ON THE IDENTITY OF CYCLORAMPHUS JORDANENSIS HEYER, 1983 (ANURA: CYCLORAMPHIDAE)

Herpetologica, 64(4), 2008, 452 457 E 2008 by The Herpetologists League, Inc. ON THE IDENTITY OF CYCLORAMPHUS JORDANENSIS HEYER, 1983 (ANURA: CYCLORAMPHIDAE) VANESSA K. VERDADE 1,2 AND MIGUEL T. RODRIGUES 1 1 Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, Caixa Postal 11.461 CEP: 05422-970, São Paulo, Brazil ABSTRACT: Cycloramphus jordanensis was described based on a single preserved specimen from Campos do Jordão (22u 449 S, 45u 359 W), State of São Paulo, Brazil. While examining the holotype; we noticed the presence of toe and tarsal fringes. Because these characters are absent in Cycloramphus, we suspected that the species was mistakenly placed in the genus. X-ray images of the holotype revealed T-shaped terminal phalanges and fang-like teeth. Together with the presence of toe and tarsal fringes, these characters squarely place the specimen in the genus Megaelosia. Considering the striking niche differences between Cycloramphus and Megaelosia, we expect the new combination will facilitate location of new individuals of this rare frog. Key words: Anura; Atlantic forest; Cycloramphus; Megaelosia; Megaelosia jordanensis (Heyer) comb. nov.; Taxonomy THE GENUS Cycloramphus Tschudi, 1838 is presently allocated to Cycloramphidae (Frost et al., 2006; Grant et al., 2006) and comprises 27 nocturnal species (Brasileiro et al., 2007; SBH, 2007) restricted to the Atlantic forest Domain (Ab Saber, 1970). Most forms are associated with the fast flowing streams in montane areas of southern and southeastern Brazil (Frost, 2007; Heyer, 1983a,b; Heyer and Maxson, 1983). Relationships among Cycloramphus species were recently assessed in a phylogenetic analysis based on morphological characters in Verdade s (2005) unpublished Ph.D. thesis. According to this analysis, Cycloramphus can be considered a monophyletic assemblage only if species of Zachaenus Cope 1866 are included in the genus. We follow such an arrangement. Cycloramphus jordanensis Heyer, 1983 was described from a single preserved specimen collected in Campos do Jordão (22u 449 S, 45u 359 W), State of São Paulo, Brazil. No other specimen has been collected since the original description. While examining the holotype, we were surprised to find welldeveloped toe and tarsal fringes. These characters are absent in Cycloramphus but are considered to be a synapomorphy of Hylodidae (Frost et al., 2006; Grant et al., 2006). Hylodids also share, among other 2 CORRESPONDENCE: e-mail, vverdade@usp.br characters, the presence of dermal scutes on the top of digital discs, and T-shaped terminal phalanges (Frost et al., 2006). Like Cycloramphus, hylodids are stream dwellers, living along the Atlantic forest and in open areas beyond the tree line in eastern and southeastern Brazil (Frost, 2007; IUCN, 2006). However members of the Hylodidae are primarily diurnal, whereas Cycloramphus are nocturnal frogs. We took X-ray images of the holotype of Cycloramphus jordanensis (MZUSP 4522) using a Faxitron MX-20 machine with a specimen radiography system formatted to take digital images captured under a 10 3 5 cm area. Museum acronyms are Museu de Zoologia da Universidade de São Paulo, São Paulo, Brazil (MZUSP) and Museu Nacional, Rio de Janeiro, Brazil (MNRJ). The external morphology of the holotype of Cycloramphus jordanensis was described and illustrated by Heyer (1983a: 308 309). Although we fully agree with most of Heyer s description, we did see the tympanum externally, and we clearly recognized a tarsal fringe on the specimen (Fig. 1). Heyer (1983a), however, described the existence of a hidden tympanum and the presence of a tarsal fold. We believe that this difference may be due to dehydration of the preserved specimen. Additionally, we noticed the existence of expanded toe tips bearing a barely visible pair of dorsal scutes (Fig. 2). 452

