Herpetology Notes, volume 10: 397-402 (2017) (published online on 22 July 2017)

New records and geographic distribution of the torrent meridionalis (Mertens, 1927) (Amphibia, Anura, ), 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 the state of Rio Grande do Sul, Brazil (Mertens, 1927; usually the only information available to assess the Braun and Braun, 1980; Kwet and Di-Bernardo, 1999; conservation status of many species (e.g. Fontana et al., Pombal et al., 2002; Vilella et al., 2004; Deiques et al., 2003; Machado et al., 2008). This is particularly relevant 2007; Lima and Colombo, 2008; Lema and Martins, for species with restrict distribution or few available data 2011; Lingnau et al., 2013) and municipalities of Bom about its biology (IUCN, 2015). Torrent of the Jardim da Serra, Lauro Müller, Praia Grande, Timbé do genus Hylodes Fitzinger, 1826 occur mainly associated Sul, Treviso and Urussanga in the state of Santa Catarina with high-gradient streams in Brazilian Atlantic Forest (Pombal et al., 2002; Toledo et al., 2006; Lucas, 2008). (Haddad and Pombal, 1995; Frost, 2015), which is one Recent field expeditions revealed the occurrence of of the most endangered ‘biodiversity hotspots’ in the Hylodes meridionalis in several new localities, suggesting world (Myers et al., 2000). the need for a revision of its known geographical Hylodes meridionalis (Mertens, 1927) is endemic distribution. Three herpetological collections from Rio to the mountain slopes of the Serra Geral, along the Grande do Sul state were revised in order to confirm southernmost portion of the Atlantic Rainforest. identity and search for additional specimens: Coleção The species lives only in well-preserved forested Herpetológica da Universidade Federal do Rio Grande areas, inhabiting streams and cascades with clear do Sul (UFRGS), Museu de Ciências e Tecnologia da running water (Kwet and Di-Bernardo, 1999). Global Pontifícia Universidade Católica do Rio Grande do population trend is supposed to be decreasing due to Sul (MCP) e Museu de Ciências Naturais da Fundação water pollution, deforestation, and Batrachochytrium Zoobotânica do Rio Grande do Sul (MCN). We also dendrobatidis infection (Garcia and Segalla, 2010; compiled all published records of H. meridionalis with Toledo et al., 2006). Previous records are known for voucher specimens deposited in scientific collections the Brazilian municipalities of Cambará do Sul, Canela, (Appendix I and Appendix II). New records were Caxias do Sul, Gramado, Itati, Maquiné, São Francisco obtained for eight localities in Rio Grande do Sul state de Paula (type locality), Terra de Areia and Torres in (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 1 Laboratório de Herpetologia, Departamento de Zoologia, MZUSP.89939 after Canedo, 2008). Actually these Instituto de Biociências, Universidade Federal do Rio Grande records refer to individuals donated from the Museum do Sul, Avenida Bento Gonçalves 9500, Agronomia, CEP of Zoology of the Universidade de Campinas (ZUEC) 91501-970, Porto Alegre, Rio Grande do Sul, Brazil 2 Museu de Ciências Naturais, Fundação Zoobotânica do Rio to the Museum of Zoology of the Universidade de Grande do Sul, Rua Dr. Salvador França 1427, Jardim São Paulo (MZUSP). The original locality was São Botânico, CEP 90690-000, Porto Alegre, RS, Brazil Francisco de Paula, according to ZUEC collection (T. * Corresponding author e-mail: [email protected] 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). locality data, since there are other individuals, housed in The two specimens from Viamão (one is currently in the the MCN collection, from different species collected in Museu de Ciências Naturais da Fundação Zoobotânica the municipality of Canela, Rio Grande do Sul, by the do Rio Grande do Sul [MCN.1890] and the other same collector (Pedro Braun) in the same date (1974). [MCN.1893] was donated to Harold Dundee of. 35/66- The last two records are additionally doubtful because USA) were obtained from the didactic collection of the there are no suitable habitats (streams inside primary or Escola Estadual Técnica de Agricultura (State School secondary advanced forests) to support the presence of of Technical Agriculture, EETA) in the municipality of H. meridionalis. Besides, sampling effort in localities Viamão, Rio Grande do Sul. EETA’s collection is not around these two records, in the last five years, have not a scientific collection and has specimens from various revealed the presence of the species. Moreover, these locations around the world, many without or with records were not considered by Pedro and Cristina Braun doubtful collection and location data. 3) Parque Estadual (1980), MCN collection managers, in their preliminary da Guarita, in the municipality of Torres (MCN.8495). list of from Rio Grande do Sul (Braun and The specimen supposedly from Torres, also deposited Braun, 1980), which suggests that they detected these in the Museu de Ciências Naturais da Fundação mistakes, or the errors may have been produced after Zoobotânica do Rio Grande do Sul, probably has a wrong 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 doubtful records, the species occurs in forested areas of westernmost record, extending the known distribution Atlantic Rainforest biome from Bom Jardim da Serra in of this species about 70 kilometers to the west. The Santa Catarina to Caraá in Rio Grande do Sul. However, new records corroborate previous suggestions that H. the northern distribution limit of H. meridionalis is not meridionalis lives in first and second order streams in the clearly defined and we are aware that other species of Atlantic Forest of Serra do Mar, inland Atlantic Forest this genus distributed in Santa Catarina also show no and Araucaria Forest (Garcia et al., 2007). Ignoring the 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 29.0289°S/ 51.6681°W UFRGS.3924 Antas, Cotiporã 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 28.9856°S/ 51.3734°W UFRGS.3934 Antas and nearby areas, Nova Roma do Sul 28.9856°S/ 51.3735°W UFRGS.3935 28.9542°S/ 51.3826°W UFRGS.4591 UFRGS.4592 Cascata da Pedra Branca, Boa União Distric, 29.3956°S/ 50.0447°W UFRGS.2726 Três Forquilhas MCP.12119 PCH (Pequena Central Hidrelétrica) Jararaca, 28.9344°S/ 51.4695°W UFRGS.3877 Rio da Prata, Veranópolis MCP.9917 PCH (Pequena Central Hidrelétrica) da Ilha, 28.8913°S/ 51.4561°W MCP.9938 Vila Flores (Coordinates from the Dam)

