Natália Dallagnol Vargas¹, *, Michelle Abadie¹, Patrick Colombo², Juliana Conte Zanotelli¹ and Márcio Borges-Martins¹

Herpetology Notes, volume 10: 397-402 (2017) (published online on 22 July 2017) New records and geographic distribution of the torrent frog Hylodes meridionalis (Mertens, 1927) (Amphibia, Anura, Hylodidae), an endemic anuran from the Atlantic Rainforest in southern Brazil Natália Dallagnol Vargas¹, *, Michelle Abadie¹, Patrick Colombo², Juliana Conte Zanotelli¹ and Márcio Borges-Martins¹ The knowledge on the geographical distribution is usually the only information available to assess the conservation status of many species (e.g. Fontana et al., 2003; Machado et al., 2008). This is particularly relevant for species with restrict distribution or few available data about its biology (IUCN, 2015). Torrent frogs of the genus Hylodes Fitzinger, 1826 occur mainly associated with high-gradient streams in Brazilian Atlantic Forest (Haddad and Pombal, 1995; Frost, 2015), which is one of the most endangered biodiversity hotspots in the world (Myers et al., 2000). Hylodes meridionalis (Mertens, 1927) is endemic to the mountain slopes of the Serra Geral, along the southernmost portion of the Atlantic Rainforest. The species lives only in well-preserved forested areas, inhabiting streams and cascades with clear running water (Kwet and Di-Bernardo, 1999). Global population trend is supposed to be decreasing due to water pollution, deforestation, and Batrachochytrium dendrobatidis infection (Garcia and Segalla, 2010; Toledo et al., 2006). Previous records are known for the Brazilian municipalities of Cambará do Sul, Canela, Caxias do Sul, Gramado, Itati, Maquiné, São Francisco de Paula (type locality), Terra de Areia and Torres in 1 Laboratório de Herpetologia, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Avenida Bento Gonçalves 9500, Agronomia, CEP 91501-970, Porto Alegre, Rio Grande do Sul, Brazil 2 Museu de Ciências Naturais, Fundação Zoobotânica do Rio Grande do Sul, Rua Dr. Salvador França 1427, Jardim Botânico, CEP 90690-000, Porto Alegre, RS, Brazil * Corresponding author e-mail: nataliadvargas@gmail.com the state of Rio Grande do Sul, Brazil (Mertens, 1927; Braun and Braun, 1980; Kwet and Di-Bernardo, 1999; Pombal et al., 2002; Vilella et al., 2004; Deiques et al., 2007; Lima and Colombo, 2008; Lema and Martins, 2011; Lingnau et al., 2013) and municipalities of Bom Jardim da Serra, Lauro Müller, Praia Grande, Timbé do Sul, Treviso and Urussanga in the state of Santa Catarina (Pombal et al., 2002; Toledo et al., 2006; Lucas, 2008). Recent field expeditions revealed the occurrence of Hylodes meridionalis in several new localities, suggesting the need for a revision of its known geographical distribution. Three herpetological collections from Rio Grande do Sul state were revised in order to confirm identity and search for additional specimens: Coleção Herpetológica da Universidade Federal do Rio Grande do Sul (UFRGS), Museu de Ciências e Tecnologia da Pontifícia Universidade Católica do Rio Grande do Sul (MCP) e Museu de Ciências Naturais da Fundação Zoobotânica do Rio Grande do Sul (MCN). We also compiled all published records of H. meridionalis with voucher specimens deposited in scientific collections (Appendix I and Appendix II). New records were obtained for eight localities in Rio Grande do Sul state (Table 1 and Figure 1). Additionally, we found a wrong record and two doubtful ones of Hylodes meridionalis, respectively: 1) Parque Estadual de Itapuã, in the municipality of Viamão, Rio Grande do Sul (MZUSP.89938 and MZUSP.89939 after Canedo, 2008). Actually these records refer to individuals donated from the Museum of Zoology of the Universidade de Campinas (ZUEC) to the Museum of Zoology of the Universidade de São Paulo (MZUSP). The original locality was São Francisco de Paula, according to ZUEC collection (T. Grant personal observation). 2) Passo do Vigário, in the

