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Reef fishes of the Anchieta Island State Park, Southwestern Atlantic, Brazil

Peixes recifais do Parque Estadual da Ilha Anchieta, Sudoeste do Atlântico, Brasil

Abstract

This paper presents a checklist of the reef fish fauna of the Anchieta Island State Park, a no-take zone in which no extractive activities are allowed, in Ubatuba, Southeastern Brazil. Data was obtained between 2011 and 2013, mainly through underwater observations with snorkelling and SCUBA, and secondarily using scientific fishing (trawling). Published and unpublished data were also verified and compiled. A total of 103 reef fish species, distributed in 78 genus and 50 families was recorded. Haemulidae was the richest family (n=7 species), followed by Epinephelidae (n=6), Pomacentridae, Carangidae and Tetraodontidae (n= 4 each). Haemulon was also the most speciose genera (n=5), followed by Stegastes, Acanthurus and Mycteroperca (n=3 each). Sixty-nine species (67%) are included in global and regional Red Lists. Twenty-five species (24.2%) are within the categories Critically Endangered (CR), Endangered (EN), Vulnerable (VU) and Near-Threathened (NT). The network of Marine Protected Areas in Southeastern Brazil is still incipient, and the considerable number of threatened species in the Anchieta Island State Park clearly indicates the importance of the study area for the conservation of coastal and reef fishes.

Key words:
rocky reefs; species richness; scientific diving; ichthyology; conservation

Resumo

Este artigo apresenta uma lista de espécies de peixes recifais do Parque Estadual da Ilha Anchieta, uma área na qual nenhuma atividade extrativista é permitida, em Ubatuba, Sudeste do Brasil. Os dados foram coletados entre 2011 e 2013, principalmente por observações subaquáticas com o uso de mergulhos livres e autônomos e, secundariamente, através de pescaria científica (arrasto). Dados publicados e não publicados também foram verificados e compilados. Foram registradas 103 espécies de peixes recifais distribuídas em 78 gêneros e 50 famílias. Haemulidae foi a família com maior número de espécies (n=7 espécies), seguida por Epinephelidae (n=6), Pomacentridae, Carangidae e Tetraodontidae (n=4 cada). Os gêneros com maior número de espécies foram Haemulon (n=5) e Stegastes¸ Acanthurus e Mycteroperca (n=3 cada). Sessenta e nove espécies (67%) estão inclusas em listas vermelhas de espécies ameaçadas globais e regionais. Vinte e cinco espécies (24,2%) são classificadas nas categorias Criticamente em Perigo (CR), Em Perigo (EN), Vulnerável (VU) e Quase Ameaçadas (NT). A rede de Áreas Marinhas Protegidas no Sudeste do Brasil ainda é incipiente e o considerável número de espécies ameaçadas no Parque Estadual da Ilha Anchieta indica claramente a importância da área de estudo para a conservação de peixes recifais e costeiros.

Palavras-chave:
recifes rochosos; riqueza de espécies; mergulho científico; ictiologia; conservação

Introduction

In Brazil, coralline and sandstone reefs occur in the Northern, Northeastern and Central coast from the Amazon River mouth south to the Doce River mouth, off Espírito Santo State (~19o50’S) (Moura et al. 2013MOURA, R.L., SECCHIN, N.A., AMADO-FILHO, G.M., FRANCINI-FILHO, R.B., FREITAS, M.O., MINTE-VERA, C.V., ... & GUTH, A.Z. 2013. Spatial patterns of benthic megahabitats and conservation planning in the Abrolhos Bank. Cont. Shelf. Res. 70: 109-117., 2016MOURA, R.L., AMADO-FILHO, G.M., MORAES, F.C., BRASILEIRO, P.S., SALOMON, P.S., MAHIQUES, M.M., ... & BRITO, F.P. 2016. An extensive reef system at the Amazon River mouth. Science Advances. 2(4): e1501252., Pinheiro et al. 2015aPINHEIRO, H.T., MAZZEI, E., MOURA, R.L., AMADO-FILHO, G.M., CARVALHO-FILHO, A., BRAGA, A.C., ... & FRANCINI-FILHO, R.B. 2015a. Fish biodiversity of the Vitória-Trindade Seamount Chain, southwestern Atlantic: an updated database. PloS one. 10(3): e0118180.), while rocky reefs predominate in the subtropical portion of the coast, southwards to Rio Grande do Sul State (~32o30’S), as well as in the three oceanic archipelagos (Ferreira et al. 2001FERREIRA, C.E.L., GONÇALVES, J.E.A. & COUTINHO, R. 2001. Community structure of fishes and habitat complexity on a tropical rocky shore. Environ. Biol. Fish. 61: 353–369., 2004FERREIRA, C.E.L., FLOETER, S.R., GASPARINI, J.L., FERREIRA, B.P. & JOYEUX, J.C. 2004. Trophic structure patterns of Brazilian reef fishes: a latitudinal comparison. J. Biogeogr. 31: 1093–1106., Krajewski & Floeter 2011KRAJEWSKI, J.P. & FLOETER, S.R. 2011. Reef fish community structure of the Fernando de Noronha Archipelago (Equatorial Western Atlantic): the influence of exposure and benthic composition. Environ. Biol. Fish., 92(1), 25., Magalhães et al. 2015MAGALHÃES, G.M., AMADO-FILHO, G.M., ROSA, M.R., MOURA, R.L., BRASILEIRO, P.S., MORAES, F.C., ... & PEREIRA-FILHO, G.H. 2015. Changes in benthic communities along a 0–60 m depth gradient in the remote St. Peter and St. Paul Archipelago (Mid-Atlantic Ridge, Brazil). B. Mar. Sci. 91(3), 377-396.). The physical complexity of coralline and rocky reefs is associated to a remarkably high diversity of fish and several other groups, which overcomes that of any other aquatic habitat (Reaka-Kudla 1997REAKA-KUDLA, M. 1997. The global biodiversity of coral reefs: a comparison with rain forests. Joseph Henry Press. Washington, DC.: 83–108., Spalding et al. 2001SPALDING, M., CORINNA, R. & EDMUND, P.G. 2001. World atlas of coral reefs. University of California Press, London.). Reefs increase shelter and provide feeding habitats for a broad taxonomic spectrum of fishes with specific morphological and functional adaptations, the so-called reef fishes (Luckhurst & Luckhurst 1978LUCKHURST, B.E. & LUCKHURST, K. 1978. Analysis of the influence of substrate variables on coral reef fish communities. Mar Biol. 49: 317–323., Alvarez-Filip et al. 2009ALVAREZ-FILIP, L., DULVY, N.K., GILL, J.A., CÔTÉ, I.M. & WATKINSON, A.R. 2009. Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. P. Roy. Soc. Lond. B Bio. 276: 3019-3025., Ménard et al. 2012MÉNARD, A., TURGEON, K., ROCHE, D.G., BINNING, S.A. & KRAMER, D.L. 2012. Shelters and their use by fishes on fringing coral reefs. PloS one,7(6): e38450, Nunes et al. 2015NUNES, J.A.C.C., SAMPAIO, C.L.S.& BARROS, F. 2015. The influence of structural complexity and reef habitat types on flight initiation distance and escape behaviors in labrid fishes. Mar. Biol. 162(3): 493-499.).

