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Two New Species of Marsupial Tree-Frogs Genus Gastrotheca Fitzinger, 1843 (Anura, Hemiphractidae) from the Brazilian Atlantic Forest

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Two New Species of Marsupial Tree-Frogs Genus Gastrotheca Fitzinger, 1843 (Anura, Hemiphractidae) from the Brazilian Atlantic Forest Zootaxa 3437: 1–23 (2012) ISSN 1175-5326 (print edition) www.mapress.com/zootaxa/ ZOOTAXA Copyright © 2012 · Magnolia Press Article ISSN 1175-5334 (online edition) Two new species of marsupial tree-frogs genus Gastrotheca Fitzinger, 1843 (Anura, Hemiphractidae) from the Brazilian Atlantic Forest MAURO TEIXEIRA JR.1,2, FRANCISCO DAL VECHIO1, RENATO SOUSA RECODER1, ANA CAROLINA C ARNAVAL 3, MARIA STRANGAS3, ROBERTA PACHECO DAMASCENO4, MARCO AURÉLIO DE SENA1, MIGUEL TREFAUT RODRIGUES1 1Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Caixa Postal 11.461, CEP 05508- 090, Brazil. 2E-mail: [email protected] 3Department of Biology, The City University of New York, 526 Marshak Science Building, City College of New York, 160 Convent Avenue, New York, NY 10031, USA. 4University of California, Berkeley, Museum of Vertebrate Zoology, 3101 Valley Life Sciences Building, Berkeley, CA 94720–3140, USA. ABSTRACT Two new species of Gastrotheca are described from northeastern Minas Gerais and southern Bahia, in the Atlantic Forest of Brazil. Data on morphology, calls, mitochondrial, and nuclear DNA are provided. Allied to G. fissipes and G. megacephala, the new taxa provide evidence for a higher diversity of species of Gastrotheca than previously thought at the Atlantic Forest. The data also suggest that G. pul chra, another Atlantic Forest taxon, is more closely related to non- Atlantic Forest species than to the remaining analyzed Brazilian Gastrotheca species. This implies that the Gastrotheca at the Brazilian coastal forests have at least two independent origins. Key words: Reserva Biológica da Mata Escura, Estação Ecológica Estadual de Wenceslau Guimarães, Jequitinhonha Riv- er, Atlantic Forest refuges. INTRODUCTION In their eighth volume of Erpétologie Générale, Duméril and Bibron (1841) described a new species of a tree- frog from Cuzco, Peru, which they attributed to the genus Hyla. The new species had a particularity that would distinguish it from all other congeners: it possessed a pouch on its back in which it carried its eggs. To this species, they gave the very appropriate name Hyla marsupiata. Two years later, Fitzinger (1843) removed this species from Hyla and created a new genus to accommodate this marsupial tree-frog, the genus Gastrotheca. Almost 160 years after Fitzinger’s (1843) work, Gastrotheca now comprises about 60 species distributed from southern Central America to northern Argentina and eastern South America (Duellman 1984). Its highest diversity is found along the Andean slopes and the tropical lowlands of northwestern South America. With fewer endemics, the genus also occurs along the Atlantic Forest of eastern Brazil (Duellman 1984; Caramaschi & Rodrigues 2007). The taxonomic history of the Brazilian Atlantic Forest’s Gastrotheca species begins when Boulenger (1888) described Nototrema fissipes from Pernambuco, in the northeastern coast. About two decades later, Andersson described Nototrema microdiscus from Paraná (Lönnberg & Andersson 1910) and N. fulvorufa (Andersson 1911) from São Paulo. Ten more years had passed before Miranda-Ribeiro (1920) described Gastrotheca ernestoi from Rio de Janeiro; two decades later, A. Lutz and B. Lutz (1939) described G. virid is and G. albolineata from São Paulo and Rio de Janeiro states, respectively. After four and a half decades of taxonomic stasis, Duellman (1984) rendered all names but G. f i s si p e s junior synonyms of G. microdiscus. A second reassessment based on newly collected specimens removed those species from G. mi cro discu s synonymy, Accepted by S. Castroviejo-Fisher: 6 Jul. 2012; published: 24 Aug. 2012 1 placing G. virid is in the synonymy of G. ernesto i, and described G. pulchra from southern Bahia (Caramaschi & Rodrigues 2007). In the subsequent year, G. flamma, also from southern Bahia, was described (Juncá & Nunes 2008). By 2009, G. fissipes was considered the most widespread species of Gastrotheca in the Atlantic Forest, ranging from southern Espírito Santo to Pernambuco. However, a recent revision described a novel species allied to G. fissipes: G. megacephala (Izecksohn et al. 2009). In their work, Izecksohn et al. (2009) recommended that only those populations from Pernambuco be considered G. fissipes, whereas populations south of Pernambuco should be called G. megacephala (Izecksohn et al. 2009). Despite Izecksohn et al.’s (2009) points, the name G. fissipes is still being applied to Gastrotheca populations in southern Bahia (Pimenta et al. 2009; Freitas 2011; Moura et al. 2012). Because the diversity of Gastrotheca in the Atlantic Forest was only recently