Herpetofauna in a Secondary Atlantic Forest Fragment in Itanhaém Municipality, Southeastern Brazil
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Herpetology Notes, volume 14: 995-1007 (2021) (published online on 28 July 2021) Herpetofauna in a secondary Atlantic Forest fragment in Itanhaém municipality, Southeastern Brazil Diego G. Cavalheri¹,*, Raissa M. S. Siqueira², Marcela Brasil-Godinho³, Renata M. Fadel4, Vivian Trevine5, Luciana P. Sartori², and Diego J. Santana4 Abstract. We present herpetological survey results from a low altitude secondary Atlantic Forest fragment in Itanhaém municipality, southeastern Brazil. Field expeditions were conducted over 21 months, at Estação Ambiental São Camilo. We recorded 22 species of amphibians and 18 species of reptiles using three different sampling methods, pitfall traps, visual encounter survey and occasional encounter. None of the observed species are listed in the São Paulo and Brazilian list of endangered species, or in the IUCN red list. This secondary-forest fragment harbours common species for Atlantic Forest, and the endemism rate for Amphibians is 81,8%, which means these “coldspots” are important to consider as an alternative for conservation in Atlantic Forest Domain. Keywords. Amphibians, Coastal São Paulo state, Conservation, Fauna, Reptiles, Species inventory Introduction how threatened species are (Cornell and Harrison, 2014; Guisan et al., 2017; Araújo et al., 2019). One of the greatest challenges in biodiversity Deforestation of tropical humid forests has caused conservation is to estimate how many species exist on unprecedented loss of biodiversity (Mace et al., Earth (Ødegaard, 2000). Species inventories are the first 2005), with protected areas being a fundamental tool step to assess local biodiversity and to assist in decision in preventing it. However, their coverage is limited making of environmental conservation and management (Rodrigues et al., 2004) and their integrity is threatened policies (Silveira et al., 2010). This knowledge helps to in areas with widespread deforestation (Pedlowski et al., understand community dynamics and to establish how 2005). Although the importance of secondary forests species are distributed in space and time (Rosenzweig, for conservation are still in debate, there is a consensus 1995; Lomolino et al., 2010). Therefore, it allows to regarding the lack of information about this type of area model habitat suitability and to clarify environmental (Thompson and Donnelly, 2018). Nowadays, since over gaps in large and small scales, which enables to evaluate half of the world’s forests are degraded (FAO, 2015), inventories of these areas are necessary to understand how species will be in future scenarios. The Atlantic Forest Domain (sensu Ab’Saber, 2003) is ¹ Instituto de Biociências, Letras e Ciências Exatas, a biodiversity hotspot with only 11.4–28% of remaining Universidade Estadual Paulista, 15054-000 São José do Rio Preto, São Paulo, Brazil. vegetation (Rezende et al., 2018; Ribeiro et al., 2009). ² Centro Universitário São Camilo, Av. Nazaré, 1501 - Ipiranga, This domain has a high longitudinal and an extensive 05025-010 São Paulo, São Paulo, Brazil. latitudinal range with great altitudinal variation, from ³ Universidade Federal do ABC, Centro de Ciências Naturais e sea level to 2800 meters elevation (Vasconcelos et al., Humanas - PPG em Evolução e Diversidade, 09606-070, São 2014). These features, associated with the topographical Bernardo do Campo, São Paulo, Brazil. complexity, could explain the high biodiversity and 4 Mapinguari - Laboratório de Biogeografia e Sistemática de endemism rates observed in its domain (Carnaval et Anfíbios e Répteis, Universidade Federal de Mato Grosso do Sul, Avenida Costa e Silva S/N - Pioneiros, 79002-970 al., 2009; Myers et al., 2000; Silva, 2017). The Atlantic Campo Grande, Mato Grosso do Sul, Brazil. Forest is under pressure by urban expansion, reforestation 5 Laboratório de Coleções Zoológicas, Instituto Butantan, Av. with exotic species, agriculture, and other exploratory Vital Brasil, 1500, 05503-900 São Paulo, São Paulo, Brazil. activities (Ribeiro et al., 2009). Such activities have led * Corresponding author. E-mail: [email protected] to habitat loss and fragmentation, leaving small islands © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. of native vegetation embedded in a poorly permeable 996 Diego G. Cavalheri et al. matrix (Ribeiro et al., 2009; Rodrigues et al., 2004). This makes species inventories an important tool to evaluate the conservation priorities in this domain. With 1188 species of amphibians (Segalla et al., 2021) and 796 species of reptiles described (Costa and Bérnils, 2018), Brazil is among the most biodiverse countries in the world. The Atlantic Forest has the biggest species richness and endemism rates of the country (Rossa- Feres et al., 2017; Tozetti et al., 2017), and new species of herpetofauna are continuously described (e.g., Magalhães et al., 2020; Mebert et al., 2020; Prates et al., 2020), as we are far from establishing an end of species inventories (Moura et al., 2018). Since there are regions, such as the low altitudes