Because the southeastern of Brazilian Coast is located in a transition zone between tropical and subtropical sharing a reef fish fauna of both regions (Floeter et al. 2001FLOETER S.R., GUIMARÃES R.Z.P., ROCHA L.A., FERREIRA C.E.L., RANGEL C.A. & GASPARINI J.L. 2001. Geographic variation in reef-fish assemblages along the Brazilian coast. Global Ecol. Biogeogr. 10: 423-431.), the region's rocky reefs may present higher local (alpha) diversity of reef fishes than coralline reefs (e.g. Moura & Francini-Filho 2005MOURA, R.L. & FRANCINI-FILHO, R.B. 2005. Reef and shore fishes of the Abrolhos Region, Brazil. Washington, DC: RAP Bulletin of Biological Assessment, 38: 40-55., Gibran & Moura 2012GIBRAN, F.Z. & MOURA, R.L. 2012. The structure of rocky reef fish assemblages across a nearshore to coastal islands' gradient in southeastern Brazil. Neotrop. Ichthyol. 10: 369–382.), and may be considered biodiversity hotspots, akin to patterns recorded in “marginal” areas of other biogeographic regions (Aburto‐Oropeza & Balart 2001ABURTO‐OROPEZA, O. & BALART, E.F. 2001. Community structure of reef fish in several habitats of a rocky reef in the Gulf of California. Mar Ecol. 22: 283–305., Sala et al. 2012SALA, E., BALLESTEROS, E., DENDRINOS, P., DI FRANCO, A., FERRETTI, F., FOLEY, D., ... & GUIDETTI, P. 2012. The structure of Mediterranean rocky reef ecosystems across environmental and human gradients, and conservation implications. PloS one. 7(2): e32742.). The Brazilian coralline reef area represent 0.4% of global reef area, with 20% of reef fishes endemism, which represent a priority in conservation (Moura 2003MOURA, R.L. 2003. Brazilian reefs as priority areas for biodiversity conservation in the Atlantic Ocean, Proceedings of the 9th International Coral Reef Syposium 9(2): 917-920., Moura & Francini-Filho 2005MOURA, R.L. & FRANCINI-FILHO, R.B. 2005. Reef and shore fishes of the Abrolhos Region, Brazil. Washington, DC: RAP Bulletin of Biological Assessment, 38: 40-55., Gibran & Moura 2012GIBRAN, F.Z. & MOURA, R.L. 2012. The structure of rocky reef fish assemblages across a nearshore to coastal islands' gradient in southeastern Brazil. Neotrop. Ichthyol. 10: 369–382.).

