Short Notes 197

The tadpole and advertisement call of aguirrei Bokermann, 1966 (Amphibia, Anura, )

Bruno V.S. Pimenta, Carlos Alberto Gonçalves Cruz

Museu Nacional/UFRJ, Departamento de Vertebrados, Quinta da Boa Vista, 20940-040, Rio de Janeiro, RJ, Brazil e-mail: [email protected]; [email protected]

The neotropical genus Physalaemus is currently composed of 41 valid species (Frost, 2002) arranged in four groups (Lynch, 1970). The group is the most diversified, with 20 species occurring from northern to southern South America (Frost, 2002). Information about tadpoles of nine species and vocalizations of fifteen species of this group are available in literature (see Bokermann, 1962, 1966a, 1966b, 1967; Barrio, 1964, 1965; Langone, 1989; Heyer et al., 1990; Rossa-Feres and Jim, 1993; Duellman, 1997; Perroti, 1997; Cannatella et al., 1998; Tárano, 2001). However, Physalaemus aguirrei is a poorly known species of this group, occurring in the Atlantic Forest in the states of Espírito Santo and Bahia, Brazil (Van Sluys, 1998; Frost, 2002). According to Bokermann (1966a), this species can be found dwelling on the forest floor litter but breeds in temporary ponds in open . Feio et al. (1999) pointed out that P. aguirrei, P. maximus, P. olfersii,andP. soaresi could compose a new species group, due to morphological similarities, and their forest breeding habits but they lacked necessary evidence to confirm this suggestion. Herein, we follow Lynch’s (1970) organisation of the P. cuvieri group. The purpose of this paper is to provide information on tadpole morphology, advertisement call structure and of P. aguirrei. Tadpoles were obtained from a foam nest collected in a temporary pond inside the forest at Parque Nacional Descobrimento (17◦06S, 39◦20W), Municipality of Prado, southern region of the State of Bahia, Brazil, on 22 April 2002. The nest was partially degraded and had a small number of embryos inside, indicating that oviposition had not occurred recently. The tadpoles were reared in laboratory. Seven tadpoles at stage 36 and two at stage 37 (Gosner, 1960) were preserved in 5% formalin and deposited at Museu Nacional, Rio de Janeiro (MNRJ 30591). Measurements (table 1) were made with an ocular grid and a caliper. The terminology we use follows Altig and Johnston (1986) and Johnston and Altig (1986). Advertisement calls were recorded with a Sony TCD-D8 DAT-recorder with a Sennheiser K6/ME66 micro- phone set, on the same date and locality where tadpoles were collected. Sonograms were analyzed with the soft- ware Avisoft-Sonagraph Light 1, version 2.7. Vocalizations were digitalized and edited at a sampling frequency of 22 KHz, FFT with 256 points, and 16 bit resolution. Air temperature was recorded with a digital thermometer to the nearest 0.1◦C. Terminology follows Duellman (1970). Description of the tadpole. Stages 36-37 (Gosner, 1960). Mean total length 20.6 mm (16.6-25.4 mm; n = 9). Body robust, oval in dorsal and ventral views, elliptical in lateral view (fig. 1A, B, C); snout rounded in dorsal and lateral views; body length about 40% (39- 43%) of total length; body width approximately 70% (62-80%) of body length. Nostrils

© Koninklijke Brill NV, Leiden, 2004 Amphibia-Reptilia 25: 197-204 Also available online - www.brill.nl 198 Short Notes

Table 1. Mean (x)¯ , range and standard deviation (s) of measurements (in mm) of Physalaemus aguirrei tadpoles (n = 9; stages 36-37).

