Accepted by M. Vences: 18 Sept.; published: 26 Oct. 2007 39

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Tadpole and advertisement call of Physalaemus erythros Caramaschi, Feio & Guimarães-Neto, 2003 (Amphibia, Anura, Leiuperidae)

DÉLIO BAÊTA1, ANA CAROLINA CALIJORNE LOURENÇO1 & LUCIANA BARRETO

NASCIMENTO2

1 Departamento de Vertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, São Cristovão, Rio de Janeiro, RJ, Brasil. E-mail: deliobaeta@gmail.com; carolcalijorne@gmail.com2 Museu de Ciências Naturais, Departamento de Ciências Biológicas, and Programa de Pós-graduação em Zoologia de Vertebrados, PUC Minas, Av. Dom José Gaspar 290, 30535-610, Belo Horizonte, Minas Gerais, Brasil, E-mail: luna@pucminas.br

Abstract

We describe the tadpole and the advertisement call of Physalaemus erythros Caramaschi, Feio & Guimarães-Neto, 2003from Parque Estadual do Itacolomi, Municipality of Ouro Preto, State of Minas Gerais, Brazil. Our data are comparedwith the information available for Physalaemus rupestris, the only species of the Physalaemus deimaticus species groupwith known tadpole and advertisement calls.

Key words: Amphibia, Anura, Leiuperidae, Physalaemus erythros, tadpole morphology, advertisement call, Brazil.

Resumo

No presente estudo, descrevemos o girino e o canto de anúncio de Physalaemus erythros Caramaschi, Feio & Guima-rães-Neto, 2003 do Parque Estadual do Itacolomi, Município de Ouro Preto, Estado de Minas Gerais, Brasil. Os dadosobtidos são comparados com as informações disponíveis para Physalaemus rupestris, a única espécie do grupo de Physa-laemus deimaticus com girino e canto de anúncio conhecidos.

Palavras-chave: Amphibia, Anura, Leiuperidae, Physalaemus erythros, morfologia do girino, canto de anúncio, Brasil

Introduction

The Neotropical frog genus Physalaemus Fitzinger, 1826 is currently composed of 41 species occurring fromsouthern Mexico to northern Argentina, 36 occurring in Brazil (Nascimento et al. 2005; Frost 2007). In theoriginal description, Physalaemus erythros Caramaschi, Feio & Guimarães-Neto, 2003 was not included inany species group, although possible relationships with Physalaemus rupestris Caramaschi, Carcerelli & Feio,1991 and Physalaemus deimaticus Sazima & Caramaschi, 1988 were suggested (Caramaschi et al. 2003).Later Nascimento et al. (2005) revised the taxonomy of the species groups in the genus Physalaemus anddefined seven groups, allocating the three species mentioned in the P. deimaticus group. Species of this groupoccur in the mountains of the State of Minas Gerais, southeastern Brazil, and are endemic of their respectivetype localities: P. deimaticus from Serra do Cipó, Municipality of Jaboticatubas (Sazima & Caramaschi 1986;Eterovick & Sazima 2004), now recognized as Municipality of Santana do Riacho; P. erythros from ParqueEstadual do Itacolomi, Municipality of Ouro Preto (Caramaschi et al. 2003); and P. rupestris from ParqueEstadual do Ibitipoca, Municipality of Lima Duarte (Caramaschi et al. 1991) (Fig. 1). Tadpole and advertise-

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ment call are known only for P. rupestris (Nascimento et al. 2001). Herein, we describe the tadpole and adver-tisement call of P. erythros.

FIGURE 1: Map showing the geographical distribution of the three species of thePhysalaemus deimaticus speciesgroup, at Minas Gerais, southeastern Brazil. Cross: Physalaemus deimaticus; Triangle: Physalaemus erythros; Star:Physalaemus rupestris.

