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Anurans from the Mountain Chain Serra Do Mar: a Critical Area for Amphibian Conservation in the Atlantic Forest, Brazil

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Anurans from the Mountain Chain Serra Do Mar: a Critical Area for Amphibian Conservation in the Atlantic Forest, Brazil Herpetology Notes, volume 10: 547-560 (2017) (published online on 16 October 2017) Anurans from the mountain chain Serra do Mar: a critical area for amphibian conservation in the Atlantic Forest, Brazil Felipe Siqueira Campos1, 2,* and Ricardo Lourenço-de-Moraes3 Abstract. We present an anuran inventory of the mountain region of the Serra do Mar, Brazil, located in the Atlantic Forest biome. We conducted a fieldwork comprising the major and best well-preserved Atlantic Forest remnants from Brazil, using acoustic and visual nocturnal/diurnal assessments. In total, we recorded 99 anuran species, of which about 70% are endemic to the Atlantic Forest and represent around 20% of all amphibian species described for this biome. The high levels of endemism, the distribution patters and the conservation status of the anuran species turn the mountains of the Serra do Mar into a key conservation region for amphibians within the Atlantic Forest hotspot. Keywords. Amphibia, Atlantic Forest, species inventory, species distribution, conservation. Introduction recognized amphibian species and several more species that still need to be described (Silva and Casteleti, 2003; The Atlantic Forest biome represents one of the Haddad et al., 2013). five most important biodiversity hotspots on Earth The Serra do Mar is a mountain chain that extends (Mittermeier et al., 2011). Originally, it covered around for more than 1,000 km (Almeida and Carneiro, 1998), 1,500,000 km2 of which only about 12% (194,524 km2) stretching from the south of the Espírito Santo state remains in Brazil, Paraguay and Argentina (Ribeiro to the North of the Rio Grande do Sul state (Rizzini, et al., 2009), corresponding to about 100,000 km2 of 1979; Olson et al., 2001). This is an area of extreme Brazilian forest remnants (Tabarelli et al., 2005). This biological importance that covers 8% of the Atlantic biome faces high rate of habitat loss (Teixeira et al., Forest biome and accounts more than 13% of the 2009), which is one of the main causes of amphibian remaining forest (Ribeiro et al., 2009). The Brazilian extinctions (Stuart et al., 2004; Becker et al., 2007; Ministry of the Environment has rated this region with Ferreira et al., 2016). Despite this, Atlantic Forest is the highest priority towards conservation within the still considered the leader biome in amphibian diversity Atlantic Forest hotspot (MMA, 2000). According to in Brazil (Haddad et al., 2013), accounting for more the biogeographical sub-regions proposed by Silva and than 50% of all amphibian species (Haddad et al., Casteleti (2003), Serra do Mar covers the best well- 2013). Their geographical characteristics with wide preserved remnants, which holds 36.5% of its original altitudinal range have favoured high species richness vegetation (Ribeiro et al., 2009). This region has been and high levels of endemism, including more than 500 highly fragmented, with 79% of the remaining forests smaller than 0.5 km2. However, part of the biome still covers wide forest remnants, with fragments larger than 1,000 km2 along the coastal mountains of São Paulo 1 Departament de Biologia Evolutiva, Ecologia i Ciències state, larger than 500 km2 in the Paraná state, and larger Ambientals, Facultat de Biologia, Universitat de Barcelona, than 300 km2 in the Santa Catarina state (Ribeiro et al., ES-08028, Barcelona, Spain. 2009). On the altitudinal gradient, Serra do Mar also 2 CAPES Foundation, Ministry of Education of Brazil, 70040- has continuous forests ranging from the sea level up to 020, Brasília, DF, Brazil. 2,300 m (Almeida and Carneiro, 1998). 3 Departamento de Ecologia, Laboratório de Herpetologia e Comportamento Animal, Universidade Federal de Goiás, A key factor accounting for amphibian species richness 74001-970, Goiânia, GO, Brazil. in the Atlantic Forest is the large number of habitats * Corresponding author e-mail: [email protected] and microhabitats (Haddad, 1998), which favours the 548 Felipe Siqueira Campos & Ricardo Lourenço-de-Moraes characterized by monthly mean temperatures of at least 18 °C and high annual rainfall averages (> 2,000 mm; Walsh, 1996). Vegetation types comprise tree mosaics with different shifts in floristic composition as elevation increases and are classified as montane and sub-montane rain forest composed of moist broadleaf trees (Rizzini, 1979; Olson et al., 2001). We sampled each Protected Area for 10 days between January and March 2015 (wet season) from 5 pm to 1 am, totalling 480 hours of sampling effort per person (i.e., two researchers). In all localities, we used acoustic and visual nocturnal/diurnal assessments at different microhabitats along a 2,000 m forest transect in each sampled site (e.g., streams, swamps, bromeliads, bamboos, burrows, rocks, vegetation, and leaf-litter). Figure 1. Map of the sampled sites in the mountain chain Serra do Mar, Brazil, representing their corresponded forest We focused the study in an altitudinal range lower than remnants and altitude at a spatial resolution of 0.1 latitude/ 300 m and higher than 700 m above sea level (asl). We longitude degrees. 