Herpetologica, 59(4), 2003, 521–526 Ó 2003 by The Herpetologists’ League, Inc.

A NEW, BRIGHTLY COLORED SPECIES OF (ANURA: ) FROM MINAS GERAIS, SOUTHEASTERN BRAZIL

1,4 2 3 ULISSES CARAMASCHI ,RENATO N. FEIO , AND ARISTIDES S. GUIMARA˜ ES-NETO 1Departamento de Vertebrados, Museu Nacional/UFRJ, Quinta da Boa Vista, 20940-040 Rio de Janeiro, RJ, Brasil 2Departamento de Biologia , Universidade Federal de Vic¸osa, 36571-000 Vic¸osa, MG, Brasil 3Instituto Estadual de Florestas, Caixa Postal 116, 35400-000 Ouro Preto, MG, Brasil

ABSTRACT: A new, brightly colored species of Physalaemus similar to P. deimaticus and P. rupestris is described from the Parque Estadual do Itacolomi, Municipality of Ouro Preto, State of Minas Gerais, southeastern Brazil. The new species is characterized by its small size (snout–vent length 23.2 mm in male, 26.2–26.6 mm in females) and by having the snout rounded in the dorsal view and protruding in profile; large inguinal glands, ovoid, light brown with a black ocellus outlined with white on their posterior half; light grayish brown dorsum with elongate longitudinal dark grayish brown stripes and blotches; venter white with gray mottling; and bright red on groin and ventral surfaces of arms, hands, thighs, tibiae, and feet. Key words: Amphibia; Anura; Leptodactylidae; Physalaemus erythros sp. nov.; Southeastern Brazil;

THE genus Physalaemus contains 41 were collected. Herein, we describe this new recognized species that are distributed from species. Mexico to southern South America (Frost, 2002). The genus has been arranged into four MATERIALS AND METHODS species groups by Lynch (1970); however, these groupings have been disputed and Specimens examined are deposited in treated as non-monophyletic (Cannatella and MNRJ (Museu Nacional, Rio de Janeiro, RJ, Duellman, 1984; Heyer and Wolf, 1989). Brazil), MZUFV (Museu de Zoologia Joa˜o Although Caramaschi et al. (1991) considered Moojen de Oliveira, Universidade Federal these groups useful in discussing diversity de Vic¸osa, MG, Brazil), and JJ (Jorge Jim within the genus, the affinities of several Collection, housed in the Departamento de species with the currently recognized species Zoologia, Universidade Estadual Paulista, groups is unclear. For instance, P. deimaticus Botucatu, SP, Brazil). Specimens examined Sazima and Caramaschi, 1988 and P. rupestris are listed in Appendix I. Caramaschi, Carcerelli and Feio, 1991 appar- Abbreviations used for measurements in ently do not belong to any of Lynch’s (1970) millimeters are SVL (snout–vent length), HL species groups. Both species are similar in (head length), HW (head width), IND (inter- morphology and , as noted by Carama- narial distance), END (eye–nostril distance), schi et al. (1991), but these authors were ED (eye diameter), UEW (upper eyelid unwilling to propose a new group for that width), IOD (interorbital distance), THL species without a more thorough study of the (thigh length), TL (tibia length), and FL (foot genus, although they recognized that it might length). Specimens were fixed in 10% formalin constitute a distinct morphological and eco- and preserved in 70% alcohol. Measurements logical unity. were made to the nearest 0.01 mm with digital During a survey of anuran species of the calipers under a Zeiss SV-4 stereomicroscope; Parque Estadual do Itacolomi in the State of drawings of the holotype were made using Minas Gerais, Brazil, specimens of a brightly a drawing tube. colored species morphologically and ecologi- Physalaemus erythros sp. nov. cally similar to P. deimaticus and P. rupestris Holotype.—MNRJ 27986, adult male (Fig. 1) from Parque Estadual do Itacolomi (208 259 S, 438 299 W, approximately 1600 m elevation), 4 CORRESPONDENCE: e-mail, [email protected] Municipality of Ouro Preto, State of Minas

521 522 HERPETOLOGICA [Vol. 59, No. 4

FIG. 1.—Dorsal and ventral views of Physalaemus erythros sp. nov. (MNRJ 27986, holotype, SVL 23.2 mm).

