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Rocky reef fish biodiversity and conservation in a Brazilian Hope Spot region

Abstract

Coastal islands of Grande Rio, located south Rio de Janeiro and Maricá cities have been under multiple anthropogenic impacts. Despite these problems, these insular systems shelter a high diversity of fish species. Reef fishes are essential components of tropical marine coastal communities, also providing food and income for millions of people around the world. In this work, we generated an updated checklist from Cagarras Islands Natural Monument and surrounding areas based on fisheries data, literature records and multiple sampling techniques, including the Submersible Rotating Video technique, used for the first time in Brazil. We present an inventory of 282 fish species representing 91 different families, with 21 new records for the study area, including a non-native species (Heniochus acuminatus). In addition, our results show a moderate endemism level for the Brazilian province (approximately 6.0%), while 10.5% of species are assigned to one of IUCN’s threatened categories. Our efforts show the fish biodiversity scenario and their distribution on coastal islands more than 10 years after the Cagarras Islands Natural Monument establishment, reinforcing the importance of monitoring research programs for the management of this Marine Protected Area and surrounding waters, that play a key role for artisanal fisheries.

Keywords:
Checklist; Marine Protected Areas; Non-destructive techniques; Richness; South Atlantic

Resumo

As ilhas costeiras do Grande Rio, ao sul das cidades do Rio de Janeiro e Maricá, têm sofrido múltiplos impactos antrópicos. Apesar destes problemas, esses sistemas insulares abrigam uma grande diversidade de espécies de peixes. Os peixes recifais são componentes essenciais das comunidades costeiras marinhas tropicais, fornecendo alimento e fonte de renda para milhões de pessoas em todo o mundo. Neste trabalho, geramos uma lista de verificação atualizada do Monumento Natural das Ilhas Cagarras e áreas do entorno com base em dados de pesca, registros da literatura e múltiplas técnicas de amostragem, incluindo a técnica de vídeo rotacional subaquático usada pela primeira vez no Brasil. Apresentamos um inventário de 282 espécies de peixes representando 91 famílias, com 21 novos registros para área de estudo, incluindo uma espécie não nativa (Heniochus acuminatus). Além disso, nossos resultados mostram um nível de endemismo moderado da província brasileira (aproximadamente 6,0%), sendo 10,5% das espécies classificadas em uma das categorias ameaçadas da IUCN. Nossos esforços mostram o cenário da biodiversidade de peixes e sua distribuição nas ilhas costeiras mais de 10 anos após o estabelecimento do Monumento Natural das Ilhas Cagarras, reforçando a importância de programas de pesquisa de monitoramento para a gestão desta Área Marinha Protegida e suas águas adjacentes, que desempenham papel fundamental para a pesca artesanal.

Palavras-chave:
Áreas Marinhas Protegidas; Atlântico Sul; Lista de espécies; Riqueza; Técnicas não-destrutivas

INTRODUCTION

Rocky reefs are among the most important marine ecosystems in the world, due to their importance in providing livelihood services for millions of people, such as fishing, medicinal compounds, and tourism (Pereira, Soares-Gomes, 2009Pereira RC, Soares-Gomes A, editors. Biologia marinha. Rio de Janeiro: Interciência; 2009. ; Laport et al., 2016Laport MS, Pontes PVM, Santos DS, Santos-Gandelman JF, Muricy G, Bauwens M et al. Antibiotic resistance genes detected in the marine sponge Petromica citrina from Brazilian coast. Braz J Microbiol. 2016; 47(3):617–20. https://doi.org/10.1016/j.bjm.2016.04.016
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). Despite all their importance, many forms of life that inhabit rocky shore ecosystems are critically endangered by human actions (Benedetti-Cecchi et al., 2001Benedetti-Cecchi L, Pannacciulli F, Bulleri F, Moschella PS, Airoldi L, Relini G, Cinelli F. Predicting the consequences of anthropogenic disturbance: large-scale effects of loss of canopy algae on rocky shores. Mar Ecol Prog Ser. 2001; 214:137–50. https://doi.org/10.3354/meps214137
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). Coastal development, urbanization and overfishing are amongst the main activities that exert pressure on coastal marine ecosystems (Elliott, 2014Elliott M. Integrated marine science and management: Wading through the morass. Mar Pollut Bull. 2014; 86(1–2):1–04. http://dx.doi.org/10.1016/j.marpolbul.2014.07.026
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), currently occurring so fast that they generally surpass our ability to understand the surrounding ecosystem functioning. In order to reduce these impacts caused by human activities, Marine Protected Areas (MPAs) have been created as an important management tool, aiming to provide protection for local marine biodiversity (Lester et al., 2009Lester SE, Halpern BS, Grorud-Colvert K, Lubchenco J, Ruttenberg BI, Gaines SD et al. Biological effects within no-take marine reserves: a global synthesis. Mar Ecol Prog Ser. 2009; 384:33–46. https://doi.org/10.3354/meps08029
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; Miller, Russ, 2014Miller KI, Russ GR. Studies of no-take marine reserves: Methods for differentiating reserve and habitat effects. Ocean Coast Manage. 2014; 96:51–60. https://doi.org/10.1016/j.ocecoaman.2014.05.003
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), especially minimizing impacts on fish assemblages and improving/preserving the essential habitats on which species depend (Gaines et al., 2010Gaines SD, White C, Carr MH, Palumbi SR. Designing marine reserve networks for both conservation and fisheries management. Proc Natl Acad Sci USA. 2010; 107(43):18286–93. https://doi.org/10.1073/pnas.0906473107
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).

As reef environments, reef fishes are important components of tropical marine communities, serving as food and income source for millions of people (Munro, 1996Munro JL. The scope of tropical reef fisheries and their management. Reef Fisheries. 1996; 20:1–14. https://doi.org/10.1007/978-94-015-8779-2_1
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; Pauly et al., 2002Pauly D, Christensen V, Guénette S, Pitcher TJ, Sumaila UR, Walters CJ et al. Towards sustainability in world fisheries. Nature. 2002; 418:689–95. https://doi.org/10.1038/nature01017
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; Nelson et al., 2016Nelson JS, Grande TC, Wilson MV, editors. Fishes of the World, Hoboken, NJ: Wiley; 2016.). In Brazil, reef fish communities are distributed along the coast, from off the mouth of the Amazon River, and the Manuel Luiz reefs (Northern Brazil) to coastal regions of Santa Catarina State in Southern Brazil (Rocha, Rosa, 2001Rocha LA, Rosa IL. Baseline assessment of reef fish assemblages of Parcel Manuel Luiz Marine State Park, Maranhão, north-east Brazil. J Fish Biol. 2001; 58(4):985–98. https://doi.org/10.1111/j.1095-8649.2001.tb00549.x
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; Hostim-Silva et al., 2005Hostim-Silva M, Andrade AB, Machado LF, Gerhardinger LC, Daros FA, Barreiros JP et al. Peixes de Costão Rochoso de Santa Catarina: Arvoredo. Itajaí: Universidade do Vale do Itajaí; 2005.; Moura et al., 2016Moura RL, Amado-Filho GM, Moraes FC, Brasileiro PS, Salomon PS, Mahiques MM et al. An extensive reef system at the Amazon River mouth. Sci Adv. 2016; 2(4):e1501252. https://www.science.org/doi/10.1126/sciadv.1501252
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), including oceanic islands (Quimbayo et al., 2019Quimbayo JP, Dias MS, Kulbicki M, Mendes TC, Lamb RW, Johnson AF et al. Determinants of reef fish assemblages in tropical Oceanic islands. Ecography. 2019; 42(1):77–87. https://doi.org/10.1111/ecog.03506
https://doi.org/10.1111/ecog.03506...
; Pinheiro et al., 2020Pinheiro HT, Macena BCL, Francini-Filho RB, Ferreira CEL, Albuquerque FV, Bezerra NPA et al. Fish biodiversity of Saint Peter and Saint Paulʼs Archipelago, Mid-Atlantic Ridge, Brazil: new records and a species database. J Fish Biol. 2020; 97(4):1143–53. https://doi.org/10.1111/jfb.14484
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). However, the rocky shore ichthyofauna on coastal regions has been under increasing human pressure, ranging from the degradation by pollution, to extractive activities, such as fishing (recreational and commercial), which can lead some species to high extinction risks (Quaas et al., 2019Quaas Z, Harasti D, Gaston TF, Platell ME, Fulton CJ. Influence of habitat condition on shallow rocky reef fish community structure around islands and headlands of a temperate marine protected area. Mar Eco Prog Ser. 2019; 626:1–13. https://doi.org/10.3354/meps13091
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). Additionally, the introduction/arrival of invasive species can pose a significant threat to local biodiversity, and may cause changes in the structure of communities, resulting in the exclusion of native species (Ruiz et al., 1997Ruiz GM, Carlton JT, Grosholz ED, Hines AH. Global invasions of marine and estuarine habitats by non-indigenous species: Mechanisms, extent, and consequences. Am Zool. 1997; 37(6):621–32. https://doi.org/10.1093/icb/37.6.621
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; Bax et al., 2003Bax N, Williamson A, Aguero M, Gonzalez E, Geeves W. Marine invasive alien species: a threat to global biodiversity. Mar Policy. 2003; 27(4):313–23. https://doi.org/10.1016/S0308-597X(03)00041-1
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). These facts contribute to the reduction of the environment quality, directly impacting the associated ichthyofauna, which demands a better understanding of the dynamics of the reef fish communities in these regions, especially within MPAs.