Material and methods

Tadpoles were collected in a rain-flooded hole of approximately 1 m deep and 0.3 m diameter at the trail toLagoa Seca (20º 25' S, 43º 29' W, 1600 m above sea level), at Parque Estadual do Itacolomi, Municipality ofOuro Preto, state of Minas Gerais, Brazil, on 19 January 2005. This locality is at the southernmost edge of theSerra do Espinhaço, a mountainous complex ranging from central Minas Gerais, southeastern Brazil, to north-ern Bahia, northeastern Brazil. Characterization of this locality and habitats are presented in Caramaschi et al.(2004) and Caramaschi et al. (2006). Eight tadpoles of Physaleaemus erythros between stages 37–39 (follow-ing Gosner 1960) were fixed and preserved in 5% formalin and deposited at the herpetological collection ofMuseu de Ciências Naturais, at Pontifícia Universidade Católica de Minas Gerais (MCNAM 7345). Addi-tional tadpoles were reared to allow specific identification but not preserved. Furthermore, identification iscorroborated by the characteristic coloration of this tadpole (similar to the adult), unique among all other spe-cies found in the site of study. Measurements and terminology to describe tadpoles follows Altig & McDi-armid (1999). Measurements (in millimeters) were taken using a caliper and an ocular grid used with a stereomicroscope.

Vocalizations were recorded with a Sony TCM 5000 EV portable cassette recorder coupled to a Sen-nheiser K6/ME66 microphone set. Sonograms were analyzed with the softwares Avisoft-SASLab Light, ver-

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Zootaxa 1623 © 2007 Magnolia Press · 41TADPOLE AND CALL OF PHYSALAEMUS ERYTHROS

sion 3.74, and SoundRuler, version 0.9.4.1. Vocalizations were digitized and edited at a sampling frequency of22050 kHz at 16 bit resolution, FFT width 256 points, overlap 50%, filter Hamming and 16bit resolution. Airand water temperatures were recorded with a digital thermometer to the nearest 0.5ºC. Description and termi-nology of acoustic parameters of advertisement calls follows Duellman & Trueb (1986).

Results

Description of tadpoleThe following description is based on eight tadpoles at stages 37–39 (Gosner 1960). Body robust, ellipti-

cal in dorsal ventral and lateral views (Fig. 2A, B, C). Body length about 39% of total length; body heightabout 62% of body length and 86.4% of body width. Snout rounded in dorsal view and nearly rounded in lat-eral view. Eyes located dorsolaterally; its diameter about 11.6% of body length. Interorbital distance about46.5% of body width. Nostrils nearly rounded, oriented dorsally, closer to the snout than to the eyes; nostril-snout distance about 12.8% of body length. Nostril diameter about 11.1% of nostril-snout distance. Spiracletubular-shaped, sinistral, posterodorsally oriented, located in the beginning of the second third of body length;spiracle inner wall present as a slight ridge. Anal tube dextral, wide, well developed, with dextral opening.Tail length about 60.6% of total length; its height smaller than body height. Dorsal fin originating at the sameplane of caudal musculature, slightly wider than ventral fin; dorsal and ventral fins slightly arched. Caudalmusculature reaches tail tip, which is pointed. Oral disc ventral, laterally emarginated; its width approxi-mately 35.8% of body width, with a wide dorsal gap, surrounded by a uniseriate row of papillaes, in alternatedposition. Upper jaw sheath ‘M’-shaped and lower sheath ‘V’-shaped, both with serrated edges. Labial toothrow formula 2(2)/3(1) (Fig. 2D). Measurements are presented in Table 1.

FIGURE 2. Tadpole assigned to Physalaemus erythros, stage 37 of Gosner (1960): (A) dorsal view; (B) ventral view;(C) lateral view (scale = 5mm); (D) oral disc (scale = 1mm).

In life dark brown on dorsum; ventral surfaces translucid. A reddish blotch from the lateral side of head(under the eyes) and flanks, extending to the ventral surface of the body. Caudal musculature with brownspots; fins with a few brown dots on the first third of the tail. Legs with dark brown transversal bars. Irisbrown.

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TABLE 1. Range, mean and standard deviation (SD) of measurements (mm) of tadpoles assigned to Physalaemus eryth-

ros (n=8, stages 37−39).

In preservative, the color pattern is the same as in life with the following exceptions: the reddish blotch onlateral surfaces became cream, and the iris became black.

Description of the advertisement callCalls of Physalaemus erythros were recorded from one male on 10 October 2006, at the type locality.

