Zootaxa, a New Species of Dendrophryniscus (Amphibia

A new species of Dendrophryniscus (Amphibia, Anura, Bufonidae) from the Atlantic Rainforest of southern Bahia, Brazil

RENATO SOUSA RECODER 1, MAURO TEIXEIRA JUNIOR, JOSÉ CASSIMIRO, AGUSTÍN CAMACHO & MIGUEL TREFAUT RODRIGUES Departamento de Zoologia, Instituto de Biociências. Universidade de São Paulo, Rua do Matão, Trav. 14, n 321, Cidade Universitária, Caixa Postal 11461, CEP 05422-970, São Paulo, SP, Brasil. 1Corresponding author. E-mail: [email protected]

Abstract

A new species of the tree toad genus Dendrophryniscus is described from a rainforest habitat at Parque Nacional de Serra das Lontras, municipality of Arataca, southern Bahia, Brazil. Dendrophryniscus oreites sp. nov. is related to the Atlantic forest brevipollicatus group by hand morphology, skin texture, ventral coloration and bromelicolous habits. The new species differs from related species by having a larger size, warty skin, inner finger reduced with presence of a dark nuptial pad in males, and a yellowish coloration with discrete dorsal pattern. This discovery highlights the importance of southern Bahia in terms of conservation, and for our understanding of the evolution of the frog diversity within the Atlantic Rainforest.

Key words: Tree toads, southern Bahia, Dendrophryniscus brevipollicatus group, frog diversity, forest remnants

Resumo

Uma nova espécie do sapo-arborícola Dendrophryniscus descrita para a Mata Atlântica do Parque Nacional de Serra das Lontras, município de Arataca, sul da Bahia, Brasil. Dendrophryniscus oreites sp. nov. relacionada ao grupo brevipollicatus da Mata Atlântica, pela morfologia da mão, textura da pele, coloração ventral e hábitos bromelícolas. A nova espécie difere das espécies relacionadas pelo maior tamanho, pele verrugosa, dedo proximal reduzido com a presença de um calo nupcial escuro em machos, e coloração amarelada com padrão dorsal discreto. Esta descoberta destaca a importância da região sul da Bahia em termos de conservação e para a compreensão da evolução da diversidade dos anuros da Mata Atlântica.

Palavras-chave: sapos-arborícolas, sul da Bahia, grupo brevipollicatus, diversidade, fragmentos florestais

Introduction

The family Bufonidae is one of the most specious among anurans with approximately 550 species in ca. 50 recognized genera, distributed nearly worldwide (Frost 2010). More than 50% of these species belong to a crown group comprising the formerly recognized genus Bufo and its closest relatives, which has been extensively studied from a taxonomic perspective (Blair 1972; Martin 1972; Graybeal 1997; Pauly et al. 2004; Frost et al. 2006; Pramuk 2006; Pramuk et al. 2008; Van Bocxlaer et al. 2010). Nevertheless, the diversity and systematics of the phylogenetically basal genera of bufonids — all restricted to the New World — are still poorly understood (Duellman & Lynch 1969; McDiarmid 1971; Cannatella 1986; Graybeal & Cannatella 1995). Recent phylogenetic studies recognized Dendrophryniscus Jiménez de la Espada 1871, also referred to as tree toads, as one of such basal bufonid lineage (Pramuk et al. 2008; Van Bocxlaer et al. 2010). These are

36 Accepted by M. Vences: 9 Sep. 2010; published: 12 Oct. 2010 small (18.0–28.0 mm SVL) forestial leaf-litter toads breeding in ponds, or in phytotelmata, where at least D. brevipollicatus and D. carvalhoi have been reported to breed (Carvalho 1949; Izecksohn & Cruz 1972; Izecksohn 1993; Pombal & Gordo 2004; Haddad & Prado 2005). Eight species are currently recognized within the genus: the Amazonian species D. minutus Melin 1941 and D. bokermanni Izecksohn 1993; and the coastal (Atlantic) rainforest species D. berthalutzae Izecksohn 1993; D. brevipollicatus Jimnez de la Espada 1871; D. carvalhoi Izecksohn 1993; D. krausae Cruz & Fusinatto 2008; D. leucomystax Izecksohn 1968 and D. stawiarskyi Izecksohn 1993. During a field trip to remnants of Atlantic Forest in the southern portion of the state of Bahia, Brazil, we collected one specimen of a new species of Dendrophryniscus tree toad. Given the unique morphology of the specimen, and in the face of the anthropogenic pressures that threaten the central corridor of the Atlantic forest, we considered it was preferable to describe it now rather than wait for additional specimens.