Along the Southeastern Brazilian coastline, the complex structure of rocky reefs is associated with a valuable diversity of fish species and other organisms, even overcoming the number of species present on other marine ecosystems (Floeter et al., 2004Floeter SR, Ferreira CEL, Dominici-Arosemena A, Zalmon IR. Latitudinal gradients in Atlantic reef fish communities: trophic structure and spatial use patterns. J Fish Biol. 2004; 64(6):1680–99. https://doi.org/10.1111/j.0022-1112.2004.00428.x
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; Souza et al., 2018Souza GRS, Gadig OBF, Motta FS, Moura RL, Francini-Filho RB, Garrone-Neto D. Reef fishes of the Anchieta Island State Park, Southwestern Atlantic, Brazil. Biota Neotrop. 2018; 18(1):e20170380. https://doi.org/10.1590/1676-0611-bn-2017-0380
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). The Grande Rio region shelters our studied islands. They are precisely located from the Guanabara Bay entrance to both sides of the E-W coastline orientation, encompassing Rio de Janeiro and Maricá municipalities, in Southeastern Brazil. These islands and surrounding waters shelter a high biodiversity of marine and terrestrial fauna and flora, and even stand out as a singular archeological site, being commonly visited by tourists, fishermen, military activities, and the general public (details in Moraes et al., 2013Moraes FC, Bertoncini ÁA, Aguiar A., editors. História, Ppesquisa e Biodiversidade do Monumento Natural das Ilhas Cagarras. 1 ed. Rio de Janeiro: Mar Adentro; 2013.; Bertoncini et al., 2019Bertoncini AA, Moraes FC, Borgonha M, Aguiar A, Duarte B, editors. Marine biodiversity and diving guide to the islands of Rio. Rio de Janeiro: Museu Nacional, Série Livros 65; 2019.). Part of these islands form an important Marine Protected Area (MPA) in Rio de Janeiro City, The Cagarras Islands Natural Monument (MONA Cagarras). Despite its importance and proximity to a highly populated Brazilian metropolis, the ichthyofauna of these coastal islands and surrounding waters are still poorly known. Nonetheless, MONA Cagarras, together with its surrounding areas (including Rasa and Cotunduba islands) was, in 2021, recognized as a Hope Spot for conservation of marine biodiversity by the international nonprofit organization Mission Blue.

The survey of biodiversity appears as a key tool in studies of fish communities (Mora et al., 2008Mora C, Tittensor DP, Myers RA. The completeness of taxonomic inventories for describing the global diversity and distribution of marine fishes. P Roy Soc B-Biol Sci. 2008; 275(1631):149–55. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2596190/
https://www.ncbi.nlm.nih.gov/pmc/article...
; Guabiroba et al., 2020Guabiroba HC, Pimentel CR, Macieira MR, Cardozo-Ferreira GC, Teixeira JB, Gasparini JL et al. New records of fishes for the Vitória-Trindade Chain, southwestern Atlantic. Check List. 2020; 16(3):699–705. https://doi.org/10.15560/16.3.699
https://doi.org/10.15560/16.3.699...
; Pereira et al., 2021Pereira PHC, Côrtes LGF, Lima GV, Gomes E, Pontes AVF, Mattos F et al. Reef fishes biodiversity and conservation at the largest Brazilian coastal Marine Protected Area (MPA Costa dos Corais). Neotrop Ichthyol. 2021; 19(4):e210071. https://doi.org/10.1590/1982-0224-2021-0071
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). Non-destructive techniques have been widely employed in marine ecosystems, especially in MPAs (Andradi-Brown et al., 2016Andradi-Brown DA, Macaya-Solis C, Exton DA, Gress E, Wright G, Rogers AD. Assessing Caribbean shallow and mesophotic reef fish communities using baited-remote underwater video (BRUV) and diver-operated video (DOV) survey techniques. PLoS ONE. 2016; 11(12):e0168235. https://doi.org/10.1371/journal.pone.0168235
https://doi.org/10.1371/journal.pone.016...
; Bayley et al., 2019Bayley DTI, Mogg OMA, Purvis A, Koldewey HJ. Evaluating the efficacy of small-scale marine protected areas for preserving reef health: A case study applying emerging monitoring technology. Aquat Conserv: Mar Freshw Ecosyst. 2019; 29 29(12):2026–44. https://doi.org/10.1002/aqc.3215
https://doi.org/10.1002/aqc.3215...
; Quaas et al., 2019Quaas Z, Harasti D, Gaston TF, Platell ME, Fulton CJ. Influence of habitat condition on shallow rocky reef fish community structure around islands and headlands of a temperate marine protected area. Mar Eco Prog Ser. 2019; 626:1–13. https://doi.org/10.3354/meps13091
https://doi.org/10.3354/meps13091...
, Schmid et al., 2020Schmid K, Silva FRM, Santos BJV, Bezerra NPA, Garla RC, Giarrizzo T. First fish fauna assessment in the Fernando de Noronha Archipelago with BRUVS: Species catalog with underwater imagery. Biota Neotrop. 2020; 20(4):e20201014. https://doi.org/10.1590/1676-0611-BN-2020-1014
https://doi.org/10.1590/1676-0611-BN-202...
). The Underwater Visual Census (UVC) is frequently used in ecological studies of reef fish communities (Chaves, Monteiro-Neto, 2009Chaves LCT, Monteiro-Neto C. Comparative analysis of rocky reef fish community structure in coastal islands of south-eastern Brazil. J Mar Biol Assoc UK. 2009; 89(3):609–19. https://doi.org/10.1017/S0025315408002695
https://doi.org/10.1017/S002531540800269...
; Daros et al., 2018Daros FA, Bueno LS, Soeth M, Bertoncini AA, Hostim-Silva M, Spach HL. Rocky reef fish assemblage structure in coastal islands of southern Brazil. Lat Am J Aquat Res. 2018; 46(1):197–211. http://dx.doi.org/10.3856/vol46-issue1-fulltext-19
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; Motta et al., 2021Motta FS, Moura RL, Neves LM, Souza GRS, Gibran FZ, Francini CL et al. Effects of marine protected areas under different management regimes in a hot spot of biodiversity and cumulative impacts from SW Atlantic. Reg Stud Mar Sci. 2021; 47:101951. https://doi.org/10.1016/j.rsma.2021.101951
https://doi.org/10.1016/j.rsma.2021.1019...
; Pereira et al., 2021Pereira PHC, Côrtes LGF, Lima GV, Gomes E, Pontes AVF, Mattos F et al. Reef fishes biodiversity and conservation at the largest Brazilian coastal Marine Protected Area (MPA Costa dos Corais). Neotrop Ichthyol. 2021; 19(4):e210071. https://doi.org/10.1590/1982-0224-2021-0071
https://doi.org/10.1590/1982-0224-2021-0...
), allowing the identification of species and the monitoring of the behavior of organisms that especially, are not affected by the presence of divers (Sale, 1997Sale PF. Visual census of fish: How well do we see what is there? In: Lessios HA, MacIntyre IG, editors. Proc Int Cor Reef Symp 2. Balboa, Smithsonian Tropical Research Institute: 1997.; Beck et al., 2014Beck HJ, Feary DA, Figueira WF, Booth DJ. Assessing range shifts of tropical reef fishes: A comparison of belt transect and roaming underwater visual census methods. Bull Mar Sci. 2014; 90(2):705–21. https://doi.org/10.5343/bms.2013.1055
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). In parallel, the evolution of non-destructive techniques through remote videos, have been employed as important complementary tools, to carry out more accurate sampling of the ichthyofauna (Mallet, Pelletier, 2014Mallet D, Pelletier D. Underwater video techniques for observing coastal marine biodiversity: A review of sixty years of publications (1952-2012). Fish Res. 2014; 154:44–62. https://doi.org/10.1016/j.fishres.2014.01.019
https://doi.org/10.1016/j.fishres.2014.0...
; Koenig, Stallings, 2015Koenig CC, Stallings CD. A new compact rotating video system for rapid survey of reef fish populations. Bull Mar Sci. 2015; 91(3):365–73. http://dx.doi.org/10.5343/bms.2015.1010
http://dx.doi.org/10.5343/bms.2015.1010...
; Pimentel et al., 2020Pimentel CR, Andrades R, Ferreira CEL, Gadig OBF, Harvey ES, Joyeux J-C et al. BRUVS reveal locally extinct shark and the way for shark monitoring in Brazilian oceanic islands. J Fish Biol. 2020; 96(2):539–42. https://doi.org/10.1111/jfb.14228
https://doi.org/10.1111/jfb.14228...
; Pinheiro et al., 2020Pinheiro HT, Macena BCL, Francini-Filho RB, Ferreira CEL, Albuquerque FV, Bezerra NPA et al. Fish biodiversity of Saint Peter and Saint Paulʼs Archipelago, Mid-Atlantic Ridge, Brazil: new records and a species database. J Fish Biol. 2020; 97(4):1143–53. https://doi.org/10.1111/jfb.14484
https://doi.org/10.1111/jfb.14484...
; Rolim et al., 2022Rolim FA, Rodrigues PFC, Langlois T, Neves LM, Gadid OBF.A comparison of stereo-videos and visual census methods for assessing subtropical rocky reef fish assemblage. Environ Biol Fish. 2022; 105:413–29. https://doi.org/10.1007/s10641-022-01240-w
https://doi.org/10.1007/s10641-022-01240...
). Such instruments allow to estimate the abundance and diversity of reef fishes, providing relevant information on the health of local marine communities, with minimum impacts.

