Mesophotic ecosystems at Fernando de Noronha Archipelago, Brazil (South-western Atlantic), reveal unique ichthyofauna and need for conservation

Caio R. Pimentel Luiz A. Rocha Bart Shepherd Tyler A. Y. Phelps Jean-Christophe Joyeux Agnaldo S. Martins Carlos Eduardo Stein João B. Teixeira João Luiz Gasparini José Amorim Reis-Filho Ricardo C. Garla Ronaldo B. Francini-Filho Stephanie D. T. Delfino Thayná J. Mello Tommaso Giarrizzo Hudson T. Pinheiro About the authors

Abstract

Although several studies on the ichthyofauna of the Fernando de Noronha Archipelago have been carried out, its mesophotic fish diversity has never been surveyed before. Here we used SCUBA and technical rebreather diving, baited remote underwater videos and remotely operated vehicle to record shallow (≤ 30 m depth) and mesophotic (31 to 150 m depth) fishes. Nineteen fish species belonging to 14 families are reported here as new records, representing an increase of 8.2% in marine fish richness for the region, which now has a total of 250 species and 77 families. These new records include four potential new species and highlight the importance of surveying mesophotic ecosystems, even in well studied sites. Our results also emphasize the need for protection and attention to the unique ichthyofauna found at mesophotic depths.

Keywords:
BRUVS; Marine Protected Area; Oceanic Island; Rebreather; Remotely Operated Vehicle

Resumo

Apesar de muitos estudos sobre a ictiofauna do Arquipélago de Fernando de Noronha terem sido realizados, sua diversidade de peixes mesofóticos nunca foi estudada antes. Neste estudo utilizamos mergulho autônomo e mergulho técnico, vídeos subaquáticos remotos com isca e veículo operado remotamente para registrar peixes de ecossistemas rasos (≤ 30 m de profundidade) e mesofóticos (31 a 150 m de profundidade). Dezenove espécies de peixes pertencentes a 14 famílias são apresentadas aqui como novos registros, representando um aumento de 8,2% na riqueza de peixes marinhos da região, que agora possui um total de 250 espécies e 77 famílias. Esses novos registros incluem quatro prováveis novas espécies e reforçam a importância de estudos em ecossistemas mesofóticos. Nossos resultados também enfatizam a necessidade de proteção e atenção à essa ictiofauna única encontrada nesses ecossistemas profundos.

Palabras-chave:
Área Marinha Protegida; BRUVS; Ilha Oceânica; Rebreather; Veículo Operado Remotamente

INTRODUCTION

Due to their geographical isolation, oceanic islands are often unique environments with biodiversity characterized by high endemism (Vaske Jr et al., 2005Vaske Jr T, Lessa RP, Nóbrega MF, Montealegre-Quijano S, Marcante Santana F, Bezerra Jr JL. A checklist of fishes from Saint Peter and Saint Paul Archipelago, Brazil. J Appl Ichthyol. 2005; 21(1):75-79. https://doi.org/10.1111/j.1439-0426.2004.00600.x
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). These environments function as true natural laboratories for evolutionary and ecological studies (Pinheiro et al., 2017Pinheiro HT, Bernardi G, Simon T, Joyeux J-C, Macieira RM, Gasparini JL, Rocha C, Rocha LA. Island biogeography of marine organisms. Nature. 2017; 549:82-85. https://doi.org/10.1038/nature23680
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). Recent studies are revealing many new species and new occurrences, filling gaps in the biodiversity knowledge and increasing our understanding about the biogeographic patterns of oceanic islands (e.g., Simon et al., 2013Simon T, Macieira RM, Joyeux J-C. The shore fishes of the Trindade-Martin Vaz insular complex: an update. J Fish Biol. 2013; 82(6):2113-27. https://doi.org/10.1111/jfb.12126
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Knowledge about reef fish biodiversity and biogeographic patterns of South Atlantic oceanic islands has steadily increased over the past two decades (e.g., Batista et al., 2012Batista H, Zill J, Veras D, Hazin F, Oliveira P, Marins Y, Oliveira D, Pereira R, Tolotti M, Silva M. New records of reef fishes (Teleostei: Perciformes) in the Rocas Atoll Biological Reserve, off northeastern Brazil. Check List. 2012; 8(3):584-88. https://doi.org/10.15560/8.3.584
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, 2018aPinheiro HT, Rocha LA, Macieira RM, Carvalho-Filho A, Anderson AB, Bender MG, Di Dario F, Ferreira CEL, Figueiredo-Filho J, Francini-Filho R, Gasparini JL, Joyeux J-C, Luiz OJ, Mincarone MM, Moura RL, Nunes JACC, Quimbayo JP, Rosa RS, Sampaio CLS, Sazima I, Simon T, Vila-Nova DA, Floeter SR. South-western Atlantic reef fishes: Zoogeographical patterns and ecological drivers reveal a secondary biodiversity centre in the Atlantic Ocean. Divers Distrib. 2018a; 24(7):951-65. https://doi.org/10.1111/ddi.12729
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). However, mesophotic ecosystems (between 31 - 150 m depth) remain largely unknown and are only now receiving some scientific attention (e.g., Rocha et al., 2018Rocha LA, Pinheiro HT, Shepherd B, Papastamatiou YP, Luiz OJ, Pyle RL, Bongaerts P. Mesophotic coral ecosystems are threatened and ecologically distinct from shallow water reefs. Science. 2018; 361(6399):281-84. https://doi.org/10.1126/science.aaq1614
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). Even though these ecosystems have been recognized since the 19th century (Sinniger et al., 2016Sinniger F, Ballantine DL, Bejarano I, Colin PL, Pochon X, Pomponi SA, Puglise KA, Pyle RL, Reaka ML, Spalding HL, Weil E. Biodiversity of mesophotic coral ecosystems. In: Baker EK, Puglise KA, Harris PT, editors. Mesophotic coral ecosystems - a lifeboat for coral reefs? Nairobi and Arendal: The United Nations Environment Programme and GRID-Arendal; 2016. p.50-62.), the first studies in Brazil date back only to the 1960s (Francini-Filho et al., 2019Francini-Filho RB, Velásquez VM, Silva MB, Rosa MR, Sumida PYG, Pinheiro HT, Rocha LA, Ferrreira CEL, Francini CLB, Rosa RS. Brazil. In: Loya Y, Puglise K, Bridge T, editors. Mesophotic Coral Ecosystems. Cham: Springer; 2019. p.163-198.). Systematic studies of the mesophotic ecosystems have however increased worldwide (e.g., Rosa et al., 2015Rosa MR, Alves AC, Medeiros DV, Coni EOC, Ferreira CM, Ferreira BP, Rosa RS, Amado-Filho GM, Pereira-Filho GH, Moura RL, Thompson FL, Sumida PYG, Francini-Filho RB. Mesophotic reef fish assemblages of the remote St. Peter and St. Paul’s Archipelago, Mid-Atlantic Ridge, Brazil. Coral Reefs. 2015; 35:113-23. https://doi.org/10.1007/s00338-015-1368-x
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; 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
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; Pyle et al., 2016Pyle RL, Boland R, Bolick H, Bowen BW, Bradley CJ, Kane C, Kosaki RK, Langston R, Longenecker K, Montgomery A, Parrish FA, Popp BN, Rooney J, Smith CM, Wagner D, Spalding HL. A comprehensive investigation of mesophotic coral ecosystems in the Hawaiian Archipelago. PeerJ. 2016; 4:e2475. https://doi.org/10.7717/peerj.2475
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; Simon et al., 2016Simon T, Pinheiro HT, Moura RL, Carvalho-Filho A, Rocha LA, Martins AS, Mazzei EF, Francini-Filho RB, Amado-Filho GM, Joyeux J-C. Mesophotic fishes of the Abrolhos Shelf, the largest reef ecosystem in the South Atlantic. J Fish Biol. 2016; 89(1):990-1001. https://doi.org/10.1111/jfb.12967
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; Rocha et al., 2018Rocha LA, Pinheiro HT, Shepherd B, Papastamatiou YP, Luiz OJ, Pyle RL, Bongaerts P. Mesophotic coral ecosystems are threatened and ecologically distinct from shallow water reefs. Science. 2018; 361(6399):281-84. https://doi.org/10.1126/science.aaq1614
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; Pinheiro et al., 2019Pinheiro HT, Shepherd B, Castillo C, Abesamis RA, Copus JM, Pyle RL, Greene BD, Coleman RR, Whitton RK, Thillainath E, Bucol AA, Birt M, Catania D, Bell MV, Rocha LA. Deep reef fishes in the world’s epicenter of marine biodiversity. Coral Reefs. 2019; 38:985-95. https://doi.org/10.1007/s00338-019-01825-5
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). Such pioneer studies have provided important baseline information, such as richness and diversity of species, and form the basis for more complex ecological and evolutionary studies.

