Herpetology Notes, volume 11: 421-428 (2018) (published online on 09 May 2018)

Anuran diversity in an Araucaria Forest fragment and associated grassland area in a sub-tropical region in Brazil

Nathalie Edina Foerster1,* and Carlos Eduardo Conte,2,3

Abstract. Considering the rapid advancement of forest fragmentation and destruction, understanding species composition, richness and distribution is crucial for the development of conservation strategies. In this context, the main goal of this study is to provide an inventory of anuran species using different sampling methods (survey at breeding sites, transect sampling and pitfall traps) and to evaluate the assemblage structure of anurans in an Araucaria Forest and its associated grasslands in a subtropical region in Brazil. For the analyses, 21 breeding sites were classified into three categories: open area (OA; n=7), forest interior (FI; n=7) and forest edge (FE; n=7). A diversity profile analysis was performed to evaluate alpha diversity. ANOSIM and SIMPER analyses were carried out to verify differences regarding species composition (beta diversity) between the categories. A total of 33 species comprising nine families were recorded, representing ca. 80% of the estimated richness for the region. The greatest alpha diversity was observed in FI, whereas OA and FE did not differ in terms of diversity. Regarding beta diversity, all categories differed amongst themselves (dissimilarity 80%), which may be related to the presence of exclusive species in each category, requiring specific habitat characteristics, due to specific reproductive modes. Furthermore, many species showed high abundance due to their generalist habits. The presence of exclusive species at OA and FI reinforces the importance of preserving different for the maintenance of local species richness and diversity.

Keywords: Anura; assemblage structure; Campos Gerais; Mixed Ombrophilous Forest; Piraí do Sul

Introduction Parris, 2004; Silva et al., 2012). Ecological studies seek to understand how these interactions occur and how Anuran assemblage compositions are determined they influence species richness and distribution (e.g., by species interactions with biotic and abiotic factors Parris, 2004; Santos et al., 2007; Ernst and Rödel, 2008; (Eterovick and Sazima, 2000; Parris, 2004; Wells, Vasconcelos et al., 2009; Silva et al., 2012). Answering 2007; Oda et al., 2016), as well as by historical and these questions is important in the present setting, since evolutionary processes (Zimmerman and Simberloff, and alterations are major threats to 1996; Piha et al., 2007). The availability of different several species, especially anurans (Dixo and Verdade, microhabitats allows for the segregation and coexistence 2006; Bishop et al., 2012). Most anurans are extremely of species in a same habitat, as well as species dependent on their habitat characteristics, due to several differentiation among habitats (Conte and Rossa-Feres, factors, including permeable skin (Wells, 2007) and 2007; Santos et al., 2007; Vasconcelos et al., 2009; reproductive modes that require specific microhabitats Silva et al., 2011). In this sense, habitat heterogeneity (Haddad and Prado, 2005; Crump, 2015). has been considered an important factor regarding This study presents an evaluation of the structure of anuran assemblage structure (Cardoso et al., 1989; an anuran assemblage at an Araucaria forest region and its associated grasslands, located in the Piraí do Sul municipality, Brazil. The study aims to (i) provide a list

1 Autonomous researcher: Major França Gomes, 673, CEP of species for the region and (ii) compare the assemblage 80310-000, Curitiba, Paraná, Brazil composition of three different habitats types: open area, 2 Instituto Neotropical: Pesquisa e Conservação (INPCON). forest interior and forest edge. Avenida Coronel Francisco Heráclito dos Santos, 100, CEP 81531-980, Curitiba, Paraná, Brazil Material and Methods 3 Criadouro Onça Pintada. Estrada do Pocinho, s/n, Campina Grande do Sul, CEP 83420-000, Paraná, Brazil This study was carried out at the Piraí do Sul * Corresponding author. E-mail: [email protected] municipality (24.5397°S, 49.9278°W; datum SIRGAS, 422 Nathalie Edina Foerster & Carlos Eduardo Conte