In the present work, we revisited and updated the checklist of fish species from Rio de Janeiro coastal islands and surrounding waters, based on a decade of field surveys, published scientific articles and fisheries records. In addition, we report the first record of the non-native species Heniochus acuminatus (Linnaeus, 1758) in Rio de Janeiro. Furthermore, we provide data of species richness on several coastal islands and surroundings by different sampling methods, improving the knowledge on ­the marine fish species of the state of Rio de Janeiro.

MATERIAL AND METHODS

Sampling sites. The present study was conducted at the coastal islands of Rio de Janeiro and Maricá cities (between 43º35’W - 42º09’W; 23º01’S - 22º09’S) (Fig. 1): from West to East, Tijucas Archipelago is located 1.7 km off Barra da Tijuca Beach and comprises Pontuda, Alfavaca, and Meio Islands; the Cagarras Archipelago is about 4 km southwards off Ipanema Beach, formed by Palmas, Cagarra, Comprida islands plus Filhote da Cagarra Islet; and along with Redonda Island and Filhote da Redonda Islet, which lie 4 km southwards the Cagarra Archipelago, they form the Cagarras Islands Natural Monument, a no-take MPA created in 2010 to protect the local biodiversity, which boundaries includes the marine area 10 m from the rockyshore of each island. Further East lies Rasa Island, while Cotunduba Island is located at the entrance of Guanabara Bay. Further East, Maricás Archipelago is spread 3.5 km from the Maricá coast and is formed by Maricá and Crioula islands and two small islets.

FIGURE 1 |
Maps and photographs of the study area (Coastal Islands of Rio de Janeiro metropolitan region). A. The State of Rio de Janeiro in Southeast Brazil; B. The Guanabara Bay and the archipelagos/islands along the southern coast, Z13 fishermen’s colony (red square) and Z7 fishermen’s colony (red circle); C. Tijucas Archipelago; D. Cagarras Archipelago and Redonda Island and Filhote da Redonda Islet forming the MONA Cagarras MPA; E. Cotunduba Island; F. Rasa Island; G. Maricás Archipelago; H. Aerial view from West of the Tijucas Archipelago; I. Aerial view from Northwest of MONA Cagarras, depicting Rasa Island in the far background; J. Aerial view from Southeast of Cotunduba Island; K. Aerial view from East of the Maricás Archipelago. Credits: Augusto A. Machado (A-G); Áthila A. Bertoncini (H, I, K); Fred Cunha (J).

Data source. The updated checklist of marine fishes presented herein was produced through non-destructive methods: (I) 696 Underwater Visual Censuses (UVC) were carried out using 40m2-belt transects by two scientific divers in all of the three archipelagos and Cotunduba Island, between 2011 and 2022, at shallow waters (<10 m) and deeper waters (>11 to 25 m); (II) 468 Submersible Rotating Videos (SRV) were obtained at three different areas on shallow (<10 m) and deep (>10 m) strata (117 hours of video); Additionally, (III) fish occurrence records were compiled from previously published scientific papers and books (e.g., Rangel et al., 2007Rangel CA, Chaves LCT, Monteiro-Neto C. Baseline assessment of the reef fish assemblage from Cagarras Archipelago, Rio de Janeiro, southeastern Brazil. Braz J Oceanogr. 2007; 55(1):7–17. https://doi.org/10.1590/S1679-87592007000100002
https://doi.org/10.1590/S1679-8759200700...
; Moraes et al., 2013Moraes FC, Bertoncini ÁA, Aguiar A., editors. História, Ppesquisa e Biodiversidade do Monumento Natural das Ilhas Cagarras. 1 ed. Rio de Janeiro: Mar Adentro; 2013.; Monteiro-Neto et al., 2013Monteiro-Neto C, Bertoncini AA, Chaves LCT, Noguchi R, Mendonça-Neto JP, Rangel CA. Checklist of marine fish from coastal islands of Rio de Janeiro, with remarks on marine conservation. Mar Biodivers Rec. 2013; 6:1–13. http://dx.doi.org/10.1017/S1755267213000973
http://dx.doi.org/10.1017/S1755267213000...
; Aguiar et al., 2015Aguiar A, Bertoncini ÁA, Moraes FC, editors. Ilhas do Rio. 1 ed. Rio de Janeiro: Mar Adentro; 2015.; Amorim, Monteiro-Neto, 2016Amorim RB, Monteiro-Neto C. Marine protected area and the spatial distribution of the gill net fishery in Copacabana, Rio de Janeiro, RJ, Brazil. Braz J Biol. 2016; 76(1):1–09. http://dx.doi.org/10.1590/1519-6984.06614
http://dx.doi.org/10.1590/1519-6984.0661...
; Garcia et al., 2018Garcia LC, Moreira CR, Carvalho-Filho A. First record of African hind, Cephalopholis taeniops (Valenciennes, 1828) (Perciformes, Epinephelidae) in the South-western Atlantic. Check List. 2018; 14(6):961–65. https://doi.org/10.15560/14.6.961
https://doi.org/10.15560/14.6.961...
; Bertoncini et al., 2019Bertoncini AA, Moraes FC, Borgonha M, Aguiar A, Duarte B, editors. Marine biodiversity and diving guide to the islands of Rio. Rio de Janeiro: Museu Nacional, Série Livros 65; 2019.; Araujo et al., 2020Araujo NLF, Lopes CA, Brito VB, Santos LN, Barbosa-Filho MLV, Amaral CRL et al. Artisanally landed elasmobranchs along the coast of Rio de Janeiro, Brazil. Bol Lab Hidrobiol. 2020; 30(1):33–53. http://dx.doi.org/10.18764/1981-6421e2020.4
http://dx.doi.org/10.18764/1981-6421e202...
; Hauser-Davis et al., 2021Hauser-Davis RA, Amorim-Lopes C, Araujo NLF, Rebouças M, Gomes RA, Rocha RCC et al. On mobulid rays and metals: Metal content for the first Mobula mobular record for the state of Rio de Janeiro, Brazil and a review on metal ecotoxicology assessments for the Manta and Mobula genera. Mar Pollut Bull. 2021; 168:112472. https://doi.org/10.1016/j.marpolbul.2021.112472
https://doi.org/10.1016/j.marpolbul.2021...
); (IV) Data were also compiled from fishery landing monitoring and personal communication with Z13 and Z7 Fishermen Colonies, providing much of the species that inhabit soft bottoms, once they have fishing grounds in the surroundings of the islands. Finally, (V) Underwater Sighting Data (approx. 603 hours of scientific diving) and sightings by colleagues and volunteers in situ were considered in the present work.