398 Natália Dallagnol Vargas et al. Figure 1. Distribution map of the torrent frog Hylodes meridionalis. The wrong record (white square) correspond to Parque Estadual de Itapuã, in the municipality of Viamão (MZUSP.89938 and MZUSP.89939). The two doubtful records (dark squares, from south to north) correspond to Passo do Vigário, in the municipality of Viamão (MCN.1890 and MCN.1893) and Parque Estadual da Guarita, in the municipality of Torres (MCN.8495). municipality of Viamão (MCN.1890 and MCN.1893). The two specimens from Viamão (one is currently in the Museu de Ciências Naturais da Fundação Zoobotânica do Rio Grande do Sul [MCN.1890] and the other [MCN.1893] was donated to Harold Dundee of. 35/66- USA) were obtained from the didactic collection of the Escola Estadual Técnica de Agricultura (State School of Technical Agriculture, EETA) in the municipality of Viamão, Rio Grande do Sul. EETA s collection is not a scientific collection and has specimens from various locations around the world, many without or with doubtful collection and location data. 3) Parque Estadual da Guarita, in the municipality of Torres (MCN.8495). The specimen supposedly from Torres, also deposited in the Museu de Ciências Naturais da Fundação Zoobotânica do Rio Grande do Sul, probably has a wrong locality data, since there are other individuals, housed in the MCN collection, from different species collected in the municipality of Canela, Rio Grande do Sul, by the same collector (Pedro Braun) in the same date (1974). The last two records are additionally doubtful because there are no suitable habitats (streams inside primary or secondary advanced forests) to support the presence of H. meridionalis. Besides, sampling effort in localities around these two records, in the last five years, have not revealed the presence of the species. Moreover, these records were not considered by Pedro and Cristina Braun (1980), MCN collection managers, in their preliminary list of amphibians from Rio Grande do Sul (Braun and Braun, 1980), which suggests that they detected these mistakes, or the errors may have been produced after they left the collection management.

New records and geographic distribution of Hylodes meridionalis in Brazil 399 Figure 2. Morphological variation in Hylodes meridionalis from different localities in the state of Rio Grande do Sul, Brazil: A and B) Fraga, Rio dos Sinos upstream, Caraá; C) UHE (Usina Hidrelétrica) 14 de Julho, Rio das Antas, Cotiporã; D) FLONA (Floresta Nacional) de São Francisco de Paula; E) Guaporé; F) Arroio Humaitá, Itati. Photos: N.D. Vargas (A); P. Colombo (B); T.S. Kunz (C); A. Jeckel (D); M. Abadie (E); L.F.M. da Fonte (F). The new locality in Guaporé represents the westernmost record, extending the known distribution of this species about 70 kilometers to the west. The new records corroborate previous suggestions that H. meridionalis lives in first and second order streams in the Atlantic Forest of Serra do Mar, inland Atlantic Forest and Araucaria Forest (Garcia et al., 2007). Ignoring the doubtful records, the species occurs in forested areas of Atlantic Rainforest biome from Bom Jardim da Serra in Santa Catarina to Caraá in Rio Grande do Sul. However, the northern distribution limit of H. meridionalis is not clearly defined and we are aware that other species of this genus distributed in Santa Catarina also show no well-defined southern distribution boundaries.