Fernando de Noronha Archipelago (FN) is the most accessible oceanic island in Brazil, as it is relatively close to the mainland and has an airport. It also offers logistical support due to the presence of a research station and several dive shops and boats. Part of the Archipelago comprises a no-take Marine Protected Area (MPA), the Fernando de Noronha Marine National Park, which protects near-shore ecosystems (e.g., tidepools, rocky shores, and reefs) to around 50 m depth. Most of the mesophotic ecosystems are located in a sustainable use MPA, the Fernando de Noronha - Rocas - São Pedro and São Paulo Environmental Protected Area, where fishing is allowed with some restrictions (ICMBio, 2017). Nearly all biodiversity and ecological studies of FN’s ichthyofauna to date have been carried out in the intertidal (e.g., Andrades et al., 2018Andrades R, Reis-Filho JA, Macieira RM, Giarrizzo T, Joyeux J-C. Endemic fish species structuring oceanic intertidal reef assemblages. Sci Rep. 2018; 8:10791. https://doi.org/10.1038/s41598-018-29088-0
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; Rodríguez-Rey et al., 2018Rodríguez-Rey GT, Carvalho Filho A, Araújo ME, Solé-Cava AM. Evolutionary history of Bathygobius (Perciformes: Gobiidae) in the Atlantic biogeographic provinces: a new endemic species and old mitochondrial lineages. Zool J Linnean Soc. 2018; 182(2):360-84. https://doi.org/10.1093/zoolinnean/zlx026
https://doi.org/10.1093/zoolinnean/zlx02...
) and shallow (≤ 20 m deep) environments (e.g., Krajewski, Floeter, 2011Krajewski JP, Floeter SR. Reef fish community structure of the Fernando de Noronha Archipelago (Equatorial Western Atlantic): the influence of exposure and benthic composition. Environ Biol Fish. 2011; 92:25-40. https://doi.org/10.1007/s10641-011-9813-3
https://doi.org/10.1007/s10641-011-9813-...
; Medeiros et al., 2011Medeiros PR, Rosa RS, Francini-Filho RB. Dynamics of fish assemblages on a continuous rocky reef and adjacent unconsolidated habitats at Fernando de Noronha Archipelago, tropical western Atlantic. Neotrop Ichthyol. 2011; 9(4):869-79. https://doi.org/10.1590/S1679-62252011005000048
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; Ilarri et al., 2017Ilarri MI, Souza AT, Rosa RS. Community structure of reef fishes in shallow waters of the Fernando de Noronha archipelago: effects of different levels of environmental protection. Mar Freshwater Res. 2017; 68(7): 1303-316. https://doi.org/10.1071/MF16071
https://doi.org/10.1071/MF16071...
; Smith-Vaniz et al., 2018Smith-Vaniz WF, Tornabene L, Macieira RM. Review of Brazilian jawfishes of the genus Opistognathus with descriptions of two new species (Teleostei, Opistognathidae). Zookeys. 2018; 794:95-133. https://doi.org/10.3897/zookeys.794.26789
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; but see Garla et al., 2006Garla RC, Chapman DD, Wetherbee BM, Shivji M. Movement patterns of young Caribbean reef sharks, Carcharhinus perezi, at Fernando de Noronha Archipelago, Brazil: the potential of marine protected areas for conservation of a nursery ground. Mar Biol. 2006; 149:189-99. https://doi.org/10.1007/s00227-005-0201-4
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; Sazima et al., 2010Sazima I, Grossman A, Sazima C. Deep cleaning: a wrasse and a goby clean reef fish below 60 m depth in the tropical south-western Atlantic. Mar Biodivers Rec. 2010; 3:E60. https://doi.org/10.1017/S1755267210000497
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; Afonso et al., 2017Afonso AS, Garla R, Hazin FHV. Tiger sharks can connect equatorial habitats and fisheries across the Atlantic Ocean basin. PLoS One. 2017; 12(9): e0184763. https://doi.org/10.1371/journal.pone.0184763
https://doi.org/10.1371/journal.pone.018...
).