December 2008] HERPETOLOGICA 453 FIG. 1. Tarsal fringe (arrow) on ventral left tarsus of Cycloramphus jordanensis holotype (MZUSP 4522); inner and outer metatarsal tubercles on left side of the picture. Despite the lateral elements of the skull being obliterated by the hands of the specimen, the X-ray images of the holotype (Fig. 3 5) allow the following osteological characterization. Premaxilla with an alary process projecting posterodorsally (Fig. 4); large fang-like teeth on premaxilla and maxilla (Figs. 4 5); vomers separated, with one vomerine tooth (Fig. 4); palatines present, projecting parallel to the base of the skull and widely separated (Fig. 3 4); pterygoids without a well developed ventral flange (Fig. 3); prootic and frontoparietal not fused (Fig. 3); condyles widely separated (Fig. 3); coracoid short, with anterior and posterior margins deeply concave (Fig. 3); clavicle slender and almost straight (Fig. 3); transverse process of presacral vertebra II the longest; transverse processes of last presacral vertebrae shortened and projecting perpendicularly to the vertebral axis; terminal phalanges T- shaped (Fig. 3); annulus tympanicus present (Fig. 5); maxilla massive with a distinctive postorbital process (Fig. 5); condition of zygomatic process of the squamosal touching the maxilla not clear (Fig. 5); mandibles bearing an odontoid ridge (Fig. 5). The images also show some of the damage inflicted to the specimen: the pelvic girdle is dislocated, the left ilium shaft is broken near the base, the sacral vertebra is lacking, and the left humerus is broken, as are the maxilla and mandible (Figs. 3 5). The following characters clearly exclude the specimen from Cycloramphus: annulus tympanicus visible externally, toe tips expanded into small disks bearing dorsal scutes, presence of inner and outer metatarsal fold, a well developed tarsal fold, terminal phalanges T- shaped, vomers widely separated bearing one large tooth, and palatines short and projecting FIG. 2. A pair of poorly developed dorsal scutes (arrow) on dorsal third toe of Cycloramphus jordanensis holotype (MZUSP 4522). parallel to the base of the skull. As pointed out earlier, the external morphology of the specimen suggests that it is a member of family Hylodidae, and the osteology strongly supports this conclusion. Our osteological observations agree with the detailed description of Hylodidae osteology presented and illustrated by Lynch (1971, under subfamily Elosiinae); in particular the T-shaped terminal phalanges and the alary processes of premaxillae with a lateral projection clearly place the species within the family. Hylodinae genera have been externally diagnosed on the basis of snout vent length (SVL) (Crossodactylus and Hylodes reaching SVL 30 45 mm; Megaelosia SVL 70 120 mm), condition of nuptial asperities (present in Crossodactylus and Hylodes; absent in Megaelosia), and vocal sac morphology (a single median vocal sac in Crossodactylus; paired lateral or absent vocal sac in Hylodes and Megaelosia) (Lynch, 1971). In terms of osteological characters, Crossodactylus lacks a quadratojugal. Megaelosia, in turn, is easily differentiated from the remaining Hylodidae by the presence of fang-like teeth (Cochran, 1955; Lynch; 1971), a massive construction of maxillae, the presence of an enlarged zygomatic ramus of the squamosal, which touches

454 HERPETOLOGICA [Vol. 64, No. 4 FIG. 3. X-ray images of Cycloramphus jordanensis (MZUSP 4522). (A) Dorsal view of head and trunk. (B) Detail of terminal phalanx on left foot. Alary process of premaxilla (a), vomer (b), palatine (c), pterygoid (d), frontoparietal not fused to prootic (e), condyle (f), coracoid (g), clavicle (h), broken humerus (i), transversal process of vertebrae V (j), and broken ilium shaft (k). the maxilla, and the presence of a distinctive odontoid ridge in the mandibles (Lynch, 1971: 41, 169). Characters of external anatomy and our X-ray images clearly indicate that C. jordanensis is a Megaelosia; accordingly, we formally transfer this species to that genus: Megaelosia jordanensis (Heyer) comb. nov.

December 2008] HERPETOLOGICA 455 FIG. 4. X-ray images of Cycloramphus jordanensis holotype (MZUSP 4522). Dorsal view of snout: alary process of premaxilla (a), fang-like tooth (b), vomerine tooth (c), and palatine (d). Currently, Megaelosia Miranda-Ribeiro 1923 is comprised of six endemic species living in the mountain streams of the Atlantic forest of southeastern Brazil: M. apuana Pombal, Prado and Canedo 2003, M. bocainensis Giaretta, Bokermann and Haddad 1993, M. boticariana Giaretta and Aguiar 1998, M. goeldi Baumann 1912, M. lutzae Izecksohn and Gouvêa 1987 1985, and M. massarti (Witte, 1930). Campos do Jordão is located in the Serra da Mantiqueira, between the ranges of M. boticariana and M. lutzae (Fig. 6). Giaretta and Aguiar (1998) referred to a Megaelosia sp2 for the same mountain range, without specifying the locality. This specimen was never again mentioned in the literature, but because its locality coincides with the Campos do Jordão general area (Fig. 6) it may be possible that the specimen corresponds to M. jordanensis. For now, we leave comparisons of M. jordanensis with its congeners until new specimens have been collected. The main characters differentiating the species within Megaelosia are skin granulation and development of finger and toe discs and dorsal scutes (Giaretta et al., 1993). These characters are barely assessable due to the poor condition of the holotype. The new generic allocation proposed here may help in locating new specimens of M. jordanensis. Despite occupying similar environments, the biology of Cycloramphus and Megaelosia differ strikingly. Megaelosia are diurnal frogs (but see Pombal et al., 2003) living on rocks near torrents; and Megaelosia tadpoles live in slow-flowing pools of forest streams. The stream-associated Cycloramphus are nocturnal and live on rock crevices, and FIG. 5. X-ray images of Cycloramphus jordanensis holotype (MZUSP 4522). Lateral view: phalanx (a), zygomatic process of squamosal (b), annulus tympanicus (c), postorbital process of maxilla (d), broken mandible (e), T-shaped terminal phalanx (f), fang-like teeth (g), and odontoid ridge on mandible (h). their semi-terrestrial tadpoles live on rocks in the splash zone (Heyer, 1983a,b; Lutz, 1928, 1929). Our field experience suggests that searches for Megaelosia should be more successful during the dry season. The paucity of data on natural history of Megaelosia is striking. Except for M. goeldi, classified as Least Concern (LC) in the Global Amphibian Assessment database (IUCN, 2006), all other species are categorized as Data Deficient (DD). It is therefore important to increase efforts searching for both new populations of these frogs and additional details concerning their natural history. These amphibians are top predators associated with mountain streams at altitudes from 800 2000 m a.s.l. in the Atlantic Forest areas, a well-known biodiversity hotspot (Giaretta and Aguiar, 1998; Giaretta et al., 1993; Myers et al., 2000). Furthermore, the distributional area of Megaelosia is entirely within the range of occurrence of Batrachochitrium dendrobatidis in Brazil (Carnaval et al., 2006; Toledo et al., 2006) suggesting a dangerous combination of factors that may lead to population crashes in the near future (e.g., Lips et al., 2003, 2006; Skerratt et al., 2007). Acknowledgments. We thank H. Zaher and C. Castro- Mello (MZUSP), and J. P. Pombal Jr. and C. Canedo (MNRJ) for access to specimens; M. C. Pinna and E. G. Baena for the X-ray images; A. B. Carvalho and J. Cassimiro for photographs; IBAMA (process 2001. 004024/01-42) and IF/COTEC (process 42.495/2003) for collection permits; the staff of the Parque Estadual Campos do Jordão for logistics and J. Cassimiro, F. F.