2000) (SISBIO license n°26992-1), in a region known The Campos Gerais climate, according to Köppen, is as Campos Gerais, in the state of Paraná, Brazil, in two Cfb (humid subtropical), with mild summers. Maximum areas: 1) Floresta Nacional de Piraí do Sul (FNPS) and average temperatures in the hottest months are below 2) Piraí da Serra (Figure 1). 22˚C, and during the coldest months are below 18˚C, The FNPS (24.5667°S, 49.9167°W) is located with frequent frost (Moro et al., 2009). between the first and second Paraná plateau, comprising Diversity data was obtained monthly at 24 sites, 152 ha. The area presents a slightly undulating relief, from October 2012 to March 2013. Three sites were with altitudes ranging between 900 and 1248m above composed of transects locates in the forest interior, 20 sea level (asl). The dominant vegetation types are Pinus, sites were breeding habitats (six puddles, nine swamps, Araucaria and Imbuia (Ocotea), and Araucaria forest in five lakes, one artificial tank and three 120-meter different successional stages where selective logging transects in streams) at FNPS and its surrounding areas, has transpired (Moro et al., 2009). Different vegetation and one site was a stream transect in Piraí da Serra (Table types, such as Pinus, Eucalyptus and crops, as well as 1). The habitats sampling sequence of each campaign different-sized Araucaria forest fragments, occur in the was altered to minimize possible variations in species surrounding areas of the FNPS (ICMBio, 2011). activities (sensu Conte and Rossa-Feres, 2006). The Piraí da Serra area (24.4667°S, 50.0167°W) is The applied sampling methods were: 1) breeding site located in the Environmental Protection Area (APA) sampling (Scott Jr. and Woodward, 1994), in which the of the Devonian Escarpment, with an elevation of perimeter of each water body and stream were slowly around 1000 m asl comprising 51.20 ha (SEMA, 2004) traversed, counting individuals from different species at approximately 15 km from the FNPS. The region is and calling males during one hour per site per campaign, formed by approximately 37% grassy-woody steppe, totalling 150 hours for all habitats; and 2) transects 18% Araucaria Forest, 45% fast-growing exotic species inside the forest, slowly traversed, counting individuals monocultures (Pinus and Eucalyptus) and crops (Veloso from different species and calling males, with an effort et al., 1991; Bilenca and Miñarro, 2004; SEMA, 2004). of one hour per transect per campaign, totalling 18

Figure 1. Map of Brazil, state of Paraná and satellite images of the sampled areas in the municipality of Piraí do Sul: A- Piraí da Serra; B- Floresta Nacional de Piraí do Sul and surrounding areas. Asterisks indicate the locations of the habitats sampled in the study area; more than one habitat can be located at the same asterisk point at the map. The red asterisks indicate the locations at the Floresta Nacional de Piraí do Sul. Satellite image: Google Earth©. Anuran diversity in an Araucaria Forest fragment in Brazil 423

Table 1. Characterization of the sampled habitats in Piraí do Sul municipality, from October 2012 to March 2013 according to the matrices in which they were inserted: Open area: swamps (SO1, SO2), lakes (LO1, LO2), ponds (PO1, PO2), stream (STO1); Forest edge: swamps (SE1, SE2), lakes (LE1), ponds (PE1-PE4); Forest interior: swamps (SF1, SF2), lakes (LF1, LF2); streams (STF1, STF2); artificial tank (ATF), Transections (TF1, TF2, TF3). Vegetation in the breeding habitat: % Interior = percentage of vegetation inside the breeding habitat, % Marginal= percentage of vegetation on the edge of breeding habitat. Type of vegetation: He = herbaceous, Sr = shrub, Ab = arboreal, Pt = pteridophyta, Aq = aquatic, Tb = Typha sp., Gr = gramineae, Br = Bryophyte. * = Not applicable.