During recordings we observed the calling specimen, but this male was not collected. It was vocalizing on aflooded floor under a rocky formation on the edge of a temporary pool. The mean air temperature was 18°Cand water temperature was 20°C. In that night, males emitted continually one type of vocalization, which wedefine as advertisement call. This call consisted of one multipulsed note, with height grouped pulse (Fig. 3),amplitude of the call between 0.66 kHZ (SD=0.01; range=0.66–0.77 kHz; n=63 calls), and 2.24 kHz(SD=0.01; range=2.15–2.24 kHz; n=63 calls); mean duration of 0.05s (SD=0.01; range=0.04–0.07s; n=63calls), and mean intercall interval (as defined by Pimenta & Cruz 2004) of 0.45s (SD=0.05; range=0.30–0.57s;n=63 calls). Dominant frequency of 1.12 kHz (SD= 0.0X; ranges=1.03–1.52 kHz; n=63 calls).

Natural HistoryCalling activity in Physalaemus erythros is related to the beginning of the rainy season that coincided with

the month of October in 2005. After this period, few males were occasionally heard calling. Males begin tovocalize at the sunset and were observed calling with half of the body submerged in the water, on shelteredsites (e.g. holes made by the steps of other animals or crevices among rocks). During heavy rains calling activ-ity was usually ceased. At the recording night on 10 October 2006, one male (MNRJ 46694) was collected.Foam nests were observed twice at two different sites: one within a flooded hole in the ground, observed on

Range Mean SD

Total length 30.7–35.6 34.3 1.85

Body length 12.4–14.3 13.4 0.76

Body width 9.4–9.9 9.6 0.16

Body height 7.9–8.6 8.3 0.25

Tail length 17.4–22.2 20.8 1.71

Tail height 6.6–8.6 7.9 0.67

Dorsal fin height 2.0–3.0 2.8 0.36

Ventral fin height 1.7–2.7 2.3 0.36

Internostril distance 1.8–1.9 1.9 0.04

Interorbital distance 4.3–4.7 4.5 0.18

Eye diameter 1.4–1.7 1.6 0.09

Nostril diameter 0.2 0.2 0.00

Eye-nostril distance 2.0–2.4 2.2 0.14

Nostril-snout distance 1.5–1.9 1.7 0.14

Eye-snout distance 3.9–4.9 4.3 0.31

Snout-spiracle distance 6.9–8.3 7.8 0.86

Oral disc width 3.2–3.6 3.4 0.11

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Zootaxa 1623 © 2007 Magnolia Press · 43TADPOLE AND CALL OF PHYSALAEMUS ERYTHROS

September 2004, and the other within a flooded rock crevice, observed in December 2005. Tadpoles were col-lected at these same sites.

Two other species of Physalaemus, P. cuvieri (P. cuvieri group) and P. evangelistai (P. gracilis group)(Pedralli et al. 2001; DB, ACCL & LBN, pers. obs.) occur at Lagoa Seca. However, during two years monthlymonitoring anurans in this location, we never observed any others species in the hole where the tapoles wascollected (Drummond, 2006). This happen, probably, because P. erythros is associated to rocky outcrops,whereas the other species are related to muddy and flooded places with emergent vegetation.

FIGURE 3. (A) Wave form, (B) wave form of a single note, (C) spectrogram and (D) power spectrum of the advertise-ment call of Physalaemus erythros; recorded at Ouro Preto, Minas Gerais, Brazil on 10 October 2006, 7:38 PM. Air tem-perature 18ºC, water temperature 20ºC. Calls recorded from unvouchered specimen.

Discussion

The tadpole of Physalaemus erythros exhibits important morphological differences compared to the tadpolesof P. rupestris (see Nascimento et al. 2001). Tadpoles of P. erythros are distinguished from P. rupestris by thelabial tooth row formula [(2(2)/3(1) in P. erythros; 2(2)/3(1-2) in P. rupestris]; nostril shape and position(nearly rounded, closer to the snout than to the eyes in P. erythros; rounded, located at an equal distance fromthe snout and the eyes in P. rupestris; orientation of anal tube opening (dextral in P. erythros; medial in P.rupestris); shape of upper jaw sheath (‘M’-shaped in P. erythros and convex in P. rupestris); and for the red-dish blotch coloration from the lateral side of head (under the eyes) and flanks, extending to the ventral sur-face (this regions is transparent in. in P. rupestris). This conspicuous reddish blotch is similar to the redblotches observed in some regions of the body of the adults of P. erythros and is an important diagnostic forthis species (Caramaschi et al. 2004).

