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Expanding the knowledge about the occurrence of anurans in the highest amphibian diversity area of Atlantic Forest: Parque Estadual da Serra do Mar, São Paulo, Brazil

Expandindo o conhecimento sobre a ocorrência de anuros na área com maior diversidade de anfíbios da Floresta Atlântica: Parque Estadual da Serra do Mar, São Paulo, Brasil

Abstract

The vegetation cover in the Atlantic Forest has been converted to human use or degraded by human activities, which declined the vegetation to 16% of its original extent. Although several protected areas have been created in this Neotropical biome over the past decades, our knowledge of the amphibian species within these areas is still far from adequate. Here, we present lists of anuran species from three different areas of Parque Estadual da Serra do Mar: núcleos Curucutu, Santa Virgínia and São Sebastião. To survey anuran species, we visited six sampling units (two ponds, two streams and two trails inside forest fragments) in each locality. Samplings were accomplished from December 2014 to February 2015, December 2015 to February 2016 and December 2016 to February 2017, totalizing 27 days of field samplings in each sampling unit. We recorded 34 anuran species in the Núcleo Curucutu, 44 species in the Núcleo São Sebastião and 42 species in the Núcleo Santa Virgínia, totalizing 65 species belonging to 12 families (number of species in parentheses): Bufonidae (5), Brachycephalidae (6), Centrolenidae (1), Craugastoridae (1), Cycloramphidae (2), Hemiphractidae (1), Hylidae (29), Hylodidae (3), Leptodactylidae (12), Microhylidae (2), Odontophrynidae (2), and Phyllomedusidae (1). We hope that these lists can be useful for future studies as well as helping in the management and conservation planning of these protected areas.

Keywords:
Amphibians; Biodiversity; Conservation; Hotspots; Species list

Resumo

A cobertura vegetal da Floresta Atlântica foi convertida para uso humano ou degradada pela atividade humana permanecendo atualmente 16% da sua extensão original. Embora muitas áreas protegidas tenham sido criadas neste bioma neotropical nas últimas décadas, nosso conhecimento sobre as espécies de anfíbios nestas áreas ainda está longe do adequado. Aqui, nós apresentamos listas das espécies de anuros para três diferentes áreas do Parque Estadual da Serra do Mar: núcleos Curucutu, Santa Virgínia e São Sebastião. Para amostrar as espécies de anuros, visitamos seis locais de amostragem (duas poças, dois riachos e duas trilhas) em cada localidade. As amostragens foram realizadas de dezembro 2014 a fevereiro de 2015, dezembro de 2015 a fevereiro de 2016 e de dezembro de 2016 a fevereiro de 2017, totalizando 27 dias de amostragens de campo em cada ponto de amostragem. Registramos 34 espécies de anuros no Núcleo Curucutu, 44 espécies no Núcleo São Sebastião, e 42 espécies no Núcleo Santa Virgínia, totalizando 65 espécies pertecentes a 12 famílias (número de espécies entre parênteses): Bufonidae (5), Brachycephalidae (6), Centrolenidae (1), Craugastoridae (1), Cycloramphidae (2), Hemiphractidae (1), Hylidae (29), Hylodidae (3), Leptodactylidae (12), Microhylidae (2), Odontophrynidae (2), e Phyllomedusidae (1). Esperamos que estas listas possam ser úteis para futuros estudos assim como auxiliar os planos de manejo e conservação destas áreas protegidas.

Palavras chaves:
Anfíbios; Biodiversidade; Conservação; Hotspots; Lista de espécies

