Zootaxa, a New Species of Elachistocleis (Anura; Microhylidae

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A new species of Elachistocleis (Anura; Microhylidae) from the Brazilian Amazon

LUÍS FELIPE TOLEDO Museu de Zoologia "Prof. Adão José Cardoso", Universidade Estadual de Campinas (UNICAMP), Instituto de Biologia, Rua Albert Einstein s/n, Caixa Postal 6109, CEP 13083-863, Campinas, São Paulo, Brasil. E-mail: [email protected]

Abstract

A new species of Elachistocleis (E. magnus) is described from the Amazon basin, in the municipality of Espigão do Oeste, state of Rondônia, Brazil. It differs from all other species of the genus by the combination of the following characters: i) size larger than 31 mm in adult males, ii) grayish ventral coloration, iii) presence of large post-commissural glands, iv) lack of red coloration in the body, and v) grayish dorsum in preserved individuals. There is dimorphism between males and females in size, structures and coloration. Vocalizations and larvae remain unknown.

Key words: Amphibia, Gastrophryninae, Elachistocleis magnus sp. nov., biodiversidade neotropical

Resumo

Uma nova espécie de Elachistocleis (E. magnus) é descrita da Amazônia Brasileira, tendo como localidade tipo o município de Espigão do Oeste, Estado de Rondônia. A espécie distingue-se das demais congenéricas pela combinação dos seguintes caracteres: i) tamanho maior que 31 mm em machos adultos, ii) coloração ventral acinzentada, iii) presença de uma grande glândula posterior à boca, iv) ausência de coloração vermelha no corpo e v) dorso acinzentado em animais em preservativo. Foi evidenciado dimorfismo sexual nesta espécie em tamanho, estruturas e coloração. A vocalização e as formas larvárias desta espécie permanecem desconhecidas.

Introduction

The Brazilian southern limits of the Amazon remains poorly explored in terms of amphibian taxonomy. In recent years some expeditions have been conduced to this region for faunal inventories. As a result, many new species are being collected in this region (i.e., south of the state of Pará, north of the state of Mato Grosso, and the state of Rondônia) and some were recently described, such as Chiasmocleis avilapiresae Peloso and Sturaro 2008, Hypsiboas leucocheilus (Caramaschi & Niemeyer, 2003), Proceratophrys concavitympanum Giaretta, Bernarde, and Kokubum, 2000, and P. rondoniae Prado and Pombal Jr., 2008. On the other hand, the natural habitats of this region are being intensively modified due to building of hydroelectric power plants, livestock, and agriculture (personal observation). Hence, this still undiscovered biodiversity may be endangered even before the description of many species. Elachistocleis Parker, 1927 is a Microhylidae genus for which recent molecular studies provide evidence for its placement in a South American microhylid radiation, the monophyletic Gastrophryninae (Van Bocxlaer et al. 2006; Van der Meijden et al. 2007). Presently the genus is composed of seven species [E. bicolor (Guérin-Méneville, 1838), E. cesarii (Miranda-Ribeiro, 1920), E. erythrogaster Kwet and Di-Bernardo, 1998, E. ovalis (Schneider, 1799), E. piauiensis Caramaschi and Jim, 1983, E. skotogaster Lavilla, Vaira, and Ferrari, 2003, and E. surinamensis (Daudin, 1802)], which certainly needs taxonomic revision. Just as one example, Nelson (1973) reported 12 different advertisement calls from 12 different populations, therefore, these populations could represent distinct, but still not described species. Recently, Lavilla et al. (2003) clarified many questions about the Elachistocleis ovalis - E. bicolor controversy, thereby making possible the

Accepted by M. Vences: 6 May 2010; published: 7 Jun. 2010 63 TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited. description of other species, such as E. skotogaster and the revalidation of E. cesarii (Lavilla et al. 2003; Toledo et al., 2010). Based on material deposited in museums, I recognized a new species from the municipality of Espigão do Oeste, state of Rondônia, Amazon basin, Brazil, which is here described.