1. Parque Ecológico Spitzkopf, SC; 2. identified the species by comparing their morphological Parque Estadual Pico do Marumbi, PR; 3. Estação Ecológica characteristics observed in the field and reviewing de Juréia-Itatins, SP; 4. Parque Estadual da Serra do Mar their original or revalidated descriptions to support the Núcleo Caraguatatuba, SP; 5. Parque Nacional da Serra dos taxonomic identifications. We followed Frost (2017) for Órgãos, RJ; 6. Reserva Biológica Augusto Ruschi, ES. the amphibian nomenclature. Results and Discussion In the six Protected Areas surveyed in the mountain number of habitat-specialist species (Lourenço-de- chain Serra do Mar, we found 99 anuran species Moraes et al., 2013). In addition, there is a high degree distributed in 13 families and 31 genera (Table 1, Figs. of isolation among populations, due to the rugged 3–8). About 70% of the sampled species are endemic relief with rivers and mountains that may represent to the Brazilian Atlantic Forest and represents around biogeographic barriers (Haddad, 1998; Marques et al., 20% of all amphibian species described for this biome. 1998). We found the highest species richness in the “Parque Species inventories are crucial for answering central Estadual da Serra do Mar Núcleo Caraguatatuba” questions in biogeography (Lomolino, 2004), ecology (34 species) and the lowest in the “Parque Ecológico (Brown et al., 1996) and evolutionary biology (Holt, Spitzkopf” (23 species). We found approximately 2003). Additionally, species lists are critical to indicate twice the number of species in lowland areas (<300 knowledge gaps, as well as to identify priority areas m asl.) than highland areas (>700 m asl.), of which for conservation (e.g., Toledo and Batista, 2012; 60 species occurred exclusively below 300 m, 22 Verdade et al., 2012; Campos et al., 2014). In this species exclusively above 700 m, and 17 species in context, we carried out fieldwork comprising the major both altitudinal ranges (Table 1). Among the different forest remnants of the mountain chain Serra do Mar, microhabitats searched, we observed 36% of the species supplementing the current amphibian dataset for this in swamps, 18% in streams, 17% in leaf-litter, 15% in region and highlighting the importance of these forests trees, 8% in bromeliads, 3% in rocks, 2% burrows, and for the species conservation status. 1% in bamboos. In this study, we presented the first anuran species Material and Methods list for the Parque Ecológico Spitzkopf, in the Santa We conducted fieldwork at six Protected Areas located Catarina state, and the Parque Estadual da Serra do in the mountain chain Serra do Mar, Brazil (Figs. 1 Mar Núcleo Caraguatatuba, in the São Paulo state. Our and 2). The general climate of this region is tropical results showed four new species distribution records for wet with frequent rain occurring every month (Walsh, the studied region, expanding the knowledge about the 1996). This non-seasonal tropical rain forest climate is occurrence of anurans in the mountain chain Serra do Anurans from the mountain chain Serra do Mar, Brazil 549 Figure 2. Some environments of the sampled sites in the mountain chain Serra do Mar, Brazil. A) Rocky stream in the Parque Ecológico Spitzkopf, SC; B) Mountain chain in the Parque Estadual Pico do Marumbi, PR; C) Forest fragment in the Estação Ecológica de Juréia-Itatins, SP; D) Forest bromeliads in the Parque Estadual da Serra do Mar Núcleo Caraguatatuba, SP; E) Mountain chain in the Parque Nacional da Serra dos Órgãos, RJ; F) Dense ombrophylous forest in the Reserva Biológica Augusto Ruschi, ES. Mar. We reported the first state records for Ischnocnema (IUCN, 2017). We found only one species classified as erythromera in the Espírito Santo state, Rhinella henseli Vulnerable (VU), three as Near Threatened (NT), and and Adenomera nana in the Paraná state, and Hylodes four as Data Deficient (DD). In this context, several pipilans in the São Paulo state. studies have highlighted that the lack of information Table 1 shows the conservation status of the recorded regarding amphibian species occurrence needs to species according to the IUCN red list categories be straightaway addressed by scientific researchers, 550 Felipe Siqueira Campos & Ricardo Lourenço-de-Moraes Figure 3. Some amphibian species sampled in the mountain chain Serra do Mar, Brazil. A) Adenomera bokermanni; B) Aplastodiscus albosignatus; C) Aplastodiscus arildae; D) Aplastodiscus ehrhardti; E) Bokermannohyla caramaschii; F) Bokermannohyla circumdata; G) Bokermannohyla hylax; H) Brachycephalus ephippium. Anurans from the mountain chain Serra do Mar, Brazil 551 Figure 4. Some amphibian species sampled in the mountain chain Serra do Mar, Brazil. A) Cycloramphus acangatan; B) Cycloramphus brasiliensis; C) Dendropsophus branneri; D) Dendropsophus microps; E) Euparkerella cochranae; F) Gastrotheca albolineata; G) Haddadus binotatus; H) Crossodactylus gaudichaudii. 552 Felipe Siqueira Campos & Ricardo Lourenço-de-Moraes Figure 5. Some amphibian species sampled in the mountain chain Serra do Mar, Brazil.
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