Information about fish assemblages associated to Brazilian subtropical rocky reefs steadily increased in the last two decades (e.g. Luiz Jr. & Floeter 2004LUIZ JR, O. & FLOETER, S.R. 2004. Occurrence of Acanthurus monroviae (Perciformes: Acanthuridae) in the south‐western Atlantic, with comments on other eastern Atlantic reef fishes occurring in Brazil. J. Fish Biol. 65: 1173–1179., Bonaldo et al. 2005BONALDO, R.M., KRAJEWSKI, J.P. & SAZIMA, I. 2005. Meals for two: foraging activity of the butterflyfish Chaetodon striatus (Perciformes) in Southeast Brazil. Braz. J. Biol. 65: 211–215., Floeter et al. 2006FLOETER, S.R., HALPERN, B.S. & FERREIRA, C.E.L. 2006. Effects of fishing and protection on Brazilian reef fishes. Bio. Conserv. 128: 391–402., Luiz Jr. et al. 2008LUIZ JR, O., CARVALHO-FILHO, A. & FERREIRA, C.E.L. 2008. The reef fish assemblage of the Laje de Santos Marine State Park, southwestern Atlantic: annotated checklist with comments on abundance, distribution, trophic structure, symbiotic associations and conservation. Zootaxa 25: 1–25., Gibran & Moura 2012GIBRAN, F.Z. & MOURA, R.L. 2012. The structure of rocky reef fish assemblages across a nearshore to coastal islands' gradient in southeastern Brazil. Neotrop. Ichthyol. 10: 369–382., Teixeira-Neves et al. 2015TEIXEIRA-NEVES, T.P., NEVES, L.M. & ARAÚJO, F.G. 2015. Hierarchizing biological, physical and anthropogenic factors influencing the structures of fish assemblages along tropical rocky shores in Brazil. Environ. Biol. Fish, 98(6): 1645-1657., Neves et al. 2016NEVES, L.M., TEIXEIRA-NEVES, T.P., PEREIRA-FILHO, G.H. & ARAÚJO, F. G. 2016. The Farther the Better: Effects of Multiple Environmental Variables on Reef Fish Assemblages along a Distance Gradient from River Influences. PloS one, 11(12): e0166679.). However, major geographic gaps still remain along this broad (~2,000 km) and highly threatened (e.g. Gibran & Moura 2012GIBRAN, F.Z. & MOURA, R.L. 2012. The structure of rocky reef fish assemblages across a nearshore to coastal islands' gradient in southeastern Brazil. Neotrop. Ichthyol. 10: 369–382.) extension of the Brazilian coast, where the country´s population is concentrated within less than 100 km from shoreline (IBGE 2016IBGE - INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA 2016. Arranjos populacionais e concentrações urbanas no Brasil/ IBGE, Coordenação de Geografia. 2 ed. Rio de Janeiro.) with several multiple and interacting environmental stressors (pollution, harbors, tourism and fishing) are observed. Such information gaps are particularly relevant for the ongoing development of management plans for the large multiple-use Marine Protected Areas (MPAs) that have been established along most of coast of the State of São Paulo.

Fish faunal assessments in the north coast of São Paulo are concentrated on demersal species associated to unconsolidated substrates (e.g. Cunningham 1983CUNNINGHAM, P.T.M. 1983. Estudo comparativo da ictiofauna da costa oeste e Enseada das Palmas da Ilha Anchieta, Enseada do Flamengo e Enseada da Fortaleza (LAT. 23°29’S - 23°33'S, LONG. 45°03'W - 45°09'W), Ubatuba, Estado de São Paulo - Brasil. Tese de doutorado, Universidade de São Paulo, São Paulo., Nonato et al. 1983NONATO, E.F., AMARAL, A.C.Z. & FIGUEIREDO, J.L. 1983. Contribuição ao conhecimento da fauna de peixes do litoral norte do Estado de São Paulo. Boletim Instituto Oceanográfico. 32: 143–152., Braga & Goitein 1984BRAGA, F.M.S. & GOITEIN, R. 1984. Lista prévia das espécies de peixes demersais na região da Ilha Anchieta (LAT. 23°33’S - LONG. 45°05'W), Ubatuba, litoral norte do Estado de São Paulo, Brasil. Naturalia. 9: 61–72., Rocha et al. 2010ROCHA, M.L.C.F., FERNANDEZ, W.S. & FILHO, A.M.P. 2010. Spatial and temporal distribution of fish in Palmas Bay, Ubatuba, Brazil. Braz. J. Oceanogr. 58: 31–43.). Only two reef fish assessments were carried out in the vicinity of the Anchieta Island State Park (AISP), the protected area focused by the present study. One of these studies tested the use of artificial reefs for habitat restoration (Cunningham & Saul, 2004CUNNINGHAM, P.T.M. & SAUL, A.C. 2004. Spatial partition of artificial structures by fish at the surroundings of the conservation unit-Parque Estadual da Ilha Anchieta, SP, Brazil. Braz. Arch. Biol. Tech. 47: 113–120.) and the other was focused on cleaning symbiosis, involving 35 fish species (Sazima et al. 2000SAZIMA, I., SAZIMA, C., FRANCINI-FILHO, R.B. & MOURA, R.L. 2000. Daily cleaning activity and diversity of clients of the barber goby, Elacatinus figaro, on rocky reefs in southeastern Brazil. Environ. Biol. Fish. 59: 69–77.). Here, we provide a checklist of teleosts and elasmobranchs of the AISP and comment upon the known distribution and conservation status of the recorded species. The information provided herein fill a relevant gap about local reef fish communities and contribute to the future management plans of the AISP and MPAs around.