Introduction

The Atlantic Forest, a global hotspot for biodiversity conservation (Mittermeier et al. 2004MITTERMEIER, R.A., GIL, P.R., HOFFMAN, M., PILGRIM, J., BROOKS, T., MITTERMEIER, C.G., LAMOREUX, J. & FONSECA, G.A.B. 2004. Hotspots revisited: earth’s biologically richest and most endangered terrestrial ecoregions. CEMEX & Agrupacion Sierra Madre, Cidade do México.), originally covered 1.3 million km2, of which between 84% and 89% have been converted to human use or degraded by human activities (Ribeiro et al. 2009RIBEIRO, M.C., METZGER, J.P., MARTENSER, A.C., PONZONI, F.J. & HIROTA, M.M. 2009. The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv. 142: 1141-1153.). This biome harbors one of the highest diversity of amphibians in the world, hosting approximately 600 species of amphibians (Haddad et al. 2013HADDAD, C.F.B., TOLEDO, L.F., PRADO, C.P.A., LOEBMANN, D., GASPARINI, J.L. & SAZIMA, I. 2013. Guide to the amphibians of the Atlantic Forest: diversity and biology. Anolis Books, São Paulo.). Although several protected areas have been created in this Neotropical biome over the past three decades, our knowledge of the amphibian species within these areas is still far from adequate. For example, the Parque Estadual da Serra do Mar (PESM) in the state of São Paulo, Brazil, is the largest protected area of the entire Atlantic Forest biome but some administrative areas such as Núcleo São Sebastião still do not have an amphibian survey published. This is worrisome because PESM harbors the highest amphibian diversity of the Atlantic Forest biome (Loyola et al. 2014LOYOLA, R.D., LEMES, P., BRUM, F.T., PROVETE, D.B. & DUARTE, D.S. 2014. Clade-specific consequences of climate change to amphibians in Atlantic Forest protected areas. Ecography 37: 65-72.). Here, we surveyed amphibian species of Núcleo Curucutu, Núcleo Santa Virgínia and Núcleo São Sebastião and present the first list of amphibian species for Núcleo São Sebastião. Natural history knowledge and species composition are the basic dataset for ecology, systematics, biogeography, and conservation biology (e.g., Collen et al. 2008COLLEN, B., RAM, M., ZAMIM, T. & McRae, L. 2008. The tropical biodiversity data gap: addressing disparity in global monitoring. Trop. Conserv. Sci. 1: 75-88., Da Silva et al. 2012DA SILVA, F.R., ALMEIDA-NETO, M., PRADO, V.H.M., HADDAD, C.F.B. & ROSSA-FERES, D.C. 2012. Humidity levels drive reproductive modes and phylogenetic diversity of amphibians in the Brazilian Atlantic Forest. J. Biogeogr. 39:1720-1732., 2014DA SILVA, F.R., ALMEIDA-NETO, M., ARENA, M.V.N. 2014. Amphibian beta diversity in the Brazilian Atlantic Forest: contrasting the roles of historical events and contemporary conditions at different spatial scales. PLoS ONE 9(10): e109642. doi:10.1371/journal.pone.0109642
https://doi.org/10.1371/journal.pone.010...
); therefore, we hope that our lists can be useful for future studies as well as helping in the management and conservation planning of these protected areas.

Material and Methods

1. Study area

The PESM (23°13'8.4”S and 24°5'42.0”S, 44°43'12.0”W and 46°33'50.4”W) is the largest protected area in the Atlantic Forest biome with 315,390 ha in the state of São Paulo, southeastern Brazil (Figure 1). Due to its large extension the PESM is managed by 11 administrative divisions named: Núcleo Bertioga, Núcleo Caminhos do Mar, Núcleo Caraguatatuba, Núcleo Cunha, Núcleo Curucutu, Núcleo Itariru, Núcleo Itutinga Pilões, Núcleo Padre Dória, Núcleo Picinguaba, Núcleo Santa Virgínia and Núcleo São Sebastião. In this study, we carried out species inventories in three of these localities (Figure 1): (i) Núcleo Curucutu (23°59'6.0”S and 46°44'34.8”W), with 12,029 ha is encompassed by four municipalities (Itanhaém, Juquitiba, Mongaguá and São Paulo) and altitudes varying from 15 to 870 m asl; (ii) Núcleo Santa Virgínia (23°21'3.6”S and 45°8'6.0”W), with 17,500 ha is encompassed by five municipalities (São Luiz do Paraitinga, Cunha, Caraguatatuba, Ubatuba and Natividade da Serra), and altitudes varying from 740 to 1620 m asl; and (iii) Núcleo São Sebastião (23°43'1.2”S and 45°42'10.8”W), with 26,268 ha is encompassed by the municipality of São Sebastião and altitudes varying from sea level to 1200 m asl.

Figure 1
Map of the state of São Paulo, Brazil, highlighting the area of the Parque Estadual da Serra do Mar and the location of Núcleo Curucutu, Núcleo São Sebastião and Núcleo Santa Virginia.

