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Mesophotic Ecosystems at Fernando De Noronha Archipelago, Brazil (South- Western Atlantic), Reveal Unique Ichthyofauna and Need for Conservation

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Mesophotic Ecosystems at Fernando De Noronha Archipelago, Brazil (South- Western Atlantic), Reveal Unique Ichthyofauna and Need for Conservation Neotropical Ichthyology Original article https://doi.org/10.1590/1982-0224-2020-0050 Mesophotic ecosystems at Fernando de Noronha Archipelago, Brazil (South- western Atlantic), reveal unique ichthyofauna and need for conservation Caio R. Pimentel1,2, Luiz A. Rocha2, Bart Shepherd2, Tyler A. Y. Phelps2, Jean-Christophe Joyeux1, Agnaldo S. Martins1, Carlos Eduardo Stein3, João B. Teixeira1,3, João Luiz Gasparini1,4, José Amorim Reis-Filho5, Correspondence: Ricardo C. Garla6, Ronaldo B. Francini-Filho7, Stephanie D. T. Delfino1, Caio R. Pimentel 8 9 2,3 [email protected] Thayná J. Mello , Tommaso Giarrizzo and Hudson T. Pinheiro 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 Submitted June 16, 2020 77 families. These new records include four potential new species and highlight Accepted October 30, 2020 the importance of surveying mesophotic ecosystems, even in well studied sites. by Fernando Gibran Our results also emphasize the need for protection and attention to the unique Epub December 14, 2020 ichthyofauna found at mesophotic depths. Keywords: BRUVS, Marine Protected Area, Oceanic Island, Rebreather, Remotely Operated Vehicle. 1 Programa de Pós-Graduação em Oceanografia Ambiental, Dep. de Oceanografia e Ecologia, Univ. Federal do Espírito Santo, Av. Fernando Ferrari, 514, Goiabeiras, 29075-910 Vitória, ES, Brazil. (CRP) [email protected], (JCJ) [email protected], (ASM) [email protected], (JBT) [email protected], (JLG) [email protected], (SDTD) [email protected]. 2 California Academy of Sciences, 94118 San Francisco, CA, USA. (LAR) [email protected], (BS) bshepherd@calacademy. org, (TP) [email protected], San Francisco State University, 94132 San Francisco, CA, USA, (HTP) [email protected]. 3 Associação Ambiental Voz da Natureza, Rua Coronel Shuwab Filho, 104, 29052-070 Vitória, ES, Brazil. (CES) [email protected]. 4 Programa de Pós-Graduação em Ciências Ambientais e Conservação, Instituto de Biodiversidade e Sustentabilidade, Univ. Federal do Rio de Janeiro, 29910-970 Macaé, RJ, Brazil. 5 ICHTUS Soluções em Meio Ambiente, R. Dep. Herculano Menezes, 10, 41335-400 Salvador, BA, Brazil. (JARF) [email protected]. Online version ISSN 1982-0224 6 Departamento de Botânica e Zoologia, Univ. Federal do Rio Grande do Norte, 59078-970 Natal, RN, Brazil. (RCG) [email protected]. Print version ISSN 1679-6225 7 Centro de Biologia Marinha, Univ. de São Paulo, 11612-109 São Sebastião, SP, Brazil. (RBFF) [email protected]. 8 Programa de Pós-Graduação em Ecologia, Centro de Biociências, Universidade Federal do Rio Grande do Norte, 59072-970 Natal, RN, Brazil (TJM) [email protected]. Neotrop. Ichthyol. 9 Núcleo de Ecologia Aquática e Pesca da Amazônia, Univ. Federal do Pará, Av. Perimetral, 2651, Terra Firme, 66040-170 Belém, vol. 18, no. 4, Maringá 2020 PA, Brazil. (TG) [email protected]. Neotropical Ichthyology, 18(4): e200050, 2020 1/17 Mesophotic ecosystems at Fernando de Noronha 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. Palavras-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., 2005; Macieira et al., 2015; Kosaki et al., 2017; Pinheiro et al., 2018a). These environments function as true natural laboratories for evolutionary and ecological studies (Pinheiro et al., 2017) and are important for understanding patterns of species dispersal and establishment (Losos, Ricklefs, 2009). 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., 2013; Macieira et al., 2015; Carvalho-Filho et al., 2016; Pinheiro et al., 2018a). 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., 2012; Wirtz et al., 2017; Hachich et al., 2015; Pinheiro et al., 2015, 2018a; Quimbayo et al., 2019). However, mesophotic ecosystems (between 31 – 150 m depth) remain largely unknown and are only now receiving some scientific attention (e.g., Rocha et al., 2018). Even though these ecosystems have been recognized since the 19th century (Sinniger et al., 2016), the first studies in Brazil date back only to the 1960s (Francini-Filho et al., 2019). Systematic studies of the mesophotic ecosystems have however increased worldwide (e.g., Rosa et al., 2015; Andradi-Brown et al., 2016; Pyle et al., 2016; Simon et al., 2016; Rocha et al., 2018; Pinheiro et al., 2019; Pimentel et al., 2020). 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 2/17 Neotropical Ichthyology, 18(4): e200050, 2020 ni.bio.br | scielo.br/ni Caio R. Pimentel, Luiz A. Rocha, Bart Shepherd, Tyler A. Y. Phelps, Jean-Christophe Joyeux, Agnaldo S. Martins, Carlos Eduardo Stein et al. 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., 2018; Rodríguez-Rey et al., 2018) and shallow (≤ 20 m deep) environments (e.g., Krajewski, Floeter, 2011; Medeiros et al., 2011; Ilarri et al., 2017; Smith-Vaniz et al., 2018; but see Garla et al., 2006; Sazima et al., 2010; Afonso et al., 2017). 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, 2006). 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, 2011). Following the pattern of low diversity typical of Atlantic oceanic islands (Ferreira et al., 2004; Floeter et al., 2008), the fish assemblages are dominated by a few very abundant species (Krajewski, Floeter, 2011; Ilarri et al., 2017). 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., 2019). 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,
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