Gerais, Brazil, 29 October 2001, collected by group of Lynch (1970) by the smaller size A. S. Guimara˜es-Neto and J. B. Isaac, Jr. (combined SVL of the three species, 15.9–23.2 Paratypes.—Collected in the type locality: mm in males, 17.2–26.6 mm in females; of the MNRJ 27539, adult female, 22 October 2001, species in the P. biligonigerus group, 40–45 by R. N. Feio and A. S. Guimara˜es-Neto; mm), relatively slender build (chubby in P. MNRJ 30608, adult female, 12–13 December biligonigerus group), tarsal tubercle absent 2002, by A. S. Guimara˜es-Neto, C. A. G. Cruz, (present in P. biligonigerus group), inner R. N. Feio, L. B. Nascimento, and J. P. metatarsal tubercle ovoid and outer metatarsal Pombal, Jr. tubercle rounded (enlarged, compressed Diagnosis.—A species ressembling P. de- metatarsal tubercles in P. biligonigerus group), imaticus and P. rupestris was diagnosed by the and absence of premaxillary and maxillary following characters: (1) relatively small size teeth (present in P. biligonigerus group, except (SVL 23.2 mm in male, 26.2–26.6 mm in P. nattereri). From the P. pustulosus group, by females); (2) snout rounded in dorsal view and the dorsal skin rugose (tuberculate in P. protruding in profile; (3) vomerine, premaxil- pustulosus group), inguinal glands present lary, and maxillary teeth absent; (4) relative (absent in P. pustulosus group), absence of lengths of fingers II , IV , I , III; (5) dorsal parotoid and flank glands (present in P. skin slightly rugose, ventral skin smooth, and pustulosus group), and tarsal tubercle absent proximal undersurfaces of thighs granular; (6) (present in P. pustulosus group, except P. parotoid glands absent; (7) inguinal glands freibergi and P. pustulatus). From the P. large, ovoid, light brown with a black, white signifer group, by the dorsal skin rugose outlined ocellus on their posterior half; (8) (smooth in P. signifer group), snout rounded dorsum light grayish brown with elongate in dorsal view (acuminate in P. signifer group), longitudinal grayish dark brown stripes and no black lateral, defined band from eye to blotches; (9) venter white with gray mottling; groin (present in P. signifer group), concealed (10) ventral surfaces of arms, hands, thighs, tympanum (evident in P. signifer group, except tibiae, feet, and inguinal region bright red. P. maculiventris and P. olfersi), and inner Comparisons with other species.—Physalae- metatarsal tubercle present (absent in P. mus deimaticus, P. erythros, and P. rupestris signifer group). From the P. cuvieri group, are excluded from the P. biligonigerus species by the absence of tarsal tubercle (inner tarsal December 2003] HERPETOLOGICA 523 tubercle present in P. cuvieri group), presence 2C); lateral sides of fingers weakly fringed; of large inguinal glands (lack or small inguinal nuptial pad large, subdivided among prepoll- glands in P. cuvieri group), and absence of ical region and dorsal surface of finger I; premaxillary and maxillary teeth (present in subarticular tubercles single, round; inner P. cuvieri group). metacarpal tubercle absent; outer metacarpal Physalaemus erythros is distinguished from tubercle large, ovoid; supernumerary tuber- P. deimaticus and P. rupestris (see Caramaschi cles present; tip of fingers slightly expanded; et al., 1991; Nascimento et al., 2001; Sazima relative lengths of fingers II , IV , I , III. and Caramaschi, 1988) by the greater size Legs robust; tibia length shorter than thigh (SVL 21.4 mm in male, 24.2–24.4 mm in length; sum of tibia and thigh lengths less than females of P. deimaticus; 15.9–18.3 mm in SVL; foot length longer than lengths of both males, 17.2–17.9 mm in females of P. rupest- tibia and thigh; toes long, free, weakly fringed ris) and the