Furthermore, we observed a great morphological Ciências e Tecnologia da Pontifícia Universidade Católica do Rio variation in dorsal, lateral and ventral of the analysed Grande do Sul (MCP/PUCRS) and Museu de Ciências Naturais specimen from Rio Grande do Sul state, not yet da Fundação Zoobotânica do Rio Grande do Sul (MCN/FZB), respectively; C. Zank and L. F. M. da Fonte helped in the revision reportet to Hylodes meridionalis (Figure 2). Hence, of MCN specimens l; D. B. Provete and M. D. Freire provided the we recommend a review of the specimens collected in original description of H. meridionalis; M. Solé for the pre peer Santa Catarina. review and the valuable comments. Four new records for the northwest of Rio Grande do Sul were obtained during surveys that were part of References the licensing process for the building of hydroelectric Braun, P.C., Braun, C.A.S. (1980): Lista prévia dos anfíbios do power plants. The construction of these hydroelectric Estado do Rio Grande do Sul, Brasil. Iheringia, Série Zoológica plants can represent an important threat to the species 56: 121-146. survival, because it converts a lotic aquatic environment Canedo, C.C. (2008): Revisão Taxonômica de Hylodes Fitzinger, into a lentic environment, unsuitable for the survival 1826 (Anura, Hylodidae). Unpublished PhD thesis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil. of Hylodes species. Other threats, like water pollution Deiques, C.H., Stahnke, L.F., Reinke, M., Schmitt, P. (2007): Guia and deforestation of native environments, have been ilustrado dos anfíbios e répteis do Parque Nacional de Aparados detected around the localities where the records were da Serra, Rio Grande do Sul, Santa Catarina, Brasil. Pelotas, compiled. Furthermore, there are populations of H. Brazil, USEB. meridionalis diagnosed with the chitrid fungus, which Fontana, C.S., Bencke, G.A., Reis, R.E. (2003): Livro Vermelho is directly linked with global anuran population declines da Fauna Ameaçada de Extinção no Rio Grande do Sul. Porto (James et al., 2015). With the data presented in this short Alegre, Brazil, EPECE. Frost, D.R. (2015): Species of the World, version note, we believe that is possible to contribute with the 5.6. American Museum of Natural History, New York, USA. enhancement of the conservation status of this species. Electronic Database available at http://research.amnh.org/ herpetology/amphibia/index.html. Accessed on 15 May 2015. Acknowledgements. We thank T. Grant for reviewing locality Garcia, P, Segalla, M.V. (2010): Hylodes meridionalis. Ln: IUCN data from MZUSP specimens; G. M. Pontes and M. F. Renner 2015. IUCN Red List of Threatened Species. 9ersion 2014.3. for allowing access to the herpetological collections of Museu de . 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): Lucas, E.M. (2008): Diversidade e conservação de anfíbios anuros Anfíbios da Região Subtropical da América do Sul, Padrões de no Estado de Santa Catarina, sul do Brasil. Unpublished PhD Distribuição. &iência & Ambiente 35: 65-100. thesis, Universidade de São Paulo, São Paulo, Brazil. Haddad, C.F.B., Pombal, J.P.Jr. (1995): A new species of Hylodes Machado, A.B.M., Drummond, G.M., Paglia, A.P. (2008): from Southeastern Brazil (Amphibia: Leptodactylidae). Livro Vermelho da Fauna Brasileira Ameaçada de Extinção, Herpetologica 51: 279–286. 1st Edition. Brasília, Brazil, Ministério do Meio Ambiente, IUCN (2015). The IUCN Red List of Threatened Species. Version Fundação Biodiversitas. 2015.3. . Accessed on 10 May Mertens, R. (1927): Neue Froschlurch aus Rio Grande do Sul, 2015. Brasilien. Blätter für Aquarien- und Terrarienkunde 38(2): 26- James, T.Y., Toledo, L.F., Rödder, D., Leite, D.S., Belasen, A., 30. Betancourt-Román, C.M., Jenkinson, T.S., Lambertini, C., Myers, N., Mittermeier, R.A., Mittermeier, C.G., Fonseca, G.A.B., Longo, A.V., Ruggeri, J., Collins, J.P., Burrowes, P., Lips, Kent, J. (2000): Biodiversity hotspots for conservation priorities. K.R., Zamudio, K.R., Longcore, J.E. (2015): Disentangling Nature 408: 853–858. host, pathogen, and environmental determinants of a recently Pombal, J.P.Jr., Feio, R.N., Haddad, C.F.B. (2002): A new species emerged wildlife disease: Lessons from the first 15 years of of torrent frog genus Hylodes (Anura: Leptodactylidae) from amphibian chytridiomycosis research. Ecology and Evolution southeastern Brazil. Herpetologica 58: 462–471. 5(18): 4079-97. Toledo, L.F., Britto, F.B., Araújo, O.G.S., Giasson, L.M.O., Kwet, A., Di-Bernardo, M. (1999): Pró-Mata – Anfíbios – Haddad, C.F.B. (2006): The occurrence of Batrachochytrium Amphibien – Amphibians. Porto Alegre, Brazil, EDIPUCRS. dendrobatidis in Brazil and the inclusion of 17 new cases of Lema, T. de, Martins, L.A. (2011): Anfíbios do Rio Grande do Sul infection. South American Journal of Herpetology 1(3): 185- – Catálogo, diagnoses, distribuição, iconografia. Porto Alegre, 191. Brazil, EDIPUCRS. Vilella, F.S., Becker, F.G., Hartz, S.M., Barbieri, G. (2004): Relation Lima, A.F.B., Colombo, P. (2008): Observação do comportamento between environmental variables and aquatic megafauna predatório de Liophis miliaris orinus (Serpentes, Colubridae) in a first order stream of the Atlantic Forest, southern Brazil. em Hylodes meridionalis (Anura, Hylodidae), Serra Geral, Rio Hydrobiologia 528: 17-30. 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. 402 Natália Dallagnol Vargas et al.

