvarado and Pollom2019), possibly a mistaken identification of one of the Squatina genus species present in Espírito Santo since the angel sharks taxonomy in the western South Atlantic was solved in the 1990s (Vooren and da Silva, Reference Vooren and Da Silva1991).
Recently, a study carried out a molecular review of the genus Gymnura van Hasselt, Reference van Hasselt1823, which was used to reconstruct the evolutionary history of the Gymnuridae family (Gales et al., Reference Gales, Parsons, Biesack, Ready, Siccha-Ramirez, Rosa, Rosa, Rotundo, Bills, Rodrigues, Rodrigues-Filho, Mcdowell and Sales2024). According to the work, the lineage of Gymnura altavela present in the southeast and south of Brazil had already been classified as Gymnura hirundo (Lowe, Reference Lowe1843) from individuals collected in this region (Ribeiro, Reference Ribeiro1907; Bigelow and Schroeder, Reference Bigelow and Schroeder1953) and later synonymized as G. altavela. However, the type specimen of G. hirundo comes from the island of Madeira in the eastern Atlantic. They indicated, therefore, that the G. altavela present in the western South Atlantic is Gymnura valenciennii (initially described as Pteroplatea valenciennii) by Duméril (Reference Duméril1865) and later synonymized as G. altavela.
Data on shipments carried out on the northern coast of the state of Espírito Santo indicated the first record for the Brazilian large-eyed stingray H. marianae, representing the southernmost record of this endemic tropical species, as it had been recorded as far south only as the state of Bahia (Gomes et al., Reference Gomes, Rosa and Gadig2000). This record reinforces the need for further monitoring efforts in Espírito Santo, as the first records for species from more easily sampled places, such as H. marianae, were obtained from fisheries monitoring.
The species compiled herein represent 43% of marine elasmobranchs in Brazil (see Gadig and Rosa, Reference Gadig, Rosa, Kotas, Vizuete, Santos, Baggio, Salge and Barreto2023), indicating a relatively high diversity in Espírito Santo when considering the state's size compared to the entire country. The state displays significant potential for the inclusion of new species, mainly due to its high but not yet investigated marine environment diversity. This indicates that further research focused on elasmobranchs and investigations in environments difficult to access, such as slopes and deeper areas, may increase the number of known Chondrichthyes species for the state of Espírito Santo.
A concerning number of threatened species was noted with regard to the national and global red list conservation status, with 52.5% of the fauna recorded for the state of Espírito Santo categorized as threatened in Brazil and 65% of the fauna recorded for the state of Espírito Santo categorized as threatened globally. An Ordinance was recently published (Ministério do Meio Ambiente (GM/MMA), 2022) listing 60 elasmobranch species as threatened with extinction at some level. This indicates that the Chondrichthyes Espírito Santo fauna comprises 70% of the 60 threatened species in Brazil, reinforcing the need for further research and conservation in the state, as mentioned by other studies (Lessa et al., Reference Lessa, Santana, Rincón, Gadig and El-Deir1999).
Data
The datasets generated and analysed during the current study are not publicly available due to additional work currently in progress but are available from the corresponding author on reasonable request.
Acknowledgements
The authors would like to thank the Coordination for the Improvement of Higher Education Personnel (CAPES) for granting a master's scholarship to Guilherme dos Santos Lírio and CNPq for a productivity scholarship granted to Mauricio Hostim Silva (process: 312278/2017-9).
Author contributions
Conceptualization, JSN; methodology, JSN, GSL and MHS; formal analysis, JSN, GSL and JVCOM; data curation, JSN, GSL, JVCOM and OBFG; writing—original draft preparation, JSN and GSL; writing-review and editing, JSN, GSL, JVCOM, OBFG, MHS.
Financial support
Instituto Federal de Educação, Ciência e Tecnologia do Espírito Santo (Ifes) for the financial assistance (PRODIF 07/2023) granted for the English translation of this manuscript. Thanks are also due to FAPES for financial support for field trips through Public Notice FAPES 002/2016 - PPE Coastal Management (process 75921944/16) and for financial support for the ‘‘Elasmobranchs (sharks and rays) captured as by-catch fauna on the south coast of Espírito Santo’ project through Public Notice FAPES 014/2014 - Junior Scientific Initiation Program (Pesquisador do Futuro) (TO 338/2016; Protocol: 30695.419.25459.26042016).
Competing interests
The authors declare no conflict of interest.
Ethical standards
Sampling was conducted under the approval of the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio, license #14258/5).
