New Records of the Snow Bass Serranus Chionaraia (Perciformes: Serranidae) Confirm an Established Population in the Brazilian Province

Received: 5 June 2019 Accepted: 5 September 2019 DOI: 10.1111/jfb.14135

BRIEF COMMUNICATION FISH

New records of the snow bass Serranus chionaraia (Perciformes: Serranidae) confirm an established population in the Brazilian Province

Caio R. Pimentel1,2 | Ciro C. Vilar1,2 | Fernanda A. Rolim3 | Maria L. Abieri4 | Jean-Christophe Joyeux1

1Departamento de Oceanografia, Universidade Federal do Espírito Santo, Vitória, Espírito Abstract Santo, Brazil The snow bass Serranus chionaraia is a small-bodied reef fish presumed to be 2 Programa de Pós-Graduação em restricted to the Caribbean Province, with a single specimen captured south of the Oceanografia Ambiental, Universidade Federal do Espírito Santo, Vitória, Brazil Amazon River mouth. Recent surveys with baited remote underwater stereo-video 3Laboratório de Pesquisa em Elasmobrânquios, systems detected the species c. 1900 km southward. Meristic and morphometric Universidade Estadual Paulista, São Vicente, São Paulo, Brazil characters of two specimens examined in this study confirmed the species identity, 4Instituto de Biologia and SAGE/COPPE, which greatly extends the speciesʼ range southward on the eastern coast of Universidade Federal do Rio de Janeiro, Rio de Brazil and indicates the presence of an established population of S. chionaraia in the Janeiro, Brazil Brazilian Province. Correspondence Caio R. Pimentel, Departamento de KEYWORDS Oceanografia, Universidade Federal do Abrolhos Bank, BRUVS, mesophotic habitats, rhodolith beds, south-western Atlantic Ocean Espírito Santo, Avenida Fernando Ferrari, 514, Goiabeiras, 29075-910, Vitória, Espírito Santo, Brazil. Email: [email protected]; [email protected]

Funding information This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. CRP also thanks to Fundação Estadual de Amparo á Pesquisa do Estado do Espírito Santo (FAPES) for the PhD scholarship.

Nine Serranus Cuvier 1816 species are currently reported in the 211605), but there were no subsequent captures of snow bass off south-western Atlantic Ocean (Pinheiro et al., 2018), comprising the Brazilian coast (Carvalho-Filho, 1999; Rocha & Costa, 1999; one undescribed and eight formally described species. The latter Lessa & Nóbrega, 2000; Menezes et al., 2003; Hostim-Silva et al., include the snow bass Serranus chionaraia Robins & Starck 1961 2005; Sampaio & Nottingham, 2008; Nóbrega et al., 2009; Lindner, (Figure 1), which has a distribution previously presumed to be 2014; Rolim et al., 2017; Francini-Filho et al., 2019), only a single restricted to the Caribbean Province (Robins & Starck, 1961; visual record from the Abrolhos Archipelago, on the eastern coast Humann & Deloach, 2014). In 1963, however, the species was of Brazil (Carvalho-Filho & Ferreira, 2013; Pinheiro et al., 2018). recorded from c. 65 m depth in the Brazilian Province, south of the Therefore, the southern range limitofsnowbassisunclearand Amazon River mouth (Florida Museum of Natural History, UF except for the records of Robertson & Van Tassel (2015), published distributions do not include the Brazilian coast (Robins & Starck, Ethics statement Sampling complied with Brazilian laws and was authorized by the Federal 1961; Humann & Deloach, 2014; Froese & Pauly, 2019; Fricke Government under the environmental permits #57819-1. No surgical procedures or experiments were performed. et al., 2019).

The best practice recommendations of Bello et al. (2014) suggest a thorough examination of all current information (e.g., catalogues and collections) and to provide the most accurate and verifiable treatment of first record material (e.g., photographs, meristic and morphometric characters, voucher specimens). Following these guidelines, we confirm the occurrence of an established population of snow bass on the eastern coast of Brazil (18–19 S), a new southern limit for the species distribution. The new records were obtained through surveys with baited remote underwater stereo-video systems (stereo-BRUVS), near or over rhodolith (calcareous nodules of coralline red algae) beds in the Abrolhos Bank (May 2017 and 2018), state of Bahia, and in the Costa das Algas multiple-use marine protected area (MPA; April 2018), state of Espírito Santo (Figure 2). Twelve individuals were filmed at depths between 62 and 65 m in the Abrolhos Bank, and another eight individuals were recorded between 43 and 50 m in the Costa das Algas MPA. To confirm the species identity, in May 2018 three individuals from the Abrolhos Bank were collected at c.62m depth, through scuba diving and hand nets. The fish died during the return to the surface due to barotrauma caused by decompression. They were morphologically identified following Robins & Starck (1961) and a voucher specimen was deposited at the Museu Nacional do Rio de Janeiro (MNRJ 51422). We also conducted an extensive search in the main Brazilian ich- FIGURE 1 (a) Serranus chionaraia filmed in its natural habitat in thyological collections. One misidentified snow bass specimen was the Costa das Algas Marine Protected Area ( ) and (b) an individual photographed immediately after collection in the Abrolhos Bank, found at the Museu de Zoologia da Universidade Estadual de Feira de eastern coast of Brazil (standard length 54.0 mm; MNRJ 51422). Santana (MZFS 3691). This individual was caught in June 1999 off the Photo by R. L. Moura southern coast of the state of Bahia (Figure 2). Meristic (dorsal fin: X,