2. Survey techniques

In each of the three localities we sampled amphibian species in two ponds, two streams and two trails inside forest fragments (Table 1, Figure 2) from December 2014 to February 2015, December 2015 to February 2016 and December 2016 to February 2017 totalizing 27 days of field samplings in each sampling unit. We selected this period because is the time of the year when most of annual rainfall occurs and most anuran species are active. We sought to choose sampling units with similar size area and physiognomic characteristics in the three núcleos (Figure 2). We carried out the surveys on streams and trails inside forest fragments considering always the same extension of 100 m in all núcleos. Furthermore, we selected trails in which there were no water bodies along the extension sampled. We used three methods to record the presence of anurans in each locality: (i) surveys at breeding sites (Scott & Woodward 1994SCOTT JR., N.J., & WOODWARD, B.D. 1994. Standard techniques for inventory and monitoring: Surveys at Breeding Sites. In Measuring and monitoring biological diversity: standard methods for amphibians (W.R. Heyer, M.A. Donnelly, R.W. McDiarmid, L.C. Hayek & M.S Foster, eds). Smithsonian Institution Press, Washington, p.118-125.) - we recorded calling males from 19.00 hours to 24.00 hours; (ii) survey of larvae with dipnetting - we used a long and wire hand net (3 mm2 mesh size) along the margins of ponds and streams, sampling the available microhabitats from 12.00 hours to 18.00 hours; and (iii) visual encounter (Crump & Scott Jr. 1994CRUMP, M.L. & SCOTT JUNIOR, N.J. 1994. Visual encounter surveys. In Measuring and monitoring biological diversity: standard methods for amphibians (W.R. Heyer, M.A. Donnelly, R.W. McDiarmid, L.C. Hayek & M.S Foster, eds). Smithsonian Institution Press, Washington, p.84-92.) - we walked slowly for 30 minutes in trails inside the forest fragment, streams and around ponds looking at microhabitats for individuals hidden under trunks, bromeliads, stones, branches, and leaf litter. All collected specimens (Table 2) were anesthetized and killed, fixed in 10% formaldehyde and stored in 70% ethanol (adults) or 10% formaldehyde (tadpoles). We also collected tissue samples that were fixed in 100% ethanol and maintained in -20ºC in freezers (Table 2). All adult specimens and tissues samples are housed in the Coleção de Anfíbios Célio F. B. Haddad (CFBH), Departamento de Zoologia, Universidade Estadual Paulista, Rio Claro and Coleção de Anfíbios do Departamento de Zoologia e Botânica (DZSJRP), Universidade Estadual Paulista, São José do Rio Preto (Appendix 1). All collected tadpoles are housed in the Laboratório de Ecologia Teórica: Integrando Biologia, Espaço e Tempo (LET.IT.BE), Departamento de Ciências Ambientais, Universidade Federal de São Carlos, campus Sorocaba (Appendix 1).

Table 1
Geographical coordinates of sample units used in the survey of anurans in Núcleo Curucutu, Núcleo São Sebastião and Núcleo Santa Virgínia of the Parque Estadual da Serra do Mar, state of São Paulo, southeastern Brazil. Geographical coordinates in degrees, minutes and seconds, based on the WGS84 datum.
Figure 2
Photographies of ponds (a-b), streams (c-d) and trails inside forest fragments (e-f) used as sample units in the survey of anurans in the núcleos Curucutu, São Sebastião and Santa Virgínia of the Parque Estadual da Serra do Mar, state of São Paulo, southeastern Brazil.
Table 2
Anuran species composition and abundance from Núcleo Curucutu (PECU), Núcleo São Sebastião (PESB) and Núcleo Santa Virgínia (PESV) of the Parque Estadual da Serra do Mar, state of São Paulo, southeastern Brazil. STATUS IUCN = threatened species categories used in the IUCN Red List Data (IUCN 2016IUCN. 2016. The IUCN Red List of Threatened Species (Version 2015-4). Available online at: http://www.iucnredlist.org (last access in 21/04/2017).
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); STATUS BRAZIL = categories of threatened species used in the Brazil Red Book of Threatened Species of Fauna (ICMBio 2015ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade) 2015. Brazil Red Book of Threatened Species of Fauna. Ministério do Meio Ambiente. Available online at: http://www.icmbio.gov.br/portal/images/stories/comunicacao/publicacoes/publicacoes-diversas/dcom_sumario_executivo_livro_vermelho_da_fauna_brasileira_ameacada_de_extincao_2016.pdf (last access in 21/04/2017).
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); STATUS SÃO PAULO = categories of threatened species used in the São Paulo Red Book of Threatened Species of Fauna (Garcia et al. 2009GARCIA, P.C.A., SAWAYA, R.J., MARTINS, I.A., BRASILEIRO, C.A., VERDADE, V.K., JIM, J., SEGALLA, M.V., MARTINS, M., ROSSA-FERES, D.C., HADDAD, C.F.B., TOLEDO, L.F., PRADO, C.P.A., BERNECK, B.M. & ARAÚJO, O.G.S. 2009. Anfíbios. In Fauna ameaçada de extinção no Estado de São Paulo, Vertebrados (P.M. Bressan, M.C.M. Kierulff & A.M. Sugieda, eds). Governo do Estado de São Paulo, Secretaria do Meio Ambiente, Fundação Parque Zoológico de São Paulo, São Paulo, p.329-347.): DD (Data Deficient), LC (Least Concern) and CE (Critically Endangered). POP. TREND = current population trends used in IUCN Red List Data: increasing, decreasing, stable or unknown. * = species not evaluated or not cited. # Cryptic species: in this case, abundance was defined as only one species in the fieldwork.