Therefore, to fill the knowledge gap about fish biodiversity from mesophotic ecosystems of the Fernando de Noronha Archipelago, we carried out a large-scale survey using sampling techniques including technical rebreather diving, baited remote underwater stereo-video systems (stereo-BRUVS) and remotely operated vehicles (ROVs). Here, we present new records and new species of fishes discovered during our expedition, discuss aspects related to the island’s biodiversity and biogeography, and highlight the need to protect insular mesophotic ecosystems.

MATERIAL AND METHODS

Study area. Fernando de Noronha Archipelago is located 345 km off the north-eastern Brazilian coast (03°50’S 32°25’W), on the Fernando de Noronha Submarine Ridge (Fig. 1). It is the largest Brazilian oceanic archipelago, composed by a volcanic island (16.4 km2) and 18 small islets (Almeida, 2006Almeida FFM. Ilhas oceânicas brasileiras e suas relações com a tectônica atlântica. Terræ Didatica. 2006; 2(1):3-18). The shallow reefs (≤ 30 m depth) are mainly composed by volcanic rocks predominantly covered by algal turfs and brown macroalgae, with low coral cover (Krajewski, Floeter, 2011Krajewski JP, Floeter SR. Reef fish community structure of the Fernando de Noronha Archipelago (Equatorial Western Atlantic): the influence of exposure and benthic composition. Environ Biol Fish. 2011; 92:25-40. https://doi.org/10.1007/s10641-011-9813-3
https://doi.org/10.1007/s10641-011-9813-...
). Following the pattern of low diversity typical of Atlantic oceanic islands (Ferreira et al., 2004Ferreira CEL, Floeter SR, Gasparini JL, Ferreira BP, Joyeux J-C. Trophic structure patterns of Brazilian reef fishes: a latitudinal comparison. J Biogeogr. 2004; 31(7):1093-106. https://doi.org/10.1111/j.1365-2699.2004.01044.x
https://doi.org/10.1111/j.1365-2699.2004...
; Floeter et al., 2008Floeter SR, Rocha LA, Robertson DR, Joyeux J-C, Smith-Vaniz WF, Wirtz P, Edwards AJ, Barreiros JP, Ferreira CEL, Gasparini JL, Brito A, Falcón JM, Bowen BW, Bernardi G. Atlantic reef fish biogeography and evolution. J Biogeogr. 2008; 35(1):22-47. https://doi.org/10.1111/j.1365-2699.2007.01790.x
https://doi.org/10.1111/j.1365-2699.2007...
), the fish assemblages are dominated by a few very abundant species (Krajewski, Floeter, 2011Krajewski JP, Floeter SR. Reef fish community structure of the Fernando de Noronha Archipelago (Equatorial Western Atlantic): the influence of exposure and benthic composition. Environ Biol Fish. 2011; 92:25-40. https://doi.org/10.1007/s10641-011-9813-3
https://doi.org/10.1007/s10641-011-9813-...
; Ilarri et al., 2017Ilarri MI, Souza AT, Rosa RS. Community structure of reef fishes in shallow waters of the Fernando de Noronha archipelago: effects of different levels of environmental protection. Mar Freshwater Res. 2017; 68(7): 1303-316. https://doi.org/10.1071/MF16071
https://doi.org/10.1071/MF16071...
). Compared to shallow reefs, the upper mesophotic reefs (31 to 60 m depth) show higher cover of sponges and the scleractinian coral Montastraea cavernosa (Linnaeus, 1767) (Matheus et al., 2019Matheus Z, Francini-Filho RB, Pereira-Filho GH, Moraes FC, Moura RLd, Brasileiro RPS, Amado-Filho GM. Benthic reef assemblages of the Fernando de Noronha Archipelago, tropical South-west Atlantic: Effects of depth, wave exposure and cross-shelf positioning. PLoS One. 2019; 14(1):e0210664. https://doi.org/10.1371/journal.pone.0210664
https://doi.org/10.1371/journal.pone.021...
). A mosaic of habitats such as patch reefs, sand bottoms and rhodolith beds compose the middle mesophotic zone (61 to 90 m depth; Fig. 2). Below 90 m depth, the edge of the insular shelf followed by a steep wall characterizes the lower mesophotic zone (91 to 150 m; Fig. 3). A strong thermocline is found just below the shelf edge, where the temperature drops from ~27 to ~14 °C. The ecosystem at the lower mesophotic zone is highly complex, formed by rocky reefs covered mostly by crustose coralline algae, black corals and sponges.

FIGURE 1 |
Location of the Fernando de Noronha Archipelago, Brazil (South-western Atlantic). Blue line indicates the area of the Marine National Park of Fernando de Noronha (no-take MPA). Dashed lines indicate the 30, 60, 90 and 150 m isobaths. Black triangles, red stars, golden squares and green dots indicate the position of stereo-BRUVS deployments, rebreather dives, SCUBA dives and ROV footages, respectively.

FIGURE 2 |
Middle mesophotic (61 to 90 m depth) mosaic of habitats sampled with stereo-BRUVS around the Fernando de Noronha Archipelago. A. Patch reefs; B. Sand bottoms; and C. Rhodoliths beds.

FIGURE 3 |
Lower mesophotic (below 90 m depth) ecosystems explored through technical rebreather diving around the Fernando de Noronha Archipelago. A.The insular shelf edge; and B. The steep wall.