(a)

N 30°

20° (b)

10°

17° BBAA 0° Abrolhos MNP

10° 18° BBrazilrazil

20° EESS FIGURE 2 (a) Distribution of 19° 50 m previous records ( )ofSerranus chionaraia and holotype ( ) with the 200 m 30° new records obtained in this study ( ) Southwestern Atlanc 20° from (b) near the Abrolhos marine Vitória Costa das Algas MPA 40° 39° 38° national park (MNP) and within the 40° Costa das Algas marine protected area (MPA). Previous occurrence records were acquired from Global 50° 0 1,000 2,000 km Biodiversity Information website (www.gbif.org). BA: Bahia; ES: Espírito 90° 80° 70° 60° 50° 40° 30° Santo PIMENTEL ET AL. FISH 3

12; anal fin: III, 7; pectoral fin: 14; gill rakers: 13 + 8; caudal peduncle importance of this poorly studied but ecologically significant benthic scales: 15; pored lateral-line scales: 45; cheek scales: 7) and morpho- megahabitat, which is under severe anthropogenic impact. metric characters (standard length 50.28 mm; total length 62.41 mm; head length 18.93 mm; body depth 16.7 mm; eye diameter 5.88 mm; pos-orbital 10.22 mm) confirmed the species identity. Serranus ACKNOWLEDGEMENTS chionaraia also can be easily distinguished from all other congeners The authors thank the Brazilian National Council for Scientific and Tech- species inhabiting the Brazilian coast by its very conspicuous snow nological Development (CNPq), the Brazilian Fund for Biodiversity white belly and the dark cross bars on the upper and lower caudal rays (Funbio) and the Rede Abrolhos for logistic support. This work was par- (Figure 1; Robins & Starck, 1961; Humann & Deloach, 2014). tially supported by the Brazilian LTER Coastal Habitats of Espírito Santo These new records extend the species known range southward in (PELD-HCES; CNPq/FAPES grant #441243/2016-9). We are very a straight line by c. 1900 km or 17 latitude. As in the Caribbean thankful to Rodrigo L. Moura and Dilson S. Cajueiro Filho for collection (Robins & Starck, 1961; Humann & Deloach, 2014), snow bass is of the voucher specimen (Figure 1). We also thank Fabio Di Dario apparently uncommon on the eastern coast of Brazil. The species (NUPEM), Alexandre Clistenes and Jonas de Andrade (UEFS), Rodrigo occurred in less than 5% and 10% of the stereo-BRUVS deployments A. Caires (MZUSP), Cristiano R. Moreira and Lucas C. Garcia (MNRJ), in the Abrolhos Bank and Costa das Algas MPA, respectively, and rep- who generously provided information about voucher specimens consul- resented less than 1% of the total fish abundance in both sites. More- ted in this study, Maik S. C. da Hora, Patrícia Stelzer and Poliana Tinelli over, Simon et al. (2016) explored these same mesophotic habitats for sampling assistance, and Stephanie D. T. Delfino, Jairo P. Neto e Gui- and did not registered the species for the region. Based on previous lherme Malagutti for her help in analysing the stereo-BRUV recordings. observations and from our recordings, snow bass is a relatively seden- tary, bottom-dwelling species usually associated with mesophotic rhodolith beds (Robins & Starck, 1961; Humann & Deloach, 2014). ORCID This might be related to the high complexity of this habitat and to the Caio R. Pimentel https://orcid.org/0000-0003-4110-1249 availability of structures that enable the individuals to hide or camou- Ciro C. Vilar https://orcid.org/0000-0002-6656-2423 flage when frightened (Humann & Deloach, 2014; BRUVS recordings). Fernanda A. Rolim https://orcid.org/0000-0003-3761-3970 In contrast with expectations, our results indicate that snow bass is established in the Brazilian Province, rather than present as vagrant individuals. The scarcity of snow bass