3. Data Analysis

To assess the sampling efficiency of surveys separately for each locality, we used species accumulation curve (Gotelli & Colwell 2001GOTELLI, N.J & COLWELL, R.K. 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4: 379-391.) 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 27 samples. Considering the diverse richness estimators available, we chose to use the Jackknife algorithm first order based on its performance when compared to other estimators (Magurran 2004MAGURRAN, A.E. 2004. Measuring biological diversity. Blackwell Publishing Company, Oxford., Walther & Moore 2005WALTHER, B.A. & MOORE, J.L. 2005. The concepts of bias, precision and accuracy, and their use in testing the performance of species richness estimators, with a literature review of estimator performance. Ecography 28: 815-829., Hortal et al. 2006HORTAL, J., BORGES, P.A.V. & GASPARE, C. 2006. Evaluating the performance of species richness estimators: sensitivity to sample grain size. J. Anim. Ecol. 75: 274-287.). All analyzes were performed in R v 3.2.2 (R Core Team 2015R CORE TEAM 2015. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. (last access in 30/09/2016).
http://www.R-project.org...
) with 1,000 randomizations using vegan (Oksanen et al. 2016OKSANEN, J., BLANCHET, F.G., KINDT, R., LEGENDRE, P., MINCHIN, P.R., O'HARA, R.B., SIMPSON, G.L., SOLYMOS, P., STEVENS, M.H.H. & WAGNER, H. 2016. vegan: Community Ecology Package. R package version 2.3-3. https://CRAN.R-project.org/package=vegan (last access in 21/04/2017).
https://CRAN.R-project.org/package=vegan...
) and BiodiversityR (Kindt & Coe 2005KINDT, R. & COE, R. 2005. Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre (ICRAF), Nairobi. ISBN 92-9059-179-X.) packages. Taxonomic nomenclature follows Frost (2017)FROST, D.R. 2017. Amphibian species of the world: an Online Reference. Version 6.0. Eletronic Database accessible at http://research.amnh.org/herpetology/amphibia/index.html. American Museum of Natural History, New York, USA (last access in 10/05/2017).
http://research.amnh.org/herpetology/amp...
. The species conservation status was obtained from The International Union for Conservation of Nature Red List of Threatened Species (IUCN 2016IUCN. 2016. The IUCN Red List of Threatened Species (Version 2015-4). Available online at: http://www.iucnredlist.org (last access in 21/04/2017).
http://www.iucnredlist.org...
), Brazil Red Book of Threatened Species of Fauna (ICMBio 2015ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade) 2015. Brazil Red Book of Threatened Species of Fauna. Ministério do Meio Ambiente. Available online at: http://www.icmbio.gov.br/portal/images/stories/comunicacao/publicacoes/publicacoes-diversas/dcom_sumario_executivo_livro_vermelho_da_fauna_brasileira_ameacada_de_extincao_2016.pdf (last access in 21/04/2017).
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) and Faunal Species of São Paulo state Threatened with Extinction (Garcia et al. 2009GARCIA, P.C.A., SAWAYA, R.J., MARTINS, I.A., BRASILEIRO, C.A., VERDADE, V.K., JIM, J., SEGALLA, M.V., MARTINS, M., ROSSA-FERES, D.C., HADDAD, C.F.B., TOLEDO, L.F., PRADO, C.P.A., BERNECK, B.M. & ARAÚJO, O.G.S. 2009. Anfíbios. In Fauna ameaçada de extinção no Estado de São Paulo, Vertebrados (P.M. Bressan, M.C.M. Kierulff & A.M. Sugieda, eds). Governo do Estado de São Paulo, Secretaria do Meio Ambiente, Fundação Parque Zoológico de São Paulo, São Paulo, p.329-347.).

