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

Augusto A. Machado^1,2, Fernando C. de Moraes², Aline A. Aguiar², Mauricio Hostim-Silva¹, Luciano N. Santos^3,4, and Áthila A. Bertoncini^2,4,5

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Abstract​

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Introduction​

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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 assemblages 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 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 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

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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., 2007; Moraes et al., 2013; Monteiro-Neto et al., 2013; Aguiar et al., 2015; Amorim, Monteiro-Neto, 2016; Garcia et al., 2018; Bertoncini et al., 2019; Araujo et al., 2020; Hauser-Davis et al., 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), 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) 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), Humann, Deloach (2014), Hostim-Silva et al. (2005), Bertoncini et al. (2019), and consultancy to experts. The families were ordered according to Dornburg, Near (2021) 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).

Results​

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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., 2021), Zapteryx brevirostris (Müller & Henle, 1841) under Trygonorrhinidae (Last et al., 2016), Acanthistius brasilianus (Cuvier, 1828) under Anthiadidae (Dornburg, Near, 2021; Anderson, 2018); and genus, i.e., from Equetus (lanceolatus) (Linnaeus, 1758) to Eques Bloch, 1793 (Parenti, 2020); and from Chromis (multilineata) (Guichenot, 1853) to Azurina Jordan & McGregor, 1898 (Tang et al., 2021).

TABLE 1 | Fish species observed in Coastal Islands of Rio de Janeiro arranged according to Dornburg, Near (2021). 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., 2007*¹, Moraes et al., 2013*², Monteiro-Neto et al., 2013*³, Amorim, Monteiro-Neto, 2016*⁴, Garcia et al., 2018*⁵, Bertoncini et al., 2019*⁶, Araujo et al., 2020*⁷, Hauser-Davis et al., 2021*⁸.