Material and methods

Museum abbreviations of specimens are CFBH (Célio F. B. Haddad amphibian collection, Departamento de Zoologia, Unesp, Rio Claro, São Paulo, Brazil), ZUEC (Museu de Zoologia “Prof. Adão José Cardoso”, Unicamp, Campinas, São Paulo, Brazil), MZUSP (Museu de Zoologia da USP, São Paulo, Brazil), and MNRJ (Museu Nacional, Rio de Janeiro, Brazil). Abbreviations used in the measurements of adults are SVL (snout- vent length), AGL (axilla-groin length), HL (head length: from the snout to the corner of the mouth), HW (head width), ED (eye diameter), UEW (upper eyelid width), END (eye to nostril distance), IOD (interorbital distance: distance between the inner corners of the eyes), IND (internarial distance), SED (snout to eye distance), PCGL (post-commissural gland maximum length), HuL (humerus length: distance from the axilla to the elbow), RUL (radio-ulna length: distance between the elbow and anterior limit of the hand), HnL (hand length: distance from the anterior limit of the hand to the longest finger), THL (thigh length), TBL (tibia length), and FL (foot length: distance from the anterior limit of the foot to the longest toe). All measurements are presented in millimeters. Most of these measurements follow Duellman (1970) and Cei (1980). For morphometric measurements I used a digital caliper of 0.01 mm of precision and an ocular micrometer in a Zeiss stereomicroscope. Drawings of the adult were made using Zeiss Stereomicroscope.

Elachistocleis magnus sp. n.

Holotype. ZUEC 11384, adult male, collected at Fazenda Jaburi, in the municipality of Espigão do Oeste, (11º35' – 11º38' S, 60º41' – 60º45' W; 280 m a.s.l.) (Bernarde, 2007), state of Rondônia, Brazil, on January 1997 by P. S. Bernarde and M. N. C. Kokubum (Figure 1). Paratopotypes. CFHB 5156, 5158 (adult female and male, respectively) collected on May 2001 by P. S. Bernarde; CFBH 5157 (juvenile) collected on April 2001 by P. S. Bernarde; ZUEC 11381-83 (adult females), and 11385-86 (adult males) collected with the holotype. Diagnosis. Elachistocleis magnus is recognized by the following combination of characters: 1) ventral coloration in preserved individuals is white with gray spots or gray with white spots (depending on the prevalence of one of the colors); 2) grayish dorsum in preserved individuals; 3) presence of post- commissural glands, behind the corner of mouth; 4) lack of red blotches in the interior portion of legs or red stripes in the legs; and 5) SVL larger than 31 mm in adult individuals. Description of the holotype. ZUEC 11384. Adult male (Figure 1). Body robust, ovoid, SVL 31.76 mm, AGL 43.51 % of the SVL. Texture of the dorsal skin and undersurface of the body smooth. Skin on ventrolateral surfaces of body and area around the cloacal smooth. Anal flap absent; vent opening positioned posterodorsally. Head small and triangular, broader than long, HL 20.87 % of the SVL. No cranial crests. A conspicuous dorsolateral skin fold from back of the head to the anterior insertion of the arm. Another conspicuous lateral skin fold from the upper region of arm to the groin. A third skin fold crossing the chest between the axillae. Small eyes, slightly prominent. Snout pointed in dorsal view, protruding in lateral view. Nostrils directed anterolaterally, slightly protuberant. Choanae relatively small and round. Internarial distance narrow. Canthus rostralis distinct, slightly convex. Loreal region slightly concave. Interorbital space slightly convex. Lips nearly horizontal. Presence of large post-commissural glands (PCGL 53 % of HL) behind the corner of mouth. Tympanum concealed. Supratympanic fold absent. Upper jaw projects 1.69 mm beyond the lower jaw. Subgular vocal sac not expanded externally. Vocal slits present. Vomerine odontophores absent. Tongue large, elliptic. Arms robust and short. Fingers robust, short, free. Finger length I

64 · Zootaxa 2496 © 2010 Magnolia Press TOLEDO TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited. mm. Toes robust and free. Toe length I

FIGURE 1. Elachistocleis magnus sp. n., ZUEC 11384 (holotype; adult male). (A) Dorsal and (B) lateral views of head. Ventral views of hand (C) and foot (D).