Results and Discussion

We recorded 34 species in Núcleo Curucutu, 44 species in Núcleo São Sebastião and 42 species in Núcleo Santa Virgínia (Tabela 2, Figures 3, 4, 5, 6), totalizing 65 anuran species belonging to 12 families (number in parentheses): Bufonidae (5), Brachycephalidae (6), Centrolenidae (1), Craugastoridae (1), Cycloramphidae (2), Hemiphractidae (1), Hylidae (29), Hylodidae (3), Leptodactylidae (12), Microhylidae (2), Odontophrynidae (2) and Phyllomedusidae (1). From the 65 species recorded, 20 species (30.7%) occurred in the three núcleos, 14 species (21.5%) occurred in two núcleos, eight species (12.3%) occurred only at Núcleo Curucutu, nine species (13.8%) occurred only at Núcleo Santa Virgínia and 14 species (21.5%) occurred only at Núcleo São Sebastião (Table 2). The observed species richness was smaller than the estimated species richness (Figure 7), indicating that 4.8 more species could be recorded at núcleos Curucutu, 6.7 more species at Núcleo Santa Virgínia and 5.7 more species at the Núcleo São Sebastião if we increase the sampling effort or utilize other sampling methods (e.g., pitfall traps). For example, Malagoli (2008MALAGOLI, L.R. 2008. Anfíbios do município de São Paulo: histórico, conhecimento atual e desafios para a conservação. In Além do concreto: contribuições para a proteção da biodiversidade paulistana (L.R. Malagoli, F.B. Bajesteiro & M. Whately, eds). Instituto Socioambiental, São Paulo, p.204-231., 2013MALAGOLI, L.R. 2013. Diversidade e distribuição dos anfíbios anuros do núcleo Curucutu, Parque Estadual da Serra do Mar, SP. Dissertação de mestrado, Instituto de Biociências, Universidade Estadual Paulista, Rio Claro.) using data gathered from fieldwork, scientific collection and grey literature recorded 66 anuran species to Núcleo Curucutu. Giasson (2008)GIASSON, L.O.M. 2008. Atividade sazonal e uso do ambiente por anfíbios da Mata Atlântica no alto da Serra do Mar. Tese de doutorado, Instituto de Biociências da Universidadade Estadual Paulista “Júlio de Mesquita Filho”, Rio Claro. carried out 25 excursions to Núcleo Santa Virgínia from January 2003 to December 2006 and recorded 50 anuran species. However, we are aware that these studies used different sampling efforts and their results are not comparable to species richness observed in our study.