Appendix I Appendix 2

List of additional specimens of Hylodes meridionalis with their List of additional literature records (not seen) of Hylodes coordinates and the voucher numbers. meridionalis with their coordinates, voucher numbers, and RIO GRANDE DO SUL: municipality of Cambará do Sul, references. without locality – 29.0478°S/ 50.1447°W – these coordinates SANTA CATARINA: Municipality of Bom Jardim da Serra are from city proper of municipality of Cambará do Sul (MCN – 28.3369°S/ 49.6247°W (CFBH 11034; Lucas, 2008) – these 6964), Faxinalzinho (MCN 1164, 1184), Itaimbezinho (MCN coordinates are from city proper of municipality of Bom 11283, 11288, 11294, 11296, 11298); municipality of Canela, Jardim da Serra; municipality of Praia Grande – 29.1967°S/ without locality – 29.3656°S/ 50.8156°W – these coordinates 49.9503°W (CFBH 3086; Pombal, Feio and Haddad, 2002) – are from city proper of municipality of Canela (MCP 309; these coordinates are from city proper of municipality of Praia MCN 1969); municipality of Caxias do Sul, without locality Grande; municipality of Treviso – 28.5156°S/ 49.4575°W – 29.1681°S/ 51.1794°W (MCN 9938); municipality of (CFBH 10324, Lucas, 2008) – these coordinates are from city Cotiporã, without locality – 29.0038°S/ 51.6822°W (UFRGS proper of municipality of Treviso. 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).

Accepted by Mirco Solé