Material and methods

The following morphological measurements were obtained with a digital calliper to the nearest 0.01 mm under a stereoscopic microscope: snout vent length (SVL); head length (HL); head width (HW); internarial distance (IND); eye-snout distance (ESD); eye to nostril distance (END); horizontal eye diameter (ED); interorbital distance (IOD); upper eyelid width (UEW); thigh length (THL); tibia length (TL); tarsal length (TAL), foot length (FL), upper arm length (UAL); forearm length; and hand length (HL); following Duellman (1970) and Kok & Kalamandeen (2008). Finger nomenclature follows Fabrezi and Alberch (1996) and Coloma et al. 2010. Specimens of Dendrophryniscus spp. available in the herpetological collection of the Museu de Zoologia da Universidade de São Paulo (MZUSP) were examined for comparative purposes (Appendix I).

Results

Dendrophryniscus oreites sp. nov. (Figs. 1, 2, and 3)

Holotype. MZUSP 142493, M.T. Rodrigues field number MTR 16368, adult male, collected in “Parque Nacional de Serra das Lontras (a national park) (15o 09' 41" S, 39o 20' 38" W; datum WGS 84; ca. 850 m a.s.l.), Municipality of Arataca, State of Bahia, Brazil; 6 March 2009, collected by A. Camacho, J. Cassimiro, M. Teixeira Jr. and R.S. Recoder. Diagnosis. The new species is assigned to Dendrophryniscus by the following suite of characters: small size, habitus atelopodiform, hind limbs well developed (THL+TL/SVL > 0.80), parotoid glands absent, cranial crests indistinct, external tympanum absent, vocal slits absent, foot basally webbed, relative toe length I

A NEW SPECIES OF DENDROPHRYNISCUS FROM BRAZIL Zootaxa 2642 © 2010 Magnolia Press · 37 region vertical. Eye diameter about 70% of the interorbital distance, upper eyelid about 55% of the interorbital distance. Tympanum absent. Tongue long, narrow and free in the anterior half, with posterior margin rounded. Choanas small and circular, maxillary and palatine teeth absent. Vocal sac and vocal slits absent. Dorsal surface of body highly granulose, with numerous large rounded warts irregularly distributed. Warts forming lines or clusters of enlarged granules in the dorso-lateral region, sacral region and nuchal region. Ventral and lateral surfaces highly granulose, but with shallow and smaller warts. Forelimbs long. Forearms longer and more robust than arms. Hands with slender fingers, not webbed and not fringed, with distal end slightly enlarged and truncate, without discs. Inner finger short and robust, with a distinct dorsal dark nuptial pad. Relative lengths of fingers: II

FIGURE 1. Dendrophryniscus oreites sp. nov., holotype (MZUSP 142493) in life, adult male from Parque Nacional de Serra das Lontras, municipalities of Una and Arataca, state of Bahia, Brazil. Photo by Mauro Teixeira Jr.

Colour of the holotype. General colour in life yellow to yellowish-brown, lighter on ventral surfaces. Dorsum with a darker X-shaped blotch on the scapular region, and two posteriorly diverging chevron-like diagonal bars with the same colour, extending transversally from sacral region to hind limbs. Presence of a

FIGURE 2. Dendrophryniscus oreites sp. nov. (Holotype, MZUSP 142493, SVL 25.0 mm), dorsal and ventral views.

FIGURE 3. Dendrophryniscus oreites sp. nov., holotype, MZUSP 142493. Left: ventral view of hand (up) and foot (bottom). Right: lateral view of head (up), and dorsal view of the head (bottom). Dark scale bar represent 1 mm.

A NEW SPECIES OF DENDROPHRYNISCUS FROM BRAZIL Zootaxa 2642 © 2010 Magnolia Press · 39 Measurements of holotype. SVL 25.00; HL 9.15; HW 7.42; IND 2.01; ESD 3.92; END 2.65; ED 2.75; IOD 3.80; UEW 2.10; THL 10.67; TL 10.38; TAL 6.23; FL 9.53; UAL 4.85; FAL 5.90; HL 6.70. Comparisons. Dendrophryniscus oreites sp. nov. is distinguished from D. minutus and D. bokermanni by (features of compared taxa in parentheses): presence of expanded tip on fourth finger (tip not expanded); inner finger reduced (slightly reduced or longer than third finger); presence of transversely elliptical subarticular tubercles (longitudinally elliptical subarticular tubercles); and ventral surfaces pale coloured (ventral bright coloured with pattern of blotches or ocelli). Dendrophryniscus oreites sp. nov. is distinguished from the remaining Dendrophryniscus species by: larger size (male size less than 22 mm), body surfaces with numerous enlarged warts (body with small warts to finely granular), and yellowish coloration with a discrete dorsal pattern (greyish to brownish colour, with a well defined dorsal pattern in most species). Furthermore, Dendrophryniscus oreites sp. nov. is distinguished from D. brevipollicatus by having a fourth finger less expanded, with tip width corresponding to 1.33 times the width at the middle of the finger (tip width 1.53 + 0.1 of width at the middle, N=12), and palms of hands without grooves (palms with grooves); from D. leucomystax by the absence of a white stripe on lips (present); from D. carvalhoi by the dark coloration of nuptial pads in males (unpigmented); from D. berthalutzae by presenting a reduced inner finger with nuptial pads in males (inner finger slightly reduced, with nuptial pads indistinct), and no distinct subrostral crests on snout (subrostral crests present); from D. stawiarskyi by the presence of a dark nuptial pad in males (absence of nuptial pads); and from D. krausae by having an elongate body (body robust and slightly enlarged posteriorly).

