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A New Crossodactylodes Cochran, 1938 (Anura: Leptodactylidae: Paratelmatobiinae) from the Highlands of the Atlantic Forests of Southern Bahia, Brazil

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A New Crossodactylodes Cochran, 1938 (Anura: Leptodactylidae: Paratelmatobiinae) from the Highlands of the Atlantic Forests of Southern Bahia, Brazil Zootaxa 3702 (5): 459–472 ISSN 1175-5326 (print edition) www.mapress.com/zootaxa/ Article ZOOTAXA Copyright © 2013 Magnolia Press ISSN 1175-5334 (online edition) http://dx.doi.org/10.11646/zootaxa.3702.5.5 http://zoobank.org/urn:lsid:zoobank.org:pub:E7D7BEC6-5DD6-47D6-BE26-904A69403C76 A new Crossodactylodes Cochran, 1938 (Anura: Leptodactylidae: Paratelmatobiinae) from the highlands of the Atlantic Forests of southern Bahia, Brazil MAURO TEIXEIRA JR.1,2, RENATO SOUSA RECODER1, RENATA CECÍLIA AMARO1, ROBERTA PACHECO DAMASCENO3, JOSÉ CASSIMIRO1& MIGUEL TREFAUT RODRIGUES1 1Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Caixa Postal 11.461, CEP 05422– 970, Brazil. 2E-mail: [email protected] 3University of California, Berkeley, Museum of Vertebrate Zoology, 3101 Valley Life Sciences Building, Berkeley, CA 94720–3140, USA. Abstract A new Crossodactylodes is described from Serra das Lontras, in the highlands of the Atlantic Forests of southern Bahia. The new species can be distinguished from all other Crossodactylodes by having Finger I ending in an acute tip, a larger body size, by cranial features, and by molecular data. Like their congeners, the new species live in bromeliads but is widely geographically disjunct, being apparently restricted to the summit of a mountain range in Northeastern Brazil. Key words: Crossodactylodes septentrionalis sp. nov., Serra das Lontras, Atlantic Forests, mountain endemism Introduction The genus Crossodactylodes Cochran, 1938, family Leptodactylidae (sensu Fouquet et al. 2013), is a poorly known bromeliad-dweller genus endemic to the Brazilian Atlantic Forests. Crossodactylodes pintoi Cochran, 1938 is the type species and “Macahé [= Serra de Macaé]”, Macaé mountains, in Nova Friburgo, state of Rio de Janeiro, is the type locality (Bokermann 1966). Given the presence of spines on the inner surface of the first finger, a similar tooth development, and the supposed presence of digital pad glands that appears when the digital tips are dried out, Cochran (1955) suggested Crossodactylodes to be closely related to Crossodactylus Duméril and Bibron, 1841. However, this last character was probably an artifact resulting from the presence of Y-shaped terminal phalanges (Lynch 1971). Lynch (1971) placed Crossodactylodes as part of his Grypiscini tribe of leptodactylids, along with Cycloramphus Tschudi, 1838 and Zachaenus Cope, 1866, and reported its occurrence from “Guanabara” (a former Brazilian state, presently the Rio de Janeiro municipality) to Espírito Santo, along the Brazilian coast. The first extensive molecular phylogenetic study on amphibians did not included Crossodactylodes (Frost et al. 2006), but based on the phylogenetic relationships of its putative relatives, from which samples were available, the genus was allocated in the resurrected family Cycloramphidae. Posterior molecular analyses, still not including Crossodactylodes, lead Pyron and Wiens (2011) to create the subfamily Paratelmatobinae to harbor Paratelmatobius and Scythophrys. Crossodactylodes and Rupirana were not included in the analysis and remained as incertae sedis. However, they did not present a diagnosis for their new subfamily, rendering Paratelmatobinae a nomen nudum. This was later emmended by Ohler and Dubois (2012) which diagnosed the Paratelmatobinae. In a recent molecular study, Fouquet et al. (2013) included Crossodactylodes in the analysis and recovered it closely related to Paratelmatobius, Scythrophrys and Rupirana. Unaware of Ohler and Dubois (2012) previous diagnosis of Paratelmatobinae (sensu Pyron & Wiens 2011), Fouquet et al. (2013) proposed the new subfamily Crossodactylodinae (Fouquet et al. 2013), now including Crossodactylodes and Rupirana, rendering it a junior synonym of Paratelmatobinae Ohler & Dubois, 2012 ( Dubois 2013). Accepted by M. Vences: 20 Aug. 2013; published: 29 Aug. 2013 459 Tadpoles of Crossodactylodes pintoi were described from Santa Teresa municipality, in Espírito Santo (Peixoto 1981). However in the following year, two additional species were described from this locality: Crossodactylodes bokermanni and C. izecksohni by Peixoto (1982). The larvae formerly attributed to C. pintoi belonged to some of the newly described species. Currently, the genus comprises the three above referred species, still known only from the vicinities of their type localities, except for Crossodactylodes pintoi from which no additional specimens have ever been collected since the type series was obtained in 1909 (Peixoto & Carvalho-e-Silva 2004; Silvano & Peixoto 2004a; b). Herein based on recently collected specimens from the highlands of the Atlantic Forests in southern Bahia, we add a new species to the genus, providing its phylogenetic placement, along with first data on its osteology and natural history. Material and methods Field samplings The new species was found during an herpetofaunistic survey at Parque Nacional Serra das