400 Natália Dallagnol Vargas et al. Table 1. Locality, coordinates (from collection sites, unless differently stated) and voucher specimens of the new records of Hylodes meridionalis from Rio Grande do Sul (RS), southern Brazil. Locality Coordinates (lat/long) Voucher Fraga, Rio dos Sinos upstream, Caraá 29.6997 S/ 50.2955 W UFRGS.6012, MCP.12070 UHE (Usina Hidrelétrica) 14 de Julho, Rio das Antas, Cotiporã 29.0289 S/ 51.6681 W UFRGS.3924 UFRGS.3925 UFRGS.6088 Guaporé 28.8504 S/ 51.8352 W UFRGS.5126 UFRGS.5334 UFRGS.5335 Arroio Humaitá, Itati 29.3700 S/ 50.1819 W UFRGS.2636 UFRGS.3937 UFRGS.3938 UHE (Usina Hidrelétrica) Castro Alves, Rio das Antas and nearby areas, Nova Roma do Sul Cascata da Pedra Branca, Boa União Distric, Três Forquilhas PCH (Pequena Central Hidrelétrica) Jararaca, Rio da Prata, Veranópolis PCH (Pequena Central Hidrelétrica) da Ilha, Vila Flores 28.9856 S/ 51.3734 W 28.9856 S/ 51.3735 W 28.9542 S/ 51.3826 W 29.3956 S/ 50.0447 W 28.9344 S/ 51.4695 W 28.8913 S/ 51.4561 W (Coordinates from the Dam) UFRGS.3934 UFRGS.3935 UFRGS.4591 UFRGS.4592 UFRGS.2726 MCP.12119 UFRGS.3877 MCP.9917 MCP.9938 Furthermore, we observed a great morphological variation in dorsal, lateral and ventral of the analysed specimen from Rio Grande do Sul state, not yet reportet to Hylodes meridionalis (Figure 2). Hence, we recommend a review of the specimens collected in Santa Catarina. Four new records for the northwest of Rio Grande do Sul were obtained during surveys that were part of the licensing process for the building of hydroelectric power plants. The construction of these hydroelectric plants can represent an important threat to the species survival, because it converts a lotic aquatic environment into a lentic environment, unsuitable for the survival of Hylodes species. Other threats, like water pollution and deforestation of native environments, have been detected around the localities where the records were compiled. Furthermore, there are populations of H. meridionalis diagnosed with the chitrid fungus, which is directly linked with global anuran population declines (James et al., 2015). With the data presented in this short note, we believe that is possible to contribute with the enhancement of the conservation status of this species. Acknowledgements. We thank T. Grant for reviewing locality data from MZUSP specimens; G. M. Pontes and M. F. Renner for allowing access to the herpetological collections of Museu de Ciências e Tecnologia da Pontifícia Universidade Católica do Rio Grande do Sul (MCP/PUCRS) and Museu de Ciências Naturais da Fundação Zoobotânica do Rio Grande do Sul (MCN/FZB), respectively; C. Zank and L. F. M. da Fonte helped in the revision of MCN specimens l; D. B. Provete and M. D. Freire provided the original description of H. meridionalis; M. Solé for the pre peer review and the valuable comments. References Braun, P.C., Braun, C.A.S. (1980): Lista prévia dos anfíbios do Estado do Rio Grande do Sul, Brasil. Iheringia, Série Zoológica 56: 121-146. Canedo, C.C. (2008): Revisão Taxonômica de Hylodes Fitzinger, 1826 (Anura, Hylodidae). Unpublished PhD thesis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil. Deiques, C.H., Stahnke, L.F., Reinke, M., Schmitt, P. (2007): Guia ilustrado dos anfíbios e répteis do Parque Nacional de Aparados da Serra, Rio Grande do Sul, Santa Catarina, Brasil. Pelotas, Brazil, USEB. Fontana, C.S., Bencke, G.A., Reis, R.E. (2003): Livro Vermelho da Fauna Ameaçada de Extinção no Rio Grande do Sul. Porto Alegre, Brazil, EPECE. Frost, D.R. (2015): Amphibian Species of the World, version 5.6. American Museum of Natural History, New York, USA. Electronic Database available at http://research.amnh.org/ herpetology/amphibia/index.html. Accessed on 15 May 2015. Garcia, P, Segalla, M.V. (2010): Hylodes meridionalis. n: IUCN 2015. IUCN Red List of Threatened Species. ersion 2014.3. <www.iucnredlist.org>. Accessed on 10 May 2015.

