Amphibians of Vassununga State Park , one of the last remnants of semideciduous Atlantic Forest and Cerrado in northeastern São Paulo state , Brazil

Although São Paulo state has one of the best known amphibian fauna in Brazil, there are still protected areas for which the species composition remains unknown. Here, we present the first species list of anuran amphibians in Vassununga State Park. This area is one of the last remnants of semideciduous Atlantic Forest and Cerrado in the northeastern region of São Paulo state, southeastern Brazil. To survey species, we visited six sites (two ponds, two streams, and two transects) in December, January, and February of 2014-2015 and 2015-2016, totalizing 18 days of field samplings at each site. We recorded 24 anuran species belonging to four families: Bufonidae (2 species), Hylidae (11 species), Leptodactylidae (10 species), and Microhylidae (1 species). Anurans consist mainly of generalist and widely distributed species. Although none of the species recorded are threatened with extinction according to the International Red List of Endangered Species (IUCN), four species have declining population and another three species have unknown population trends.


Introduction
Knowing the species composition of a region is important because it is the basic dataset for ecology, systematics, biogeography, and conservation biology (e.g., Collen et al. 2008;Da Silva et al. 2012, 2014).It is recognized that Brazil has an amazing amphibian diversity (1080 species; Segalla et al. 2016), with the São Paulo state harboring 22% of known species (Rossa-Feres et al. 2011).Although, the amphibian fauna of São Paulo state is one of the best known in the country, there are still considerable herpetological survey gaps in some regions (Rossa-Feres et al. 2011).These gaps are more evident inland (i.e., northwestern and northeastern regions of the state) than in the coastal region of the state, where most surveys have been conducted (Rossa-Feres et al. 2011).For example, the increased number of anuran surveys in the last decade has contributed to records of new species in the inland areas of the state (Vasconcelos et al. 2006, Prado et al. 2008, Da Silva et al. 2009, 2010).Even protected areas such as the Vassununga State Park (created in 1970) still have not been subject to a complete faunal survey.This is worrisome because this protected area harbors one of the last remnants of Cerrado and semideciduous Atlantic Forest in the region, two biomes that are considered global hotspots for biodiversity conservation (Myers et al. 2000, Mittermeier et al. 2004).The Vassununga State Park is located in the northeastern region of the São Paulo state, which is considered one of the most deforested and fragmented regions in the state (Rodrigues et al. 2008).The vegetation cover has been removed for the establishment of agricultural crops, pastures and urban areas, which reduced the vegetation to 9% of its original extent (Kronka et al. 1993).
Here, we provide the first list of anuran species of the Vassununga State Park, a region considered to be a geographical gap in the inventories of species in the Sao Paulo state, Brazil.

Study area
The Vassununga State Park (PEV; 21°43'05"S, 47°35'49"W; 553 m above sea level) is located in the municipality of Santa Rita do Passa Quatro, northeastern São Paulo state (Figure 1).It is a Protected Area with 2071.42 ha created on October 26, 1970.The region holds different physiognomies of two Brazilian biomes, Atlantic Forest and Cerrado, which are considered global hotspots for biodiversity conservation (Myers et al. 2000, Mittermeier et al. 2004).In the PEV, the Atlantic Forest is represented by the Seasonal Semideciduous Forest sensu stricto (Veloso et al. 1991, Pennington et al. 2006), which is characterized by having 20-50% of tree species that lose part or all their leaves in the winter or during the dry season.The Cerrado is represented by three formations (Oliveira-Filho & Ratter 2002): (i) "campo cerrado", which is formed by dry grassland scattered with shrubs and small trees; (ii) "cerrado sensu stricto", which is dominated by trees and shrubs that are often 3-8 m tall but still with a fair amount of herbaceous vegetation among them; and (iii) "cerradão", which is an almost closed woodland with crown cover of 50% to 90% that is made up of trees, often of 8-12 m or even taller, that cast considerable shade so that the ground layer is greatly reduced.The climate of this region is characterized by two well-defined seasons during the year: hot and wet (September to April), during which approximately 85% of the annual rainfall occurs, and a pronounced dry season (May to August), with average precipitation of only 15% of the annual rainfall.The average annual precipitation is 1,427 mm (± 246.83 SD, http://www.ciiagro.sp.gov.br/ciiagroonline/).