Breeding habitat vegetation Maximum Habitat Vegetation type % Interior % Marginal depth (m) SO1 60 80 Sr, He, Gr,Aq 1,30 SO2 100 100 Sr, Ab, Hb, Gr 0,40 SE1 55 60 Sr, Ab, He, Pt, Gr, Aq 0,80 SE2 60 65 Sr, Ab, He, Gr 0,25 SF1 100 100 Sr ,Ab, He, Gr, Pt, Aq 0,40 SF2 100 100 Sr, Ab, He, Gr, Pt, Aq 4,00 LO1 10 75 Sr, He, Gr, Aq 5,40 LO2 50 90 Sr, He, Tb, Aq 3,60 LE1 30 75 Sr, Ab, He, Aq, Gr 3,40 LF1 5 100 Sr, Ab, He, Tb, Aq, Gr 6,00 LF2 40 100 Sr, Ab, He, Aq, Gr 4,40 PO1 5 60 Sr, He, Aq, Gr 1,15 PO2 1 30 Br, Gr 1,00 PE1 5 75 Sr, Ab, He 3,00 PE2 98 25 Sr, Ab, He, Gr 0,25 PE3 80 25 Sr, Ab, He 0,40 PE4 2 30 Sr, Ab, He, Gr 1,50 STO1 0 100 Sr, He, Gr, Br 2,00 STF1 0 95 Sr, Ab, He, Gr, Pt 0,30 STF2 0 100 Sr, Ab, He, Pt 0,40 ATF 90 100 Sr, Ab, He, Aq, Gr 0,45 TF1 * 100 Sr, Ab, He, Gr, Pt * TF2 * 100 Sr, Ab, He, Pt * TF3 * 100 Sr, Ab, He, Pt *

hours for all transects, jointly. Pitfall traps were used as differences in capture and recapture results. These the inventory method (Corn, 1994). Five sites with three results demonstrate that, despite differences between trap lines were sampled. Each line was composed by species, the number of individuals present in more than four 60-liter buckets, located 10 meters apart from each one breeding event tends to be lower than the number of other, connected by drift fences, set in a way to induce individuals present at only a single breeding event. individual capture. The buckets remained open for five The first-order Jackknife estimator extrapolation consecutive nights per campaign, totalling an effort of method was applied to evaluate species richness 60 buckets per night per campaign. Samplings using estimates of the study area and sampling efforts, where pitfall traps were carried out bimonthly from November random samples were added to the species accumulation 2012 to September 2013. Only species richness data curve until an asymptote was obtained (Colwell et was collected using this method. Data obtained in this al., 2004). The analyses were carried out using the manner was not used for the diversity analyses. EstimateS version 9.0.0 software (Colwell, 2013). Total abundance at each site was considered as the sum The 21 breeding habitats, with the exception of the of abundances of all sampled months. This estimate was forest transects, were classified into three categories used to avoid population underestimations, considering for the diversity analyses: seven in the forest interior the observation made by Nomura et al. (2012) when (FI), comprising two swamps, two ponds, three evaluating a compilation of studies that indicated streams and one artificial tank; seven at the forest 424 Nathalie Edina Foerster & Carlos Eduardo Conte edge (FE), composed of five swamps, one pond and four puddles; and seven in an open area (OA), namely two swamps, two ponds, two puddles and one stream (Table 1). A Diversity Profile analysis was performed to verify differences regarding alpha diversity between categories applying the Rénvi index, in which α=0 is the total number of species, where α=1 gives a greater weight to richness according to the Shannon Index, and α>2 attributes weight to equitability according to the Simpson Index. As different α values were observed, there was no problem in applying the diversity and interpretation indexes, since each of these indices attributes different weights to rare species (Mendes et al., 2008). This analysis generates curves that graphically Figure 2. Observed richness during the six months of sampling, represent which habitats are more diverse. However, if from October 2012 to March 2013 (●) and expected richness the curves connect at a certain point, it is not possible to with additional samples to reach the estimated number of define which one is more diverse, and, in this case, they species (○), at Piraí do Sul, Paraná, Brazil. cannot be compared (Tóthmérész, 1995). The analyses and curves were plotted and evaluated using the Past version 2.17c software package (Hammer et al., 2001). A similarity analysis (ANOSIM) was conducted americanus), and three by the sampling habitats method to evaluate differences in beta diversity among the [Bokermannohyla circumdata, Scinax sp. (gr. ruber) categories, measuring the difference between two or and Crossodactylus sp.] more groups from a certain distance (Clarke, 1993). A No significant difference between OA and FE was similarity percentage analysis (SIMPER) was used to observed when evaluating diversity profiles, whereas evaluate species relative contribution for the dissimilarity FI displayed a significantly higher alpha diversity in in each category (Clark, 1993). Due to the high relation to the other categories (Figure 3). Regarding values for species richness, species that cumulatively beta diversity, all categories differed amongst themselves contributed up to 90% were considered. The applied (r = 0.199, p = 0.006), with an 80% species composition distance measurement for these analyses was the Bray- dissimilarity among categories. Of the 27 species Curtis Index that evaluates the dominance and rarity considered in this study, only 14 contributed with between species by applying richness and abundance 90.51% for this inter-categories differentiation (Table data (Krebs, 1999). The analyses were carried out using the Past version 2.17c software package (Hammer et al., 2001).