shape of the snout, which is more (Fig. 2D); tarsal tubercle absent; inner meta- elongate, round in dorsal view and protruding tarsal tubercle large, ovoid, protruding; outer in profile (short, slightly acuminate in dorsal metatarsal tubercle small, conical, protuber- view and truncate in profile in P. deimaticus, ant; subarticular tubercles single, round, pro- see figures 2–3 in Sazima and Caramaschi, truding; supernumerary tubercles absent; tip 1988; short, rounded in dorsal and lateral of toes slightly expanded; relative lengths of views in P. rupestris, see figures 2A–B in toes I , II , V , III , IV; tarsal fold, crest, Caramaschi et al., 1991). The color pattern of and tubercles absent. Inguinal glands large, the inguinal glands is light brown with a black, ovoid, with an ocellus on posterior half. Dorsal white outlined ocellus on the posterior half skin slightly rugose, ventral skin smooth; (inguinal glands dark brown to black with a fine proximal undersurfaces of thighs granular. light brown to white border in P. deimaticus In life, ground color of dorsum grayish light and P. rupestris). There is also a bright red brown with irregular, longitudinal grayish dark color on the ventral surfaces of the arms, brown stripes; an irregular grayish dark brown hands, thighs, tibiae, feet, and inguinal region blotch on each upper eyelid; a dark brown, (hands, feet, and inguinal region pink to light white outlined, longitudinal and semidivided red in P. deimaticus; palms and soles reddish mark from shoulder to region of urostyle; with scattered black dots in P. rupestris). dorsal surfaces of arms and limbs grayish light Description of holotype.—General aspect brown with grayish dark brown transverse robust; head slightly longer than wide; head stripes and bars. Loreal region gray dorsally width approximately one-third SVL; snout and grayish brown ventrally. A distinct lateral rounded in dorsal view (Fig. 2A), protruding black stripe from posterior corner of eye to in profile (Fig. 2B); nostrils slightly protuber- groin, dorsally outlined by a white line; small ant, directed anterolaterally, nearer to tip of white dots scattered within this lateral black snout than to eyes; internarial distance slightly stripe. Inguinal glands light brown with a black, smaller than eye–nostril distance, equal to white outlined ocellus on the posterior half. upper eyelid width; canthus rostralis rounded, Gular region gray, venter white with gray slightly concave; loreal region concave; eye mottling. Red blotch extending from lateral lateral, slightly protuberant; eye diameter regions of chest and proximal undersurfaces of larger than internarial and interorbital dis- arms to elbow. Ventral surfaces of hands and tances; tympanum concealed; supratympanic fingers red. Dorsal surfaces of hands and fold indistinct; vocal sac poorly developed, fingers III and IV grayish red, fingers I and subgular; vocal slits present; choanae large, II red. A large red blotch extending from rounded, widely separated; tongue narrow, inguinal region to middle of ventral surface of long, not notched posteriorly; vomerine, pre- thighs and immediately below anal region. maxillary, and maxillary teeth absent; a single, Undersurfaces of tibiae and internal area of very small odontoid process protrudes dorsally feet to toes I, II, and III, red; toes IV and V from the symphysis of the mentomeckelian grayish red with subarticular tubercles red; cartilage. Arms robust, forearms slightly hy- metatarsal tubercles red. Iris yellow with pertrophied; fold and crest on forearm absent; intense black vermiculation. In preservative, fingers long, slender, lacking webbing (Fig. general color becomes gray with dark gray 524 HERPETOLOGICA [Vol. 59, No. 4