Figure 3
Anuran species recorded at the Parque Estadual da Serra do Mar, Núcleo Curucutu, Núcleo São Sebastião and Núcleo Santa Virgínia, state of São Paulo, southeastern Brazil. a = Rhinella icterica, b = R. hoogmoedi, c = R. ornata, d = Dendrophryniscus brevipollicatus, e = Brachycephalus pitanga, f = Ischnocnema gr. guentheri (CS1 lineage Gehara et al. 2013GEHARA, M., CANEDO, C., HADDAD, C.F.B. & VENCES, M. 2013. From widespread to microendemic: molecular and acoustic analyses show that Ischnocnema guentheri (Amphibia: Brachycephalidae) is endemic to Rio de Janeiro, Brazil. Conserv. Genet. 14: 973-982.), g = Ischnocnema gr. guentheri (CS4 lineage Gehara et al. 2013GEHARA, M., CANEDO, C., HADDAD, C.F.B. & VENCES, M. 2013. From widespread to microendemic: molecular and acoustic analyses show that Ischnocnema guentheri (Amphibia: Brachycephalidae) is endemic to Rio de Janeiro, Brazil. Conserv. Genet. 14: 973-982.), h = I. henselii, i = I. parva, j = Haddadus binotatus, k = Proceratophrys melanopogon, l = Cycloramphus boraceiensis, m = Hylodes asper, n = H. phyllodes and o = Thoropa taophora.
Figure 4
Anuran species recorded at the Parque Estadual da Serra do Mar, Núcleo Curucutu, Núcleo São Sebastião and Núcleo Santa Virgínia, state of São Paulo, southeastern Brazil. p = Megaelosia cf. bocainensis, q = Adenomera marmorata, r = Adenomera sp., s = Leptodactylus furnarius, t = L. fuscus, u = L. latrans, v = Physalaemus atlanticus, w = P. bokermanni, x = P. cuvieri, y = P. olfersii, z = Paratelmatobius cardosoi, a1 = Chiasmocleis leucosticta, b1 = Myersiela microps, c1 = Fritziana sp. (aff. fissilis) and d1 = Phrynomedusa dryade.
Figure 5
Anuran species recorded at the Parque Estadual da Serra do Mar, Núcleo Curucutu, Núcleo São Sebastião and Núcleo Santa Virgínia, state of São Paulo, southeastern Brazil. e1 = Aplastodiscus leucopygius, f1 = Bokermannohyla circumdata, g1 = B. hylax, h1 = B. izecksohni, i1 = Dendropsophus berthalutzae, j1 = D. elegans, k1 = D. microps, l1 = D. minutus, m1 = D. seniculus, n1 = Boana albomarginata, o1 = B. albopunctata, p1 = B. bandeirantes, q1 = B. bischoffi, r1 = B. faber and s1 = B. pardalis.
Figure 6
Anuran species recorded at the Parque Estadual da Serra do Mar, Núcleo Curucutu, Núcleo São Sebastião and Núcleo Santa Virgínia, state of São Paulo, southeastern Brazil. t1 = B. semilineata, u1 = Ololygon argyreornata, v1 = O. littoralis, w1 = O. perpusilla, x1 = O. rizibilis, y1 = Scinax crospedospilus, z1 = S. fuscovarius, a2 = S. hayii, b2 = S. perereca, c2 = S. tymbamirim, d2 = Trachycephalus imitatrix, e2 = T. mesophaeus and f2 = Vitreorana uranoscopa.
Figure 7
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 2017 at the Parque Estadual da Serra do Mar, Núcleo Curucutu, Núcleo São Sebastião and Núcleo Santa Virgínia, state of São Paulo, southeastern Brazil. The dots show the mean generated by 1000 randomizations and the vertical bars indicate the standard deviation.

According to the threatened species categories used in IUCN (2016)IUCN. 2016. The IUCN Red List of Threatened Species (Version 2015-4). Available online at: http://www.iucnredlist.org (last access in 21/04/2017).
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, Bokermannohyla izecksohni is classified as critically endangered, Physalaemus atlanticus is classified as vulnerable, Adenomera ajurauna, Megaelosia cf. bocainensis, Paratelmatobius cardosoi and P. bokermanni are classified as data deficient and other anuran species are classified as least concern (Table 2).On the other hand, considering threatened species categories used in the Brazilian (ICMBio 2015ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade) 2015. Brazil Red Book of Threatened Species of Fauna. Ministério do Meio Ambiente. Available online at: http://www.icmbio.gov.br/portal/images/stories/comunicacao/publicacoes/publicacoes-diversas/dcom_sumario_executivo_livro_vermelho_da_fauna_brasileira_ameacada_de_extincao_2016.pdf (last access in 21/04/2017).
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) and state of São Paulo (Garcia et al. 2009GARCIA, P.C.A., SAWAYA, R.J., MARTINS, I.A., BRASILEIRO, C.A., VERDADE, V.K., JIM, J., SEGALLA, M.V., MARTINS, M., ROSSA-FERES, D.C., HADDAD, C.F.B., TOLEDO, L.F., PRADO, C.P.A., BERNECK, B.M. & ARAÚJO, O.G.S. 2009. Anfíbios. In Fauna ameaçada de extinção no Estado de São Paulo, Vertebrados (P.M. Bressan, M.C.M. Kierulff & A.M. Sugieda, eds). Governo do Estado de São Paulo, Secretaria do Meio Ambiente, Fundação Parque Zoológico de São Paulo, São Paulo, p.329-347.) lists, B. izecksohni, Cycloramphus boraceiensis, Trachycephalus imitatrix and Megaelosia cf. bocainensis are classified as data deficient and other anuran species are classified as least concern (Table 2). Considering the trend populations of IUCN (2016)IUCN. 2016. The IUCN Red List of Threatened Species (Version 2015-4). Available online at: http://www.iucnredlist.org (last access in 21/04/2017).
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, 14 species have declining populations (Ischnocnema parva, Vitreorana uranoscopa, C. boraceiensis, B. izecksohni, B. circumdata, B. hylax, Ololygon littoralis, Ololygon cf. obtriangulata, O. rizibilis, T. imitatrix, T. mesophaeus, Hylodes phyllodes, P. bokermanni and Proceratophrys melanopogon), and other six species have unknown population trends (I. henselli, Scinax perereca, Megaelosia cf. bocainensis, P. cardosoi, P. atlanticus and Rhinella hoogmoedi) (Table 2). It is important to recognize that IUCN trend populations it is not consensual among researchers and it may contain imprecisions. For example, the populations of widespread species with recognized tolerance to anthropogenic habitats such as T. mesophaeus probably may not be declining (Carvalho-e-Silva & Garcia 2004CARVALHO-E-SILVA, S.P. & GARCIA, P. 2004.Trachycephalus mesophaeus. The IUCN Red List of Threatened Species 2004: e.T55822A11372732.http://dx.doi.org/10.2305/IUCN.UK.2004.RLTS.T55822A11372732.en (last access in 29/03/2017)
http://dx.doi.org/10.2305/IUCN.UK.2004.R...
).