Submersible Rotating Videos (SRV). The SRV system (Fig. 2), developed by Koenig, Stallings, (2015)Koenig CC, Stallings CD. A new compact rotating video system for rapid survey of reef fish populations. Bull Mar Sci. 2015; 91(3):365–73. http://dx.doi.org/10.5343/bms.2015.1010
http://dx.doi.org/10.5343/bms.2015.1010...
, is an innovative rotational underwater video technique, and consists of a stainless-steel frame with an engine inside (2 rpm) and a camera of high resolution attached (e.g., GoPro). This technique simulates the renowned stationary census technique, developed by Bohnsack, Bannerot, (1986)Bohnsack JA, Bannerot SP. A stationary visual census technique for quantitatively assessing community structure of coral reef fishes. NOAA Technical Report NMFS [Internet]. Washington; 1986. Available from: https://repository.library.noaa.gov/view/noaa/1005
https://repository.library.noaa.gov/view...
and excludes the potential influence of the diver on the behavior of fishes. From each deployment, a 15-minute-video was recorded, and then after analyzed using the VLC multimedia player (http://www.videolan.org/vlc/index.html).

FIGURE 2 |
Submersible Rotating Videos “SRV” in operation on Redonda Island. Photo: Áthila A. Bertoncini.

Data analysis. The species were identified based on Figueiredo, Menezes, (2000)Figueiredo JL, Menezes NA. Manual de peixes marinhos do sudeste do Brasil VI. Teleostei. 5 ed. São Paulo: Museu de Zoologia da Universidade de São Paulo; 2000., Humann, Deloach, (2014)Humann P, Deloach N. Reef fish identification - Florida Caribbean Bahamas. 4 ed. Florida: New World Publications; 2014., Hostim-Silva et al., (2005)Hostim-Silva M, Andrade AB, Machado LF, Gerhardinger LC, Daros FA, Barreiros JP et al. Peixes de Costão Rochoso de Santa Catarina: Arvoredo. Itajaí: Universidade do Vale do Itajaí; 2005., Bertoncini et al., (2019)Bertoncini AA, Moraes FC, Borgonha M, Aguiar A, Duarte B, editors. Marine biodiversity and diving guide to the islands of Rio. Rio de Janeiro: Museu Nacional, Série Livros 65; 2019., and consultancy to experts. The families were ordered according to Dornburg, Near, (2021)Dornburg A, Near TJ. The emerging phylogenetic perspective on the evolution of Actinopterygian fishes. Annu Rev Ecol Evol Syst. 2021; 52:427–52. https://doi.org/10.1146/annurev-ecolsys-122120-122554
https://doi.org/10.1146/annurev-ecolsys-...
and species were arranged in alphabetic order inside each family. The IUCN Red List of threatened species and the Brazilian environmental agency, Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) - Red list of Brazilian Fauna Threatened of Extinction were addressed to classify the conservation status of each species (ICMBio, 2018Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). Livro vermelho da fauna brasileira ameaçada de extinção: Volume VI – Peixes. In: Instituto Chico Mendes de Conservação da Biodiversidade, organizers. Livro vermelho da fauna brasileira ameaçada de extinção. Brasília: ICMBio/MMA; 2018. Available from: https://www.gov.br/icmbio/pt-br/centrais-de-conteudo/publicacoes/publicacoes-diversas/livro_vermelho_2018_vol6.pdf
https://www.gov.br/icmbio/pt-br/centrais...
; IUCN, 2020International Union for Conservation of Nature (IUCN). The IUCN Red List of Threatened Species; 2021 [Internet]. Available from: https://www.iucnredlist.org
https://www.iucnredlist.org...
). The sites where the species were reported are presented here and the records of species not observed by this study are referenced. Data analyses were performed using Software R (R Development Core Team, 2020R Development Core Team. R: The R project for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2020. Available from: https://www.r-project.org/
https://www.r-project.org/...
) and maps were elaborated through QGIS 3.16 (QGIS Development Team, 2022QGIS Development Team. QGIS Geographic Information System. Open Source Geospatial Foundation Project, 3.16 version; 2022. Available from: http://qgis.osgeo.org
http://qgis.osgeo.org...
).

RESULTS

Fish database. The annotated checklist includes 282 fish species, belonging to 192 genera and 91 families cataloged at the coastal Islands of Rio de Janeiro and surrounding waters, including soft bottom habitats (Tab. 1). It is important to note in Tab. 1 that phylogenetic updates are considered for recent changes in families, i.e., Galeocerdo cuvier (Péron & Lesueur, 1822) under Galeocerdonidae (Ebert et al., 2021Ebert DA, Dando M, Fowler S, editors. Sharks of the world - A complete guide, Wild Nature Press, Plymounth, UK. 2021.), Zapteryx brevirostris (Müller & Henle, 1841) under Trygonorrhinidae (Last et al., 2016Last PR, Séret B, Naylor GJP. A new species of guitarfish, Rhinobatos borneensis sp. nov. with a redefinition of the family-level classification in the order Rhinopristiformes (Chondrichthyes: Batoidea). Zootaxa. 2016; 4117(4):451–75. https://doi.org/10.11646/zootaxa.4117.4.1
https://doi.org/10.11646/zootaxa.4117.4....
), Acanthistius brasilianus (Cuvier, 1828) under Anthiadidae (Dornburg, Near, 2021Dornburg A, Near TJ. The emerging phylogenetic perspective on the evolution of Actinopterygian fishes. Annu Rev Ecol Evol Syst. 2021; 52:427–52. https://doi.org/10.1146/annurev-ecolsys-122120-122554
https://doi.org/10.1146/annurev-ecolsys-...
; Anderson, 2018Anderson WD Jr. Annotated checklist of anthiadine fishes (Percoidei: Serranidae). Zootaxa. 2018; 4475(1):1–62. https://doi.org/10.11646/zootaxa.4475.1.1
https://doi.org/10.11646/zootaxa.4475.1....
); and genus, i.e., from Equetus (lanceolatus) (Linnaeus, 1758) to Eques Bloch, 1793 (Parenti, 2020Parenti P. An annotated checklist of fishes of the family Sciaenidae. J Animal Divers. 2020; 2(1):1–92. https://doi.org/10.29252/JAD.2020.2.1.1
https://doi.org/10.29252/JAD.2020.2.1.1...
); and from Chromis (multilineata) (Guichenot, 1853) to Azurina Jordan & McGregor, 1898 (Tang et al., 2021Tang KL, Stiassny MLJ, Mayden RL, DeSalle R. Systematics of damselfishes. Ichthyol Herpetol. 2021; 109(1):258–318. https://doi.org/10.1643/i2020105
https://doi.org/10.1643/i2020105...
).

From this total, 176 (62.4%) species were observed during Projeto Ilhas do Rio fieldwork surveys. Among the species listed herein: 102 (36.2%) were observed in SRV videos, 160 (56.7%) species were recorded by UVC, being 86 (30.5%) registered in both sampling techniques. In addition, 16 (5.6%) species were only observed by SRV, while 73 (25.9%) species were exclusively observed through UVC. Lastly, 149 (52.8%) species were recorded in spearfishing/ artisanal fisheries’, being 63 (22.3%) exclusive.

