Range extension and upated distribution of Hypsiboas pardalis (Spix, 1824) (Anura, Hylidae)

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1 Herpetology Notes, volume 7: (2014) (published online on 23 December 2014) Range extension and upated distribution of Hypsiboas pardalis (Spix, 1824) (Anura, Hylidae) Camila Mattedi 1, * and Rafael Pontes 1 Hypsiboas pardalis (Spix, 1824) is a medium-sized treefrog which inhabits open areas and the border of Atlantic Forest fragments of Southeastern Brazil. It also occurs along gallery forests from sea level up to 1000 m a.s.l. (Nascimento et al., 2004). Currently, molecular, morphological, and behavioral evidences support this species in the Hypsiboas faber species group (e.g. Cochran, 1955; Caramaschi and Napoli, 2004; Faivovich et al., 2005). At present, this group consists of eight species (sensu Faivovich et al., 2005) that are distributed throughout South America: Hypsiboas albomarginatus (Spix, 1824), Hypsiboas crepitans (Wied-Neuwied, 1824), Hypsiboas exastis (Caramaschi and Rodrigues, 2003), Hypsiboas faber (Wied-Neuwied, 1821), Hypsiboas lundii (Burmeister, 1856), Hypsiboas pardalis, Hypsiboas pugnax (Schmidt, 1857), and Hypsiboas rosenbergi (Boulenger, 1898). The type locality of Hypsiboas pardalis is in the State of Rio de Janeiro (Spix, 1824), based on two syntypes, which were declared lost (Hoogmoed and Gruber, 1983). Caramaschi and Napoli (2004), based on notes published by Vanzolini (1981), Lutz (1973), and Izecksohn and Carvalho-e-Silva (2001), restricted the type locality of H. pardalis to Fazenda Mandioca (approximately S, W), in the vicinities of Santo Aleixo, Municipality of Magé, State of Rio de Janeiro, Brazil. Herein, we examined specimens of H. pardalis preserved in herpetological collections, provide a geographical map and discuss on its current distribution. Like other species of the Hypsiboas faber group, H. pardalis is also known as gladiator-frog in view 1 Universidade Federal do Rio de Janeiro, Museu Nacional, Departamento de Vertebrados, Setor de Herpetologia. Quinta da Boa Vista s/ nº, São Cristóvão, Rio de Janeiro, RJ. * Corresponding author: ca.mattedi@gmail.com of its extremely pugnacious behavior and the welldeveloped prepollical spines that males use in fighting behaviors (Kluge, 1979). Nevertheless, Faivovich et al. (2005) preferred to use the term gladiator-frogs to refer collectively to the mostly South American species that have a prepollical spine, since other groups contain species with similar morphological and behavioral characteristics. Hypsiboas pardalis usually lays eggs in footsteps of cow s hooves (Bokermann, 1968) and, eventually, in tank-bromeliads Alcantarea extensa (L.B. Smith) J.R. Grant (Moura et al., 2011). In general, males of the H. faber group are conspicuous due to the construction of nests in mud, but it is also known that males of H. pardalis can take advantage of small concavities in the soil and use them for nesting (Bokermann, 1968). In order to better understand the geographic distribution of Hypsiboas pardalis, we examined 243 preserved specimens from the following collections: MNRJ (Museu Nacional, Rio de Janeiro, Rio de Janeiro), MZUSP (Museu de Zoologia, Universidade de São Paulo, São Paulo), MBML (Museu de Biologia Prof. Mello Leitão, Santa Teresa), ZUEC (Museu de História Natural, Universidade Estadual de Campinas, Campinas), UFES (Coleção Herpetológica, Universidade Federal do Espírito Santo, Vitória) (see Appendix 1 for examined material). We conducted direct comparisons with preserved specimens and diagnosed them using specific characters of Hypsiboas pardalis contained in Caramaschi and Napoli (2004), as follow: the rough aspect of the dorsal skin; presence of developed dermal ridges on arms; hands fully webbed; presence of calcar appendix, cloacal flap, and cloacal lichenous plate. Those characters promptly distinguish H. pardalis from the most similar species H. crepitans, H. lundii, and H. pugnax. Dorsal roughness, dermal ridges, calcars, and cloacal flap are poorly developed in H. lundii and absent in H. crepitans; in H. pugnax the cloacal plate is absent. Furthermore, hand and feet are less webbed in those three species.