x¯ Range s

Total length 20.6 16.6-25.4 3.50 Body length 8.2 7.9-8.8 0.28 Body width 5.7 5.1-6.5 0.48 Body height 4.5 3.8-5.3 0.49 Tail length 12.4 8.5-16.6 3.29 Tail height 4.0 3.6-4.6 0.33 Distance nostril-snout 1.2 0.9-1.6 0.22 Distance eye-nostril 1.0 0.8-1.2 0.12 Interorbital distance 2.6 2.5-2.8 0.10 Internostril distance 0.9 0.8-1.0 0.05 Eye diameter 1.1 1.0-1.2 0.08 Oral disc width 2.2 1.8-2.5 0.21 large, nearly round, located and oriented dorsally, closer to eyes than to snout; internostril distance about 35% of interocular distance; eyes located dorsolaterally; eye-nostril distance about 89% of eye diameter; spiracle single, sinistral, short and projected, opening at the end of the second third of body length and posterodorsally oriented; vent tube medial, wide and long, attached to ventral fin, with opening oriented posteriorly (fig. 1C). Tail with approximately 60% of total length, with nearly the same height of body; tail musculature moderated; dorsal fin extending onto the posterior third of body; ventral fin wide arched, narrower than dorsal, that is nearly rectilineal; tail tip slightly directed upwards (fig. 1A). Oral disc anteroventral, laterally emarginated, its width approximately 38% of body width; one series of marginal papillae in the upper lip, interrupted by a wide medial gap; lower lip with two emarginations; marginal papillae of medial margin have their bases in one series, but with alternate papillae projected anteriorly and posteriorly, emulating a double row; margins on each side of the emarginations with one series of marginal papillae and one series of submarginal papillae; labial tooth row formula 2(2)/3(1). The two anterior and the first posterior teeth rows have approximately the same length; second posterior teeth row slightly shorter than first, and third posterior teeth row with nearly half length of first; upper jaw sheath arch-shaped and lower sheath “V”-shaped (fig. 1D). Color of tadpole in 5% formalin: Body translucent with many brown spots on dorsum; two or three weakly pigmented brown transverse stripes on the dorsal surface of tail, lateral surfaces with scattered brown dots; fins translucent with brown dots, more abundant on dorsal fin; legs with brown spots on dorsal surfaces. A brown blotch between the eyes, extending to the middle of body. Advertisement call consisted of a single note with a fundamental frequency and seven harmonics between 0.43 and 4.73 kHz, with descendent frequency modulation (fig. 2A). The mean duration of the advertisement call was 0.23 s (s = 0.01, range = 0.21-0.25, n = 55 calls of one male) (fig. 2B), and the mean intercall interval (defined here as the time from the end of one call to the beginning of the next call) was 1.22 s (s = 0.80, Short Notes 199

Figure 1. Tadpole of Physalaemus aguirrei, stage 37 of Gosner (1960): (A) lateral view; (B) dorsal view; (C) ventral view (scale = 5 mm); (D) oral disc (scale = 1 mm). range = 0.65-6.57, n = 55 calls of one male). Fundamental frequency was about 0.43 and 1.03 kHz; the dominant frequency was 3.10 kHz, corresponding to the sixth harmonic (fig. 2C); the eighth harmonic ranged from 3.53 to 4.73 kHz. Foam nests and tadpoles of P. aguirrei and P. signifer were found in the same pond. tadpoles are smaller (maximum total length 17.5 mm on stage 36, n = 13), have no emarginations on lower lip, and posterior teeth rows with approximately the same length. Adults diverged spatially on calling and oviposition sites: males of P. signifer were calling under leaf litter on humid ground, 1.0-3.0 meters away from the edges of the pond, whereas males of P. aguirrei were calling hidden under fallen trunks and in small water-filled holes on the edges of the pond; nests of P. signifer were on humid ground at the edges of the pond, partially or completely covered by leaf detritus (cf. Weber and 200 Short Notes

Figure 2. (A) Sonogram, (B) waveform, and (C) spectrogram of the advertisement call of Physalaemus aguirrei; recorded at Parque Nacional Descobrimento, Prado, Bahia, Brazil on 22 April 2002, 06:51 PM. Air temperature = 26.6◦C. Unvouchered specimen.

Carvalho-e-Silva, 2001; Wogel et al., 2002), whereas the nests of P. aguirrei were floating on the water, anchored by emergent vegetation. Short Notes 201

