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Anuran diversity of four taxocenoses of the subtropical Atlantic Forest from Santa Catarina and Paraná states Brazil

Local fauna inventories provide primary key information on diversity and distribution of species for conservation purposes. The Atlantic Forest holds 50% of anuran species in the country and the main threats to the conservation of this fauna are habitat reduction and fragmentation. The present study brings information on the local richness and species composition of four anuran taxocenoses from the subtropical Atlantic Forest of Paraná and Santa Catarina states, Brazil. Data collection included breeding sites surveys (N = 56) and literature review. Richness and beta diversity were compared through rarefaction/ extrapolation curves, local contribution to beta diversity (LCBD), beta partitioning and cluster analysis. Anuran from 46 species were registered and local richness differences were observed on the rarefaction/extrapolation curves and on asymptotic analysis. Nevertheless, the LCBD did not detect differences in species composition among the four taxocenoses. The turnover was the predominant component of beta diversity. The geographical distances explain species composition for all localities compiled in this study. The differences among local richness may be related to environmental impacts, emphasizing the need for conservation of biodiversity in the remnants of Atlantic forest. Key-Words. Species richness; Species composition; Inventory; Atlantic Forest; Conservation.


INTRODUCTION
Brazil withholds one of the highest diversity of anurans in the world (Segalla et al., 2019), whereas 530 species are found in the Atlantic Forest and 85% of these species are endemic of this biome (Haddad & Prado, 2005;Haddad et al., 2013). The original forest covered 150 million hectares of the Brazilian northeast coast to the south of the country, going as far as Paraguay and Argentina with formations of Interior and Araucaria Forests. Nowadays, only 11.73% of the original forest remains, in a fragmented landscape formed in its majority by small fragments (< 50 hectares) (Ribeiro et al., 2009), making it one of the 25 hotspots for the conservation of world-wide biodiversity (Myers et al., 2000). Anuran diversity suffers a negative impact with the fragmentation of habitats (Silvano et al., 2003). Habitats that are better preserved possess greater environmental heterogeneity and high number of micro environments improves the coexistence of species (Sazima & Eterovick, 2000;Vasconcelos et al., 2009;Silva et al., 2012a, b). Therefore, the diminishing habitat quality, fragmentation, homogenization and loss of habitats are considered the main causes of the decline of anuran populations and biodiversity loss in Brazil and in the world (Young et al., 2001;Cushman, 2006;ICMBio, 2018;IUCN, 2020).
Southern Brazil is mostly included in the subtropical Atlantic Forest which is divided by sub-regions, wherein a valuable diversity of anurans still resides: Atlantic Coast Restingas of Brazil -79 species, seven exclusive species (Garcia et al., 2007); Araucaria Forest 129 species, 13 being endemic (Conte, 2010); Serra do Mar 165 species, being 38 endemic (Garcia et al., 2007); and the Interior Forests 111 species, being only five endemic (Garcia et al., 2007).
Environmental studies that perform local inventories and use parameters of richness and species composition to describe taxocenoses allow us to access information on biodiversity, as well as to carry through a diagnosis on the conservation status and conduct actions of biodiversity preservation (Verdade et al., 2012). Therefore, this work aims to make an anuran inventory of four areas of the subtropical Atlantic Forest and to compare them, through local richness and species composition parameters, with other anuran taxocenoses from southern Brazil.