Results Thirty three anuran species were recorded at Piraí do Sul, distributed throughout 17 genera and nine families, namely (Table 2): Brachycephalidae (1), Bufonidae (2), Centrolenidae (1), Hylidae (19), Hylodidae (1), Leptodacylidae (5), Michohylidae (1), and Odontophrynidae (2), Phyllomedusidae (1). According to the data generated by the richness estimation method, the registered richness corresponds to 80% Figure 3. Diversity Profile among treatments of the theoretical richness (N=40, Figure 2). Twenty- (OA- open area; FE- forest edge; FI- forest interior) sampled eight of the 33 species were recorded by the breeding at Piraí do Sul from October 2012 to March 2013. The curves site sampling method (Table 2), seven by transection are generated by different α values given by different diversity inside the forest, two exclusively by the pitfall trap indices, so the generated curves represent which are the most method ( leucosticta and Odontophrynus diverse (alpha diversity) habitats. Anuran diversity in an Araucaria Forest fragment in Brazil 425

Table 2. Anuran species composition and abundance and method by which they were sampled during the sampling period from October 2012 to March 2013 at the Piraí do Sul municipality, and the respective treatments in which they were recorded. Forest edge (FE); Open area (OA); Forest interior (FI); Sampling method: breeding site visual encounter survey (BS); Transects in forest Table 2. Anuran species composition and abundance and method by which they were sampled during the sampling period from October 2012 to March 2013 at interiorthe (TF); Piraí Pitfall do Sul trapsmunicipality, (PT); and* Species the respective recorded treatments outside in which the breedingthey were recorded.habitats Forestsampled; edge (FE);Note: Open species area (OA);collected Forest in interior pitfall (FI); traps Sampling and recordedmethod: outside breeding thesite visualsampled encounter habitats survey do (BS); not Transects have abundance in forest interior data. (TF); Pitfall traps (PT); * Species recorded outside the breeding habitats sampled; Note: species collected in pitfall traps and recorded outside the sampled habitats do not have abundance data.