456 HERPETOLOGICA [Vol. 64, No. 4 FIG. 6. Distribution of the Megaelosia in southeastern Brazil (adapted from Giaretta and Aguiar, 1998; including also localities listed at Appendix 1). Areas above 800 m are shaded in gray. Curcio, and D. Pavan for helping in the field; T. Mott and R. Moretti for reading and criticizing early versions of the manuscript; and A. Mathis, M. Harvey, J. P. Pombal Jr., W. R. Heyer, and A.C. Carnaval for making valuable suggestions to improve it. The research was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) processes 2001/05470-8 and 2003/10335-8. LITERATURE CITED AB SABER, A. N. 1970. Províncias geológicas e Domínios morfoclimáticos no Brasil. Geomorfologia 20:1 25. BRASILEIRO, C. A., C. F. B. HADDAD, R.J.SAWAYA, AND I. SAZIMA. 2007. A new and threatened island-dwelling species of Cycloramphus (Anura: Cycloramphidae) from Southeastern Brazil. Herpetologica 63:501 510. CARNAVAL, A. C. O. Q., R. PUSCHENDORF, O. L. PEIXOTO, V. K. VERDADE, AND M. T. RODRIGUES. 2006. Amphibian chytrid fungus broadly distributed in the Brazilian Atlantic Rain forest. EcoHealth 3:41 48. COCHRAN, D. M. 1955. Frogs of southeastern Brazil. Bulletin of the United States Natural Museum 206:1 411. FROST, D. R. 2007. Amphibian Species of the World: an Online Reference. Version 5.1 (10 October, 2007). Eletronic Database available at http://research.amnh. org/herpetology/amphibia/index.php. American Museum of Natural History, New York, New York, U.S.A. FROST, D. R., T. GRANT, J.FAIVOVICH, R.H.BAIN, A.HAAS, C. F. B. HADDAD, R. O. DE SÁ, A. CHANNING, M. WILKINSON, S.C.DONNELLAN, C.J.RAXWORTHY, J.A. CAMPBELL,B.L.BLOTTO,P.MOLER,R.C.DREWES,R.A. NUSSBAUM, J. D. LYNCH, D. M. GREEN, AND W. C. WHEELER. 2006. The amphibian tree of life. Bulletin of the American Museum of Natural History 297:1 370. GIARETTA, A. A., AND O. AGUIAR. 1998. A new species of Megaelosia from the Mantiqueira range, Southeastern Brazil. Journal of Herpetology 32:80 83. GIARETTA, A. A., W. C. A. BOKERMANN, AND C. F. B. HADDAD. 1993. A review of the genus Megaelosia (Anura, Leptodactylidae) with a description of a new species. Journal of Herpetology 27:276 285. GRANT, T., D. R. FROST, J. P. CALDWELL, R. GAGLIARDO, C. F. B. HADDAD, P. J. R. KOK, D. B. MEANS, B. P. NOONAN, W. E. SCHARGELK, AND W. C. WHEELER. 2006. Phylogenetic systematics of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bulletin of the American Museum of Natural History 299:1 262. HEYER, W. R. 1983a. Variation and systematics of frogs of the genus Cycloramphus (Amphibia, Leptodactylidae). Arquivos de Zoologia, São Paulo 30:235 339. HEYER, W. R. 1983b. Notes on the frog genus Cycloramphus (Amphibia: Leptodactylidae), with descriptions of two new species. Proceedings of the Biological Society of Washington 96:548 559. HEYER, W. R., AND L. R. MAXSON. 1983. Relationships, zoogeography, and speciation mechanisms of frogs of

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