Only one type of call was observed in P. erythros, whereas P. rupestris presents two different calls types

(Nascimento et al. 2001). Although we present the analysis of a single recording of the vocalizations of onlyone male, we observed this species vocalizing in many opportunities. Adults collected on these occasions arelisted in appendix and were deposited in herpetologicals collections of Laboratório de Zoologia de Vertebra-dos housed in Universidade Federal de Ouro Preto (LZV) and Museu Nacional do Rio de Janeiro (MNRJ). We

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could never verify the emission of other types of calls than the call described in this study, neither when maleswere calling isolated nor when calling neighbors, co-specific or not, were present (Dendropsophus minutus,Iscnocnema juipoca, Leptodactylus jolyi, L. ocellatus, Phyllomedusa itacolomi, Scinax curicica, Scinax gr.ruber, S. squalirostris). The same call was emitted in response even when we used playbacks to localize malesof P. erythros. In contrast to prolonged-breeders, a vocal repertoire compound for one or two types of vocal-izations is commonly observed in explosive-breeders (Wells 1977; Arak 1983), due, probably, the brevity ofthe reproductive period in these species and great number of clustered males, where vocal interactions amongindividuals seem not be so important. This brevity or clumping reflects a limited or absent of vocal interac-tions between males and females and between males in short or long distance, factors that can be responsibleby development of a high call diversity in several species where these interactions commonly occurs (e.g.Toledo & Haddad 2005; Hartmann et al., 2006; Prado et al. 2007). Physalaemus erythros does not seem to bean explosive-breeder, nevertheless, considering that its call activity is related to the beginning of the rainyseasons, this specific condition could shorten its reproductive period and, consequently, restrict vocal interac-tions among individuals.

Nascimento et al. (2001) did not associate each of the two types of calls observed in P. rupestris to a spe-cific social context. The advertisement call of P. erythros is distinguished from the first call of P. rupestris bythe number of notes per call (one in P. erythros and 14–24 in of P. rupestris followed of one isolated note);dominant frequency (1.03–1.52kHz in P. erythros and 1.6–2.8kHz in P. rupestris); and call duration (0.04–0.07s in P. erythros and 2.43–3.56s in P. rupestris). From the second call of P. rupestris, it is distinguished bythe dominant frequency (1.03-1.52 in P. erythros; 1.55-1.72kHz in P. rupestris); and call duration (0.04-0.07sin P. erythros; 0.10-0.16 in P. rupestris)

Acknowledgements

We thank Leandro O. Drummond, Tiago L. Pezzuti, Vinícius S. Monteiro (Universidade Federal de OuroPreto - UFOP) and Aristides S. Guimarães-Neto (IBAMA) for field assistance; Mirele C. Brant for the linedrawings; Bruno V.S. Pimenta (Museu Nacional, Rio de Janeiro), Jörn Köhler and Henrique Wogel for criti-cally reading the manuscript and suggestions; Instituto Estadual de Florestas de Minas Gerais (IEF-MG) andAlberto V.M. Mattos, the director of Parque Estadual do Itacolomi, for the permission to collect in this conser-vation area; Délio Baêta and Ana Carolina Calijorne Lourenço thanks Conselho Nacional de Desenvolvi-mento Científico e Tecnológico (CNPq) for the fellowships granted (procs. 130993/2007-7 and 130995/2007-0); Luciana Barreto Nascimento thanks Fundo de Incentivo à Pesquisa (FIP/PUC Minas) for the fellowshipgranted.

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Zootaxa 1623 © 2007 Magnolia Press · 45TADPOLE AND CALL OF PHYSALAEMUS ERYTHROS

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Appendix 1. Examined material (8 tadpoles)

Physalaemus erythros: BRAZIL, Minas Gerais, Ouro Preto, Parque Estadual do Itacolomi, Lagoa Seca: Tadpoles:MCNAM 7345; collected by Délio Baêta, on 19 January 2005. Adult male: LZV 272A, collected by Ana Carolina Cali-jorne Lourenço, Délio Baêta, Leandro Oliveira Drummond and Renato Neves Feio on 06 October 2004; LZV 547A, col-lected by Breno de Assis and Leandro Oliveira Drummond on 26 November 2005; LZV 610A, collected by Délio Baêta,Leandro Oliveira Drummond and Keicilane Aparecida Guedes on 31 November 2005; MNRJ 46694, collected by DélioBaêta and Ana Carolina Calijorne Lourenço, on 10 October 2006.

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