The P. cuvieri group is extremely heterogeneous in external tadpole morphology, presenting no larval synapomorphies to define the group (Langone, 1989; Perroti, 1997). The tadpole of P. aguirrei is distinguished from the others known of the P. cuvieri group by differences in size, nostrils shape, labial tooth row formula, arrangement and distribution of marginal papillae, jaw shape, spiracle position and vent tube orientation. Data about the tadpole of P. aguirrei and other species of this group, were obtained from Bokermann (1962), Barrio (1964), Langone (1989), Rossa-Feres and Jim (1993), Duellman (1997), and Perroti (1997), and are summarized in table 2. The labial tooth row formula of P. cuvieri is presented by Heyer et al. (1990) as 2(2)/3(1) and by Perroti (1997) as 2(2)/2. The latter work cites Bokermann (1962) as the source of this information. The oral disc drawn by Bokermann (1962), however, shows the 2/3(1) formula, as cited by Rossa-Feres and Jim (1993). It seems that some aspects of the oral morphology of this species vary between populations. Bokermann (1962) shows a medial gap on the lower lip, while Heyer et al. (1990) show three gaps. Rossa-Feres and Jim (1993) also mentioned the presence of a ventral gap in the oral disc of P. gracilis, while it is absent according to Perroti (1997). Both cited Langone (1989), whose research shows no ventral gap. Bokermann (1966a) described the advertisement call of P. aguirrei with a fundamental frequency and seven harmonics, an intercall interval of 0.5-0.7 s, and a dominant frequency between 2.0 and 3.0 kHz, corresponding to the third to seventh harmonics. Our analysis agrees with this in terms of call duration (0.25-0.27 s) and the number of harmonics. Differences between our analysis and Bokermann’s (1966a) could be due to the equipment used, environmental factors, male density and inter-population variability. Acoustic parameters of vocalizations of the P. cuvieri group are not comparable because most of the descriptions were made in the 1960’s, when analyses were limited by the technology available. Presentation patterns of the parameters vary substantially: call duration, for example, is shown as a range, a mean or an approximate value. The dominant frequency is commonly presented as a range, according to the aspect of sidebands in a sonogram. These parameters and intercall interval, call structure, and frequency modulation were used to distinguish the advertisement call of P.aguirrei from other species of the group. Table 3 summarizes these data, based on Barrio (1965), Bokermann (1966b, 1967), Heyer et al. (1990), Cannatela et al. (1998), Tárano (2001), and the present study. Data are preferentially presented as ranges. This study indicates that the external morphology of P. aguirrei tadpole corroborates the absence of larval synapomorphies to define the P. cuvieri group. Physalaemus aguirrei is a forest dweller, also breeding in forest edge ponds.

Acknowledgements. We thank U. Caramaschi and L.B. Nascimento for comments on the manuscript; L.B. Nascimento also contributed with valuable suggestions and information; R.J. Young (PUC Minas) for the revision of the typescript; H. Wogel for his help with the vocalization analysis; P.H.C. Cordeiro for field assistance; P.R. Nascimento for the drawings; Instituto Brasileiro de Meio Ambiente e Recursos Naturais Renováveis 202 Short Notes densis -shaped “U”-shaped ? tinuous continuous continuous t present, present, present, present, -shaped “V”-shaped “U” group. Data from Bokermann (1962), Barrio (1964), Langone (1989), l sinistral dextral dextral dextral dextral r (1960). Measurements in mm. ML = maximum length. ee text 2(1)/3 2(2)/3(1) 2(2)/3(1) 2/3(1) 2(2)/2(1) 6 continuous continuous con Physalaemus cuvieri -shaped “U”-shaped “V” aped arch-shaped arch-shaped arch-shaped hipped arch arch-shaped arch-shaped arch-shaped sent with a present with a present, absen aracteristics of larvae of the -shaped “V”-shaped “V” an (1997), and Perroti (1997). Stages follow Gosne the ventralgap papillae (1 to the ventral 10) gap sinistral sinistral sinistral sinistral sinistral sinistral sinistral sinistral sinistral lower lipemarginations each side of papillae on ventral medial each side of papillae on P. aguirrei P. albonotaus P. centralis P. cuqui P. cuvieri P. enesefae P. fernandezae P. gracilis P. henselii P. riogran- Comparison of morphological ch SpiracleVent tube lateral medial lateral dextral latero-ventral latero-dorsal medial lateral dextral lateral lateral dextra lateral lateral ? Upper jaw sheathLower jaw sheath arch-shaped “V”-shaped arch-shaped “V” arch-sh Marginal papillaerow dorsal gapSubmarginalpapillae dorsal row and present on dorsal gap each side of present, dorsal with and ab a row of 3 dorsal and short dorsal row gap of row dorsal of and 5 ventral to gaps dorsal gap dorsal and dorsal gap ventral gaps ventral gaps ventral gaps ventral gaps Table 2. Total length (stage) 25.4Tooth (37) row formula 2(2)/3(1) 11.27 (40) 2(2)/3 20.23 (37) 22.21 (37) 2(2)/2 26 (ML) 2(2)/3(1) 19.5 (39) 35 s (ML) 30.7 (37) 35 (ML) ? Rossa-Feres and Jim (1993), Duellm Short Notes 203