Study Areas
The states of Rio Grande do Sul, Santa Catarina and Paraná are mostly located in the subtropical region, in the Atlantic Tropical Morphoclimatic Domain and in the Araucaria Plateau (Ab'Saber, 1977) (Fig. 1). Four areas in the eastern region of Santa Catarina and Paraná states, Brazil (Fig. 2) were sampled for this study. The first area (BR-470), which included phytophysiognomies of the Lowland Dense Ombrophilous Forest (Veloso et al., 2012), was sampled along the BR-470 highway, between the municipalities of Ilhota and Indaial, Santa Catarina state. The second studied location (MGAN) included Sub-montane Dense Ombrophilous Forest (Veloso et al., 2012) lying between the municipalities of Major Gercino and Angelina, in the state of Santa Catarina, close to a small hydropow-er plant reservoir. The third area (SC-370) included the Mixed Ombrophilous Forest's phytophysignomy (Veloso et al., 2012) along the SC-370 highway located in Urubici municipality, Santa Catarina state. Finally, the fourth area (BR-116) included the Mixed Ombrophilous Forest phytophysignomy (Veloso et al., 2012), sampled along BR-116 highway, between the municipalities of Curitiba and Mandirituba, Paraná state. The search for frogs was conducted in several breeding sites (streams, permanent ponds and temporary swamps) found in open areas and forest fragments (Fig. 2, see Appendix 1).

Sampling
The fieldworks were conducted from 2010 to 2013: the BR-470 was sampled in 2010, SC-370 and MGAN in 2010and BR-116 in 2012  campaign of five days per trimesters and an effort of about 20 hours of search for each campaign. The samples occurred within the four seasons in each area, except for the winter campaign in SC-370 which was not held. The BR-116 was sampled twice during each season (see Appendix 2).

Data analysis
The sum of the higher abundance recorded for each species in each breeding site during sampling campaigns was used as the value of abundance of each area for the following diversity analysis (Table 1).
Rarefaction curves based on abundance were done using the iNEXT package (Hsieh et al., 2016) in R environment (R Core Team, 2020) to compare local richness among the four taxocenoses. In this analysis, the curves were generated by rarefaction/extrapolation of the values of richness and abundance from each taxocenose (Hill's number q = 0), resulting in a curve with the value of observed and estimated richness (the standard function remained, with it being twice the sample size) (Chao et al., 2014). This analysis also calculates the index of Chao's richness which is an asymptote analysis (Hsieh et al., 2016). To evaluate whether the anuran taxocenoses were well represented by the sampling effort in all localities, the sample completeness curves analysis was performed using the iNEXT package (Hsieh et al., 2016) in R environment (R Core Team, 2020).
The LCBD (Local Contribution of Beta Diversity -comparative indicators of the ecological uniqueness of the site) and SCBD (Species contribution of Beta Diversity -associated to degree of abundance, occupancy, niche position, niche breadth and species traits) (Heino & Grönroos, 2016) were used to compare the species composition of four sampled taxocenoses using the data of richness and abundance with the function beta.div (Legendre & Cáceres, 2013). In this analysis, the abundance data was transformed by the Hellinger method (Legendre & Legendre, 2012).
The rarefaction/extrapolation curves showed a difference of richness within the anuran taxocenoses of BR-116 and MGAN in relation of the anuran taxocenoses of BR-470 and SC-370, both on interpolation and on extrapolation (Fig. 4). Only the MGAN and BR-116 taxocenoses differed in the values of Chao's richness in the asymptotic analysis ( Table 2).
The result of the cluster analysis separated the four taxocenoses, grouping them with other localities from the southern region of Brazil (Fig. 5). Out of all the studied taxocenoses, only BR-116 and MGAN were similar to the clusters that they formed by the 40% criterion of dissimilarity. It was possible to observe some groups related to the geographical distances, vegetation and landscapes, such as the Pampas and Restinga of the Rio Grande Do Sul areas (Sentinela do Sul/RS, PE Itapeva, APA Ibirapuitã, FEPA), among the coastal areas of Serra do Mar and Serra     (Fig. 5).