Taxa FE OA FI BS TF PT Brachycephalidae Ischnocnema henselii (Peters1872) 8 X X X Bufonidae Rhinella abei (Baldissera-Jr, Caramaschi and Haddad 2004) 1 X X Rhinella icterica (Spix 1824) X Centrolenidae Vitreorana uranoscopa (Müller 1924) 13 X Odontophrynidae Odontophrynus americanus (Duméril and Bibron, 1841) X Proceratophrys boiei (Wied-Neuwied, 1825) 9 19 X X X Hylidae Aplastodiscus perviridis A. Lutz in B. Lutz 1950 34 4 31 X X Boana. sp (gr. pulchellus) 2 X Aplastodiscus albosignatus (A.Lutz and B. Lutz 1938) 4 7 34 X Boana albopunctata (Spix 1824) 95 337 146 X Boana bischoffi (Boulenger 1887) 150 73 222 X X Boana faber (Wied-Neuwied 1821) 18 7 5 X Boana jaguariaivensis Caramaschi, Cruz and Segalla, 2010 306 X Boana prasina (Burmeister, 1856) 5 64 27 X X Bokermannohyla circumdata (Cope 1871) * Dendropsophus microps (Peter 1872) 19 48 55 X X Dendropsophus minutes (Peters1872) 117 466 230 X Dendropsophus sanborni (Schmidt 1944) 137 430 49 X Ololygon aromothyella Faivovich, 2005 2 X Ololygon rizibilis (Bokermann, 1964) 10 32 X X Scinax fuscovarius (A. Lutz, 1925) 8 8 65 X Scinax sp.(gr. ruber)* Scinax squalirostris (A. Lutz, 1925) 10 X Sphaenorhynchus caramaschii Toledo, Garcia, Lingnau and Haddad, 2007 99 3 201 X Hylodidae Crossodactylus sp.* Leptodactylidae Physalaemus cuvieri Fitzinger, 1826 46 102 55 X X Physalaemus aff. gracilis 31 78 17 X X Physalaemus lateristriga (Steindachner, 1864) 21 X Leptodactylus cf. latrans (Steffen, 1815) 19 33 9 X Leptodactylus notoaktites Heyer, 1978 1 8 X Chiasmocleis leucosticta (Boulenger, 1888) X Phyllomedusidae Phyllomedusa tetraploidea Pombal and Haddad, 1992 2 4 14 X

3), identified as the species displaying the greatest al., 2010). This is similar to other studies conducted in abundance (Table 2). AF areas, such as at the Fazenda Experimental Gralha Azul, in the Fazenda Rio Grande municipality (n = 32; Discussion Conte and Rossa-Feres, 2007) and Floresta Nacional The species richness recorded herein represents 23% Chapecó (n = 29; Lucas and Fortes, 2008), and higher of the richness reported for the state of Paraná and when compared to the Parque Municipal São Luís de 25.6% for Araucaria Forest (AF) (Conte, 2010; Conte et Tolosa, located in the Rio Negro (n = 24; Santos and 426 Nathalie Edina Foerster & Carlos Eduardo Conte

Table 3. Percentage of dissimilarity contribution for the 14 species that contributed most to the difference on species composition between the sampled habitats in Piraí do Sul municipality from October 2012 to March 2013 categorized accordingly to the Table 3. Percentage of dissimilarity contribution for the 14 species that contributed most to the difference on species treatments: forest compositioninterior (FI); between forest the edge sampled (FE); habitats open in area Piraí do(OA). Sul municipalityDissimilarity from %: October percentage 2012 to of March species 2013 individually to the categorized accordingly to the treatments: forest interior (FI); forest edge (FE); open area (OA). Dissimilarity %: difference; Accumulatedpercentage %: of speciesthe sum individually of percentage to the difference; contribution Accumulated between %: the the sum previous of percentage species contribution to the between differentiation. Average abundance: the proportionthe previous of species abundance to the differentiation. of each species Average between abundance: treatments. the proportion of abundance of each species between treatments.

Average abundance Species Dissimilarity % Accumulated % FI FE OA Dendropsophus minutus 14,86 17,98 28,8 12,5 66,6 Boana bischoffi 10,11 30,22 27,8 18,6 10,4 Dendropsophus sanborni 9,65 41,89 6,13 13,7 61,4 Boana albopunctata 9,188 53,01 18,3 10,7 48,1 Boana jaguariaivensis 5,91 60,16 0 0 43,7 Physalaemus cuvieri 4,185 65,22 6,88 5,4 14,6 Sphaenorhynchus caramaschii 3,481 69,43 25,1 9,9 0,429 Physalaems aff.gracilis 2,998 73,06 2,13 3,1 11,1 Leptodactylus cf. latrans 2,606 76,21 1,13 3,2 4,71 Dendropsophus microps 2,605 79,37 6,88 1,9 6,86 Aplastodiscus perviridis 2,569 82,48 3,88 3,4 0,571 Boana prasina 2,277 85,23 3,38 1,6 9,29 Scinax fuscovarius 2,238 87,94 8,13 0,8 1,14 Aplastodiscus albosignatus 2,122 90,51 4,25 0,6 1