areas in the south Figure 1. Geographic localisation of the Estação Ambiental coastal of São Paulo, with a low number of inventories São Camilo (EASC). (A) Location of the São Paulo state (in (e.g. Marques and Sazima, 2004; Pombal Jr. and Gordo, black) in relation to South America. (B) Location of Itanhaém 2004; Campos and Lourenço-de-Moraes, 2017) lacunas municipality (in grey) in relation to the State of São Paulo and about biodiversity composition need to be filled. the EASC (black dot). (C) Sample points (white dots, as shown on Table 1) and the fragment where the work was conducted. Therefore, considering the lack of information in relation to secondary forest fragments and how the Atlantic Forest is threatened by deforestation, especially of African buffaloes - Syncerus caffercaffer); hotel on the coastal region of São Paulo state, we present here research structure, a regeneration area with exotic a herpetofauna inventory of Estação Ambiental São vegetation, Pinus sp. and Eucaliptus sp.; and an area of Camilo, a low altitude secondary fragment of Atlantic Submontane Atlantic Rainforest in regeneration for over Forest in the south coast of São Paulo state, southeastern 20 years (until the beginning of our fieldwork) reserved Brazil. for environmental education and research activities. Data sample. We conducted 40 field expeditions Material and Methods during 21 months, between October 2011 and June Study area. Extensive fieldwork was conducted at the 2013, regular sampling lasted two days per expedition Estação Ambiental São Camilo (EASC) (-24.14305º, for a total of 80 sampling days. During these expeditions, -46.76028º), a private reserve located in the Itanhaém three different sampling methods were employed: municipality, São Paulo State (Fig. 1). The EASC pitfall traps (PT), visual encounter surveys (VES), belongs to a fragment of ~1500 ha (altitude range 5– and occasional encounters (OE) (Crump and Scott-Jr, 290 m) of the Atlantic Forest Domain, characterised by 1994; Martins and Oliveira, 1998; Cechin and Martins, Flooded Restinga and Submontane Atlantic Rainforest 2000). The VES occurred during night and day, once transition, in proximity to the Serra do Mar mountain per expedition and always conducted by two people, range (Sartori and Vercellino, 2018). This area can be and in three different sampling points: one in the forest divided into three occupation categories: anthropic area and two adjacent to water bodies. The PT method use (pasture and swamp areas, used for the ranching consisted of three pitfall trap arrays, composed by three Table 1. Sampling points in the EASC, municipality of Itanhaém, state of São Paulo, Brazil. Sample method: VES. Visual encounter survey; PT. pitfall traps. See text and Figure 1 for details. Point Coordinates Sample Method Description 1 -24.1409°S, -46.7583°W PT/VES Pond in secondary forest 2 -24.1406°S, -46.7568°W PT/VES Perennial stream in secondary forest 3 -24.1399°S, -46.7568°W VES Pond in secondary forest 4 -24.1390°S, -46.7562°W PT Secondary forest Herpetofauna in a secondary Atlantic Forest fragment in Itanhaém municipality 997 stations with 15 buried buckets of 30 litres with a total Teiidae (n = 1), Colubridae (n = 3), Dipsadidae (n=4), of 45 buckets (Table 1). The buckets were checked Elapidae (n = 1) and Viperidae (n = 2) (Table 2). The every day and kept open for 30 hours per expedition. most common species was Bothrops jararaca (n = 11), Specimens recorded outside of the VES and PT efforts followed by Enyalius iheringii (n = 8) and Helicops were considered as OE: including individuals registered carinicaudus (n = 7). Some species had only one along the transect, between the sample points, and the specimen recorded, such as Hydromedusa tectifera, swamps closed to the building of the EASC. Leposternon microcephalum, Ophiodes sp., Placosoma Voucher specimens and tissues were housed in the glabellum, Chironius bicarinatus, and Micrurus Museu de Zoologia da Universidade de São Paulo corallinus. Among the 18 species of reptiles sampled in (MZUSP) (Appendix S1). Specimens were collected EASC, seven (38.8%) are endemic from Atlantic Forest according to permits granted by ICMBio (31557- Domain. 2). Nomenclature follows: Duellman et al. (2016) No registered species of amphibian or reptile is listed for Hylidae, and Frost (2021) for the other families in the São Paulo, nor on the Brazilian list of endangered of amphibians, and Uetz et al. (2020) for reptiles. To species, or is threatened according to the IUCN red determine the endemism of species in the Atlantic Forest, list. However, Proceratophrys pombali is listed as a we follow Rossa-Feres et al. (2017) for amphibians and Data Deficient species in the Brazilian list, due to its Tozetti et al. (2017) for reptiles. To determine the level restricted distribution and the lack of information about of threat, lists of global (IUCN, 2021), national (MMA, natural history (Haddad et al., 2016). 2018) and state (SMA, 2018) level of endangered The richness estimator Jackknife 1 recovered 25 species were used. species of amphibians suggesting three more than we Analysis. An individual-based dataset accumulation recorded.