2 792 Camila Mattedi & Rafael Pontes Figure 1. Male specimen of Hypsiboas pardalis (MNRJ 46836) from Guaratinga ( S; W; 200 m a.s.l.), State of Bahia. SVL = 59.31mm Hypsiboas pardalis was previously known from the states of São Paulo, Rio de Janeiro, Minas Gerais, and Espírito Santo. Our museum survey covered its distribution in those states and resulted in the identification of new localities. A specimen collected by C. Canedo and F. Falcão, on February 2007 (MNRJ 46836, SLV = 59.31mm, Figure 1) at the Municipality of Guaratinga ( S; W; 200 m a.s.l.), State of Bahia, was misidentified as H. crepitans; this specimen actually corresponds to an adult male of H. pardalis. The new record extends the geographic range of H. pardalis in ca. 300 km north from the previous northernmost locality, the Municipality of Sooretama, State of Espírito Santo. Furthermore, our finding is the first record of H. pardalis for the State of Bahia (Figure 2). Additionally, we found a female labeled as Hypsiboas pardalis from the State of Goiás (MNRJ 128, SLV = 71.80mm); no precise geographic information was available (Figure 3). Although Lutz (1973) reported H. pardalis in the state of Goiás, the author did not assign a voucher, probably such specimen was the same examined in the present study (MNRJ 128). Subsequent studies including H. pardalis did not make reference to this record (e.g. Caramaschi and Napoli, 2004) and considered only the states of Espírito Santo, Minas Gerais, Rio de Janeiro, and São Paulo in the H. pardalis distribution. Within the Hypsiboas faber species group, Hypsiboas lundii is the species that occupies the Cerrado biome and its external morphology resembles H. pardalis. However, this specimen from Goiás does not fit into the H. lundii diagnosis (Caramaschi and Napoli, 2004), in fact it shows the aforementioned diagnostic characters of H. pardalis. The occurrence of Hypsiboas pardalis in the Cerrado of Goiás State is plausible and can be explained by the resemblance between the vegetation formations of the Atlantic Forest of southern and southeastern Brazil, and the vegetation along water courses in the Cerrado, known as gallery or riparian forests (Oliveira-Filho and Ratter, 2000). To reinforce this assumption, recently species which geographic distribution mostly associated to Atlantic Forest, such as Vitreorana eurygnatha (Lutz, 1925), have been recorded in gallery forests of the Cerrado (Cintra et al., 2013). The referred specimen from Goiás was collected by Dr. Rudolph Pfrimmer, a professional collector who extensively collected anurans, fishes, and marsupials in central Brazil (Miranda-Ribeiro, 1936; Bertaco et al., 2010). However, the lack of information on the label

3 Range extension and distribution updated of Hypsiboas pardalis 793 Figure 2. Distribution map of Hypsiboas pardalis. Legend: Yellow circle: type-locality; Green circle: known localities of occurrence; Red circle: new record for Guaratinga, Bahia state, Brazil. Biomes: Green: Atlantic Forest; Cream: Cerrado; Light orange: Caatinga. Figure 3. Female specimen of Hypsiboas pardalis (MNRJ 128) from Goiás. SVL = 71.8 mm

4 794 (containing only Goiyaz ) does not allow us to infer a more inclusive location where this specimen was collected and confirm its reliability. Thus, to avoid the inclusion of an imprecise record on our map, we chose not to include this point in the distribution of this species. Only increasing survey efforts in this region will reveal if Hypiboas pardalis occurs in fact in this region or if it is a label mistake. Acknowledgements. We are grateful to scientific collections curators, Hussam Zaher (MZUSP), Felipe Toledo (ZUEC), Hélio Fernades (MBML), Leonora Pires (UFES), Ulisses Caramaschi and José Peres Pombal Júnior (MNRJ) for loan or permission to examine specimens under their care. CM and RP thank to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES for their scholarship grants. We also thank Conselho Nacional de Desenvolvimento Científico e Tecnológico CNPq and Fundação de Amparo a Pesquisa do Estado do Rio de Janeiro FAPERJ for the equipment support to Setor de Herpetologia, Museu Nacional / Universidade Federal do Rio de Janeiro. References Camila Mattedi & Rafael Pontes Miranda-Ribeiro, A. (1936): Didelphia ou Mammalia-ovovípara marsupiães, didelphos, pedimanos ou Metaterios. Revista Museu Paulista 20: Moura, M.R., Motta, A.P., Feio, R.N. (2011): An unusual reproductive mode in Hypsiboas (Anura: Hylidae). Zoologia 28(1): Nascimento, L.B., Caramaschi, U., Silvano, D. (2004): Hypsiboas pardalis. In: IUCN IUCN Red List of Threatened Species. Version Available at: http//: Last accessed on 04 October Oliveira-Filho, A.T., Ratter, J.A. (2000): Padrões florísticos das matas ciliares da região dos cerrados e a evolução das paisagens do Brasil Central durante o Quaternário tardio. In: Matas Ciliares: Bases Multidisciplinares para Estudo, Conservação e Restauração, p Rodrigues, R.R., Leitão-Filho, H.F., Eds., Editora da Universidade de São Paulo, São Paulo. Spix, J.B. (1824): Animalia Nova sive Species Novae Testudinum ET Ranarum, quas in Itinere per Brasiliam Annis MDCCCXVII MDCCCXX Jussuet Auspiciis Maximiliani Josephi I. Bavariae Regis. Typis Franc. Seraph. Hübschmanni, Munich, Germany. Vanzolini, P.E. (1981): The scientific and political contexts of the Bavarian Expedition to Brasil. In: Herpetology of Brazil, p Spix, J.B., Wagler, J.G. Society for the Study of Amphibians and Reptiles, Ithaca, NY. Bertaco, V.A., Carvalho, F.R., Jerep, F.C. (2010): Astyanax goyanensis (Miranda-Ribeiro, 1944), new combination and Astyanax courensis, new species (Ostariophysi: Characiformes): two Characidae from the upper rio Tocantins basin, Central Brazil. Neotropical Ichthyology 8(2): Bokermann, W.C.A. (1968): Observações sobre Hyla pardalis Spix (Anura, Hylidae). Revista Brasileira de Biologia 28(1): 1-5. Caramaschi, U., Napoli, M.F. (2004): The nomenclatural status of the synonyms of Hyla pardalis Spix, 1824, and the taxonomic position of Hyla biobeba Bokermann and Sazima, Journal of Herpetology 38: Cintra, C.E.D., Silva, H.L.R., Junior, N.J.S. (2013): New state record of Vitreorana eurygnatha (Lutz 1925) (Anura: Centrolenidae) in Brazil. Herpetology Notes, volume 6: Cochran, D.M. (1955): Frogs of Southeastern Brazil. Bulletin of the United States National Museum 206: Faivovich, J., Haddad, C.F.B., Garcia, P.C.A., Frost, D.R., Campbell, J.A., Wheeler, W.C. (2005): Systematic review of the frog family Hylidae, with special reference to Hylinae: a phylogenetic analysis and taxonomic revision. Bulletin of the American Museum of Natural History 294: Hoogmoed, M.S., Gruber, U. (1983): Spix and Wagler type specimens of reptiles and amphibians in the Natural History Musea in Munich (Germany) and Leiden (The Netherlands). Spixiana 9: Izecksohn, E., Carvalho-e-Silva, S.P. (2001): Anfíbios do Município do Rio de Janeiro. Rio de Janeiro: Editora da UFRJ, 73 pp. Kluge, A.G. (1979): Gladiator frogs of Middle America and Colombia a reevaluation of their systematics (Anura: Hylidae). Occasional Papers of the Museum of Zoology 688: Lutz, B. (1973): Brazilian Species of Hyla. Austin: University of Texas Press. 29pp.