New records and geographic distribution of Hylodes meridionalis in Brazil 401 Garcia, P.C.A., Lavilla, E., Langone, J., Segalla, M.V. (2007): Anfíbios da Região Subtropical da América do Sul, Padrões de Distribuição. iência & Ambiente 35: 65-100. Haddad, C.F.B., Pombal, J.P.Jr. (1995): A new species of Hylodes from Southeastern Brazil (Amphibia: Leptodactylidae). Herpetologica 51: 279 286. IUCN (2015). The IUCN Red List of Threatened Species. Version 2015.3. <http://www.iucnredlist.org>. Accessed on 10 May 2015. James, T.Y., Toledo, L.F., Rödder, D., Leite, D.S., Belasen, A., Betancourt-Román, C.M., Jenkinson, T.S., Lambertini, C., Longo, A.V., Ruggeri, J., Collins, J.P., Burrowes, P., Lips, K.R., Zamudio, K.R., Longcore, J.E. (2015): Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: Lessons from the first 15 years of amphibian chytridiomycosis research. Ecology and Evolution 5(18): 4079-97. Kwet, A., Di-Bernardo, M. (1999): Pró-Mata Anfíbios Amphibien Amphibians. Porto Alegre, Brazil, EDIPUCRS. Lema, T. de, Martins, L.A. (2011): Anfíbios do Rio Grande do Sul Catálogo, diagnoses, distribuição, iconografia. Porto Alegre, Brazil, EDIPUCRS. Lima, A.F.B., Colombo, P. (2008): Observação do comportamento predatório de Liophis miliaris orinus (Serpentes, Colubridae) em Hylodes meridionalis (Anura, Hylodidae), Serra Geral, Rio Grande do Sul, Brasil. Revista Brasileira de Zoociências 10: 73-76. Lingnau, R., Zank, C., Colombo, P., Kwet, A. (2013): Vocalization of Hylodes meridionalis (Mertens 1927) (Anura, Hylodidae) in Rio Grande do Sul, Brazil, with comments on nocturnal calling in the family Hylodidae. Studies on Neotropical Fauna and Environment 48(1): 76-80. Lucas, E.M. (2008): Diversidade e conservação de anfíbios anuros no Estado de Santa Catarina, sul do Brasil. Unpublished PhD thesis, Universidade de São Paulo, São Paulo, Brazil. Machado, A.B.M., Drummond, G.M., Paglia, A.P. (2008): Livro Vermelho da Fauna Brasileira Ameaçada de Extinção, 1st Edition. Brasília, Brazil, Ministério do Meio Ambiente, Fundação Biodiversitas. Mertens, R. (1927): Neue Froschlurch aus Rio Grande do Sul, Brasilien. Blätter für Aquarien- und Terrarienkunde 38(2): 26-30. Myers, N., Mittermeier, R.A., Mittermeier, C.G., Fonseca, G.A.B., Kent, J. (2000): Biodiversity hotspots for conservation priorities. Nature 408: 853 858. Pombal, J.P.Jr., Feio, R.N., Haddad, C.F.B. (2002): A new species of torrent frog genus Hylodes (Anura: Leptodactylidae) from southeastern Brazil. Herpetologica 58: 462 471. Toledo, L.F., Britto, F.B., Araújo, O.G.S., Giasson, L.M.O., Haddad, C.F.B. (2006): The occurrence of Batrachochytrium dendrobatidis in Brazil and the inclusion of 17 new cases of infection. South American Journal of Herpetology 1(3): 185-191. Vilella, F.S., Becker, F.G., Hartz, S.M., Barbieri, G. (2004): Relation between environmental variables and aquatic megafauna in a first order stream of the Atlantic Forest, southern Brazil. Hydrobiologia 528: 17-30.