Regarding environmental management, the Archipelago encompasses two different types of Marine Protected Areas, the no-take zone of the Fernando de Noronha Marine National Park (Brasil, 1988Brasil. Decreto no 96.693, de 14 de setembro de 1988. Diário Oficial da União, Poder Executivo, Brasília, DF, 15 set. 1988. Available at: https://www2.camara.leg.br/legin/fed/decret/1988/decreto-96693-14-setembro-1988-447461-publicacaooriginal-1-pe.html
https://www2.camara.leg.br/legin/fed/dec...
), and the sustainable use zone of the Fernando de Noronha - Rocas - São Pedro and São Paulo Environmental Protected Area (Brasil, 1986Brasil. Decreto no 92.755, de 5 de junho de 1986. Diário Oficial da União, Poder Executivo, Brasília, DF, 6 jun. 1986. Available at: http://www.planalto.gov.br/ccivil_03/decreto/1980-1989/1985-1987/D92755.htm
http://www.planalto.gov.br/ccivil_03/dec...
) (Fig. 1). The Marine National Park comprises about 70% of the main island (i.e., all the windward coast and part of the leeward coast), all smaller islands and extends to around the 50 m isobath, with fishing prohibited and tourism regulated (Brasil, 1988Brasil. Decreto no 96.693, de 14 de setembro de 1988. Diário Oficial da União, Poder Executivo, Brasília, DF, 15 set. 1988. Available at: https://www2.camara.leg.br/legin/fed/decret/1988/decreto-96693-14-setembro-1988-447461-publicacaooriginal-1-pe.html
https://www2.camara.leg.br/legin/fed/dec...
; Ibama, 1990Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (Ibama). Plano de Manejo do Parque Nacional Marinho de Fernando de Noronha. Brasília, 1990. Available from: https://www.icmbio.gov.br/portal/images/stories/biodiversidade/_PARNA_MARINHA_DE_FERNANDO_DE_NORONHA.pdf
https://www.icmbio.gov.br/portal/images/...
). The area of sustainable use aims to make human occupation, tourism and fishing compatible with environmental protection and preservation of natural resources (Brasil, 1986Brasil. Decreto no 92.755, de 5 de junho de 1986. Diário Oficial da União, Poder Executivo, Brasília, DF, 6 jun. 1986. Available at: http://www.planalto.gov.br/ccivil_03/decreto/1980-1989/1985-1987/D92755.htm
http://www.planalto.gov.br/ccivil_03/dec...
; ICMBio, 2017Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). Plano de Manejo da Área de Proteção Ambiental de Fernando de Noronha - Rocas - São Pedro e São Paulo. Brasília, 2017. Available from: https://www.icmbio.gov.br/portal/images/stories/plano-de-manejo/plano_de_manejo_parna_ferando-de-noronha.pdf
https://www.icmbio.gov.br/portal/images/...
). The use of trawl nets, longlines, drift nets and spears, as well as the capture of sharks, rays and parrotfishes are not allowed (Brasil, 1986Brasil. Decreto no 92.755, de 5 de junho de 1986. Diário Oficial da União, Poder Executivo, Brasília, DF, 6 jun. 1986. Available at: http://www.planalto.gov.br/ccivil_03/decreto/1980-1989/1985-1987/D92755.htm
http://www.planalto.gov.br/ccivil_03/dec...
; ICMBio, 2017Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). Plano de Manejo da Área de Proteção Ambiental de Fernando de Noronha - Rocas - São Pedro e São Paulo. Brasília, 2017. Available from: https://www.icmbio.gov.br/portal/images/stories/plano-de-manejo/plano_de_manejo_parna_ferando-de-noronha.pdf
https://www.icmbio.gov.br/portal/images/...
).

Sampling procedures. The data presented here were obtained during a 15-day expedition in October 2019. Fish were recorded with SCUBA (ca. 30 h sampling in the euphotic zone) and technical rebreather diving (ca. 6 h sampling in the upper and 2 h in the lower mesophotic zone), remotely operated vehicle (ROV -ca. 8 h of footage) and baited remote underwater stereo-video systems (stereo-BRUVS - 42 deployments of 1 h footage each). Some fishes were collected using hand-nets and pole-spears, and voucher specimens were deposited in the ichthyological collection of the Universidade Federal do Espírito Santo (CIUFES; see Tab. 1 for catalogue numbers).

Data analysis. Species identification was performed using taxonomic keys (e.g., Menezes, 1971Menezes NA. A new species of Paratrachichthys from the coast of Brazil (Pisces, Trachichthyidae). Pap Avulsos Zool. 1971; 25:143-48; Knudsen, Clements, 2013Knudsen SW, Clements KD. Revision of the fish family Kyphosidae (Teleostei: Perciformes). Zootaxa. 2013; 3751(1):1-101. https://doi.org/10.11646/zootaxa.3751.1.1
https://doi.org/10.11646/zootaxa.3751.1....
) and, when necessary, comparing our collected specimens with others available at the ichthyological collection of CIUFES. We then classified the species according to: 1) depth zone of the record, i.e., euphotic (≤ 30 m) or mesophotic (> 30 - 150 m), 2) habitat (reef or rhodolith), 3) the type of the record (collected, photographed or filmed with ROV or stereo-BRUVS), 4) geographic range (following Pinheiro et al., 2018aPinheiro HT, Rocha LA, Macieira RM, Carvalho-Filho A, Anderson AB, Bender MG, Di Dario F, Ferreira CEL, Figueiredo-Filho J, Francini-Filho R, Gasparini JL, Joyeux J-C, Luiz OJ, Mincarone MM, Moura RL, Nunes JACC, Quimbayo JP, Rosa RS, Sampaio CLS, Sazima I, Simon T, Vila-Nova DA, Floeter SR. South-western Atlantic reef fishes: Zoogeographical patterns and ecological drivers reveal a secondary biodiversity centre in the Atlantic Ocean. Divers Distrib. 2018a; 24(7):951-65. https://doi.org/10.1111/ddi.12729
https://doi.org/10.1111/ddi.12729...
), and 5) conservation status, following the International Union for Conservation of Nature’s (IUCN) Red List of Threatened Species (https://www.iucnredlist.org).

RESULTS

Nineteen fish species belonging to 14 families are reported here as new records for FN (Tab. 1). The most speciose families were Kyphosidae and Serranidae, with three new records each, followed by Pomacentridae, with two new records. Fourteen new records (74% of total) were from the mesophotic ecosystems (Figs. 4-5; Tab. 1) and five (26%) from the euphotic zone (Fig. 6; Tab. 1). Seven species are distributed throughout the Western Atlantic, and the three Kyphosidae are circumtropical species. Three other species are amphi-Atlantic, one of which also occurs in the Mediterranean (Balistes capriscus Gmelin, 1789). Aulotrachichthys argyrophanus (Woods, 1961) occurs only in the South-western Atlantic and Chromis scotti Emery, 1968 is found in the Caribbean Sea and Northern Brazil (Moura et al., 1999Moura RL, Rodrigues MCM, Francini-Filho RB, Sazima I. Unexpected richness of reef corals near the southern Amazon River mouth. Coral Reefs. 1999; 18:170. https://doi.org/10.1007/s003380050175
https://doi.org/10.1007/s003380050175...
). Four new records are probable new species (Synodus sp., Scorpaena sp., Psilotris sp., and Tosanoides sp.) with unknown geographic range (Fig. 4E-G; Tab. 1). In terms of conservation status, only B. capriscus is listed as threatened, being currently classified as vulnerable in the IUCN Red List (Liu et al., 2015Liu J, Zapfe G, Shao K-T, Leis JL, Matsuura K, Hardy G, Liu M, Tyler J. Balistes capriscus. The IUCN Red List of Threatened Species 2015: e.T193736A97662794. (errata version published in 2016). Downloaded on 06 March 2020.).