records in Brazil before our REFERENCES study appears to be related, at least in part, to the low sampling effort directed toward the ichthyofauna associated with rhodolith beds. This Amado-Filho, G. M., Moura, R. L., Bastos, A. C., Salgado, L. T., Sumida, P. Y., Guth, A. Z., … Thompson, F. L. (2012). Rhodolith beds is possibly due to the risks and difficulties associated with the tech- are major CaCO3 bio-factories in the tropical south West Atlantic. niques and logistics required to survey mesophotic habitats (Pinheiro PLoS One, 7(4), e35171. https://doi.org/10.1371/journal.pone. et al., 2015; Rosa et al., 2016; Simon et al., 2016; Rocha et al., 2018). 0035171. Brazil harbours the worldʼs largest continuous rhodolith beds Bello, G., Causse, R., Lipej, L., & Dulcic, J. (2014). A proposed best practice approach to overcome unverified and unverifiable “first records” in (Amado-Filho et al., 2012). These complex habitats cover almost the ichthyology. Cybium, 38(1), 9–14. – entire continental shelf, mainly in the mesophotic zone (30 150 m Bourguignon, S. N., Bastos, A. C., Quaresma, V. S., Vieira, F. V., depth), the tops of seamounts and the shelf around oceanic islands Pinheiro, H., Amado-Filho, G. M., … Teixeira, J. B. (2018). Seabed mor- (Horta et al., 2016). Brief explorations of mesophotic environments on phology and sedimentary regimes defining fishing grounds along the eastern Brazilian shelf. Geosciences, 8, 91. https://doi.org/10.3390/ the Brazilian coast (Carvalho-Filho & Ferreira, 2013; Simon et al., geosciences8030091. 2016; Smith-Vaniz et al., 2018; present study) and elsewhere have Carvalho Filho, A., & Ferreira, C. E. L. (2013). A new species of dwarf sea repeatedly demonstrated that many new species and occurrences bass, genus Serranus (Serranidae: Actinopterygii), from the southwest- remain to be discovered in this low-light zone. However, industrial ern Atlantic Ocean. Neotropical Ichthyology, 11(4), 809–814. https:// activities, particularly large-scale mining and hydrocarbon exploitation, doi.org/10.1590/S1679-62252013000400008. Carvalho-Filho, A. (1999). Peixes: Costa Brasileira (3rd ed., p. 320). São are already threatening some endangered, endemic and data deficient Paulo: Melro. species inhabiting rhodolith beds (Moura et al., 2013; Simon et al., Francini-Filho, R. B., Velásquez, V. M., Silva, M. B., Rosa, M. R., 2016). Other threats are bottom trawling and the aquarium trade in Sumida, P. Y. G., Pinheiro, H. T., … Rosa, R. S. (2019). Brazil. In Y. Loya, which sea basses are appreciated due to their attractive colour and K. A. Puglise, & T. C. L. Bridge (Eds.), Mesophotic coral ecosystems, coral reefs of the world 12. Cham, Switzerland: Springer. https://doi.org/10. easy maintenance. Despite southernmost known specimens being 1007/978-3-319-92735-0_10. localized within a multiple-use MPA (Figure 2), this region is a major Fricke, R., Eschmeyer, W. N. & Van der Laan, R. (eds) (2019). Eschmeyerʼs shrimp-fishing ground where intense trawling takes place catalog of fishes: genera, species, references. World Wide Web elec- (Bourguignon et al., 2018). The widespread exploitation of sea tronic publication. Retrieved from http://researcharchive.calacademy. org/research/ichthyology/catalog/fishcatmain.asp. resources even within Costa das Algas MPA arise concerns about Froese, R. & Pauly, D. (eds) (2019). FishBase: World Wide Web electronic human pressures on snow bass and other poorly-know organisms publication. Version (02/2019). Retrieved from http://www. associated with mesophotic ecosystems. Our findings highlight the fishbase.org. 4 FISH PIMENTEL ET AL.