TABLE 1 |
Fish species observed in Coastal Islands of Rio de Janeiro arranged according to Dornburg, Near, (2021)Dornburg A, Near TJ. The emerging phylogenetic perspective on the evolution of Actinopterygian fishes. Annu Rev Ecol Evol Syst. 2021; 52:427–52. https://doi.org/10.1146/annurev-ecolsys-122120-122554
https://doi.org/10.1146/annurev-ecolsys-...
. Observed sites: Tijucas Archipelago = TA; Cagarras Islands Natural Monument = MCA; Maricás Archipelago = MA; Rasa Island = RI; Cotunduba Island = CI; Conservation Status (IUCN/ICMBio): CR = Critically Endangered, EN = Endangered, VU = Vulnerable, NT = Near Threatened, LC = Least Concern, DD = Data Deficient, and NE = Not Evaluated. Record type: SIG = Sighted, LIT = Literature; FIS = Fishery (Fishermen’s colony and spearfishing), MUS = Museum Voucher, SRV= Submersible Rotating Video and UVC = Underwater Visual Census. † New Records for the area. # Exotic species, Ψ Brazilian endemic species; Rangel et al., 2007Rangel CA, Chaves LCT, Monteiro-Neto C. Baseline assessment of the reef fish assemblage from Cagarras Archipelago, Rio de Janeiro, southeastern Brazil. Braz J Oceanogr. 2007; 55(1):7–17. https://doi.org/10.1590/S1679-87592007000100002
https://doi.org/10.1590/S1679-8759200700...
*¹, Moraes et al., 2013Moraes FC, Bertoncini ÁA, Aguiar A., editors. História, Ppesquisa e Biodiversidade do Monumento Natural das Ilhas Cagarras. 1 ed. Rio de Janeiro: Mar Adentro; 2013.*², Monteiro-Neto et al., 2013Monteiro-Neto C, Bertoncini AA, Chaves LCT, Noguchi R, Mendonça-Neto JP, Rangel CA. Checklist of marine fish from coastal islands of Rio de Janeiro, with remarks on marine conservation. Mar Biodivers Rec. 2013; 6:1–13. http://dx.doi.org/10.1017/S1755267213000973
http://dx.doi.org/10.1017/S1755267213000...
*³, Amorim, Monteiro-Neto, 2016Amorim RB, Monteiro-Neto C. Marine protected area and the spatial distribution of the gill net fishery in Copacabana, Rio de Janeiro, RJ, Brazil. Braz J Biol. 2016; 76(1):1–09. http://dx.doi.org/10.1590/1519-6984.06614
http://dx.doi.org/10.1590/1519-6984.0661...
*4, Garcia et al., 2018Garcia LC, Moreira CR, Carvalho-Filho A. First record of African hind, Cephalopholis taeniops (Valenciennes, 1828) (Perciformes, Epinephelidae) in the South-western Atlantic. Check List. 2018; 14(6):961–65. https://doi.org/10.15560/14.6.961
https://doi.org/10.15560/14.6.961...
*5, Bertoncini et al., 2019Bertoncini AA, Moraes FC, Borgonha M, Aguiar A, Duarte B, editors. Marine biodiversity and diving guide to the islands of Rio. Rio de Janeiro: Museu Nacional, Série Livros 65; 2019.*6, Araujo et al., 2020Araujo NLF, Lopes CA, Brito VB, Santos LN, Barbosa-Filho MLV, Amaral CRL et al. Artisanally landed elasmobranchs along the coast of Rio de Janeiro, Brazil. Bol Lab Hidrobiol. 2020; 30(1):33–53. http://dx.doi.org/10.18764/1981-6421e2020.4
http://dx.doi.org/10.18764/1981-6421e202...
*7, Hauser-Davis et al., 2021Hauser-Davis RA, Amorim-Lopes C, Araujo NLF, Rebouças M, Gomes RA, Rocha RCC et al. On mobulid rays and metals: Metal content for the first Mobula mobular record for the state of Rio de Janeiro, Brazil and a review on metal ecotoxicology assessments for the Manta and Mobula genera. Mar Pollut Bull. 2021; 168:112472. https://doi.org/10.1016/j.marpolbul.2021.112472
https://doi.org/10.1016/j.marpolbul.2021...
*8.

The fish inventory contains 254 (90.1%) species of Osteichthyes and 28 (9.9%) Chondrichthyes. Carangidae was the richest family with 22 species, followed by Labridae with 21 fish species, Sciaenidae (14), Epinephelidae (11), Serranidae (9), Haemulidae and Pomacentridae (8), and Labrisomidae with 7 species (Fig. 3). The most common genera were Halichoeres Rüppell, 1835, Sparisoma Swainson, 1839, and Cynoscion Gill, 1861 with five species each, followed by Gymnothorax Bloch, 1795, Mycteroperca Gill, 1862, Caranx Lacepède, 1801, Lutjanus Bloch, 1790, and Trachinotus Lacepède, 1801, with four species each. In addition, this study revealed 21 new records of fish species, as follows: Rhincodon typus, Notorynchus cepedianus, Rhinoptera bonasus), Lampris guttatus, Ctenogobius saepepallens, Gobulus myersi, Hippocampus patagonicus, Halicampus crinitus), Mulloidichthys martinicus, Opistognathus vicinus, Chromis vanbebberae, Decapterus macarellus, Decapterus punctatus), Sarda sarda, Rachycentron canadum, Xiphias gladius, Pomadasys ramosus, Centropomus parallelus, Xyrichtys splendens, Mola mola), and last but not the least, Heniochus acuminatus, an exotic fish species herein reported in MONA Cagarras (see † in Tab. 1).

FIGURE 3 |
The richest families reported along the coastal islands and surrounding waters of Rio de Janeiro metropolitan region, Brazil.

The three most common elasmobranch species were Gymnura altavela, Myliobatis freminvillei, and Z. brevirostris (Figs. 4A,B,C). The Fig. 4 (D,E) brings two new records S. sarda and C. vanbebberae, and the most common species in the Archipelagos, which were D. argenteus, C. pullus, and H. aurolineatum (Figs. 4 F,G,H).

FIGURE 4 |
Elasmobranchs commonly observed on Rio de Janeiro coastal islands rockyreefs: A. Gymnura altavela, B. Myliobatis freminvillei, and C. Zapteryx brevirostris; new records D. Sarda sarda and E. Chromis vanbebberae; and the most common species: F. Diplodus argenteus, G. Cantherhines pullus, and H. Haemulon aurolineatum. Photos: Augusto A. Machado (A–B), Suzana Guimarães (D), Áthila A. Bertoncini (C, E–H).

Yet, rare species recorded in situ are depicted in Fig. 5, Thalassoma noronhanum, Paranthias furcifer, X. splendens. Yet, rare species recorded in situ are depicted in Fig. 5, T. noronhanum, P. furcifer, X. splendens, C. brasiliensis, E. lanceolatus, U. secunda, S. zelindae, and P. randalli, and in Fig. 6, Hippocampus reidi, Callionymus bairdi, Haemulon plumierii, Sargocentron bullisi, Chromis flavicauda, Pronotogrammus martinicensis, Centropyge aurantonotus, and Bodianus rufus. Finally, the rare cryptic species Gobulus myersi, and Paraclinus spectator are depicted in Fig. 7.

FIGURE 5 |
Rare fish species recorded on Rio de Janeiro coastal islands rocky reefs: A. Thalassoma noronhanum, B. Paranthias furcifer, C. Xyrichtys splendens, D. Clepticus brasiliensis, E. Eques lanceolatus, F. Uraspis secunda, G. Scarus zelindae and H. Ptereleotris randalli. Photos: Áthila A. Bertoncini (A–B, E–H), Augusto A. Machado (C, D).

FIGURE 6 |
Rare fish species recorded on Rio de Janeiro coastal islands rockyreefs: A. Hippocampus reidi, B. Callionymus bairdi, C. Haemulon plumierii, D. Sargocentron bullisi, E. Chromis flavicauda, F. Pronotogrammus martinicensis, G. Centropyge aurantonotus, and H. Bodianus rufus. Photos: Áthila A. Bertoncini.

FIGURE 7 |
Two cryptic species observed at a particular gravel bottom at Tijucas Archipelago. A. Gobulus myersi (new record) and Paraclinus spectator. Photos: Áthila A. Bertoncini.

Exotic fish record. Among the fishes listed, the SRV recorded an exotic species, originally widespread throughout the Indo-Pacific Ocean, from East Africa and Persian Gulf to the Society Islands, north to southern Japan, south to Lord Howe Island and throughout Micronesia. Heniochus acuminatus, commonly known as Longfin Bannerfish, was observed in Redonda Island at 8 meters deep. A single individual was sighted at a sampling video (Fig. 8A and in the videoS1) in March 2019 swimming over the rocky reef covered by turf algae, among native fish species (i.e., Acanthurus bahianus, Acanthurus chirurgus among others) and in February 2022, it was again observed at the same location (Suzana Guimarães, Projeto Ilhas do Rio researcher) at the same location, and on April 2022 by the authors (Fig. 8B). This species is easily identified observing its color pattern, white body with a pair of black bands, yellow truncate caudal fin, and dorsal fin spine especially long (Randall, 1995Randall JE, editors. Coastal fishes of Oman. Bathurst, Australia: Crawford House Publishing; 1995.; Adelir-Alves et al., 2018Adelir-Alves J, Soeth M, Braga RR, Spach HL. Non-native reef fishes in the Southwest Atlantic Ocean: a recent record of Heniochus acuminatus (Linnaeus, 1758) (Perciformes, Chaetodontidae) and biological aspects of Chromis limbata (Valenciennes, 1833) (Perciformes, Pomacentridae). Check List. 2018; 14(2):379–85. https://doi.org/10.15560/14.2.379
https://doi.org/10.15560/14.2.379...
; Froese, Pauly, 2022Froese R, Pauly D. FishBase. World Wide Web electronic publication, version (02/2022). 2022 [Internet]. Available from: https://www.fishbase.de/summary/5588
https://www.fishbase.de/summary/5588...
).