TABLE 1 |
New records of fishes from Fernando de Noronha Archipelago, north-eastern Brazil. Families are presented in phylogenetic order according to Nelson et al. (2016)Nelson JS, Grande TC, Wilson MVH. Fishes of the world. Hoboken, New Jersey: Wiley & Sons; 2016.. Information about depth zone, habitat, record type and voucher of the new records, as well as distribution and conservation status of the species are presented. Depth zone of the record: euphotic (≤ 30 m deep) and mesophotic (31 to 150 m deep). Geographic range: amphi-Atlantic (AA), Caribbean Sea (CS), Circumtropical (CT), Mediterranean (M), Northern Brazil (NB), South-western Atlantic (SW) and Western Atlantic (WA). International Union for Conservation of Nature and Natural Resources (IUCN) conservation status: data deficient (DD), least concern (LC), and vulnerable (VU); N/A: not applicable.

FIGURE 4 |
New records of fishes at the mesophotic ecosystems. A. Chromis enchrysura(~ 10 cm total length); B. Balistes capriscus(~ 30 cm total length); C. Chromis scotti (~ 7.5 cm total length); D. Prognathodes guyanensis (~ 15 cm total length); E. Synodus sp. (~ 15 cm total length); F. Scorpaena sp. (~ 7.5 cm total length); G. Psilotris sp. (~ 5 cm total length); and H. Cosmocampus profundus(white arrow; ~ 15 cm total; I. Lutjanus buccanella (~ 50 cm total length). Photos by L. A. Rocha (A, C-G) and stereo-BRUVS (B, Hand I). Tosanoidessp. is under description and its picture is not shown.

FIGURE 5 |
New records of fishes from the mesophotic ecosystems collected and photographed in aquarium. A. Aulotrachichthys argyrophanus(~ 6.5 cm total length; CIUFES 3909); B. Corniger spinosus(~ 15 cm total length; CIUFES 3922); C. Decodon puellaris (~ 7.5 cm total length; CIUFES 3914); and D. Pronotogrammus martinicensis(~ 20 cm total length; CIUFES 3939 / 3960). Photos by J. L. Gasparini.

FIGURE 6 |
New records of fishes from the euphotic ecosystems. A. Kyphosus bigibbus(~ 25 cm total length); B. Kyphosus cinerascens (~ 25 cm total length); C. Kyphosus vaigiensis(~ 25 cm total length; CIUFES 4050); and D. Pseudogramma gregoryi(~ 6.5 cm total length; CIUFES 4029). Photos A, B and C by J. L. Gasparini and photo D by R. M. Macieira. Apogon pseudomaculatus(CIUFES 3957) is not shown.

DISCUSSION

Fernando de Noronha Archipelago harbours the greatest richness of marine fish among the oceanic islands of the South Atlantic (Floeter et al., 2008Floeter SR, Rocha LA, Robertson DR, Joyeux J-C, Smith-Vaniz WF, Wirtz P, Edwards AJ, Barreiros JP, Ferreira CEL, Gasparini JL, Brito A, Falcón JM, Bowen BW, Bernardi G. Atlantic reef fish biogeography and evolution. J Biogeogr. 2008; 35(1):22-47. https://doi.org/10.1111/j.1365-2699.2007.01790.x
https://doi.org/10.1111/j.1365-2699.2007...
; Pinheiro et al., 2018aPinheiro HT, Rocha LA, Macieira RM, Carvalho-Filho A, Anderson AB, Bender MG, Di Dario F, Ferreira CEL, Figueiredo-Filho J, Francini-Filho R, Gasparini JL, Joyeux J-C, Luiz OJ, Mincarone MM, Moura RL, Nunes JACC, Quimbayo JP, Rosa RS, Sampaio CLS, Sazima I, Simon T, Vila-Nova DA, Floeter SR. South-western Atlantic reef fishes: Zoogeographical patterns and ecological drivers reveal a secondary biodiversity centre in the Atlantic Ocean. Divers Distrib. 2018a; 24(7):951-65. https://doi.org/10.1111/ddi.12729
https://doi.org/10.1111/ddi.12729...
). The 19 new records presented here represent an increase of 8.2% in its marine ichthyofauna, now composed of 250 species and 77 families. Fernando de Noronha Archipelago is now between 22% and 36% richer, in fishes, than Trindade Island, Santa Helena Island, Ascension Island, Rocas Atoll and St. Paul’s Archipelago (see Wirtz et al., 2017Wirtz P, Bingeman J, Bingeman J, Fricke R, Hook TJ, Young J. The fishes of Ascension Island, central Atlantic Ocean: new records and an annotated checklist. J Mar Biol Assoc UK. 2017; 97(4):783-98. https://doi.org/10.1017/S0025315414001301
https://doi.org/10.1017/S002531541400130...
; Pinheiro et al., 2018aPinheiro HT, Rocha LA, Macieira RM, Carvalho-Filho A, Anderson AB, Bender MG, Di Dario F, Ferreira CEL, Figueiredo-Filho J, Francini-Filho R, Gasparini JL, Joyeux J-C, Luiz OJ, Mincarone MM, Moura RL, Nunes JACC, Quimbayo JP, Rosa RS, Sampaio CLS, Sazima I, Simon T, Vila-Nova DA, Floeter SR. South-western Atlantic reef fishes: Zoogeographical patterns and ecological drivers reveal a secondary biodiversity centre in the Atlantic Ocean. Divers Distrib. 2018a; 24(7):951-65. https://doi.org/10.1111/ddi.12729
https://doi.org/10.1111/ddi.12729...
, 2020Pinheiro HT, Macena BCL, Francini-Filho RB, Ferreira CEL, Albuquerque FV, Bezerra NPA, Carvalho-Filho A, Ferreira RCP, Luiz OJ, Mello TJ, Mendonça SA, Nunes DM, Pimentel CR, Pires AMA, Soares-Gomes A, Viana DL, Hazin FHV, Rocha LA. Fish biodiversity of Saint Peter and Saint Paul’s 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...
; Brown et al., 2019Brown J, Beard A, Clingham E, Fricke R, Henry L, Wirtz P. The fishes of St Helena Island, central Atlantic Ocean-new records and an annotated check-list. Zootaxa. 2019; 4543(2):151-94. http://dx.doi.org/10.11646/zootaxa.4543.2.1
http://dx.doi.org/10.11646/zootaxa.4543....
). This higher fish richness is probably related to FN being the largest and oldest island, situated relatively close to the continental shore, and being the most studied oceanic island in Brazil.