REMARKS The specimens were collected at the Serra do Itacolomi, in the Espinhac¸o Mountain Range, in an ephemeral pond at approximately 1600 m above sea level. This pond consists of a rain-flooded depression of approximately 800 m2 located in a rocky field called ‘‘campo rupestre,’’ with bushes and small trees on a sandy soil predominantly covered with grasses. Some scattered massifs of quartzitic rocks emerge in the field. The sparse bushes and small trees emerging from the continuous herbaceous layer are typical elements also found in other regions of ‘‘campos rupestres,’’ such as Velloziaceae, Orchidaceae, Bromelia- ceae, and Eryocaulaceae (mainly Paepalan- thus), and isolated Melastomataceae. The perimeter of the flooded area is densely covered by Juncaceae (mainly Juncus cf. FIG. 2.—Physalaemus erythros sp. nov. (MNRJ 27986, microcephalus), Cyperaceae, and grasses, leav- holotype). (A) Dorsal view of head; (B) lateral view of head; (C) ventral view of hand; (D) ventral view of foot. ing only a small central portion of standing water, which is a typical ephemeral pond in an open area. During the dry months (April– marks on dorsum, grayish cream on arms and September), the pond becomes totally dry, and limbs; red color fades to cream. peats and lichens cover the exposed areas Measurements of holotype.—SVL 23.2; HL between grasses. The regional climate is of 7.8; HW 7.5; IND 1.8; END 1.9; ED 2.4; CwB type (Ko¨ppen), that is, wet temperate UEW 1.8; IOD 2.2; THL 10.3; TL 10.0; FL with dry winters and hot and rainy summers. 11.0. The annual rain mean is 1450–1900 mm Measurements of paratypes.—SVL 26.2– (Pedralli et al., 2001). The site, despite its 26.6; HL 7.5–7.9; HW 8.1; IND 1.8–1.9; location in a conservation area, undergoes END 1.9; ED 2.4–2.7; UEW 1.9–2.0; IOD anthropogenic pressures, including frequent 2.3–2.5; THL 10.7–11.2; TL 10.6–10.8; FL visitations by horses (feces were observed in 12.2–12.8. the pond where the were collected). In Variation.—Besides the measurements and addition, the area was accidentally burned. details of color pattern involving the shape of Specimens of P. erythros were occasionally the dorsal marks and minor differences in the collected in October and December, in the extension of red areas, there is little variation rainy season. The advertisement call and among the type specimens. This small varia- tadpole of this species are unknown. tion in color probably is not associated with In a more extensive survey of anuran species sexual dimorphism, as also referred to P. of the Parque Estadual do Itacolomi, con- rupestris by Nascimento et al. (2001). The ducted between January 1998 and April 1999 male holotype has slightly hypertrophied arms; in two areas covered by ciliary and seasonal the first finger has a nuptial pad; the vocal sac forests and ponds, Pedralli et al. (2001) is poorly developed; and the venter has a finer registered 24 species. These included bufonids mottling. The female paratype MNRJ 27539 (Bufo crucifer), hylids (Hyla albopunctata, H. has a slim aspect and the venter is withered, arildae, H. cavicola, H. decipiens, H. elegans, which suggests recent egg laying. H. faber, H. martinsi, H. minuta, H. pardalis, Etymology.—The specific name ‘‘erythros,’’ H. polytaenia, H. semilineata, Hyla sp. of the meaning ‘‘red,’’ is a Greek adjective used in circumdata group, Scinax eurydice, S. flavogut- reference to the remarkably bright ventral tatus, S. longilineus, S. luizotavioi, and S. rizi- color pattern of the species. bilis), and leptodactylids (Eleutherodactylus December 2003] HERPETOLOGICA 525 izecksohni, Hylodes sp. of the lateristrigatus zentado, ventre branco com marmoreado group, fuscus, L. labyrinthicus, cinza e forte colorido vermelho nas superfı´cies L. ocellatus, and ). ventrais dos brac¸os, ma˜os, coxas, tı´bias, pe´se regia˜o ingu¨ inal. DISCUSSION Acknowledgments.