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

Coastal islands of


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, 2009;Laport et al., 2016;Riofrío-Lazo et al., 2022). Despite all their importance, many forms of life that inhabit rocky shore ecosystems are critically endangered by human actions (Benedetti-Cecchi et al., 2001;Pereira, Soares-Gomes, 2009;Mendez et al., 2019). Coastal development, urbanization and overfishing are amongst the main activities that exert pressure on coastal marine ecosystems (Elliott, 2014;Alves et al., 2019;Figueroa-Pico et al., 2021), 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., 2009;Miller, Russ, 2014), especially minimizing impacts on fish a ssemblages and improving/preserving the essential habitats on which species depend (Gaines et al., 2010;Sciberras et al., 2015).
As reef environments, reef fishes are important components of tropical marine communities, serving as food and income source for millions of people (Munro, 1996;Pauly et al., 2002;Nelson et al., 2016). In Brazil, reef fish communities are distributed along the coast, from off the mouth of the Amazon River, and the Manuel Luiz 3/29 ni.bio.br | scielo.br/ni Augusto A. Machado, Fernando C. de Moraes, Aline A. Aguiar, Mauricio Hostim-Silva, Luciano N. Santos and Áthila A. Bertoncini reefs (Northern Brazil) to coastal regions of Santa Catarina State in Southern Brazil (Rocha, Rosa, 2001;Hostim-Silva et al., 2005;Moura et al., 2016), including oceanic islands (Quimbayo et al., 2019;Pinheiro et al., 2020). 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., 2019). 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., 1997;Bax et al., 2003). 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., 2004;Souza et al., 2018). 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., 2013;Bertoncini et al., 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., 2008;Guabiroba et al., 2020;Pereira et al., 2021). Non-destructive techniques have been widely employed in marine ecosystems, especially in MPAs (Andradi-Brown et al., 2016;Bayley et al., 2019;Quaas et al., 2019, Schmid et al., 2020. The Underwater Visual Census (UVC) is frequently used in ecological studies of reef fish communities (Chaves, Monteiro-Neto, 2009;Daros et al., 2018;Motta et al., 2021;Pereira et al., 2021), allowing the identification of species and the monitoring of the behavior of organisms that especially, are not affected by the presence of divers (Sale, 1997;Beck et al., 2014). 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, 2014;Koenig, Stallings, 2015;Pimentel et al., 2020;Pinheiro et al., 2020;Rolim et al., 2022). 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 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, 2018;IUCN, 2020). 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, 2020) and maps were elaborated through QGIS 3.16 (QGIS Development Team, 2022).            was observed in Redonda Island at 8 meters deep. A single individual was sighted at a sampling video ( Fig. 8A and in the video S1) 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, 1995;Adelir-Alves et al., 2018;Froese, Pauly, 2022). 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, 2018) 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.

RESULTS
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).
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   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), 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., 2013, Bertoncini et al., 2019. Marine coastal areas are known as important habitats for fish communities (Kume et al., 2021), 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., 2012), 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., 2013;Bertoncini et al., 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., 2007;Melià et al., 2020). Previous studies have indicated that MPAs are appropriate places for, in addition to preserving biodiversity, recovering exploited stocks (Roberts et al., 2001;Halpern, 2003), 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., 2018 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, 2000), while in 2013 it was recorded at Laje de Santos, São Paulo State (Luiz et al., 2014), and in 2017 it was sighted in a shipwreck in South Brazil (Paraná) (Adelir-Alves et al., 2018). According to Luiz et al. (2014) 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., 2009;Anderson et al., 2017), and the Toadfish, Opsanus beta (Goode & Bean, 1880), both established in some Brazilian estuaries (Cordeiro et al., 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., 2021). 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., 2013;Samhouri, Stier, 2021). The introduction of nonnative species through human vectors is globally acknowledged to represent a major threat to biodiversity and ecosystem health (Sutherland et al., 2010), and, according to IOC-UNESCO (2022) 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.
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, 2020). 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.