Material and Methods

1. Study represent 0.4% of global reef area

Sampling was carried out between 2011 and 2013 in the AISP, municipality of Ubatuba, northern coast of São Paulo (23°31’-23°34’S, 45°02’-45°05’W) (Figure 1). The AISP was created in 1977 by the State Government (Decree 9,629, March 29 1977), covering the terrestrial part of the island. In 1983, a fishing ban perimeter with 17.37 km2 was established around the AISP (Portaria SUDEPE 56, November 10 1983). This perimeter is relatively well enforced, due to the considerable movement of people who visit the park. In addition, the park's own security guards carry out frequent inspections around the island. Anchieta Island is separated from the mainland by a narrow (0.5 km) and relatively deep (33 m) channel. Its shoreline is predominantly granitic, with the exception of a 1.5 km length sandy beach in its northern, shallower and less exposed side. Depths reach up to 37 m around the island, with a benthic mosaic encompassing sandy, gravel and rocky bottom (Guillaumon et al. 1989GUILLAUMON, J.R., MARCONDES, M.A.P., NEGREIROS, O.D., MOTA, I.S., EMMERICH, W., BARBOSA, A.F. & SCORVO FILHO, J.D. 1989. Plano de Manejo do Parque Estadual da Ilha Anchieta. São Paulo: Instituto Florestal.).

Figure 1
Study area, (A) Brazil in grey, São Paulo State in black and north coast of São Paulo inside the circle; (B) Anchieta Island inside the circle with the points of data collect: specific for this work (squares), Cunningham & Saul 2004 (triangle) and the area of bottom trawling (lines); (C) photograph of the Anchieta Island (credits: http://www.ambiente.sp.gov.br/parque-ilha-anchieta/galeria-de-fotos/).

2. Data collection

The checklist was compiled from snorkelling and SCUBA observations, scientific bottom trawling operations (research permit – SISBIO nº 32352-3), as well as from published (e.g. Sazima et al. 2000SAZIMA, I., SAZIMA, C., FRANCINI-FILHO, R.B. & MOURA, R.L. 2000. Daily cleaning activity and diversity of clients of the barber goby, Elacatinus figaro, on rocky reefs in southeastern Brazil. Environ. Biol. Fish. 59: 69–77. and Cunningham & Saul 2004CUNNINGHAM, P.T.M. & SAUL, A.C. 2004. Spatial partition of artificial structures by fish at the surroundings of the conservation unit-Parque Estadual da Ilha Anchieta, SP, Brazil. Braz. Arch. Biol. Tech. 47: 113–120.) and unpublished data (e.g. museum records – ZUEC). In total, 142 hours were spent on dives: (i) 20 hours with snorkelling and SCUBA for this work; (ii) 42 hours by Sazima et al. (2000)SAZIMA, I., SAZIMA, C., FRANCINI-FILHO, R.B. & MOURA, R.L. 2000. Daily cleaning activity and diversity of clients of the barber goby, Elacatinus figaro, on rocky reefs in southeastern Brazil. Environ. Biol. Fish. 59: 69–77.; and (iii) 80 hours by Cunningham & Saul (2004)CUNNINGHAM, P.T.M. & SAUL, A.C. 2004. Spatial partition of artificial structures by fish at the surroundings of the conservation unit-Parque Estadual da Ilha Anchieta, SP, Brazil. Braz. Arch. Biol. Tech. 47: 113–120.. Dives were concentrated in the south and east sides of the island (i.e. South Beach and East Beach), and inside Palmas Bay, a cove in the west face of the island with depths of up to 12 m. All the reef fish observed during the dives were noted and, eventually, divers searched for cryptic species beneath crevices and rocks. Considering the different samplings, dives were carried over a depth range of 2-17 meters (for more details see Sazima et al. 2000SAZIMA, I., SAZIMA, C., FRANCINI-FILHO, R.B. & MOURA, R.L. 2000. Daily cleaning activity and diversity of clients of the barber goby, Elacatinus figaro, on rocky reefs in southeastern Brazil. Environ. Biol. Fish. 59: 69–77. and Cunningham & Saul 2004CUNNINGHAM, P.T.M. & SAUL, A.C. 2004. Spatial partition of artificial structures by fish at the surroundings of the conservation unit-Parque Estadual da Ilha Anchieta, SP, Brazil. Braz. Arch. Biol. Tech. 47: 113–120.). Twelve bottom trawls of 12 minutes each were carried out around the island, in the sand substrate adjacent to the rocky reefs, between 10 and 16 m depths. The trawl had 25mm of mesh size, three meters height and 7 meters length.