Coloration. In preservative (70 % ethanol), dorsum and limbs are uniform dark grayish, with scarce minute brighter dots in the outer boundaries of the dorsum. Presence of a slim mid-dorsal (vertebral) white stripe, from the vent to the anterior third of the dorsum. Belly gray with minute scattered with white spots, mainly in the belly and ventral surfaces of legs. There are large irregular white spots in the groin and in the axillary region. There is also a broad, not well defined femoral light stripe. Throat brownish dark, darker than chest and belly. The chest presents a large yellowish blotch. In life the general coloration was quite the same but the inguinal spots and femoral stripe were yellow (P. S. Bernarde, personal communication). Variation. Females are larger than males (see Table 1). The throat of males is darker than the ones of the females ones (the throat of females is of the same color of the belly). The vertebral stripe may or may not be present in adult individuals. When present, it never reached the read in the observed individuals. The ventral spots may reach the flanks and the groin region of the animals. The white blotches in the groin and inner portions of the legs vary in size and shape. In half of the individuals blotches are present in the dorsal surface of feet. Geographical distribution. Only known from the type locality. Natural history notes. Elachistocleis magnus was misidentified as E. ovalis by Bernarde (2007) during

DESCRIPTION OF ELACHISTOCLEIS MAGNUS Zootaxa 2496 © 2010 Magnolia Press · 65 TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited. anuran fauna study in Jaburi farm. This species calls during October to March (wet season) in temporary ponds in the pasture areas (Bernarde, 2007).

FIGURE 2. Ventral (A) and dorsal (B) views of the holotype (ZUEC 11384; adult male) of Elachistocleis magnus sp. n.

Etymology. The specific name is an adjective derived from Latin meaning large, in allusion to the great size of this species in comparison to its congeners. It is one of the largest described species for the genus Elachistocleis. Comparison with other species. From Elachistocleis bicolor and E. ovalis the new species is readily distinguished by not presenting the immaculate, yellow, ventral coloration (belly gray with minute scattered with white spots in E. magnus) (see Lavilla et al., 2003 and Figure 2). From E. erythrogaster Kwet and Di- Bernardo, 1998 it is distinguished by the absence of the reddish coloration of the ventral portion of its body. From E. surinamensis (Daudin, 1802) it is distinguished by differences in body coloration (see plate XIII in Kenny, 1969 and Figure 3 in Toledo et al., 2010), bluish dorsum and presence of red blotches in the internal region of the legs of E. surinamensis and grayish dorsum and absence of red stripes in the legs in E. magnus. From E. skotogaster it is distinguished by presenting large post-commissural glands (absent in E. skotogaster). From E. bicolor, E. cesarii, E. piauiensis Caramaschi and Jim, 1983, and E. skotogaster it is distinguished by having a larger SVL in males (greater than 31 mm in males of E. magnus and smaller than 29 mm in males of the other referred species). Elachistocleis magnus is also larger than E. erythrogaster, but there is a small overlap in the SVL of these species (SVL range 29.1 – 32.3 mm in E. erythrogaster, and SVL range 31.8 – 36.6 in E. magnus). Discussion. While investigating museum specimens and pictures of live individuals from different sites in South America, I have noticed several different morphotypes (in regard to external morphology and classic measurements) assigned to the genus Elachistocleis. These different forms (in body coloration and shape) may represent different species that need to be evaluated, such as early suggestions based on the record of different advertisement calls (Nelson, 1973). Therefore, further taxonomical work within this group is a necessity, reinforced by the fact that habitat destruction is getting faster recently and declines of undescribed species may be ongoing.

TABLE 1. Measurements of the holotype and paratypes of Elachistocleis magnus.