Conte, 2014) and Campo Largo (n = 21; Trevisan and restrict species to certain breeding sites, leading to Hiert, 2016) municipalities. The observed richness can difference between habitat compositions. be considered high and is probably due to the high The breeding site sampling method was very effective number of sampled habitats and the great difference in for recording species. However, the other methods landscape composition, as well as the environmental were also important, allowing for encounters with heterogeneity of these environments. Santos and Conte exclusive species, such as Chiasmocleis leucosticta (2014) observed that a higher number of species are and Odontophrynus americanus, recorded only by registered when a greater scope of site types is sampled pitfall traps. These species present fossorial, cryptic and in an AF area (e.g., puddles, lakes, and streams). This is explosive breeding habits. Furthermore, a record for C. due to the breeding requirements for each species, that leucosticta in the study area is of remarkable importance, may require specific conditions in each habitat (e.g., since this is the most western record of this species for different microhabitats and humidity for calling activity, the state of Paraná (Segalla and Langone, 2004; Conte, among others), inserted in different matrices (Gonçalves 2010; Crivellari et al., 2011). The importance of using et al., 2015). Ischnocnema henselii and Vitreorana different methods has been pointed out by other studies,  uranoscopa are the most demanding species concerning such as the one carried out by Silva (2010), in which the habitat quality among forest-dependent anuran species. author evaluates different studies that applied adult and Vitreorana uranoscopa was recorded only in one stream tadpole sampling techniques, and reported that species within the forest, because of its reproductive mode, richness in all studies would be reduced if only one dependent upon lotic habitats like streams (Heyer, 1985; method were to be applied, instead of more. Haddad and Prado, 2005). The reproductive mode of The FI category displayed a greater alpha diversity Ischnocnema henselii consists of laying eggs in litter. in relation to OA, with higher equitability among These eggs exhibit direct development, requiring forest species, which can be related to the high forest habitat environments that can provide an adequate amount of heterogeneity (Eterovick, 2003; Santos et al., 2007; litter and humidity (Haddad and Prado, 2005). Boana Vasconcelos et al., 2009; Ramos and Santos, 2006). The jaguariaivensis, is noteworthy among species with generalist or specialist character of a species may reflect habitat specificities in the open area, since it present a in their presence or absence in a certain environment displays mode linked to streams on outcrops in native (Wells, 2007). Forest environments present vertical grassland fields (Caramaschi et al., 2010). These stratification, allowing species to segregate and coexist specifications mostly linked to reproductive modes in this habitat (Silvano et al., 2003; Silva et al., 2012). Anuran diversity in an Araucaria Forest fragment in Brazil 427

Open areas present lower stratification, excluding Caramaschi, U., Cruz. C. A. G., Segalla, M.V. (2010): A new species that undergo direct development, due to lower species of Hypsiboas of the H. polytaenius clade from the state litter moisture and less shading. Because of this, the OA of Paraná, Southern Brazil (Anura: Hylidae). South American Journal of Herpetology 5 (3):169 –174. habitats presented a higher amount of habitat-generalist Cardoso, A. J., Andrade, G. V., Haddad, C. F. B. (1989): Distribuição species (Oda et al., 2016). espacial em comunidades de anfíbios no sudeste do Brasil. A high differentiation among species composition Revista Brasileira de Biologia 49: 241– 249. (beta diversity) was observed, since each category Clarke, K. R. (1993): Non-parametric multivariate analyses of recorded exclusive species and differences regarding changes in community structure. Australian Journal of Ecology species abundance. 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