Identifications were based on Menezes & Figueiredo (1980MENEZES, N.A. & FIGUEIREDO, J.L. 1980. Manual de peixes marinhos do sudeste do Brasil: IV. Teleostei (3). São Paulo: Museu de Zoologia da Universidade de São Paulo., 1985MENEZES, N.A. & FIGUEIREDO, J.L. 1985. Manual de peixes marinhos do sudeste do Brasil: V Teleostei (4). São Paulo: Museu de Zoologia da Universidade de São Paulo.), Figueiredo & Menezes (1978FIGUEIREDO, J.L. & MENEZES, N.A. 1978. Manual de peixes marinhos do sudeste do Brasil: II. Teleostei (1). São Paulo: Museu de Zoologia da Universidade de São Paulo., 1980FIGUEIREDO, J.L. & MENEZES, N.A. 1980. Manual de peixes marinhos do sudeste do Brasil: II. Teleostei (2). São Paulo: Museu de Zoologia da Universidade de São Paulo., 2000FIGUEIREDO, J.L. & MENEZES, N.A. 2000. Manual de peixes marinhos do sudeste do Brasil: VI. Teleostei (5). São Paulo: Museu de Zoologia da Universidade de São Paulo.), and Humann & DeLoach (2002)HUMMAN, P. & DELOACH, N. 2002. Reef fish identification: Florida, Caribbean, Bahamas. 3 ed. New World Publications, Inc. Florida.. The species were organized alphabetically within families, following Betancur-R et al. (2014)BETANCUR-R, R., WILEY, E., BAILLY, N., MIYA, M., LECOINTRE, G. & ORTÍ, G. 2014. Phylogenetic classification of bony fishes--Version 3. http://www.deepfin.org/Classification_v3.htm.
http://www.deepfin.org/Classification_v3...
for teleosts, Rosa & Gadig (2014)ROSA R.S. & GADIG O.B.F. 2014. Conhecimento da diversidade dos Chondrichthyes marinhos no Brasil: a contribuição de José Lima de Figueiredo. Arquivos de Zoologia 45: 89–104. for sharks and Last et al. (2016)LAST, P.R., WHITE, W.T., CARVALHO, M.R., SÉRET, B., STEHMANN, M.F.W. & NAYLOR, G.J.P. 2016. Rays of the World. 1 ed. CSIRO Publishing, Clayton South, AU. for rays. Reef fish were considered as species that spend most of their time associated with consolidate substrates, and that commonly use these habitats for feeding, shelter or reproduction, including nektonic species (cf. Luiz Jr. et al. 2008LUIZ JR, O., CARVALHO-FILHO, A. & FERREIRA, C.E.L. 2008. The reef fish assemblage of the Laje de Santos Marine State Park, southwestern Atlantic: annotated checklist with comments on abundance, distribution, trophic structure, symbiotic associations and conservation. Zootaxa 25: 1–25.). Geographical distributions followed Luiz Jr. et al. (2008)LUIZ JR, O., CARVALHO-FILHO, A. & FERREIRA, C.E.L. 2008. The reef fish assemblage of the Laje de Santos Marine State Park, southwestern Atlantic: annotated checklist with comments on abundance, distribution, trophic structure, symbiotic associations and conservation. Zootaxa 25: 1–25., where: CT, Circumtropical; SE, Southeastern Brazil (endemic from between 20 - 27° S); TA, Trans-Atlantic (both sides of the Atlantic); WA, Western Atlantic (Northern and Southwestern Atlantic); BR, Brazilian Province endemic; SCa, Southern Caribbean (Venezuela, Trinidad and Tobago and other nearby islands); Pat, Patagonian (primarily occurring in temperate rocky reefs south to Argentina); EA, Eastern Atlantic. Conservation status were based on the International Red List of threatened species (IUCN – International Union for Conservation of Nature), the National Endangered Fauna – Fish and Aquatic Invertebrates (MMAMMA - MINISTÉRIO DO MEIO AMBIENTE. 2014. Portaria MMA n°445, de 17 de Dezembro de 2014. Diário Oficial da União 18/12/2014 - Seção 01: 126. – Ministério do Meio Ambiente) and on the São Paulo State List of threatened species (SMA – Secretaria do Meio Ambiente). Although the classification “Near Threatened (NT) is often not considered a threatened species, we have decided to include it because species in this category may be considered threatened in the near future.

As non-lethal methods were primarily adopted, “voucher-specimens” were stored as videos and photos in the ichthyological collection “Victor Sadowsky – UNESP Registro” (SADUNESP#0001). Specimens collected during past surveys (e.g. Sazima et al. 2000SAZIMA, I., SAZIMA, C., FRANCINI-FILHO, R.B. & MOURA, R.L. 2000. Daily cleaning activity and diversity of clients of the barber goby, Elacatinus figaro, on rocky reefs in southeastern Brazil. Environ. Biol. Fish. 59: 69–77.) were also deposited at the Museu de Zoologia/Universidade Estadual de Campinas - ZUEC Coleção de Peixes/Fish Collection.

Results

A total of 103 species belonging to 78 genera and 49 families were recorded (Table 1), comprising 16 elasmobranchs and 87 actinopterygians. Haemulidae (n=7 species; 6.7%) and Epinephelidae (n=6; 5.8%) were the richest families. Haemulon (n=5 species) was the most speciose genus, followed by Stegastes, Acanthurus and Mycteroperca (n=3 each). With almost 90% of the geographic range classifications, the species classified as Western Atlantic, Trans-Atlantic and Circumtropical were dominant (56%, 17% and 14% respectively) (Figure 2).

Table 1
– Checklist of the reef fish species recorded at the Anchieta Island State Park. Geographic Range: CT, Circumtropical; SE, Southeastern Brazil; TA, Trans-Atlantic; WA, Western Atlantic; BR, Brazilian province; SCa, Southern Caribbean; Pat, Patagonian; EA, Eastern Atlantic. Main Threats: OF, Overfishing; BC, Bycatch; AT, Aquarium Trade. IUCNIUCN - ITERNATIONAL UNION FOR CONSERVATION OF NATURE. 2014. The IUCN Red List of Threatened Species. Version 2014.2. www.iucnredlist.org. (last acess November 8).: CR, Critically Endangered; EN, Endangered; VU, Vulnerable; NT, Near Threatened; LC, Least Concern. BRAZIL: CR, Critically Endangered; VU, Vulnerable; SÃO PAULO STATE: NT, Near Threatened; NMA, Need Management Action; DD, Deficient Data. Record type: VIS, Visually (underwater observation); CTF, Scientific Fisheries; UND, Unpublished Data (Sazima et al.); REP, Reports (O.B.F. Gadig); PHO, Photographic Record; LIT, Literature (Sazima et al., 2000SAZIMA, I., SAZIMA, C., FRANCINI-FILHO, R.B. & MOURA, R.L. 2000. Daily cleaning activity and diversity of clients of the barber goby, Elacatinus figaro, on rocky reefs in southeastern Brazil. Environ. Biol. Fish. 59: 69–77.; Cunningham & Saul, 2004CUNNINGHAM, P.T.M. & SAUL, A.C. 2004. Spatial partition of artificial structures by fish at the surroundings of the conservation unit-Parque Estadual da Ilha Anchieta, SP, Brazil. Braz. Arch. Biol. Tech. 47: 113–120.); MUS, Museum Vaucher (ZUEC).
Figure 2
Geographic distribution of the species recorded at Anchieta Island State Park: WA, Western Atlantic (Northern and Southern West Atlantic); TA, Trans-Atlantic (both sides of the Atlantic); CT, Circumtropical; BR, Brazilian Province; SE, Southeastern Brazil (20- 27° S); ; SCa, Southern Caribbean (Venezuela, Trinidad and Tobago and other neighboring islands); CA, Central Atlantic; Pat, Patagonian (primarily in temperate rocky reefs south to Argentina); EA, Eastern Atlantic.