FIGURE 8 |
Heniochus acuminatus. A. The SRV frame recorded on MAR 2019 at Redonda Island, inside of the MPA, close to Acanthurus bahianus; B. H. acuminatus photographed in April 2022 (photo by Augusto A. Machado).

Conservation status. The fish species of coastal islands and surroundings were categorized following IUCN and ICMBio Red lists of threatened species (Fig. 9). According to IUCN, approximately 71.28% of species are assigned as Least Concern (LC), 7.45% are Data Deficient (DD), 4.26% Near Threatened (NT), and 6.74% Not Evaluated (NE). A total of 10.3% are considered threatened, being 7.45% assigned as Vulnerable (VU), 2.13% Endangered (EN) and 0.71% as Critically Endangered (CR). In parallel, the Brazilian red list (ICMBio, 2018Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). Livro vermelho da fauna brasileira ameaçada de extinção: Volume VI – Peixes. In: Instituto Chico Mendes de Conservação da Biodiversidade, organizers. Livro vermelho da fauna brasileira ameaçada de extinção. Brasília: ICMBio/MMA; 2018. Available from: https://www.gov.br/icmbio/pt-br/centrais-de-conteudo/publicacoes/publicacoes-diversas/livro_vermelho_2018_vol6.pdf
https://www.gov.br/icmbio/pt-br/centrais...
) considers 66.31% of the species as LC, 12.41% are DD, 7.8% NT, and 2.84% are NE. Threatened species account to 10.6%, where 6.03% are VU, 2.13% EN, and 2.48% CR.

FIGURE 9 |
Doughnut chart showing the assigned categories (%) of threatened fish species according to the IUCN and the Brazilian (ICMBio, 2018Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). Livro vermelho da fauna brasileira ameaçada de extinção: Volume VI – Peixes. In: Instituto Chico Mendes de Conservação da Biodiversidade, organizers. Livro vermelho da fauna brasileira ameaçada de extinção. Brasília: ICMBio/MMA; 2018. Available from: https://www.gov.br/icmbio/pt-br/centrais-de-conteudo/publicacoes/publicacoes-diversas/livro_vermelho_2018_vol6.pdf
https://www.gov.br/icmbio/pt-br/centrais...
) red lists. CR = Critically Endangered, DD = Data Deficient, EN = Endangered, LC = Least Concern, NE = Not Evaluated, NT = Near Threatened, VU = Vulnerable.

Fish richness along Rio de Janeiro and Maricás coastal islands. The richness from coastal islands of Rio de Janeiro and surroundings were widely represented through different sampling techniques (Tab. 1). We present the numbers of species recorded per archipelago, disregarding the number of islands sampled in each archipelago, where Cagarras Islands Natural Monument presented 181 fish species, with 58 exclusive species. In the Maricás Archipelago, 120 fish species, being six exclusives, whereas 115 species were recorded in Tijucas Archipelago, with 11 exclusive records (Fig. 10). In addition, samples from Rasa Island provided 108 records and in Cotunduba island, which is located within the Paisagem Carioca Municipal Natural Park - at the entrance to Guanabara Bay - 62 fish species were recorded.

We assessed the number of reef fish occurring simultaneously among archipelagos. The MONA Cagarras (MCA) and Maricás Archipelago presented the highest number of species in common with 112 fish species, representing 39.8% of total, that can be seen in both areas, followed by 102 species in MONA Cagarras and Tijucas Archipelago (36.3%), Maricás and Tijucas Archipelago with 93 species (approximately 33.1%) and finally only 91 or 32.4% species that can be seen in the three archipelagos (Fig. 10).

FIGURE 10 |
Venn diagram representing exclusive and shared species richness recorded in the study areas: large-bold-grey numbers are the total number of species in each area; small numbers represent exclusive species in each area; medium size numbers represent the share between/among areas.

New records. This study provides 21 new records never reported for these archipelagos, occurring along the coasts of Rio de Janeiro and Maricá cities (Fig. 1). Among the sampled areas, four new occurrences were reported in the Tijucas Archipelago: Xiphias gladius by spearfishing close to the islands, D. macarellus (UVC), C. parallelus (SRV), and G. myersi (UVC, Fig. 7A). The MONA Cagarras presented the greatest number of new records: M. mola was sighted on board close to Cagarra Island, while D. punctatus was observed by UVC in Comprida Island. Redonda Island provided the following new records: Rhincodon typus sighted on board within the MONA Cagarras Island ring, R. bonasus, C. vanbebberae (Fig. 4E), and M. martinicus by UVC, S. sarda (Fig. 4D) was sighted by Ilhas do Rio associated researchers, H. patagonicus was detected through fishing activities in the surroundings of the MPA and the non-native species H. acuminatus registered by SRV, within of the MPA. Additionally, O. vicinus was observed on Rasa Island inside its sand burrow and H. crinitus was seen amongst the gravel bottom. The samples performed on Cotunduba Island, at the entrance of Guanabara Bay, provided records of R. canadum by SRV and D. macarellus (UVC), while Maricás Archipelago contributed with three new records from UVC: X. splendens, M. martinicus and C. saepepallens. Finally, at the Z13 Fishermen colony, which fishing grounds are in the vicinity of the MONA Cagarras, three records were provided: N. cepedianus, P. ramosus, and L. guttatus.

DISCUSSION

In order to carry out scientific research and survey of marine species biodiversity, the Ilhas do Rio Project started in 2011 to improve knowledge, developing a huge effort in the biodiversity assessment in the Coastal Islands of Rio de Janeiro, specially, the then recently created MPA, MONA Cagarras. Since then, SCUBA diving surveys, documenting the rich biodiversity have been carried out to provide basic knowledge to build up public policies, such as the MPA’s Management Plan and to enhance the knowledge of the surrounding islands.

To assess fish species richness and reduce impacts, non-destructive techniques have been employed, providing relevant scientific results with minimal environmental disturbance. The use of complementary sampling techniques, especially UVC and SRV, was essential to achieve the important new records (n = 12) of species never recorded before in this study, such as the Green razorfish, X. splendens (Maricá Islands) (Fig. 5C); and the collaboration of Ilhas do Rio associated researchers (n = 2), that in situ reported the Sunfish, M. mola, and the Atlantic bonito, S. sarda (Fig. 4D).

Also, the important long-lasting relationship of researchers from Ilhas do Rio Project and the fishermen colony, provided unique records (n = 4), such as the offshore Opah, L. guttatus; the Broadnose sevengill shark (N. cepedianus), that was reported by fishing data at Z13 fishermen colony from Copacabana, Rio de Janeiro. We had 63 species (22.3%) being provided by fishermen, which is similar with the reported by Pinheiro et al., (2015)Pinheiro HT, Madureira JMC, Joyeux J-C, Martins AS. Fish diversity of a southwestern Atlantic coastal island: aspects of distribution and conservation in a marine zoogeographical boundary. 2015; Check List 11(2):1–17. https://doi.org/10.15560/11.2.1615
https://doi.org/10.15560/11.2.1615...
, where out of the 221 recorded species, 26% were exclusively provided by fishermen. In addition, the spearfishing activity recorded the Broadbill swordfish (X. gladius) and the Patagonian seahorse (H. patagonicus) was caught by bottom trawling. It is paramount to develop a good relationship and share the knowledge with fishermen in order to receive new records for the studies sites.

The submersible rotating video system (SRVs) proved to be of great power in detecting species, such as the exotic Longfin Bannerfish, H. acuminatus, first observed by this method, in a site often visited by researchers at Redonda Island. We emphasize the importance of using multiples and complementary techniques in fish biodiversity survey studies.