Lontras, Bahia, Brazil, in which pitfall traps and active search were used as sampling techniques. The pitfall traps were installed in four sets, ranging from 400 to about 600 m a.s.l. Each set consisted of five traps, with four 20 L buckets buried at the ground level, arranged in “Y” shape, and connected by a 4 m long and 50 cm high plastic fences. Traps remained open from 2nd to 9th March 2009, during the rainy season, totalizing an effort equivalent to 1,000 buckets/day. Active searches were carried out from 200 to 900 m a.s.l. by four to six people, during four to six hours per night, totalizing an effort of about 200 h/person, exploring the whole range of available habitats. Collected specimens were fixed in 10% formalin, preserved in 70% ethanol, and housed at Museu de Zoologia da Universidade de São Paulo (MZUSP). External Morphology and Morphometrics External morphology nomenclature follows Duellman (1970). Examination of morphological characters and measurements were taken after fixation, using a micrometric ruler and a Mitutoyo digital caliper (to the nearest 0.01 mm) under a stereomicroscope Zeiss STEMI SV6. Morphometric measurements were: snout-vent length, from the tip of snout to the vent (SVL); thigh length, from vent to knee (THL); tibia length, from knee to heel (TL); foot length, from tip of the longest toe to heel (FL); arm length, from arm insertion to elbow (AL); forearm length, from elbow to tip of the longest finger (FAL); eye-eye distance, between the anterior margin of orbit (EE); eye- nostril distance, between anterior margin of orbit to nostril (EN); eye diameter, measured horizontally (ED); head length, from posterior end of jaw to snout (HL), and head width, on its widest point (HW). Comparisons were made with voucher specimens housed at MZUSP (Appendix I) and with data from the literature (Lynch 1971; Peixoto 1982; Gomes 1988). Osteology Individuals from each currently recognized species (Crossodactylodes pintoi: MZUSP 104; C. bokermanni: MZUSP 58079; C. izecksohni: MZUSP 109013) and the holotype of the new species were scanned with a SkyScan digital microtomograph (www.skyscan.be), with a resolution of 9µm and no filters added. The images were processed in CT Analyzer v. 1.11 software, setting an automatic threshold point at the skull level, for filtering low- density matter (soft tissue). The resulting 3D models were visualized on CT Volume v. 2.2. Osteological nomenclature follows Duellman and Trueb (1994). Phylogenetics We generated partial sequences of four mitochondrial (12S, 16S, cyt b and COI) and two nuclear (TYR and RHO) genes from one individual of the new species, six individuals of Crossodactylodes izecksohni and five of C. 460 · Zootaxa 3702 (5) © 2013 Magnolia Press TEIXEIRA JR. ET AL. bokermanni. As outgroups we used: Paratelmatobius sp. (aff. cardosoi), Pleurodema diplolister, Lithodytes lineatus, Adenomera lutzi, Leptodactylus mystaceus, Rupirana cardosoi, and Odontophrynus americanus from Fouquet et al. (2013) (Appendix II). Total genomic DNA was extracted from liver and muscle according to Fetzner (1999) and amplification was carried using standard PCR protocols with primers 16SAR and 16SBR (Palumbi 1996) for amplification of 16S, primers LGL765 and V for cyt b (Bickham et al. 1995; Palumbi 1996), primers t-Phe-frog and t-Val-frog for 12S (Wiens et al. 2005), primers dgLCO1490 and dgHCO2198 for COI (Folmer et al 1994), primers TYR1E and TYR1G for tyrosinase (Bossuyt & Milinkovitch 2000), and primers Rhod1A and Rhod1C for rhodopsin (Bossuyt & Milinkovitch 2000). The PCR cycle protocol consisted of one initial cycle of 94 °C for 5 min followed by 35 cycles of 94 °C for 40 sec, 50 °C for 16S and cyt b, 55 °C for 12S, 60 °C for tyrosinase and 50-55 °C for rhodopsin for 40 sec, 72 °C for 40 sec. PCR products were directly purified with Exonuclease I and Shrimp Alkaline Phosphatase (USB or Fermentas). Automated sequencing was carried out using BigDye Terminator v3.1 Cycle Sequencing kit (Applied Biosystems), followed by analysis on ABI Prism 310, 3700 or 3170 Genetic Analyzer Sequencers (Applied Biosystems) according to the manufacturer’s instructions. Sequences were edited in CodonCode Aligner (CodonCode Corporation). The resulting sequences were aligned in ClustalX v. 2. (Larkin et al. 2007), and combined on BioEdit v. 7.2 (Hall 1999) in a matrix of 3,667 bp (16S: 891 bp; 12S: 554 bp; cyt b: 691 bp; COI: 658 bp; TYR: 532 bp; RHO: 341 bp). We selected the best fit model of nucleotide substitution per marker using jModelTest v. 2.1 (Darriba et al. 2012) and the Akaike Information Criterion (AIC): GTR+G for 16S and 12S; GTR+I+G for cyt b and COI; SYM+I+G for TYR and HKY +I for RHO. We inferred phylogenetic relationships using Bayesian and Maximum Likelihood methods on a concatenated dataset. Heterozygous sites for both nuclear markers were treated as ambiguities. The Bayesian analysis was implemented in MrBayes v. 3.2 (Ronquist et al. 2012), available on Cipres Science Gateway (Miller, Pfeiffer & Schwartz 2010) with four partitions, each including a set of genes with the same selected substitution model. Two independent runs were performed, with a random starting tree, four incrementally heated Markov chains each, and 20,000,000 generations, with trees sampled every 1,000.
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