Data Analysis
To assess the sampling efficiency of the surveys, we used a species accumulation curve (Gotelli & Colwell 2001) generated from the data of incidence of anurans during the inventory period.The total number of species recorded each day was considered as a sample, totaling 18 samples.
Considering the diverse richness estimators available, we chose to use the first-order Jackknife algorithm based on its performance when compared to other estimators (Magurran 2004, Walther & Moore 2005, Hortal et al. 2006).All analyzes were performed in R v 3.2.2(R Core Team, 2016) using the vegan (Oksanen et al. 2016) and BiodiversityR (Kindt & Coe 2015) packages with 1,000 randomizations.Taxonomic nomenclature follows Frost (2016).The conservation status of species was obtained from the International Red List of Endangered Species (IUCN 2015).

Results and Discussion
We recorded 24 species of anuran amphibians (Table 1, Figure 3) belonging to four families: Bufonidae (2 species), Hylidae (11 species), Leptodactylidae (10 species), and Microhylidae (1 species).Although the species accumulation curve is close to achieving asymptote, the observed species richness was smaller than the estimated species richness, indicating that more species could be recorded if we increase the sampling effort or utilize other sampling methods (e.g., pitfall traps, Figure 4).Since Vizotto (1967), 37 anuran species have been recorded in the northwestern region of the São Paulo state (Provete et al. 2011).In this study, we recorded approximately 65% of all species that occur in the region.Only Hypsiboas albopunctatus had already been recorded at the study site (Toledo et al. 2007) 2009).Although none of the recorded species is currently threatened with extinction, three species (Dendropsophus elianeae, Physalaemus centralis, and P. marmoratus) have unknown population trends, and four species (Rhinella ornata, Hypsiboas lundii, Itapotihyla langsdorffii, and Physalaemus nattereri) have declining population (IUCN 2015).Furthermore, Vasconcelos & Doro (2016) showed that habitat loss has negative impacts in the geographic ranges of R. ornata, H. lundii, and I. langsdorffii.This fact becomes even more worrying considering that northeastern region of the São Paulo state has one of highest deforestation and fragmentation rates in the state (Rodrigues et al. 2008).
Approximately 50% of the species (Dendropsophus elianeae, D. jimi, D. minutus, Hypsiboas faber, Leptodactylus latrans, L. mystacinus, L. podicipinus, Physalaemus centralis, P. cuvieri, P. marmoratus, P. nattereri, and Elachistocleis cesarii) occurred exclusively in ponds in open areas, while 10 species (Rhinella schneideri, Dendropsophus nanus, Hypsiboas albopunctatus, H. lundii, Itapotihyla langsdorffii, Scinax fuscovarius, S. similis, Trachycephalus typhonius, Leptodactylus labyrinthicus, and L. mystaceus) occurred in streams and ponds.Hypsiboas lundii was the only species found vocalizing exclusively on streams inside gallery forest (Table 1).The large number of anuran species associated with water bodies in Cerrado and semideciduous forest fragments during the reproductive period has been demonstrated in other studies (Brasileiro et al. 2005, Bertoluci et al. 2007, Araujo et al. 2009, Santos et al. 2009, Araujo & Almeida-Santos 2011, 2013, Valdujo et al. 2012).According to Santos et al. (2009), anuran communities from Semideciduous Atlantic Forest and Cerrado environments are more similar to each other than they are to those of Ombrophilous Forest environments.This pattern of similarity in anuran communities can be interpreted as a result of the seasonally dry climate that most likely limits the occurrence of anuran species typical of the Ombrophilous Atlantic Forest in Semideciduous Atlantic Forest and Cerrado areas (Santos et al. 2009, Da Silva et al. 2012).
Family  This study area is one of the most deforested and fragmented in the state, and because of the lack of biological knowledge, it is classified as a priority for fauna and flora inventories (Rodrigues et al. 2008, Rossa-Feres et al. 2011).In this sense, the species list of anurans for Vassununga State Park represents an important step in increasing the knowledge about the distribution of diversity of São Paulo state.

Figure 1 .
Figure 1.Maps showing the São Paulo state highlighted in Brazil (at right) and the study area highlighted in northeastern São Paulo state (at center).In detail (at left), the six isolated forest fragments (named Glebe) that comprise the total area of the Vassununga State Park.

Figure 4 .
Figure 4. Species accumulation curve (black line) and Jackknife algorithm first order (gray line) representing the anuran species richness observed and estimated, respectively, based on 18 samples from December 2014 to February 2016.The dots show the mean generated by 1000 randomizations and the vertical bars indicate the standard deviation.
. The species richness observed in this study was similar to those found both in areas with predominance of Cerrado formations such