Males including the holotype Females (N=4) Holotype (male; (N=4) ZUEC 11384) Sonut-vent length 33.80 ± 2.05 41.81 ± 1.94 31.8 (31.8 – 36.6) (39.8 – 43.8) Axila-groin length 15.99 ± 1.51 21.53 ± 1.46 13.8 (13.8 – 17.1) (20.2 – 23.1) Head length 7.09 ± 0.41 7.94 ± 0.76 6.6 (6.6 –7.6) (7.0 – 8.7) Head width 8.48 ± 0.51 10.01 ± 0.60 8.0 (8.0 – 9.1) (9.2 – 10.5) Eye diameter 1.89 ± 0.62 1.85 ± 0.08 1.4 (1.4 – 2.8) (1.7 – 1.9) Upper eyelid width 1.23 ± 0.07 1.32 ± 0.19 1.3 (1.1 – 1.3) (1.2 – 1.6) Eye-nostril distance 2.65 ± 0.45 3.10 ± 0.35 2.1 (2.1 – 3.1) (2.6 – 3.5) Interorbital distance 3.56 ± 0.23 4.28 ± 0.53 3.5 (3.3 – 3.8) (3.5 – 4.6) Internostril distance 1.96 ± 0.31 2.20 ± 0.16 1.7 (1.7 – 2.2) (2.1 – 2.4) Snout-eye distance 3.83 ± 0.29 4.51 ± 0.38 3.5 (3.5 – 4.2) (4.2 – 5.0) Post-commissural gland maximum length 3.68 ± 0.46 4.68 ± 0.43 3.5 (3.4 – 4.4) (4.4 – 5.3) Humerus length 4.53 ± 0.82 5.43 ± 1.17 3.9 (3.8 – 5.5) (4.0 – 6.6) Radio-ulna length 5.60 ± 0.34 6.78 ± 0.72 5.1 (5.1 – 5.9) (6.1 – 7.8) Hand length 7.53 ± 0.54 8.97 ± 1.06 7.4 (6.9 – 8.2) (7.4 – 9.6) Thigh length 11.59 ± 0.83 14.12 ± 0.82 11.8 (10.8 – 12.7) (13.0 – 14.9) Tibia length 12.28 ± 0.30 15.16 ± 0.92 11.9 (11.9 – 12.6) (13.9 – 15.9) Foot length 14.84 ± 0.38 17.15 ± 1.11 14.7 (14.4 – 15.2) (16.2 – 18.7)

Acknowledgments

Esteban O. Lavilla and Miguel Vences reviewed the manuscript. Paulo S. Bernarde provided unpublished information about live individuals. Célio F. B. Haddad, José Pombal Jr., and Hussan Zaher allowed the access to the amphibian collections CFBH, MNRJ, and MZUSP, respectively. Samira Rolim prepared the line drawings. FAPESP provided a grant (proc. no. 2008/50325-5) and a scholarship (proc. no. 2008/52847-9).

References

Bernarde, P.S. (2007) Ambientes e temporada de vocalização da anurofauna no Município de Espigão do Oeste, Rondônia, Sudoeste da Amazônia - Brasil (Amphibia: Anura). Biota Neotropica, 7(2), 87–92. Caramaschi, U. & Jim, J. (1983) A new microhylid frog, genus Elachistocleis (Amphibia, Anura), from northeastern Brasil. Herpetologica, 39(4), 390–394.

DESCRIPTION OF ELACHISTOCLEIS MAGNUS Zootaxa 2496 © 2010 Magnolia Press · 67 TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited.