Even though we have also explored shallow ecosystems, this is the first systematic survey of the fish biodiversity of FN mesophotic ecosystems. Despite the logistical difficulties and risks associated with this type of exploration, our effort was rewarded as most of the new records (74%) came from the mesophotic ecosystems. In fact, we still know very little about mesophotic reefs in comparison to shallow ones, albeit they represent about 80% of the potential reef habitat worldwide (Pyle, Copus, 2019Pyle RL, Copus MJ. Mesophotic coral ecosystems: introduction and overview. In: Loya Y, Puglise KA, Bridge TCL, editors. Mesophotic coral ecosystems. Cham: Springer; 2019. p.3-27.). Although they have been considered potential refuges for shallow water organisms and less susceptible to human and natural impacts, mesophotic reefs are increasingly being recognized as unique ecosystems, home to largely distinct and independent communities that are also impacted and in need of protection as much as shallow reefs (Rocha et al., 2018Rocha LA, Pinheiro HT, Shepherd B, Papastamatiou YP, Luiz OJ, Pyle RL, Bongaerts P. Mesophotic coral ecosystems are threatened and ecologically distinct from shallow water reefs. Science. 2018; 361(6399):281-84. https://doi.org/10.1126/science.aaq1614
https://doi.org/10.1126/science.aaq1614...
; Pyle, Copus, 2019Pyle RL, Copus MJ. Mesophotic coral ecosystems: introduction and overview. In: Loya Y, Puglise KA, Bridge TCL, editors. Mesophotic coral ecosystems. Cham: Springer; 2019. p.3-27.). As reported elsewhere (Rocha et al., 2018Rocha LA, Pinheiro HT, Shepherd B, Papastamatiou YP, Luiz OJ, Pyle RL, Bongaerts P. Mesophotic coral ecosystems are threatened and ecologically distinct from shallow water reefs. Science. 2018; 361(6399):281-84. https://doi.org/10.1126/science.aaq1614
https://doi.org/10.1126/science.aaq1614...
), we found plastic trash and fishing debris (in 6% and 18% of the visual censuses, respectively) in mesophotic ecosystems explored around FN (Fig. 7), evidence of human impacts, which are even more noticeable in the intertidal and shallow ecosystems. Despite an island-wide ban on single use plastics (Pernambuco, 2018Pernambuco. Decreto Distrital no 002, de 12 de dezembro de 2018. Diário Oficial do Estado de Pernambuco, Poder Executivo, Recife, PE, 13 dez. 2018. Available at: http://www.noronha.pe.gov.br/instLegislacao.php?cat=3
http://www.noronha.pe.gov.br/instLegisla...
) and the presence of a program to eliminate plastic bags from the island, most of the goods that can be obtained in stores come wrapped in plastic.

FIGURE 7 |
Evidence of human impacts (arrows) by fishing debris, plastics and other trash found in the ecosystems explored around the Fernando de Noronha Archipelago. A.and B.Mesophotic (> 30 m deep); C. Intertidal; and D. Shallow ecosystems (≤ 30 m deep). Photos Aand B by L. A. Rocha and photos Cand D by J. L. Gasparini.

Several studies addressing the diversity, biology and ecology of the shallow water fish assemblages of FN have been carried out (e.g., Krajewski, Floeter, 2011Krajewski JP, Floeter SR. Reef fish community structure of the Fernando de Noronha Archipelago (Equatorial Western Atlantic): the influence of exposure and benthic composition. Environ Biol Fish. 2011; 92:25-40. https://doi.org/10.1007/s10641-011-9813-3
https://doi.org/10.1007/s10641-011-9813-...
; Ilarri et al., 2017Ilarri MI, Souza AT, Rosa RS. Community structure of reef fishes in shallow waters of the Fernando de Noronha archipelago: effects of different levels of environmental protection. Mar Freshwater Res. 2017; 68(7): 1303-316. https://doi.org/10.1071/MF16071
https://doi.org/10.1071/MF16071...
). However, even for the relatively well explored euphotic zone, we obtained new records such as Apogon pseudomaculatus Longley, 1932 and Pseudogramma gregoryi (Breder, 1927) (Tab. 1), reinforcing the need for further studies and a better understanding of the local cryptobenthic fish diversity. Currently, the cryptobenthic fishes represent only about 17% (~ 42 species) of the ichthyofauna of FN. Due to its small size and cryptic behaviour, most cryptobenthic fishes cannot be properly accessed by standard technics (e.g., underwater visual censuses and videos). Thus, in order to increase our knowledge of this hidden fish diversity, the scientific use of anaesthetics to collect specimens should be promoted (Collette et al., 2003Collette BB, Williams JT, Thacker CE, Smith ML. Shore fishes of Navassa Island, West Indies: a case study on the need for rotenone sampling in reef fish biodiversity studies. Aqua. 2003; 6(3):89-131.; Williams et al., 2010Williams JT, Carpenter KE, Van Tassell JL, Hoetjes P, Toller W, Etnoyer P, Smith M. Biodiversity assessment of the fishes of Saba Bank Atoll, Netherlands Antilles. PLoS One. 2010; 5(5):e10676. https://doi.org/10.1371/journal.pone.0010676
https://doi.org/10.1371/journal.pone.001...
). The importance of these underestimated assemblages of cryptobenthic fishes goes far beyond diversity. In a recent study, Brandl et al. (2019)Brandl SJ, Tornabene L, Goatley CH, Casey JM, Morais RA, Côté IM, Baldwin CC, Parravicini V, Schiettekatte NMD, Bellwood DR. Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning. Science. 2019; 364(6446):1189-92. https://doi.org/10.1126/science.aav3384
https://doi.org/10.1126/science.aav3384...
showed that through their extraordinary larval dynamics, rapid growth, and extreme mortality, the hyperdiverse assemblages of abundant, small, and short-lived cryptobenthic species appear to be a critical functional group on the trophodynamics of coral reefs.

