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Anuran Community in a Neotropical Natural Ecotone

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Anuran Community in a Neotropical Natural Ecotone Herpetology Notes, volume 12: 1145-1156 (2019) (published online on 05 November 2019) Anuran community in a Neotropical natural ecotone Rodrigo Matavelli1,2,*, Aldenise Martins Campos1, Clarenice Loiola Santos1, and Gilda Vasconcellos de Andrade3 Abstract. Little attention has been given to natural ecotone areas around the world. However, natural ecotones play an important role in sustaining high species richness and a unique biodiversity that do not exist in the adjacent ecosystems. We present the first anuran fauna inventory in a natural ecotone between Cerrado and restinga in northeastern Maranhão State, Brazil. The survey was conducted at 24 sampling points in an area of 14,360 km2. We sampled anurans during the rainy season (January to July 2010) using the visual search (youth and adults) and acoustic search (male reproductive activity of vocalization) methods simultaneously to detect the presence of adult individuals. We recorded 50 anuran species belonging to 15 genera and five families. The anuran fauna showed high species richness, which may be explained by the fact that the study area is a natural biogeographic transition zone. Keywords. Amphibians, Conservation efforts, Inventory, Maranhão, Transition areas Introduction 2014; Johnson et al., 2017), mainly because the species’ two-phase life cycle makes them very sensitive to any Brazil has the largest anuran diversity in the world, with changes in both aquatic and terrestrial environments approximately 1,090 species (Frost, 2019; Segalla et al., (Stuart et al., 2008; Adeba et al., 2010). 2019). This great diversity is probably due to its large Most previous studies on anurans in Brazil evaluated territorial extent, and to a high geographical complexity their distribution patterns and species composition involving various natural biomes that comprise different in Cerrado (Giaretta et al., 2008; Valdujo et al., 2011; phytophysiognomies (IBGE, 1994; Olson et al., 2001) Moraes et al., 2012; Gambale et al., 2014) and restinga and natural ecotone areas. areas (Wachlevski and Rocha, 2010; Vilela et al., 2011; Despite this great diversity, several Brazilian anuran Telles et al., 2012; Gondim-Silva et al., 2016), but little populations have declined in recent decades (Eterovick attention has been paid to the world’s natural ecotone et al., 2005; Becker et al., 2007; Verdade et al., 2010) areas (Smith et al., 2001; Kark and van Rensburg, as a result of human activities that lead to degradation, 2006), including the Brazilian ones. fragmentation, and habitat loss. These processes are the Natural ecotones sustain high species richness and a primary causes of local extinctions and the global decline unique biodiversity. These areas play an important role in in anuran populations (Gibbs et al., 2005; Dirzo et al., maintaining a biodiversity that does not exist in adjacent ecosystems (Ruggiero and Ezcurra, 2003; Kark and van Rensburg, 2006; Kark, 2013; Kark, 2017), justifying a greater conservation effort than they currently receive (Smith et al., 2001; Kark, 2013). Maranhao State acts 1 Universidade Federal do Maranhão (UFMA), Programa de Pós-Graduação em Biodiversidade e Conservação. Avenida as a natural biogeographic transition zone between the dos Portugueses 1966, Campus do Bacanga, CEP: 65.080- Amazon, Caatinga and Cerrado biomes (IBGE, 1984; 805, São Luis, MA, Brasil. AbSaber, 1989; Rebêlo et al., 2010); thus its biodiversity 2 Universidade Estadual Paulista (UNESP), Departamento de needs to be further researched, better understood and, Ecologia, Laboratório de Ecologia Espacial e Conservação ultimately, preserved. (LEEC). Avenida 24A, nº 1515, CEP: 13.506-900, Rio Although there are some recently published lists of Claro, SP, Brasil. the anuran species in Maranhão State, encompassing 3 Universidade Federal do Maranhão (UFMA), Departamento de Biologia, Avenida dos Portugueses 1966, Campus do the Amazon biome (Freitas et al., 2017), Cerrado biome Bacanga, CEP: 65.080-805, São Luis, MA, Brasil. (Brasileiro et al., 2008; Andrade et al., 2017) and also * Corresponding author. E-mail: [email protected] some islands (Andrade et al., 2012; Andrade et al., 2016), 1146 Rodrigo Matavelli et al. no survey was conducted in natural ecotone areas in this The average annual rainfall is high, around 2,325 mm region. Despite the basic format of species compilations (CPTEC/INPE, 2010). lists, these lists can provide important information The Cerrado biome comprises about 65% of the for research, legislation and other activities related to vegetation cover in Maranhão (Sano et al., 2008) biodiversity management and conservation (Hamer et and occurs on a flat and smooth relief known locally al., 