5 Range extension and distribution updated of Hypsiboas pardalis 795 APPENDIX 1 Examined specimens Hypsiboas pardalis (243 specimens) Brazil: State of Bahia: MNRJ Guaratinga (red circle in the map). Brazil: State of Espírito Santo: MNRJ 26023, 26884, , MBML 514, 4204, MZUSP 34056, Santa Teresa; MBML 2578, 2581, 3992, 4076, 4536, 4714 Lombardia, Santa Teresa; MNRJ 26083, MBML 60, 1194, 1195, 1553, 4325 Estação Biológica de Santa Lúcia, Santa Teresa; MBML 383 Bairro do Eco, Santa Teresa; MBML 3943, 3944, 3945 Alto Rio Saltinho, Santa Teresa; MBML 2576 Sítio Pousada Canaã, Santa Teresa; MBML 1124 Vila Nova, Santa Teresa; MBML 3596 Associação do Banestes, Santa Teresa; MNRJ 27958, MBML 6400, 6401, 6487, 6488, 6495, 6497 Reserva Biológica de Duas Bocas, Cariacica; MBML 6403, 6404, 6405, 6490, 6501, 6502, 6511, 6525 Alto Reserva Biológica de Duas Bocas, Cariacica; MBML 6115 Cariacica; MNRJ 76937, 76945, 77050, MBML 1617 Parque Estadual do Forno Grande, Castelo; MBML 56, 7264 Castelo; MNRJ 1452 FLONA Goytacazes, Linhares; MNRJ Fazenda Oliveira, Guaçuí; MNRJ Fazenda dos Japoneses, Vargem Alta; MNRJ 13263, MBML 4912, 4913 Parque Municipal Goiapabaçu, Fundão; MNRJ Alto Nova Almeida, Marechal Floriano; MBML 4449, 5753, 5754, 5929 Sítio Amarildo, Marechal Floriano; MNRJ Afonso Claudio; MNRJ , Domingos Martins; MBML 6625 Pedra Azul, Domingos Martins; MBML 6300, 6302, 6984, 6985 RPPN Oiutrem, Matilde, Alfredo Chaves; MBML 2081 Povoação de Baunilha, Córrego Santinho, Colatina; MBML 242 Crubixá-Mirim, Santa Leopoldina; MBML 3592 Pousada Vila Suíça, Santa Leopoldina; MZUSP 200, 269, 2155 Rio Doce; MZUSP 7794 Sooretama. Brazil: State of Goiás: MNRJ 128 Goyaz. Brazil: State of Minas Gerais: MNRJ , MZUSP 65261, Fazenda Montes Claros, Reserva Ecológica de Caratinga, Caratinga; MNRJ 78252, Sítio 2, Chiador; MNRJ Sítio 3, Chiador; MNRJ Mata dos Pena, Eugenópolis; MNRJ Paula Candido; MNRJ Sítio 6, Além Paraíba; MNRJ Sítio 8, Além Paraíba; MNRJ Sítio 9, Além Paraíba; MNRJ Fazenda Cachoeirão, Além Paraíba; MNRJ Além Paraíba; MNRJ UHE Guilman Amorim, Antônio Dias; MZUSP PCH Cachoeira Grande, Antônio Dias; MZUSP PCH Cocais Grande, Antônio Dias; MNRJ Estação Biológica Mata do Sossego, Simonésia; MNRJ 26017, 27502, Fazenda Olinda, São José, Belmiro Braga; MNRJ Água Limpa, Juiz de Fora; MNRJ Torrões, Juiz de Fora; MNRJ Lagoa do Maximus, próximo a Santa Rita de Ouro Preto, Ouro Preto; MNRJ 38114, 66650, 66653, Viçosa; MNRJ Muriaé; MNRJ Reserva Biológica de Mar de Espanha, Mar de Espanha; MNRJ Fazenda da Prata, Sapucaia; MNRJ Mata de Gruta, Santana do Deserto; MNRJ 66652, Eugenópolis; MNRJ Fazenda Cachoeira Alegre, Abre Campo; MZUSP , PARNA do Caparaó; MZUSP , UHE Fumaça, Mariana. Brazil: State of Rio de Janeiro: MNRJ Paracambi; MNRJ 21674, 21888, 25747, Morro Azul, Engenheiro Paulo de Frontin; MNRJ Tinguá, Nova Iguaçu; MNRJ 53603, , Taquara, Duque de Caxias; MNRJ 75289, 77028, 77030, Visconde de Mauá, Resende; MNRJ Fazenda Marimbondo, Resende; MNRJ Fazenda Barreto, Nova Friburgo; MNRJ Theodoro de Oliveira, Nova Friburgo; MNRJ Fazenda João Fernando, RJ 151, Valença; MNRJ Capela, Petropólis; MNRJ 42500, CEDEA, Rocio, Petrópolis; MNRJ 2004, Petrópolis; MNRJ k UTM , Sapucaia, Três Rios ou Mar de Espanha; MNRJ Reserva Ecológica de Guapiaçu, Cachoeiras de Macacu; MNRJ Fazenda Santa Bárbara, P.E. Três Picos, Cachoeiras de Macacu; MNRJ , Duas Barras; MNRJ 75536, Volta Redonda; MNRJ Vale da Revolta, Teresópolis; MNRJ 25778, MZUSP ; MNRJ Teresópolis; MNRJ PNM Fazenda Atalaia, Macaé; MNRJ 49635, 51056, Comendador Levy Gasparian; MNRJ Rialto, Barra Mansa; MNRJ Floriano, entrada do km 290, Via Dutra, Barra Mansa; MNRJ Patronato, Três Rios; MNRJ Acampamento Batista Carioca, Areal, Três Rios; MNRJ Área da PCH Santa Fé, Três Rios; MNRJ Fazenda Canan, Três Rios; MNRJ Lídice, Rio Claro; MNRJ Itaperuna; MNRJ Trajano de Moraes; MNRJ Parati; MNRJ Fazenda Barra da Água Limpa, Bom Jesus do Itabapoana, MZUSP Itatiaia; MZUSP Miguel Pereira. Brazil: State of São Paulo: MNRJ Aparecida; MZUSP Parque das Neblinas, Bertioga; MZUSP Praia de Boracéia, Bertioga; MZUSP , Juquitiba; MZUSP Parque Estadual de Carlos Botelho, São Miguel Arcanjo; MZUSP São Miguel Arcanjo; MZUSP 4075, 4571, Boracéia, Salesópolis; MZUSP Boracéia; MZUSP E.E. de Bananal; MZUSP , Piedade; MZUSP 225, 76519, 95840, Campo Grande da Serra; MZUSP Fazenda Intervales; MZUSP Serra da Bocaina; MZUSP Ferraz de Vasconcelos; MZUSP , Ribeirão Grande. Accepted by Mirco Solé