—We thank C. A. G. Cruz, J. B. The peculiar areas of open vegetation Isaac, Jr., J. P. Pombal, Jr., and L. B. Nascimento for help occurring above 1000 m high in montane in the field work, H. C. Souza for botanical information on regions of southeastern Brazil, mainly associ- the surveyed area, P. R. Nascimento for the line drawings, ated with the Cerrados and Atlantic Rain and C. A. G. Cruz and J. P. Pombal, Jr. for critically reviewing the manuscript. We acknowledge the Instituto Forest Morphoclimatic Domains (Ab’Saber, Estadual de Florestas de Minas Gerais for permission to 1977), are called ‘‘campos rupestres’’ (see collect in the Parque Estadual do Itacolomi; U. Carama- Rizzini, 1979 for definition). These isolated schi thanks the Conselho Nacional de Desenvolvimento highland areas commonly contain faunistic and Cientı´fico e Tecnolo´gico (CNPq) for the fellowship. floristic endemics (see Heyer, 1999 for com- ments), as exemplified by the three species of LITERATURE CITED Physalaemus, respectively associated with the AB’SABER, A. N. 1977. Os domı´nios morfoclima´ticos na Serra do Cipo´ (P. deimaticus, see Sazima and Ame´rica do Sul. Primeira aproximac¸a˜o. Geomorfologia Caramaschi, 1988), to the Serra do Ibitipoca 52:1–21, 1 map. CANNATELLA, D. C., AND W. E. DUELLMAN. 1984. (P. rupestris, see Caramaschi et al., 1991; Leptodactylid frogs of the Physalaemus pustulosus Nascimento et al., 2001), and to the Serra do group. Copeia 1984:902–921. Itacolomi (P. erythros, present study). In CARAMASCHI, U., L. C. CARCERELLI, AND R. N. FEIO. 1991. addition to sharing similar , the three A new species of Physalaemus (Anura: Leptodactylidae) species share morphological traits such as from Minas Gerais, Southeastern Brazil. Herpetologica 47:148–151. relatively small size for the genus, poorly FROST, D. R. 2002. Species of the World: An developed vocal sacs, large inguinal glands, Online Reference, Version 2.21. http://research.amnh. and the presence of red or reddish areas on org/herpetology/amphibia/index.html fore and hindlimbs. Deimatic behavior, as HEYER, W. R. 1999. A new genus and species of frog from Bahia, Brazil (Amphibia: Anura: Leptodactylidae) with reported for P. deimaticus by Sazima and comments on the zoogeography of the Brazilian campos Caramaschi (1988), was not observed for P. rupestres. Proceedings of the Biological Society of rupestris (Nascimento et al., 2001) or for P. Washington 112:19–39. erythros. The advertisement call and tadpole HEYER, W. R., AND A. J. WOLF. 1989. Physalaemus are known only for P. rupestris (Nascimento crombiei (Amphibia: Leptodactylidae), a new frog species from Espı´rito Santo, Brazil with comments on et al., 2001). It is possible that, as knowledge the P. signifer group. Proceedings of the Biological of the morphological relationships of the spe- Society of Washington 102:500–506. cies of the genus Physalaemus grows, a dis- LYNCH, J. D. 1970. Systematic status of the American tinct group will be recognized for these three leptodactylid frog genera , Eupemphix, species. and Physalaemus. Copeia 1970:488–496. NASCIMENTO, L. B., R. R. CARVALHO,JR., H. WOGEL,D.S. FERNANDES, AND R. N. FEIO. 2001. Reproduc¸a˜oe RESUMO descric¸a˜o do girino de Physalaemus rupestris Carama- Uma nova espe´cie de Physalaemus de schi, Carcerelli & Feio, 1991 (Amphibia, Anura, colorido vistoso, relacionada a P. deimaticus e Leptodactylidae). Boletim do Museu Nacional, Nova Se´rie, Zoologia 450:1–10. P. rupestris,e´ descrita do Parque Estadual do PEDRALLI, G., A. S. GUIMARA˜ ES-NETO, AND M. C. B. Itacolomi, Municı´pio de Ouro Preto, Estado TEIXEIRA. 2001. Diversidade de anfı´bios na regia˜ode de Minas Gerais, sudeste do Brasil. A nova Ouro Preto. Cieˆncia Hoje 30:70–73. espe´cie e´ caracterizada pelo tamanho pequeno RIZZINI, C. T. 1979. Tratado de Fitogeografia do Brasil. Editora Hucitec and Editora da Universidade de Sa˜o (comprimento rostro–anal 23,2 mm no macho, Paulo, Brazil. 26,2–26,6 mm nas feˆmeas), focinho arredon- SAZIMA, I., AND U. CARAMASCHI. 1988 [1986]. Descric¸a˜ode dado em vista dorsal e saliente em perfil, Physalaemus deimaticus, sp. n., e observac¸ooes~ sobre o glaˆndulas ingu¨ inais grandes, ovo´ides, marrom comportamento deima´tico em P. nattereri (Steindn.)— claro e com um ocelo preto delineado por uma Anura, Leptodactylidae. Revista de Biologia 13: 91–101. linha branca na sua metade posterior, dorso marrom claro acinzentado com linhas e Accepted: 4 June 2003 manchas longitudinais marrom escuro acin- Associate Editor: Joseph Mendelson III 526 HERPETOLOGICA [Vol. 59, No. 4

APPENDIX I Physalaemus erythros.—BRAZIL: Minas Gerais: Par- que Estadual do Itacolomi, Ouro Preto (MNRJ 27539, Specimens Examined holotype; MNRJ 27986, 30608, paratypes). Physalaemus rupestris.—BRAZIL: Minas Gerais: Par- Physalaemus deimaticus.—BRAZIL: Minas Gerais: que Estadual do Ibitipoca, Lima Duarte (MNRJ 10551, Serra do Cipo´, Jaboticatubas (JJ 6057, holotype; JJ 6058, holotype; MNRJ 10552–53, paratypes; MNRJ 28812–24; paratype). MZUFV 4083–84).