Horta, P. A., Riul, P., Amado-Filho, G. M., Gurgel, C. F. D., Berchez, F., Robins, C. R., & Starck, W. A. (1961). Materials for a revision of Serranus Nunes, J. M. C., … Figueiredo, M. (2016). Rhodoliths in Brazil: Current and related fish genera. Proceedings of the Academy of Natural Sciences knowledge and potential impacts of climate change. Brazilian Journal of of Philadelphia, 113, 259–314. Oceanography, 64(2), 117–136 https://doi.org/10.1590/S1679- Rocha, L. O. F., & Costa, P. A. S. (1999). Manual de identificação de peixes 875920160870064sp2. marinhos para a Costa Central (p. 66). Rio de Janeiro, RJ, Brazil: Hostim-Silva, M., Andrade, A. B., Machado, L. F., Gerhardinger, L. C., Programa REVIZEE / SCORE-Central. Daros, F. A., Barreiros, J. P., & Godoy, E. A. S. (2005). Peixes de Costão Rocha, L. A., Pinheiro, H. T., Shepherd, B., Papastamatiou, Y. P., Luiz, O. J., Rochoso de Santa Catarina: I. Arvoredo (p. 135). Itajaí: Univale. Pyle, R. L., & Bongaerts, P. (2018). Mesophotic coral ecosystems are Humann, P., & Deloach, N. (2014). Reef fish identification: Florida, Carib- threatened and ecologically distinct from shallow water reefs. Science, bean, Bahamas. Interactive (4th ed.). Jacksonville, Florida: New World 361, 281–284. Publications, Inc. Rolim, F. A., Rodrigues, P. F. C., & Gadig, O. B. F. (2017). Peixes de recife Lessa, R., & Nóbrega, M. F. (2000). Guia de identificação de peixes marinhos rochoso: Estação Ecológica de Tupinambás (p. 80). São Paulo: Anolis da Região Nordeste (p. 128). Recife, PE, Brazil: Programa REVIZEE, Books. Score-NE. Rosa, M. R., Alves, A. C., Medeiros, D., Coni, E. O. C., Ferreira, C. M., Lindner, A. (2014). A vida marinha de Santa Catarina (p. 128p). Ferreira, B. P., … Francini-Filho, R. B. (2016). Mesophotic reef fish Florianópolis: UFSC. assemblages of the remote St. Peter and St. Paul's Archipelago, Mid- Menezes, N. A., Buckup, P. A., Figueiredo, J. L., & Moura, R. L. (2003). Atlantic Ridge, Brazil. Coral Reefs, 35, 113–123. Catálogo das espécies de peixes marinhos do Brasil (p. 160). São Paulo, Sampaio, C. L. S., & Nottingham, M. C. (2008). Guia para identificação de BR: Museu de Zoologia da Universidade de São Paulo. peixes ornamentais brasileiros - volume I: espécies marinhas (p. 205). Moura, R. L., Secchin, N. A., Amado-Filho, G. M., Francini-Filho, R. B., Brasília: Ibama. Freitas, M. O., Minte-Vera, C. V., … Bastos, A. C. (2013). Spatial pat- Simon, T., Pinheiro, H. T., Moura, R. L., Carvalho-Filho, A., Rocha, L. A., terns of benthic megahabitats and conservation planning in the Martins, A. S., … Joyeux, J.-C. (2016). Mesophotic fishes of the Abrolhos Bank. Continental Shelf Research, 70, 109–117. https://doi. Abrolhos Shelf, the largest reef ecosystem in the South Atlantic. Jour- org/10.1016/j.csr.2013.04.036. nal of Fish Biology, 89, 990–1001. https://doi.org/10.1111/jfb.12967. Nóbrega, M. F., Lessa, R., & Santana, F. M. (2009). Peixes Marinhos da reg- Smith-Vaniz, W. F., Tornabene, L., & Macieira, R. M. (2018). Review of Bra- ião Nordeste do Brasil (p. 208). Fortaleza: Martins & Cordeiro. zilian jawfishes of the genus Opistognathus with descriptions of two Pinheiro, H. T., Mazzei, E., Moura, R. L., Amado-Filho, G. M., Carvalho- new species (Teleostei, Opistognathidae). ZooKeys, 794,95–133. Filho, A., Braga, A. C., … Joyeux, J.-C. (2015). Fish biodiversity of the https://doi.org/10.3897/zookeys.794.26789. vitória-trindade seamount chain, Southwestern Atlantic: An updated database. PLoS One, 10, e0118180. Pinheiro, H. T., Rocha, L. A., Macieira, R. M., Carvalho-Filho, A., Anderson, A. B., Bender, M. G., … Floeter, S. R. (2018). South-western How to cite this article: Pimentel CR, Vilar CC, Rolim FA, Atlantic reef fishes: Zoogeographical patterns and ecological drivers Abieri ML, Joyeux J-C. New records of the snow bass Serranus reveal a secondary biodiversity centre in the Atlantic Ocean. Diversity chionaraia (Perciformes: Serranidae) confirm an established and Distributions, 24, 951–965. population in the Brazilian Province. J Fish Biol. 2019;1–4. Robertson, D. R., & Van Tassell, J. (2015). Shorefishes of the Greater Carib- bean: online information system. Version 1.0. Balboa, Panamá: https://doi.org/10.1111/jfb.14135 Smithsonian Tropical Research Institute.