We registered 1282 individuals being that Ololygon perpusillus and Boana albopunctata were the most abundant species at Núcleo Curucutu (Figure 8B), Ischnocnema parva and Dendropsophus microps were the most abundant species at Núcleo Santa Virgínia (Figure 8C) and Adenomera marmorata and Ololygon littoralis were the most abundant species at Núcleo São Sebastião (Figure 8D). Most anuran species were recorded more than once during the sampling period; however, Thoropa taophora, B. izecksohni, O. argyreornata, Ololygon cf. obtriangulata, T. mesophaeus, Megaelosia cf. bocainensis and R. hoogmoedi were recorded on only one occasion based on a single individual (Figure 8A). Except for Megaelosia cf. bocainensis whose natural history and population trend are unknown, Thoropa taophora, B. izecksohni, O. argyreornata, Ololygon cf. obtriangulata, T. mesophaeus and R. hoogmoedi are common species that reproduce during one or few days along the year (i.e. explosive breeding). Therefore, the low abundance recorded for these species probably is due to sampling effort. Information about species richness and composition are the basic dataset for ecology, systematics, biogeography and conservation biology (e.g., Collen et al. 2008COLLEN, B., RAM, M., ZAMIM, T. & McRae, L. 2008. The tropical biodiversity data gap: addressing disparity in global monitoring. Trop. Conserv. Sci. 1: 75-88., Da Silva et al. 2012DA SILVA, F.R., ALMEIDA-NETO, M., PRADO, V.H.M., HADDAD, C.F.B. & ROSSA-FERES, D.C. 2012. Humidity levels drive reproductive modes and phylogenetic diversity of amphibians in the Brazilian Atlantic Forest. J. Biogeogr. 39:1720-1732., 2014DA SILVA, F.R., ALMEIDA-NETO, M., ARENA, M.V.N. 2014. Amphibian beta diversity in the Brazilian Atlantic Forest: contrasting the roles of historical events and contemporary conditions at different spatial scales. PLoS ONE 9(10): e109642. doi:10.1371/journal.pone.0109642
https://doi.org/10.1371/journal.pone.010...
) as well as they are relevant to subsidize management plans and conservation strategies. Therefore, we hope that these lists can be useful for future studies as well as helping in the management and conservation planning of these protected areas.