revealed, it has not yet been properly addressed in existing phylogenetic studies. Mendelson et al. (2000) used a morphological approach to address the relationship of hemiphractine frogs. This study proposed G. fissipes as the sister group of G. microdiscus, nested deeply within the Gastrotheca genus. However, those were the only two species recognized for the Atlantic Forest at that time, and the individuals of G. fissipes included likely represent G. megacaphala, as the specimens are from Vila Velha, Espírito Santo, and those of G. microdiscus may represent G. f ulvo rufa, G. ernestoi or G. albolineata, as the specimens are from Teresópolis, Rio de Janeiro. Therefore, data about their relationships with westernmost species are still scarce, and the monophyly of the Atlantic Forest assemblage has been debated (Duellman 1984; Caramaschi & Rodrigues 2007). Recent molecular phylogenetic studies recovered Gastrotheca fissipes as the basal lineage among all Gastrotheca (Wiens et al. 2007; Pyron & Wiens 2011), but no other species from the Atlantic Forest were surveyed. Through recent field work efforts, tied to molecular DNA sequencing, we discovered a population of Gastrotheca in southern Bahia that is morphologically and genetically distinct from both G. fissipes and G. megacephala. We also collected a series belonging to yet another distinct population from northeastern Minas Gerais. Here we describe both species, provide notes on their natural history, describe their advertisement call, and present a preliminary molecular phylogenetic analysis to demonstrate the uniqueness of these lineages. To this end, we include other available samples of Atlantic Forest species. MATERIAL AND METHODS Morphological assessment Morphometric variable terminology and definition, morphological descriptions, and diagnosis follow Caramaschi and Rodrigues (2007) and Izecksohn et al. (2009); snout terminology follows Heyer et al. (1990), web formulae follow Savage and Heyer (1997). After fixation, measurements were taken with an electronic caliper to the nearest 0.01mm and rounded to the first decimal unit (Hayek et al. 2001) to avoid pseudoprecision. Measurements are: SVL (snout-vent length); HL (head length); HW (head width); ED (eye diameter); TD (tympanum diameter); END (eye to nostril distance); ESD (eye-snout distance); THL (thigh length); TL (tibia length); FL (foot length); EW (eyelid width); IOS (interorbital space); 3FD (diameter of third finger disk); 4TD (diameter of fourth toe disk). Observations of morphological characters were performed with a stereomicroscope Zeiss STEMI SV6. Small-sized individuals (all about 20mm SVL) were considered to be juveniles and were not measured. All others (larger than 65mm SVL) were included in the measurements. Literature data (Duellman 1984; Mendelson et al. 2000; Caramaschi & Rodrigues 2007; Izecksohn & de Carvalho-e-Silva 2008; Juncá & Nunes 2008; Izecksohn et al. 2009) and examination of collection vouchers housed at Museu de Zoologia da Universidade de São Paulo (MZUSP) and Museu de História Natural da Universidade Federal de Alagoas (UFAL) (Appendix I) enabled morphological comparisons among the newly described species and other congeners. Osteological comparisons were made through three-dimensional images generated by a computerized tomography using an x-ray micro-tomographer in median and low resolution, without filter. This examination was performed for specimens housed in MZUSP. 2 · Zootaxa 3437 © 2012 Magnolia Press TEIXEIRA JR. ET AL. Distribution To map the known distributional ranges of Gastrotheca species over the Atlantic Forest we complied locality from the literature (Duellman 1984; Sachsse et al. 1999; Mendelson et al. 2000; Caramaschi & Rodrigues 2007; Carvalho-e-Silva et al. 2008; Gressler et al. 2008; Izecksohn & de Carvalho-e-Silva 2008; Juncá & Nunes 2008; Freitas et al. 2009; Santos & Santos 2009; GBIF 2011; Siqueira et al. 2011; SpeciesLink 2011; Mendes et al. 2012), personal communications (J. Rodrigues), and museum specimens (MZUSP and UFAL). Field sampling methods Active searches were carried out in all forest types available at Estação Ecológica Estadual de Wenceslau Guimarães (EEEWG, state of Bahia, Brazil) and Reserva Biológica da Mata Escura (RBME, state of Minas Gerais, Brazil). Field work was performed during the rainy season (EEEWG: Dec 8th–Dec 20th 2011; RBME: Dec 1st 2009–Jan 4th 2010) by four to six people, for four to six hours per night. Collected specimens were fixed in 10% formalin, preserved in 70% ethanol, and housed at MZUSP. Bioacoustics At RBME, calls were recorded with a Panasonic RR-US450 portable digital audio recorder with built-in microphone under a sampling rate of 44.1 kHz, 16 bit resolution, and recording pitch up to 7 kHz in a mono channel. At EEEWG, calls were recorded with an Olympus LS-10 portable digital audio recorder using built-in microphones with recording
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