Caramaschi, U & Niemeyer, H. (2003) New species of the Hyla albopunctata group from central Brazil (Amphibia, Anura, Hylidae). Boletim do Museu Nacional, zoologia, 504, 1–8. Cei, J.M. (1980) Amphibians of Argentina. Monit. Zool. Ital. (N.S.). Monogr., 2, 1–609. Duellman, W.E. (1970) The hylid frogs of Middle America. Monogr. Museum of Natural History of the University of Kansas, 1, 1–753. Giaretta, A.A., Bernarde, P.S. & Kokubum, M.N.C. (2000) A new species of Proceratophrys (Anura: Leptodactylidae) from the Amazon rain forest. Journal of Herpetology, 34(2), 173–178. Kenny, J.S. (1969) The Amphibia of Trinidad. In: P. W. Hummelinck (Ed.). Studies on the fauna of Curaçao and other Caribbean islands, 108, 1–78. Kwet, A. & Di–Bernardo, M. (1998) Elachistocleis erythrogaster, a new microhylid species from Rio Grande do Sul, Brazil. Studies on Neotropical Fauna and Environment, 33, 7–18. Lavilla, E.O., Vaira, M. & Ferrari, L. (2003) A new species of Elachistocleis (Anura: Microhylidae) from the Andean Yungas of Argentina, with comments on the Elachistocleis ovalis – E. bicolor controversy. Amphibia-Reptilia, 24, 269–284. Nelson, C.E. (1973) Mating calls of the Microhylinae: descriptions and phylogenetic and ecological considerations. Herpetologica, 29(2), 163–176. Peloso, P.L.V. & Sturaro, M.J. (2008) A new species of narrow-mouthed frog of the genus Chiasmocleis Méhelÿ 1904 (Anura, Microhylidae) from the Amazonian rainforest of Brazil. Zootaxa, 1947, 39–52. Prado, G.M. & Pombal Jr., J.P. (2008) Espécies de Proceratophrys Miranda-Ribeiro, 1920 com apêndices palpebrais (Anura; Cycloramphidae). Arquivos de Zoologia, 39(1), 1–85. Toledo, L.F., Loebmann, D. & Haddad, C.F.B. (2010). Revalidation and redescription of Elachistocleis cesarii (Miranda- Ribeiro, 1920) (Anura: Microhylidae). Zootaxa, 2418, 50–60. Van Bocxlaer, I., Roelants, K., Biju, S.D., Nagaraju, J. & Bossuyt, F. (2006) Late Cretaceous vicariance in Gondwanan amphibians. Plos One 2006(1), e74. Van der Meijden, A., Vences, M., Hoegg, S., Boistel, R., Channing, A. & Meyer, A. (2007) Nuclear gene phylogeny of narrow-mouthed toads (Family: Microhylidae) and a discussion of competing hypotheses concerning their biogeographical origins. Molecular Phylogenetics and Evolution, 44, 1017–1030.

Appendix I. Additional specimens examined

Elachistocleis bicolor: CFBH 3841; 3859; 4010 São Domingos, state of Santa Catarina, Brazil; CFBH 4225 Tabapuã, state of São Paulo, Brazil; CFBH 13608-10 Três Lagoas, state of Mato Grosso do Sul, Brazil; CFBH 18199 Bom Jesus, state of Rio Grande do Sul, Brazil. E. cesarii: MZUSP 529 Lectotype, Piquete, state of São Paulo, Brazil; CFHB 4132–37; 4147–48; 4209; 4230–31; 4233–37; 4256–7 Rio Claro, state of São Paulo, Brazil; ZUEC 8054 Campinas, state of São Paulo, Brazil; ZUEC 12031 Itirapina, state of São Paulo, Brazil, CFBH 4997 Itirapina, state of São Paulo, Brazil; CFBH 3768 Pontalina, state of Goiás, Brazil; CFBH 6575-6578 Rio Claro, state of São Paulo, Brazil; CFBH 10907 Ubatuba, state of São Paulo, Brazil; CFBH 23136 Angatuba, state of São Paulo, Brazil; ZUEC 599-600 São Paulo, state of São Paulo, Brazil; ZUEC 4246-48, 4250-51, 4263 Munhoz, state of Minas Gerais, Brazil; ZUEC 1417-18, 2848, 2862-63, 3031-32, 3069, 3072-76 Jaboticatubas, state of Minas Gerais, Brazil; ZUEC 6157 Viçosa, state of Minas Gerais, Brazil; ZUEC 4995-97 Santana do Riacho, state of Minas Gerais, Brazil. E. erythrogaster: MNRJ 39098 Paratype, Rio Grande do Sul, Brazil. E. piauiensis: CFBH: 15880; 15902-03; 23465-71 Viçosa do Ceará, state of Ceará, Brazil. E. surinamensis: ZUEC 9422–23 Rapidos de Komoiran, Estado Bolivar, Venezuela.