Figure 8
Relative abundance of anuran species (%) observed at the Parque Estadual da Serra do Mar, state of São Paulo, southeastern Brazil. (A) sum of all individuals observed at the Núcleo Curucutu, Núcleo Curucutu and Núcleo Santa Virgínia; (B) individuals observed only at the Núcleo Santa Virgínia; (C) individuals observed only at the Núcleo São Sebastião; (D) individuals observed only at the Núcleo São Sebastião. The total number of recorded individuals per species is indicated above each column. Anuran species: Rict, Rhinella icterica; Rhoog, R. hoogmoedi; Rorn, R. ornata; Dbre, Dendrophryniscus brevipollicatus; Bpit, Brachycephalus pitanga; Igue1, Ischnocnema gr. guentheri (CS1 lineage Gehara et al. 2013GEHARA, M., CANEDO, C., HADDAD, C.F.B. & VENCES, M. 2013. From widespread to microendemic: molecular and acoustic analyses show that Ischnocnema guentheri (Amphibia: Brachycephalidae) is endemic to Rio de Janeiro, Brazil. Conserv. Genet. 14: 973-982.); Igue3, I. gr. guentheri (CS3 lineage Gehara et al. 2013GEHARA, M., CANEDO, C., HADDAD, C.F.B. & VENCES, M. 2013. From widespread to microendemic: molecular and acoustic analyses show that Ischnocnema guentheri (Amphibia: Brachycephalidae) is endemic to Rio de Janeiro, Brazil. Conserv. Genet. 14: 973-982.); Igue4, I. gr. guentheri (CS4 lineage Gehara et al. 2013GEHARA, M., CANEDO, C., HADDAD, C.F.B. & VENCES, M. 2013. From widespread to microendemic: molecular and acoustic analyses show that Ischnocnema guentheri (Amphibia: Brachycephalidae) is endemic to Rio de Janeiro, Brazil. Conserv. Genet. 14: 973-982.); Ihen, I. henselii; Ipar, I. parva, Hbin, Haddadus binotatus; Pmel, Proceratophrys melanopogon; Cbor, Cycloramphus boraceiensis; Hasp, Hylodes asper; Hphy, H. phyllodes; Ttao, Thoropa taophora; Mboc, Megaelosia cf. bocainensis; Amar, Adenomera marmorata; Aden.sp, Adenomera sp.; Lfur, Leptodactylus furnarius; Lfus, L. fuscus; Llat, L. latrans; Patl, Physalaemus atlanticus; Pbok, P. bokermanni; Pcuv, P. cuvieri; Polf, P. olfersii; Pcar, Paratelmatobius cardosoi; Cleu, Chiasmocleis leucosticta; Mmic, Myersiela microps; Frit.sp, Fritziana sp. (aff. fissilis); Pdry, Phrynomedusa dryade; Aleu, Aplastodiscus leucopygius; Bcir, Bokermannohyla circumdata; Bhyl, B. hylax; Bize, B. izecksohni; Dber, Dendropsophus berthalutzae; Dele, D. elegans; Dmic, D. microps; Dmin, D. minutus; Dsen, D. seniculus; Balbm, Boana albomarginata; Balbp, B. albopunctata; Bban, B. bandeirantes; Bbis, B. bischoffi; Bfab, B. faber; Bpar, B. pardalis; Bsem, B. semilineata; Oarg, Ololygon argyreornata; Olit, O. littoralis; Oper, O. perpusilla; Oriz, O. rizibilis; Scro, Scinax crospedospilus; Sfus, S. fuscovarius; Shay, S. hayii; Sper, S. perereca; Stym, S. tymbamirim; Timi, Trachycephalus imitatrix; Tmes, T. mesophaeus; Vura, Vitreorana uranoscopa.

Supplementary material

The following online material is available for this article:

Appendix 1:Vouchers of anurans collected at núcleos Curucutu, São Sebastião and Santa Virgínia of the Parque Estadual da Serra do Mar state of São Paulo, southeastern Brazil. VOUCHER AND TISSUES = register number of the Coleção de Anfíbios Célio F. B. Haddad, Departamento de Zoologia, Universidade Estadual Paulista, Rio Claro (CFBH); Coleção de Anfíbios do Departamento de Zoologia e Botânica, Universidade Estadual Paulista, São José do Rio Preto (DZSJRP); Laboratório de Ecologia Teórica:Integrando Biologia, Espaço e Tempo (LET.IT.BE), Departamento de Ciências Ambientais, Universidade Federal de São Carlos, campus Sorocaba (FRS). * Species recorded by vocalization in the fieldwork.

Acknowledgements

We thank the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) for providing collection permits (SISBIO/41282-1) and the Instituto Florestal de São Paulo for the permission to perform the study in the Parque Estadual da Serra do Mar, núcleos Curucutu, São Sebastião and Santa Virgínia (Proc. 260108-004.608/2014). We thank all the staff of the núcleos Curucutu, São Sebastião and Santa Virgínia for helping us during fieldworks. FRS thanks São Paulo Research Foundation (FAPESP - grant #2013/50714-0) for financial support. MLL thanks FAPESP and Coordenação de Aperfeiçoamento de Pessoal do Nível Superior (CAPES) for postdoctoral fellowships (grants #2010/50124-0; 88881.062205/2014-01). CFBH thanks Fundação Grupo Boticário de Proteção à Natureza and FAPESP (grants #2013/50741-7 and #2014/50342-8) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq – Proc. 302518/2013-4) for a research fellowship. DCRF thanks CNPq (Proc. 303522/2013-5).

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Publication Dates

  • Publication in this collection
    2017

History

  • Received
    19 Oct 2016
  • Reviewed
    18 May 2017
  • Accepted
    17 June 2017
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