402 Natália Dallagnol Vargas et al. Appendix I List of additional specimens of Hylodes meridionalis with their coordinates and the voucher numbers. RIO GRANDE DO SUL: municipality of Cambará do Sul, without locality 29.0478 S/ 50.1447 W these coordinates are from city proper of municipality of Cambará do Sul (MCN 6964), Faxinalzinho (MCN 1164, 1184), Itaimbezinho (MCN 11283, 11288, 11294, 11296, 11298); municipality of Canela, without locality 29.3656 S/ 50.8156 W these coordinates are from city proper of municipality of Canela (MCP 309; MCN 1969); municipality of Caxias do Sul, without locality 29.1681 S/ 51.1794 W (MCN 9938); municipality of Cotiporã, without locality 29.0038 S/ 51.6822 W (UFRGS 6088), UHE 14 de Julho, Antas River 29.0289 S/ 51.6681 W (UFRGS 3924-25); municipality of Gramado, Horto-Florestal Alfredo Renner 29.3786 S/ 50.8739 W these coordinates are from city proper of municipality of Gramado (MCN 9818-21); municipality of Itati, without locality 29.3838 S/ 50.1880 W (UFRGS 2500-01), 29.3797 S/ 50.1872 W (UFRGS 2020-22), without coordinates (MCP 9531-34, 9536); municipality of Maquiné, Barra do Ouro, Carvão creek 29.54 S/ 50.23 W (UFRGS 2074-76, 2078, 2079), RPPN (Reserva Particular do Patrimônio Natural) Águas do Garapiá, 29.5004 S/ 50.2187 W (UFRGS 6779); municipality of São Francisco de Paula, Boca da Serra (MCN 841), Hotel Parque Veraneio Hampel 29.4430 S/ 50.6110 W (MCN 6628-30, 7490-95, 7555-62, 7565-85, 7602-07, 7702-06, 7708-13, 7715-32, 8266-74, 11215-17, 12397), Lagoas (MCN 8625, 8638; UFRGS 662, 678, 816), road to Lagoas (MCN 5075, 5084, 5085), without locality 29.4500 S/ 50.2166 W (MCP 10711-13), 29.4213 S/ 50.3769 W (MCP 11022), 29.3727 S/ 50.1880 W (MCP 11546, 11547), 29.4511 S/ 50.5577 W (MCP 11982, 11983), without coordinates (MCN 824, 825, 827, 831, 833, 835, 840, 4676, 12632-38; MCP 2495, 2576, 4950, 7194, 7248, 7249, 7251, 7253-55, 7265, 8316-22, 9535, 9893, 9894); municipality of Terra de Areia, without locality 29.5853 S/ 50.0708 W these coordinates are from city proper of municipality of Terra de Areia (MCP 1653, 1659, 1660). SANTA CATARINA: municipality of Lauro Müller, Serra Rio do Rastro 28.3984 S/ 49.5504 W these coordinates are taken from free software Google Earth (MCP 12329-31, 12333); municipality of Timbé do Sul, without locality 28.8303 S/ 49.8472 W these coordinates are from city proper of municipality of Timbé do Sul (MCP 3314); municipality of Urussanga, without locality 28.5018 S/ 49.3798 W (UFRGS 2608, 2611). Appendix 2 List of additional literature records (not seen) of Hylodes meridionalis with their coordinates, voucher numbers, and references. SANTA CATARINA: Municipality of Bom Jardim da Serra 28.3369 S/ 49.6247 W (CFBH 11034; Lucas, 2008) these coordinates are from city proper of municipality of Bom Jardim da Serra; municipality of Praia Grande 29.1967 S/ 49.9503 W (CFBH 3086; Pombal, Feio and Haddad, 2002) these coordinates are from city proper of municipality of Praia Grande; municipality of Treviso 28.5156 S/ 49.4575 W (CFBH 10324, Lucas, 2008) these coordinates are from city proper of municipality of Treviso. Accepted by Mirco Solé