Sixty-nine species (67%) had their conservation status evaluated in at least one geographic scale, with 25 included within categories Critically Endangered (CR), Endangered (EN), Vulnerable (VU) and Near-Threathened (NT) (Table 1), eight of these species are represented in Figure 3. Highlighting some species that are highly targeted by fisheries, we had most from the Epinephelidae family, such as Epinephelus marginatus, E. morio, Hyporthodus niveatus and Mycteroperca bonaci, and some taxa of Lutjanidae like Lujanus analis.

Figure 3
Some species included within threatened categories that were recovered on the AISP. A, Elacatinus figaro Sazima, Moura & Rosa, 1997 (<2cm); B, Lutjanus analis (Cuvier, 1828); C, Pomacanthus paru (Bloch, 1787) (juvenile) (2-10cm); D, Sparisoma axillare (Steindachner, 1878) (terminal phase) (>30cm); E, Epinephelus marginatus (Lowe, 1834); F, Hyporthodus niveatus (Valenciennes, 1828) (juvenile) (2-10cm); G, Mycteroperca acutirostris (Valenciennes, 1828); H, Mycteroperca interstitialis (Poey, 1860) (juvenile) (2-10cm).

Discussion

We provide a checklist of 103 reef fishes that occur in the AISP, 77 of which appearing for the first time in the literature for this area. Seventeen (22%) species refer to elasmobranchs which, due to specific habits and extremely reduced abundance, are only rarely recorded in faunal surveys, especially using visual census. The fact that several elasmobranchs were recorded by consulting experts, highlight the importance of secondary unpublished data. The use of BRUVS (Baited Remoted Underwater Video Stations) was also particularly relevant, once this tool allows recording species that often remain unseen by divers, such as elasmobranchs. Its use along the Brazilian coast is recent, but preliminary results have shown great potential to record sharks and rays in reef environments (Rolim et al. 2017ROLIM, F.A., RODRIGUES, P.F.C. & GADIG, O.B.F. 2017. Peixes de recife rochoso: Estação Ecológica de Tupinambás - São Paulo. 1. ed. Curitiba: Anolis Books, 2017. v. 1. 80p). For instance, we recorded comparatively more reef fish species than other surveys conducted in nearby areas, i.e. 106 species in Gibran & Moura (2012)GIBRAN, F.Z. & MOURA, R.L. 2012. The structure of rocky reef fish assemblages across a nearshore to coastal islands' gradient in southeastern Brazil. Neotrop. Ichthyol. 10: 369–382. and 67 species in Teixeira-Neves et al. (2015)TEIXEIRA-NEVES, T.P., NEVES, L.M. & ARAÚJO, F.G. 2015. Hierarchizing biological, physical and anthropogenic factors influencing the structures of fish assemblages along tropical rocky shores in Brazil. Environ. Biol. Fish, 98(6): 1645-1657..