FIGURE 4. Geographic distribution of Dendrophryniscus oreites sp. nov. in the context of its congeners. Blue dots: distribution of formerly known species in the genus; star: type locality of D. oreites sp. nov.

Distribution and natural history. Dendrophryniscus oreites sp. nov. is known solely from the type locality, Parque Nacional de Serra das Lontras, in the Atlantic Forest of the southern portion of the state of Bahia (Figure 4). This is the northernmost record for the genus in the Atlantic Forest domain (extending ca.

40 · Zootaxa 2642 © 2010 Magnolia Press RECODER ET AL. 540 km north of Santa Teresa, state of Espírito Santo, where D. carvalhoi occurs), and the only species known for the state. The single specimen was collected perching on a leaf of an epiphytic bromeliad, 1.2 to 1.5 meters high, at the border of a trail, between 12:00 pm and 13:00 pm. When approached, the individual hid within the sheaths of the leaves of the bromeliad. The habitat consisted of a steep and tall rainforest, with closed canopy, at the slope of a hill, about 850 m a.s.l. (Figure 5). Bromeliads and palms were abundant at the site, as well as mosses and lichens covering trunks and fallen logs. Dense leaf-litter covered the soil. Near the summit (950 m a.s.l.) the vegetation becomes lower, with several thin-trunk small trees. At this altitude there is almost no soil, and the vegetation grows on a tangle of leaves, roots and peat. Neither the call nor the tadpole of the new species are known. Etymology. The specific epithet is a noun in apposition from the Greek word oreites which means mountaineer. It is a reference to the locality of the holotype, a steep forest on the slope of a hill summit. Although the species may occur through lowland forests, it is more likely that the species would persist at mountainous forests in the future, due to the current high rates of vegetation conversion in lowlands of the Atlantic Rainforest. Remarks. Based on hand morphology (expanded toe tips, reduced inner finger, and transversely elliptical subarticular tubercles), body colour (pale ventral colour), ecology (use of epiphytic bromeliads as perch site) and geography, Dendrophryniscus oreites sp. nov. appears to be more related to the Atlantic Forest brevipollicatus group than to Amazonian species.

FIGURE 5. Habitat and landscape where the new species was found. Upper left: rain forest habitat at the slope of the Peito de Moça hill, at 850 m a.s.l. Upper right: the Peito de Moça hill (to 950 m a.s.l.), placed at Parque Nacional de Serra das Lontras, municipalities of Una and Arataca, state of Bahia. Bottom: panoramic view of the landscape in the surroundings of the type locality, showing the typical undulating relief of southern Bahia. Photos by Mauro Teixeira Jr.