2012), especially in natural ecotone areas, which as “Chapada”, where Cerradão is the predominant sustain high species richness and a unique biodiversity physiognomy (IBGE, 1984). Cerrado is considered (Risser, 1995; Kark and van Rensburg, 2006; Kark et a biodiversity hotspot (Klink and Machado, 2005) al., 2007; Kark, 2017). because it presents a great heterogeneity in its plant The main purpose of this study was to reveal for the formations (Ratter et al., 1997), which include campestre first time the anuran community composition in a natural formations, savannahs and tropical forests (Ribeiro and ecotone between Cerrado and restinga in northeastern Walter, 2008). Maranhão State, Brazil. The restingas, a phytophysiognomy of the Atlantic Forest biome typical of the sandy coastal plains Material and Methods (IBGE, 1984; Araujo et al., 1998) - also considered a biodiversity hotspot (Myers, 2000) - presents a diverse Study area.—The study was carried out in nine phytophysiognomy ranging from coastal herbaceous to municipalities in northeastern Maranhão, covering an dense forests in sandy soils (Araujo and Lacerda, 1987). area of 14,360 km2 (Figure 1). In northeastern Maranhão, the restingas are composed The region’s climate is mesothermal and humid of species endemic to the biome itself and species that tropical with two well-defined seasons: a rainy season also occupy the Atlantic Forest, Caatinga and Cerrado (January to June), which receives about 94% of the biomes (Silva et al., 2009). annual rainfall, and the dry or drought season (July to Specifically, our sampling design consisted of 12 sites December), which receives only 6% of the precipitation. in Cerrado areas and 12 sites in restinga areas (Figure Figure 1. Study region encompassing 24 sampled points in a Neotropical natural ecotone between Cerrado and restinga in northeastern Maranhão State, Brazil. Triangles: Cerrado areas; Circles: restinga areas. Anuran community in a Neotropical natural ecotone 1147 1) distributed in lentic and/or temporary environments increased. In addition, seven (14%) were classified as (two small floodplain and eight ponds) and in lotic/ “data unknown”, and five (10%) as “no data” (Table permanent environments called “buritizais” (14 gallery 1). forests with crystalline waters and a predominance of Regarding conservation status (43 species or 86%) are the palm tree Mauritia flexuosa L. [Arecaceae]) along actually listed as “Least Concern” (LC), two (4%) as a natural ecotone between Cerrado and restinga in “Data Deficient” (DD) on a global level (IUCN, 2019), northeastern Maranhão State, Brazil. and five (10%) as “no data” (Table 1). Anuran fauna sampling.—The qualitative sampling Discussion of the anurans (presence of species) was conducted monthly during the rainy season (January to August The anuran species richness recorded in the present 2010) at 24 sampling points in northeastern Maranhão study was higher in comparison to other works State, Brazil (Figure 1). conducted in Cerrado areas (Valdujo et al., 2011; Morais We sampled the anuran communities using the et al., 2012; Silva et al., 2015), restinga areas (Bastazini visual search (youth and adults) and acoustic search et al., 2007; Vilela et al., 2011; Gondim-Silva et al., (male reproductive activity of vocalization) methods 2016), and other natural ecotones comprised of different simultaneously to maximize the number of species biomes (Bitar et al., 2012; Magalhães et al., 2013; Silva observed by sampling (Heyer et al., 1994; Pearman et et al., 2013; Batista and Bastos, 2014; Borges-Leite et al., 1995). al., 2014). Anurans were sampled in areas up to 1 m from the This higher anuran richness found in our study margins surrounding the lentic environments (two small is perhaps explained simply by the sampled area’s floodplains and eight ponds), and in 300-m transects location within a natural ecotone (IBGE 1984; along the two margins of the lotic environments (14 Ab’Saber 1989; Rebêlo et al., 2010). For example, we buritizais). All environments and adjacent vegetation recorded some species that are commonly found in were inspected between 18:00h and 24:00h for the the Amazon (Boana boans and Boana geographica), presence of species (Heyer et al., 1994). Data sampling Caatinga (Corythomantis greeningi and Rhinella jimi), was standardized to 1h/day at each of the 24 sampled and Cerrado (Leptodactylus pustulatus, Physalaemus points to equalize the sampling effort among them. centralis and Rhinella ocellata) biomes, as well as some Unidentified adult anurans were collected, euthanized species with wide distribution (Leptodactylus fuscus, with xylocaine 5%, fixed in 10% formalin and then Physalaemus cuvieri and Scinax fuscomarginatus), preserved in 70% alcohol. All material collected which supports the hypothesis that a natural ecotone was deposited in the
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