The inventory herein brings a combination of different observational and fisheries records, allowing the scientific assessment of rocky reefs and the surrounding pelagic and soft-bottom environments from Coastal islands of Rio de Janeiro and Maricá, contributing thus to improve conservation and management efforts in a broader area. Our observations provided 282 fish records and 21 new species, including an exotic species, representing a significant increase (over 7.6%) in the checklist, considering previous studies in these Islands (Monteiro-Neto et al., 2013Monteiro-Neto C, Bertoncini AA, Chaves LCT, Noguchi R, Mendonça-Neto JP, Rangel CA. Checklist of marine fish from coastal islands of Rio de Janeiro, with remarks on marine conservation. Mar Biodivers Rec. 2013; 6:1–13. http://dx.doi.org/10.1017/S1755267213000973
http://dx.doi.org/10.1017/S1755267213000...
, Bertoncini et al., 2019Bertoncini AA, Moraes FC, Borgonha M, Aguiar A, Duarte B, editors. Marine biodiversity and diving guide to the islands of Rio. Rio de Janeiro: Museu Nacional, Série Livros 65; 2019.). Marine coastal areas are known as important habitats for fish communities (Kume et al., 2021Kume M, Lavergne E, Ahn H, Terashima Y, Kadowaki K, Ye F et al. Factors structuring estuarine and coastal fish communities across Japan using environmental DNA metabarcoding, Ecol Indic. 2021; 121:107216. https://doi.org/10.1016/j.ecolind.2020.107216
https://doi.org/10.1016/j.ecolind.2020.1...
), thus recognizing the attributes of fish communities for future comparisons is likely to have consequences for the provision of ecosystem services such as fisheries and tourism (Chong-Seng et al., 2012Chong-Seng KM, Mannering TD, Pratchett MS, Bellwood DR, Graham NAJ. The influence of coral reef benthic condition on associated fish assemblages. PLoS ONE. 2012; 7(8):e42167. https://doi.org/10.1371/journal.pone.0042167
https://doi.org/10.1371/journal.pone.004...
), mainly in areas with a moderate-rate of endemic species like the Rio de Janeiro and Maricá coastal islands, circa 6%, and with circa 10.5% of the species in a threatened category according to IUCN and ICMBio.

These coastal islands are known to host a high diversity of terrestrial and marine species like seabirds, fishes, corals, and other organisms (for details, see Moraes et al., 2013Moraes FC, Bertoncini ÁA, Aguiar A., editors. História, Ppesquisa e Biodiversidade do Monumento Natural das Ilhas Cagarras. 1 ed. Rio de Janeiro: Mar Adentro; 2013.; Bertoncini et al., 2019Bertoncini AA, Moraes FC, Borgonha M, Aguiar A, Duarte B, editors. Marine biodiversity and diving guide to the islands of Rio. Rio de Janeiro: Museu Nacional, Série Livros 65; 2019.). Our study contributes to the update and improvement in the knowledge about fish biodiversity in each archipelago and surrounding areas. Data revealed the greatest fish richness within the Cagarras Islands Natural Monument, comprising about the 64.2% (181 spp.) (Fig. 10) of the total fish species encountered in Coastal islands of Rio de Janeiro and Maricá cities, showing the importance of this MPA for the conservation of fish species.

Long-term monitoring efforts are widely needed in coastal islands in order to better understand the structure of fish communities and the ecological relationships of this vertebrate group with other organisms. In addition, fish monitoring data provide important information for coastal management, to protect marine resources and efforts to assess MPA effectiveness (Jentoft et al., 2007Jentoft S, Van Son TC, Bjørkan M. Marine protected areas: A governance system analysis. Hum Ecol. 2007; 35:611–22. https://doi.org/10.1007/s10745-007-9125-6
https://doi.org/10.1007/s10745-007-9125-...
; Melià et al., 2020Melià P, Casagrandi R, Di Franco A, Guidetti P, Gatto M. Protection reveals density-dependent dynamics in fish populations: A case study in the central Mediterranean. PLoS ONE. 2020; 15(2):e0228604. https://doi.org/10.1371/journal.pone.0228604
https://doi.org/10.1371/journal.pone.022...
). Previous studies have indicated that MPAs are appropriate places for, in addition to preserving biodiversity, recovering exploited stocks (Roberts et al., 2001Roberts CM, Bohnsack JA, Gell F, Hawkins JP, Goodridge R. Effects of marine reserves on adjacent fisheries. Science. 2001; 294(5548):1920–23. https://doi.org/10.1126/science.294.5548.1920
https://doi.org/10.1126/science.294.5548...
; Halpern, 2003Halpern BS. The impact of marine reserves: Do reserves work and does reserve size matter? Ecol Appl. 2003; 13(1):117–37. https://doi.org/10.1890/1051-0761(2003)013[0117:TIOMRD]2.0.CO;2
https://doi.org/10.1890/1051-0761(2003)0...
), especially considering that most of the studied area is subject to recreational and artisanal fisheries. It is important to highlight that the MONA Cagarras, together with its surrounding areas (including Rasa and Cotunduba islands) was, in 2021, recognized as a Hope Spot for conservation of marine biodiversity by the international nonprofit organization Mission Blue (www.mission-blue.org/hope-spots).

However, this international recognition along with the national protection such as the “Natural Monument” category, bring the spotlight to these islands, but alone they will not save nor guarantee the protection of the reef fish fauna. It is important to rethink the design and limits of the MPA, in order to provide a proper protection for deeper rocky reefs, once the MPA limits of 10m from the island’s coast leave much of these areas unprotected.

The presence of exotic species such as the H. acuminatus, and Cephalopholis taeniops (Valenciennes, 1828) - previously collected in 2006 (Garcia et al., 2018Garcia LC, Moreira CR, Carvalho-Filho A. First record of African hind, Cephalopholis taeniops (Valenciennes, 1828) (Perciformes, Epinephelidae) in the South-western Atlantic. Check List. 2018; 14(6):961–65. https://doi.org/10.15560/14.6.961
https://doi.org/10.15560/14.6.961...
) within MONA Cagarras, calls the attention for the management and conservation of this important area. In Brazil, there is no evidence of successful invasion of the Longfin Bannerfish. The first report occurred in 1999 from Armação dos Búzios, Rio de Janeiro State (Moura, 2000Moura RL. Non-indigenous reef fishes in the southwestern Atlantic. In: Abstracts of the 9th International Coral Reef Symposium, Bali, Indonesia. 2000. ), while in 2013 it was recorded at Laje de Santos, São Paulo State (Luiz et al., 2014Luiz OJ, Comin EJ, Madin JS. Far away from home: the occurrence of the Indo-Pacific bannerfish Heniochus acuminatus (Pisces: Chaetodontidae) in the Atlantic. Bull Mar Sci. 2014; 90(2):741–44. https://doi.org/10.5343/bms.2013.1046
https://doi.org/10.5343/bms.2013.1046...
), and in 2017 it was sighted in a shipwreck in South Brazil (Paraná) (Adelir-Alves et al., 2018Adelir-Alves J, Soeth M, Braga RR, Spach HL. Non-native reef fishes in the Southwest Atlantic Ocean: a recent record of Heniochus acuminatus (Linnaeus, 1758) (Perciformes, Chaetodontidae) and biological aspects of Chromis limbata (Valenciennes, 1833) (Perciformes, Pomacentridae). Check List. 2018; 14(2):379–85. https://doi.org/10.15560/14.2.379
https://doi.org/10.15560/14.2.379...
). According to Luiz et al., (2014)Luiz OJ, Comin EJ, Madin JS. Far away from home: the occurrence of the Indo-Pacific bannerfish Heniochus acuminatus (Pisces: Chaetodontidae) in the Atlantic. Bull Mar Sci. 2014; 90(2):741–44. https://doi.org/10.5343/bms.2013.1046
https://doi.org/10.5343/bms.2013.1046...
there are two possible hypotheses for the introduction in Brazil: an aquarium release or long-distance natural dispersal from the Indian-Ocean. We suspect that the former hypothesis might be the case once this species is commonly traded by aquarists in the metropolis of Rio de Janeiro. Nevertheless, H. acuminatus is a planktivorous species and its occurrence is unlikely to cause significant impacts in the ecosystem’s health.