Regarding the species registered in the mesophotic ecosystems, we emphasize that this is only the second record of the genus Tosanoides for the Atlantic Ocean, with a new species previously recorded on mesophotic reefs of St. Paul’s Archipelago (Pinheiro et al., 2018bPinheiro HT, Rocha C, Rocha LA. Tosanoides aphrodite, a new species from mesophotic coral ecosystems of St. Paul’s Rocks, Mid Atlantic Ridge (Perciformes, Serranidae, Anthiadinae). ZooKeys. 2018b; 786:105-115. https://doi.org/10.3897/zookeys.786.27382
https://doi.org/10.3897/zookeys.786.2738...
). The present record corroborates the hypothesis that this genus is probably widely distributed in peripheral Atlantic sites (Pinheiro et al., 2018bPinheiro HT, Rocha C, Rocha LA. Tosanoides aphrodite, a new species from mesophotic coral ecosystems of St. Paul’s Rocks, Mid Atlantic Ridge (Perciformes, Serranidae, Anthiadinae). ZooKeys. 2018b; 786:105-115. https://doi.org/10.3897/zookeys.786.27382
https://doi.org/10.3897/zookeys.786.2738...
). Differences in colour pattern suggest Tosanoides sp. from FN might be a new species, different from Tosanoides aphrodite Pinheiro, Rocha & Rocha, 2018, and genetic analyses are being carried out to confirm the species identity. Similarly, Aulotrachichthys argyrophanus (Woods, 1961) was previously known only from the type locality in the Southwest Atlantic, on the continental shelf slope off the Amazon River mouth, northern Brazil (Froese, Pauly, 2019Froese R, Pauly D. FishBase. World Wide Web electronic publication. Version (12/2019). 2019. Available from: https://www.fishbase.org
https://www.fishbase.org...
; Moore, 2019Moore J. Aulotrachichthys argyrophanus. The IUCN Red List of Threatened Species 2019: e.T20662062A20682663. https://dx.doi.org/10.2305/IUCN.UK.2019-2.RLTS.T20662062A20682663.en. Downloaded on 06 March 2020.
https://dx.doi.org/10.2305/IUCN.UK.2019-...
). Finally, Cosmocampus profundus (Herald, 1965) is for the first time recorded in Brazil, previously known to occur only from eastern Florida to south Caribbean (Robertson, Van Tassell, 2019Robertson DR, Van Tassell J. Shorefishes of the Greater Caribbean: online information system. Version 2.0. Balboa: Smithsonian Tropical Research Institute; 2019. Available from: https://biogeodb.stri.si.edu/caribbean/en/pages
https://biogeodb.stri.si.edu/caribbean/e...
).

Another curious new record is the common B. capriscus, an amphi-Atlantic species widespread in the Atlantic Ocean (Liu et al., 2015Liu J, Zapfe G, Shao K-T, Leis JL, Matsuura K, Hardy G, Liu M, Tyler J. Balistes capriscus. The IUCN Red List of Threatened Species 2015: e.T193736A97662794. (errata version published in 2016). Downloaded on 06 March 2020.; Froese, Pauly, 2019Froese R, Pauly D. FishBase. World Wide Web electronic publication. Version (12/2019). 2019. Available from: https://www.fishbase.org
https://www.fishbase.org...
), which is also present at Trindade Island (Miranda Ribeiro, 1919Miranda Ribeiro A. A fauna vertebrada da Ilha da Trindade. Arch Mus Nac (Rio de J). 1919; 22:171-194) and St. Paul’s Archipelago (Pinheiro et al., 2020Pinheiro HT, Macena BCL, Francini-Filho RB, Ferreira CEL, Albuquerque FV, Bezerra NPA, Carvalho-Filho A, Ferreira RCP, Luiz OJ, Mello TJ, Mendonça SA, Nunes DM, Pimentel CR, Pires AMA, Soares-Gomes A, Viana DL, Hazin FHV, Rocha LA. Fish biodiversity of Saint Peter and Saint Paul’s 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...
). At FN and St. Paul’s Archipelago, the species has been observed several times in groups of up to four individuals. In contrast, the only record of this species on Trindade Island dates from 1916, when one individual was collected during a scientific expedition by the National Museum of Rio de Janeiro (Miranda-Ribeiro, 1919Miranda Ribeiro A. A fauna vertebrada da Ilha da Trindade. Arch Mus Nac (Rio de J). 1919; 22:171-194). All recent extensive samplings around Trindade, in both euphotic and mesophotic ecosystems, including the use of technical dive (Pereira-Filho et al., 2011Pereira-Filho GH, Amado-Filho GM, Guimarães SMPB, Moura RL, Sumida PYG, Abrantes DP, Bahia RG, Güth AZ, Jorge RR, Francini Filho RB. Reef fish and benthic assemblages of the Trindade and Martin Vaz Island group, southwestern Atlantic. Braz J Oceanogr. 2011; 59(3):201-12. https://doi.org/10.1590/S1679-87592011000300001
https://doi.org/10.1590/S1679-8759201100...
) and BRUVS (Pimentel et al., 2020Pimentel CR, Andrades R, Ferreira CEL, Gadig OBF, Harvey ES, Joyeux J-C, Giarrizzo T. 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...
), yielded no record for this species. New records of common and large fishes such as B. capriscus may result from the attractiveness of the BRUVS bait and sampling in the mesophotic ecosystems, however this does not appear to be the case here. Alternatively, this could represent a recent colonization and successful establishment in these oceanic islands (e.g., Mazzei et al., 2019Mazzei EF, Pinheiro HT, Morais RA, Floeter SR, Veras DP, Queiroz LV, Joyeux J-C, Ferreira CEL. Parrotfishes of the genus Scarus in southwestern Atlantic oceanic reef environments: occasional pulse or initial colonization?. Mar Biodivers. 2019; 49:555-61. https://doi.org/10.1007/s12526-017-0827-8
https://doi.org/10.1007/s12526-017-0827-...
). These observations involving colonization, establishment and extinction are in accordance with the Theory of Island Biogeography (e.g., Pinheiro et al., 2017Pinheiro HT, Bernardi G, Simon T, Joyeux J-C, Macieira RM, Gasparini JL, Rocha C, Rocha LA. Island biogeography of marine organisms. Nature. 2017; 549:82-85. https://doi.org/10.1038/nature23680
https://doi.org/10.1038/nature23680...
), representing the main drivers balancing island diversity.