DISCUSSION
BR-116 and MGAN presented the highest richness, and BR-470 and SC-370 the lowest richness among the study areas. All sampled breeding sites at MGAN were at small rural properties, away from large urban centers and highways, in a countryside region near the Serra do Tabuleiro in the Santa Catarina state. Most of the sampled breeding sites were in well preserved permanent preservation areas (APP) of a small hydropower plant reservoir between Major Gercino and Angelina municipalities. The other areas are urban centers and highways with medium to great flow of vehicles within these three areas, with many commercial, industrial and agricultural properties. The fieldworks in these areas were conducted along the highways. The high richness of anuran species at BR-116 might be explained by many breeding sites being a little farther away from the highway, in forest environments or on the edge of well preserved fragments. The other two areas (BR-470 and SC-370) have less species richness with similar environmental impacts (many disturbed open land environments). Nevertheless, in remark of the LCBD among these four taxocenoses, none of them have a unique species composition (Legendre & Cáceres, 2013).
The species that better contributed to the beta diversity (SCBD) are less generalist and present narrow niches (Heino & Grönroos, 2016). Taking that into account, the SCBD analysis for the four studied taxocenoses showed some interesting ecological aspects. First in relation to the species distribution, where Scinax imbegue, S. tymbamirim and Dendropsophus werneri are distributed in lowlands and coastal regions of Serra do Mar in Atlantic Forest (Pombal Jr. & Bastos, 1998;Nunes et al., 2012).  (Table 3). The red line represents the criterion of 40% dissimilarity.
These three species were registered with higher abundance only at the breeding sites of BR-470 and MGAN (Table 1). D. nahdereri and Physalaemus aff. gracilis are distributed in highlands and mountain regions of subtropical Atlantic Forest (Nascimento et al., 2005;Conte et al., 2010;Kwet et al., 2010). These two species were registered with higher abundance at the breeding sites of SC-370 and BR-116 (Table 1). D. sanborni is distributed in highlands and grassland vegetation from the central-west to southern Brazil (Gavira et al., 2016). This species was registered with higher abundance at the breeding sites of BR-116 (Table 1). However, these six species are characterized by their tendency to occupy open land or edge forest breeding sites. Adenomera araucaria and A. nana are distributed in lowlands and highlands of subtropical Atlantic Forest and found only in forest breeding sites, even in urban forest fragments (Kwet & Angulo, 2002;Conte et al., 2010), due to their terrestrial reproduction mode (Heyer, 1973;Kwet et al., 2010). The two Adenomera species were registered with higher abundance at forest fragments of MGAN and BR-470 (Table 1).
The influence of geographic distances in anuran species composition was also evidenced in other studies (Bertoluci et al., 2007;Lucas & Fortes, 2008;Iop et al., 2011;Almeida-Gomes & Rocha, 2014;Bolzan et al., 2014) and the turnover is the major component that explains the differences of species composition of subtropical Atlantic Forest. The association between the turnover and geographical distances may be related to the differences in climate, phytophysionomy and landscape (Vasconcelos et al., 2014), in which the groups of cluster analysis have some correlation with the sub-regions of subtropical Atlantic Forest (Garcia et al., 2007).
The few similarities within species composition of the areas studied may be also associated to habitat quality. The BR-116 and MGAN anuran taxocenoses are similar to two other taxocenoses within well preserved localities: Parque Estadual da Serra do Tabuleiro and Tijucas do Sul/PR, while the BR-470 anuran taxocenose (northern region of Santa Catarina state) is grouped with the anuran taxocenose of Siderópolis (southern region of Santa Catarina state). There is coal mining in the Siderópolis region, which is an activity that negatively affects the environment (De Lucca et al., 2017). Thus, this area is grouped, but not similar to the impacted area and the differences of species composition might be related to the effect of environmental impacts.

CONCLUSIONS
The subtropical anuran taxocenoses differences on species composition seem associated to changes of phytophysionomy, landscape and geographic distances. The highest richness at BR-116 and MGAN may relate to habitats of higher quality, as these taxocenoses are similar to other well preserved areas from the subtropical Atlantic Forest. The lowest richness found in the BR-470 and SC-370 anuran taxocenoses may be related to low habitat quality. Regardless, the data gathered points to the importance of preservation and maintenance of forest fragments, even in agricultural and urban environments due to the possibility that these fragments may hold valuable biodiversity.