Additionally, the detection of alien species such as the Azores Chromis, Chromis limbata (Valenciennes, 183) (Leite et al., 2009Leite JR, Bertoncini ÁA, Bueno L, Daros F, Adelir-Alves J, Hostim-Silva M. The occurrence of Azores Chromis, Chromis limbata in the south-western Atlantic. J Mar Biol Assoc UK. 2009; 2:e145. https://doi.org/10.1017/S1755267209990637
https://doi.org/10.1017/S175526720999063...
; Anderson et al., 2017Anderson AB, Salas EM, Rocha LA, Floeter SR. The recent colonization of south Brazil by the Azores chromis Chromis limbata. J Fish Biol. 2017; 91(2):558–73. https://doi.org/10.1111/jfb.13363
https://doi.org/10.1111/jfb.13363...
), and the Toadfish, Opsanus beta (Goode & Bean, 1880), both established in some Brazilian estuaries (Cordeiro et al., 2020Cordeiro BD, Bertoncini AA, Abrunhosa FE, Corona LS, Araújo FG, Santos LN. First report of the non-native gulf toadfish Opsanus beta (Goode, Bean, 1880) on the coast of Rio de Janeiro – Brazil. Bioinvasions Rec. 2020; 9(2):279–86. Available from: https://www.reabic.net/journals/bir/2020/2/BIR_2020_Cordeiro_etal.pdf
https://www.reabic.net/journals/bir/2020...
) warns about the need to prevent the arrival and establishment of other exotic species, such as the lionfish (Pterois spp.) which has recently been continuously recorded in the Brazilian offshore island of Fernando de Noronha, and in coastal fisheries in North Brazil (Luiz et al., 2021Luiz OJ, Santos WCR, Marceniuk AP, Rocha LA, Floeter SR, Buck CE et al. Multiple lionfish (Pterois spp.) new occurrences along the Brazilian coast confirm the invasion pathway into the Southwestern Atlantic. Biol Invasions. 2021; 23:3013–19. https://doi.org/10.1007/s10530-021-02575-8
https://doi.org/10.1007/s10530-021-02575...
). In the Caribbean Sea, the lionfish invasion caused several impacts due to the voracious generalist predatory behavior, while depicting exponential increases in its abundance without significant natural predatory control (Côté et al., 2013Côté IM, Green SJ, Hixon MA. Predatory fish invaders: Insights from Indo-Pacific lionfish in the western Atlantic and Caribbean. Biol Conserv. 2013; 164:50–61. https://doi.org/10.1016/j.biocon.2013.04.014
https://doi.org/10.1016/j.biocon.2013.04...
; Samhouri, Stier, 2021Samhouri JF, Stier AC. Ecological impacts of an invasive mesopredator do not differ from those of a native mesopredator: lionfish in Caribbean Panama. Coral Reefs. 2021; 40:1593–600. https://doi.org/10.1007/s00338-021-02132-8
https://doi.org/10.1007/s00338-021-02132...
). The introduction of non-native species through human vectors is globally acknowledged to represent a major threat to biodiversity and ecosystem health (Sutherland et al., 2010Sutherland WJ, Clout M, Côté IM, Daszak P, Depledge MH, Fellman L et al. A horizon scan of global conservation issues for 2010. Trends Ecol Evol. 2010; 25(1):1–07. https://doi.org/10.1016/j.tree.2009.10.003
https://doi.org/10.1016/j.tree.2009.10.0...
), and, according to IOC-UNESCO, (2022)Intergovernmental Oceanographic Commission of UNESCO (IOC-UNESCO). Multiple ocean stressors: A scientific summary for policy makers. In: Boyd PW, Dupont S, Isensee K, editors [Internet]. Paris, France, UNESCO (IOC Information Series, 1404); 2022. http://dx.doi.org/10.25607/OBP-1724
http://dx.doi.org/10.25607/OBP-1724...
it is critical to understand multiple ocean stressors and target efforts at minimizing their impacts to lessen the cumulative pressure on the resilience and health of marine life.

Besides the exotic fish species, the presence of other invasive species along Brazilian reef environments, specially composing the bottom community, such as cnidarians, e.g., Stereonephthya sp. (Ferreira, 2003Ferreira CEL. Non-indigenous corals at marginal sites. Coral Reefs. 2003; 22:498. https://doi.org/10.1007/s00338-003-0328-z
https://doi.org/10.1007/s00338-003-0328-...
), Sarcotheliasp. (Xeniidae), and Briareum hamrum(Gohar, 1948) (Briareidae) (Menezes et al., 2022Menezes NM, McFadden CS, Miranda RJ, Nunes JACC, Lolis L, Barros F et al. New non-native ornamental octocorals threatening a South-west Atlantic reef. J Mar Biol Assoc UK. 2022; 101(6):911–17. https://doi.org/10.1017/S0025315421000849
https://doi.org/10.1017/S002531542100084...
) and the Sun coral (Tubastraea spp.), already established in the study area (Silva et al., 2022Silva MS, Moraes FC, Batista D, Bahia RG, Bertoncini AA, Machado AA et al. Distribution, population structure and settlement preference of Tubastraea spp. (Cnidaria: Scleractinia) on rocky shores of the Cagarras Islands Natural Monument and surroundings, Rio de Janeiro, Brazil. Reg Stud Mar Sci. 2022; 52:102245. https://doi.org/10.1016/j.rsma.2022.102245
https://doi.org/10.1016/j.rsma.2022.1022...
), may cause negative impacts on rocky reef fish communities (Miranda et al., 2018Miranda RJ, Nunes JACC, Mariano-Neto E, Sippo JZ, Barros F. Do invasive corals alter coral reef processes? An empirical approach evaluating reef fish trophic interactions. Mar Environ Res. 2018; 138:19–27. https://doi.org/10.1016/j.marenvres.2018.03.013
https://doi.org/10.1016/j.marenvres.2018...
), being studied (AAM, work in progress) in Rio de Janeiro’s archipelagos.

Coastal islands from Rio de Janeiro and Maricá cities are close to large urban centers (7 million people live around Guanabara Bay) and suffer a great influence of marine pollution (Guanabara Bay and Ipanema Sewage Outfall), unmanaged tourism, ornamental fish trade, illegal and unregulated fishing practices, and marine exotic species (ICMBio, 2020Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). Plano de manejo do monumento natural do arquipélago das Ilhas Cagarras. Brasília, DF; 2020. Available from: http://www.femerj.org/wp-content/uploads/plano_manejo_mona_arquipelago_das_ilhas_cagarras.pdf
http://www.femerj.org/wp-content/uploads...
). In order to understand how these impacts may influence the health of fish communities, this background knowledge about biodiversity and their ecological relationships is paramount. In this context, long-term monitoring programs are crucial to assist MPA managers in the development of preventive plans for biodiversity conservation of this area, that shelters one of the Brazilian hope spots.

ACKNOWLEDGEMENTS

We thank Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) for research permits (SISBio 74219–1). Part of the results were granted through Ilhas do Rio Project sponsored by Petrobras (2011–2019) and by AIEP and JGP (2020–2022). Doctoral scholarship was granted to AAM by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) through Programa de Pós-Graduação em Oceanografia Ambiental-UFES. AAB benefited from a Postdoctoral scholarship from CAPES/PNPD (23102.004667/2014–42) and CNPq/PDS (160133/2018–1). We also thank Dr. Liliane Lodi for the Ocean sunfish sighting reports and Dr. Suzana Guimarães for the Longfin Bannerfish records, Carlos Augusto Rangel for support in field campaigns, Alfredo Carvalho-Filho and Cláudio L. S. Sampaio for the help in identification of species. We would like to thank Manasi Rebouças and Z13 fishermen’s colony for their invaluable records and long lasting partnership; and finally the field support from Caio Salles (Projeto Verde Mar), Luiz “Cação”, Welington Vieira, Eduardo Licurci and Wagner Rodrigues from Mergulho Carioca.

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ADDITIONAL NOTES

  • HOW TO CITE THIS ARTICLE

    Machado AA, Moraes FC, Aguiar AA, Hostim-Silva M, Santos LN, Bertoncini AA. Rocky reef fish biodiversity and conservation in a Brazilian Hope Spot region. Neotrop Ichthyol. 2022; 20(3):e220032. https://doi.org/10.1590/1982-0224-2022-0032

Edited-by

Osmar Luiz

Publication Dates

  • Publication in this collection
    14 Oct 2022
  • Date of issue
    2022

History

  • Received
    14 May 2022
  • Accepted
    23 Aug 2022
Sociedade Brasileira de Ictiologia Neotropical Ichthyology, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá., Av. Colombo, 5790, 87020-900, Phone number: +55 44-3011-4632 - Maringá - PR - Brazil
E-mail: neoichth@nupelia.uem.br