Although Dendrophryniscus represent a relatively small group within Bufonidae, its diversity might be underestimated (Fouquet et al. 2007). The widespread Amazonian D. minutus, although locally common, occurs patchily throughout its distribution, shows notable colour variation (Duellmann 1978; Caldwell & Araújo 2005) and high molecular divergence among populations (Fouquet et al. 2007) — thus may represent a complex of species (Caldwell & Araújo 2005). In contrast, the Atlantic Forest group is composed of small- ranged species, which have been recorded in low numbers (Heyer et al. 1990; Dixo & Verdade 2006; Moraes et al. 2007; van Sluys et al. 2007; Haddad et al. 2008; Cichi et al. 2009). Most species occur in steep rainforest habitats associated with hills or mountain ridges, which imposes logistical constrains on sampling. Additionally, some nominal species of Atlantic Forest Dendrophryniscus also show intraspecific morphological variation that might as well be attributed to unrecognized species (Izecksohn 1993). Many genera of bufonids lack unambiguous synapomorphies supporting their monophyly (Graybeal & Cannatella 1985). Although the monophyly of Dendrophryniscus is supported by an extensive list of morphological characters (McDiarmid 1971), the genus is heterogeneous and just the unique skin texture is considered a synapomorphy (Cannatella 1986). Although there is no previous discussion about species relationships within Dendrophryniscus, Izecksohn (1993), proposed an infrageneric grouping based on reproductive mode, with D. minutus, D. bokermanni and D. leucomystax, belonging to a “pool-breeding group and D. brevipollicatus, D. carvalhoi, D. berthalutzae and D. stawiarskyi to a “bromeliad-breeding group. Cruz and Fusinatto (2008) followed this arrangement, and called the bromeliad-breeding species as the brevipollicatus group. Based on our morphological comparisons we propose, rather, a geographical grouping, with an Atlantic Forest brevipollicatus group characterized by cryptic ventral color, expanded tip of fourth finger, reduction of inner finger and subarticular tubercles transversely elliptical on hands, thus containing D. berthalutzae, D. brevipollicatus, D. carvalhoi, D. krausae, D. leucomystax, D. oreites sp. nov. and D. stawiarskyi. The Atlantic Forest of eastern South America is one of the richest and most threatened tropical rainforests of the world. It is thus ranked among the biodiversity hotspots (Myers et al. 2000), which harbours a high diversity of frogs (Haddad et al. 2008). Despite the extensive deforestation, local numbers of species and genera are still underestimated (Haddad & Prado 2005). The highly fragmented condition of the Atlantic forest coupled to other threats such as the upcoming climatic change and spread of amphibian diseases — such as chytridiomycosis — may be causing the loss of an inestimable number of species of frogs before we can make appropriate plans for their conservation (Eterovick et al. 2005). The mountains of southern Bahia have been suggested as a target for conservation, as they probably have remained forested as refuges during dry climatic periods in the Pleistocene, harbouring high diversity of species (Rodrigues et al. 2002). Paleoclimatic models and molecular data from lowland and mid-elevation hylid frogs showed high climatic stability in the Bahia region during the last glacial maximum and high levels of local genetic diversity, pinpointing the region as a hotspot within the Atlantic forest hotspot and predicting the occurrence of many yet undescribed local endemics (Carnaval et al. 2009). The discovery of a new species of Dendrophryniscus from an isolated montane forest remnant in southern Bahia gives support to Rodrigues et al. (2002) and Carnaval et al. (2009), and highlights the importance of the region for understanding and preserving biodiversity in the Brazilian Atlantic Forest.

Acknowledgements

We thank to Fundação de Amparo Pesquisa do Estado de São Paulo (FAPESP), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and National Science Foundation (NSF, DEB 0817035 to C. Moritz) for financial support. We are grateful to Gabriel Rodrigues dos Santos from the Instituto de Estudos Socioambientais do Sul da Bahia (IESB) and Bird Life for allowing access to the Parque Nacional de Serra das Lontras, and providing logistical support. Hussam Zaher and C. Castro-Mello allowed us to examine

42 · Zootaxa 2642 © 2010 Magnolia Press RECODER ET AL. specimens under their care at MZUSP. We also thank R.P. Damasceno and R.C. Amaro-Guilardi for help in fieldwork. Nerivaldo and “Zezito” from Fazenda Dois Braços for guidance on the trails of the reserve, and help in the field; A. Fouquet and A.C. Carnaval for critical reading and comments on a preliminary draft of the manuscript, and M. Vences and two anonymous reviewers for their critical review of the manuscript. Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) provided collection permit (14555-5).

References

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APPENDIX I. Specimens examined.

Dendrophryniscus berthalutzae—BRAZIL: SANTA CATARINA: Apiúna: Parque Nacional da Serra do Itaja (MZUSP 138813). PARANÁ: Guaraqueçaba: Reserva Natural Salto Morato (MZUSP 137962).

Dendrophryniscus bokermanni— BRAZIL: PARÁ: Rio Curuá-Una: Igarapé do Anta (MZUSP 58746–58747), Igarap do Poraquê (MZUSP 60281).

Dendrophryniscus brevipollicatus— BRAZIL: SÃO PAULO: Bertioga: Parque das Neblinas (MZUSP 139133– 139134); Santo André: Paranapiacaba (MZUSP 104000, 104003–104005). RIO DE JANEIRO: Resende (MZUSP 103872); Rio de Janeiro: Tijuca (MZUSP 103905–103957), Sumaré (MZUSP 103874).

Dendrophryniscus carvalhoi— BRAZIL: ESPÍRITO SANTO: Santa Teresa (MZUSP 104124–104135).

Dendrophryniscus leucomystax— BRAZIL: SÃO PAULO: Cananéia: Ilha do Cardoso (MZUSP 92521); Registro (MZUSP 138277).

Dendrophryniscus minutus— BRAZIL: MATO GROSSO: Apiacás (MZUSP 80735–41); Aripuanã (MZUSP 80551– 80591).