Biogeographic affinities of the AISP reef fish fauna are similar to those recorded in other similar assessments carried out in Southeastern Brazil (Luiz Jr. et al. 2008LUIZ JR, O., CARVALHO-FILHO, A. & FERREIRA, C.E.L. 2008. The reef fish assemblage of the Laje de Santos Marine State Park, southwestern Atlantic: annotated checklist with comments on abundance, distribution, trophic structure, symbiotic associations and conservation. Zootaxa 25: 1–25., Daros et al. 2012DAROS, F.A., BUENO, L.S., VILAR, C.C., PASSOS, A.C. & SPACH, H.L. 2012. Checklist of rocky reef fishes from the Currais Archipelago and Itacolomis Island, Paraná state, Brazil. Check List. 8(3): 349-354., Pinheiro et al. 2015bPINHEIRO, H.T., MADUREIRA, J.M.C., JOYEUX, J.C. & MARTINS, A.S. 2015b. Fish diversity of southwestern Atlantic coastal island: aspects of distribution and conservation in a marine zoogeographical boundary. Check List 11: 1615.), with most species being widely ranging across the Western Atlantic (WA). Anchieta Island is a coastal site largely dominated by the warm and less saline (due to riverine inflow) Coastal Water (CW), as well as by the warm (>18oC) and saline water from the south-flowing Brazil Current (BC) (Matsuura 1986MATSUURA, Y. 1986. Contribuição ao estudo da estrutura oceanográfica da região sudeste entre Cabo Frio (RJ) e Cabo de Santa Marta Grande (SC). Ciência e Cultura 38: 1439-1450.). Luiz Jr. et al. (2008)LUIZ JR, O., CARVALHO-FILHO, A. & FERREIRA, C.E.L. 2008. The reef fish assemblage of the Laje de Santos Marine State Park, southwestern Atlantic: annotated checklist with comments on abundance, distribution, trophic structure, symbiotic associations and conservation. Zootaxa 25: 1–25. pointed out the importance of the BC to provide a proper water temperature and larval input to the subtropical rocky reefs, explaining the large amount of tropical reef fishes in this subtropical area. In addition, the region is affected by upwellings of the cold (8-18oC) South Atlantic Central Water (SACW) during the austral summer and spring (Matsuura 1986MATSUURA, Y. 1986. Contribuição ao estudo da estrutura oceanográfica da região sudeste entre Cabo Frio (RJ) e Cabo de Santa Marta Grande (SC). Ciência e Cultura 38: 1439-1450.). Such frequent cold water intrusions, as well as the relatively wide depth range of the AISP, account for the presence of several reef fishes with subtropical and temperate affinities (Floeter et al. 2001FLOETER S.R., GUIMARÃES R.Z.P., ROCHA L.A., FERREIRA C.E.L., RANGEL C.A. & GASPARINI J.L. 2001. Geographic variation in reef-fish assemblages along the Brazilian coast. Global Ecol. Biogeogr. 10: 423-431., Luiz Jr. et al. 2008LUIZ JR, O., CARVALHO-FILHO, A. & FERREIRA, C.E.L. 2008. The reef fish assemblage of the Laje de Santos Marine State Park, southwestern Atlantic: annotated checklist with comments on abundance, distribution, trophic structure, symbiotic associations and conservation. Zootaxa 25: 1–25., Gibran & Moura 2012GIBRAN, F.Z. & MOURA, R.L. 2012. The structure of rocky reef fish assemblages across a nearshore to coastal islands' gradient in southeastern Brazil. Neotrop. Ichthyol. 10: 369–382., Pinheiro et al. 2015bPINHEIRO, H.T., MADUREIRA, J.M.C., JOYEUX, J.C. & MARTINS, A.S. 2015b. Fish diversity of southwestern Atlantic coastal island: aspects of distribution and conservation in a marine zoogeographical boundary. Check List 11: 1615.). Furthermore, the high structural complexity of rocky shores (Ferreira et al. 2001FERREIRA, C.E.L., GONÇALVES, J.E.A. & COUTINHO, R. 2001. Community structure of fishes and habitat complexity on a tropical rocky shore. Environ. Biol. Fish. 61: 353–369., Dominici-Arosema & Wolf 2006DOMINICI-AROSEMENA, A. & WOLFF, M. 2006. Reef fish community structure in the Tropical Eastern Pacific (Panamá): living on a relatively stable rocky reef environment. Helgo. Mar. Res. 60(4): 287., Gibran & Moura 2012GIBRAN, F.Z. & MOURA, R.L. 2012. The structure of rocky reef fish assemblages across a nearshore to coastal islands' gradient in southeastern Brazil. Neotrop. Ichthyol. 10: 369–382., Teixeira-Neves et al. 2015TEIXEIRA-NEVES, T.P., NEVES, L.M. & ARAÚJO, F.G. 2015. Hierarchizing biological, physical and anthropogenic factors influencing the structures of fish assemblages along tropical rocky shores in Brazil. Environ. Biol. Fish, 98(6): 1645-1657.) and the broad depth range of coastal islands (Pereira-Filho et al. 2011PEREIRA-FILHO, G.H., AMADO-FILHO, G.M., GUIMARÃES, S.M., MOURA, R.L., SUMIDA, P.Y., ABRANTES, D.P., ... & FRANCINI FILHO, R.B. 2011. Reef fish and benthic assemblages of the Trindade and Martin Vaz island group, southwestern Atlantic. Braz. Jour. Ocean. 59(3): 201-212., Gibran & Moura 2012GIBRAN, F.Z. & MOURA, R.L. 2012. The structure of rocky reef fish assemblages across a nearshore to coastal islands' gradient in southeastern Brazil. Neotrop. Ichthyol. 10: 369–382., Teixeira-Neves et al. 2015TEIXEIRA-NEVES, T.P., NEVES, L.M. & ARAÚJO, F.G. 2015. Hierarchizing biological, physical and anthropogenic factors influencing the structures of fish assemblages along tropical rocky shores in Brazil. Environ. Biol. Fish, 98(6): 1645-1657.), as well as the proximity to large estuaries and the protected status of the AISP, are responsible for the relatively high richness of fishes recorded herein.