Other probable new species include Psilotris sp., Scorpaena sp. and Synodus sp., which have been only photographed. The goby resembles a Psilotris species (Luke Tornabene, 2020, pers. comm.), both in colour/appearance and in meristics: VII, 10 dorsal fin spines, with no visible scales and split pelvic fins. Psilotris sp. is closest in appearance to Psilotris kaufmani Greenfield, Findley & Johnson, 1993, but differs from it in having a unique body coloration, and not having a dark upper pectoral fin. The scorpaenid seems to belong to the genus Scorpaena (Alfredo Carvalho-Filho, 2020, pers. comm.) because the specimen has several pectoral fin rays well branched, especially the lower ones, whereas species of Pontinus have all rays unbranched. This Scorpaena sp. is different from the undescribed St. Paul’s Archipelago species (Feitoza et al., 2003; CIUFES 0349), which has a snout larger than the eye. The synodontid is different from all other species occurring in Brazil (Alfredo Carvalho-Filho, 2020, pers. comm.). It differs from Synodus synodus (Linnaeus, 1758) in not having a characteristic black spot at the tip of the snout; from Synodus intermedius (Spix & Agassiz, 1829) and Synodus macrostigmus Frable, Luther & Baldwin, 2013 in not having a dark spot at upper right corner of the operculum; and from Synodus poeyi Jordan, 1887 in overall coloration, the latter being bluish. Therefore, these three species are likely undescribed. Considering that four possible new species were disclosed in two hours of exploration of the lower mesophotic ecosystems (four divers with an average of 30 min each), the discovery rate herein reported is of two new species per hour, which is consistent with recent findings in other unexplored mesophotic ecosystems of the world (Pinheiro et al., 2019Pinheiro HT, Shepherd B, Castillo C, Abesamis RA, Copus JM, Pyle RL, Greene BD, Coleman RR, Whitton RK, Thillainath E, Bucol AA, Birt M, Catania D, Bell MV, Rocha LA. Deep reef fishes in the world’s epicenter of marine biodiversity. Coral Reefs. 2019; 38:985-95. https://doi.org/10.1007/s00338-019-01825-5
https://doi.org/10.1007/s00338-019-01825...
; Pyle et al., 2019Pyle RL, Kosaki RK, Pinheiro HT, Rocha LA, Whitton RK, Copus JM. Fishes: biodiversity. In: Loya Y, Puglise KA, Bridge TCL, editors. Mesophotic coral ecosystems. Cham: Springer; 2019. p.749-77.).

Here we have shown that the mesophotic ecosystems and the shallow cryptobenthic ichthyofauna need to be better studied, even in well-studied oceanic islands such as FN. We emphasize the need for protection of the mesophotic ecosystems of FN, looking for ways to conciliate activities such as fishing and tourism, with the preservation of the unique biodiversity and ecosystems found at mesophotic depths. As with shallow reefs, significant progress in the conservation of mesophotic ecosystems of FN could be reached by expanding the no-take zone of the Marine National Park beyond the 50 m isobath, or by creating some fishing exclusion zones inside the sustainable use MPA (Araújo, Bernard, 2016Araújo JL, Bernard E. Management effectiveness of a large marine protected area in Northeastern Brazil. Ocean Coast Manag. 2016; 130: 43-49. https://doi.org/10.1016/j.ocecoaman.2016.05.009
https://doi.org/10.1016/j.ocecoaman.2016...
).

ACKNOWLEDGEMENTS

We are grateful to NGO Voz da Natureza for supporting the project, and to Fundação Grupo Boticário de Proteção à Natureza and Hope for Reefs initiative (California Academy of Sciences) for funding. This work was partially supported by the Brazilian LTER Coastal Habitats of Espírito Santo (PELD-HCES; CNPq/FAPES grant #441243/2016-9) and by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. Caio R. Pimentel also thanks the Fundação Estadual de Amparo à Pesquisa do Estado do Espírito Santo (FAPES) for the PhD scholarship. Tommaso Giarrizzo received a productivity grant from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq #311078/2019-2). We would like to thank our great friend Mauricio Vilella and the staff at his Pizzaria Namoita for all their care during our stay in Noronha. We are very grateful to Patrick Muller, Ismael Escote and the great team of Atlantis Divers for all logistical and technical diving support. We also thank Raphael M. Macieira for helping with the fieldwork; Mauritius V. Bell and Allison Shafer for technical diving support; Zaira Matheus for sharing photos and deep dive sites; Kathiani V. Bastos (CIUFES) and Cristina Castillo for help with logistics; José Carlos Marenga, Alexandre Carvalho and the crew of the vessel Capitania I; the whole Marine National Park team for their support; Gabriel Cardozo-Ferreira, Alfredo Carvalho-Filho and Luke Tornabene kindly helped us identify several species. Fee waivers, administrative and environmental authorizations were provided by the Administration of Fernando de Noronha (ATDEFN), the Brazilian Environmental Agency (ICMBio, license #64991-3), Universidade Federal do Espírito Santo (PRPPG and Reitoria) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). Fish collections followed the California Academy of Sciences Institutional Animal Care and Use Committee (IACUC) policies and procedures.

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ADDITIONAL NOTES

  • HOW TO CITE THIS ARTICLE

    Pimentel CR, Rocha LA, Shepherd B, Phelps T, Joyeux J-C, Martins AS, Stein CE, Teixeira JB, Gasparini JL, Reis-Filho JA, Garla RC, Francini-Filho RB, Delfino SDT, Mello TJ, Giarrizzo T, Pinheiro HT. Mesophotic ecosystems at Fernando de Noronha Archipelago, Brazil (South-western Atlantic), reveal unique ichthyofauna and need for conservation. Neotrop Ichthyol. 2020; 18(4):e200050. https://doi.org/10.1590/1982-0224-2020-0050

Publication Dates

  • Publication in this collection
    14 Dec 2020
  • Date of issue
    2020

History

  • Received
    16 June 2020
  • Accepted
    30 Oct 2020
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