Overfishing and bycatch are the main stressors operating over 85% of the endangered species recorded at AISP, which mostly include mesopredators (i.e. medium to large size carnivores) such as groupers (E. marginatus, E. morio, M. acutirostris and M. bonaci), and large herbivorous like S. axillare (Floeter et al. 2006FLOETER, S.R., HALPERN, B.S. & FERREIRA, C.E.L. 2006. Effects of fishing and protection on Brazilian reef fishes. Bio. Conserv. 128: 391–402., Francini-Filho & Moura 2008FRANCINI-FILHO, R.B. & MOURA, R.L. 2008. Evidence for spillover of reef fishes from a no-take marine reserve: An evaluation using the before-after control-impact (BACI) approach. Fish. Res. 93(3): 346-356., Teixeira-Neves et al. 2015TEIXEIRA-NEVES, T.P., NEVES, L.M. & ARAÚJO, F.G. 2015. Hierarchizing biological, physical and anthropogenic factors influencing the structures of fish assemblages along tropical rocky shores in Brazil. Environ. Biol. Fish, 98(6): 1645-1657.). These species are targeted by both professional and recreational fisheries, including spearfishing, which is poorly regulated and monitored in Brazil (Nunes et al. 2012NUNES, J.A.C.C., MEDEIROS, D.V., REIS-FILHO, J.A., SAMPAIO, C.L.S. & BARROS, F. 2012. Reef fishes captured by recreational spearfishing on reefs of Bahia State, northeast Brazil. Bio. Neo. 12(1):179-185.; Freire et al. 2016FREIRE, K.M.F., TUBINO, R.A., MONTEIRO-NETO, C., ANDRADE-TUBINO, M.F., BELRUSS, C.G., TOMÁS, A.R.G., ... & CREPALDI, D.V. 2016. Brazilian recreational fisheries: current status, challenges and future direction. Fisheries Manag. Ecolo., 23(3-4): 276-290.). Most of the species of elasmobranchs recorded (64.7%) are either CR, EN, VU or NT, e.g. Sphyrna lewini, Pseudobatos horkelii and Rhinoptera brasiliensis, and its population status is more critical than that of actinopterygians. With extremely reduced populations, elasmobranchs are curently captured mostly as bycatch (Rosa & Gadig 2014ROSA R.S. & GADIG O.B.F. 2014. Conhecimento da diversidade dos Chondrichthyes marinhos no Brasil: a contribuição de José Lima de Figueiredo. Arquivos de Zoologia 45: 89–104.), and therefore deserve specific mitigation measures directed to fisheries targeting other resources (especially longlines, gillnets and trawls). Among actinopterygians, it is remarkable that 83.3% of the recorded epinephelids (groupers) are either CR, EN, VU or NT. Besides being protogynous hermaphrodites, epinephelids are slow-growing and long-living species with late maturity (Andrade et al. 2003ANDRADE, Á.B., MACHADO, L.F., HOSTIM-SILVA, M. & BARREIROS, J.P. 2003. Reproductive biology of the dusky grouper Epinephelus marginatus (Lowe, 1834). Braz. Arch. Biol. Tech. 46(3): 373-382., Mitcheson et al. 2008MITCHESON, D., SADOVY, Y. & LIU, M. 2008. Functional hermaphroditism in teleosts. Fish Fish. 9(1): 1-43., Reñones et al. 2010REÑONES, O., GRAU, A., MAS, X., RIERA, F. & SABORIDO-REY, F. 2010. Reproductive pattern of an exploited dusky grouper Epinephelus marginatus (Lowe 1834)(Pisces: Serranidae) population in the western Mediterranean. Sci. Mar. 74(3): 523-537.), being thus highly vulnerable to fishery.

The protected status of the marine perimeter of AISP is well justified by its relatively high fish richness and concentration of threathened species. However, the population status of these species and the reef fish community structure are still poorly known (e.g. Sazima et al. 2000SAZIMA, I., SAZIMA, C., FRANCINI-FILHO, R.B. & MOURA, R.L. 2000. Daily cleaning activity and diversity of clients of the barber goby, Elacatinus figaro, on rocky reefs in southeastern Brazil. Environ. Biol. Fish. 59: 69–77.), impeding a thorough assessment of long-term of population viability and the potential of AISP to outsource unprotected areas in the vicinities (e.g. Floeter et al. 2006FLOETER, S.R., HALPERN, B.S. & FERREIRA, C.E.L. 2006. Effects of fishing and protection on Brazilian reef fishes. Bio. Conserv. 128: 391–402., Francini-Filho & Moura 2008FRANCINI-FILHO, R.B. & MOURA, R.L. 2008. Evidence for spillover of reef fishes from a no-take marine reserve: An evaluation using the before-after control-impact (BACI) approach. Fish. Res. 93(3): 346-356.). For instance, it is unclear whether the current no-take zoning at the regional level is sufficient to ensure long term biodiversity persistence and fisheries sustainability, as stated in the objectives of the State MPA network under development along the São Paulo coast.

Acknowledgments

Field work was assisted by Jayson B. Huss, Lucas V. Garcia, Mitchell M. Sisak, Carolina B. Tiveron and Diego A. Solano. The AISP staff kindly provided operational support. The Brazilian Ministry of the Environment (SISBIO 32352-3) and the Environmental Agency of São Paulo (COTEC/SMA 260108-004.934/2012) provided research permits. OBFG, RLM, RBFF acknowledge CNPq research grants. RLM also acknowledges FAPERJ and CAPES grants.

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Publication Dates

  • Publication in this collection
    2018

History

  • Received
    20 May 2017
  • Reviewed
    03 Nov 2017
  • Accepted
    18 Dec 2017
Instituto Virtual da Biodiversidade | BIOTA - FAPESP Departamento de Biologia Vegetal - Instituto de Biologia, UNICAMP CP 6109, 13083-970 - Campinas/SP, Tel.: (+55 19) 3521-6166, Fax: (+55 19) 3521-6168 - Campinas - SP - Brazil
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