Table 3. Comparison between acoustic parameters of calls of the Physalaemus cuvieri group. Data from Barrio (1965), Bokermann (1966b, 1967), Heyer et al. (1990), Cannatela et al. (1998), and Tárano (2001). agui = P. aguirrei (present study); albf = P. albifrons;albn=P. albonotatus;barr=P. barrioi;cica=P. cicada; cuvi = P. cuvieri;ensf=P. enesefae; ephp = P. ephippifer; evng = P. evangelistai; fndz = P. fernandezae;grac=P. gracilis; hens = P. henselii;jord=P. jordanensis;kroy=P. kroyeri;rgrd=P. riograndensis. H = harmonic structure; P = pulsed structure; D = descendent frequency modulation.

Call Intercall Dominant Call Frequency duration (s) interval (s) frequency (kHz) structure (s) modulation

agui 0.21-0.25 0.65-6.57 3.1 H D albf 0.2a 0.5-0.8 1.0-2.0b HD albn 1.4-1.5 3.0-4.0 2.1-4.0b HD barr 1.2-1.4 6.7a ?HD cica ? ? 2.0-3.0b P? cuvi 0.25-0.35 0.66-1.11 0.58-0.8 H D ensf 0.47-0.93 2.7-7.5 0.67-1.10 H D ephp 0.24-0.31 ? 0.85-1.03 H ? evng 1.0-1.2 9.5a 2.0-4.0b HD fndz 0.5-0.7 2.0a ?HD grac 0.9-1.0 1.5a 4.0-5.0b HD hens 0.2 0.7a 4.8-6.2b P? jord 1.4-1.6 6.0a ?H/P? kroy 0.7-0.9 0.5-3.0 ? H D rgrd 0.8-0.9 2.0a 1.2-6.0b HD a Approximate value. b Values given according to the aspects of sidebands in the sonograms.

(IBAMA) for the license and permission for study on Parque Nacional Descobrimento; Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the grants and financial support. This work is part of the project “Coleta, organização de dados e análise sobre biodiversidade das comunidades de anfíbios anuros da Mata Atlântica do Sul da Bahia — Parque Nacional Descobrimento”, supported by Conservation International do Brasil (CI-Brasil) and coordinated by Instituto de Estudos Sócio-Ambientais do Sul da Bahia (IESB).

References

Altig, R., Johnston, G.F. (1986): Major characteristics of free-living anuran tadpoles. Smithsonian Herpetological Information Service 67: 1-75. Barrio, A. (1964): Relaciones morfologicas, eto-ecologicas y zoogeographicas entre (Peters) y P. fernandezae (Muller) (Anura, Leptodactylidae). Acta Zoologica Lilloana 20: 285-305. Barrio, A. (1965): El genero Physalaemus (Anura, Leptodactylidae) en la Argentina. Physis 70: 421-448. Bokermann, W.C.A. (1962): Observações biológicas sobre Physalaemus cuvieri Fitz., 1826 (Amphibia, Salien- tia). Revista Brasileira de Biologia 22: 391-399. Bokermann, W.C.A. (1966a): Dos nuevas especies de Physalaemus de Espiritu Santo, Brasil. Physis 26: 193-202. Bokermann, W.C.A. (1966b): Notas sobre três espécies de Physalaemus de Maracás, Bahia (Amphibia, Lepto- dactylidae). Revista Brasileira de Biologia 26: 253-259. Bokermann, W.C.A. (1967): Três novas espécies de Physalaemus do sudeste brasileiro (Amphibia, Leptodactyli- dae). Revista Brasileira de Biologia 27: 135-143. Cannatella, D.C., Hillis, D.M., Chippindale, P.D., Weigt, L., Rand, A.S., Ryan, M.J. (1998): Phylogeny of of the Physalaemus pustulosus species group, with an examination of data incongruence. Systematic Biology 47: 311-335. 204 Short Notes

Duellman, W.E. (1970): The hylids frogs of Middle America. Monograph of the Museum of Natural History 21: 1-372. Duellman, W.E. (1997): of La Escalera region, southeastern Venezuela: , ecology, and biogeography. Scientific Papers of the Natural History Museum of the University of Kansas 2: 1-52. Feio, R.N., Pombal, Jr., J.P., Caramaschi, U. (1999): New Physalaemus (Anura: Leptodactylidae) from the Atlantic Forest of Minas Gerais, Brazil. Copeia 1999: 141-145. Frost, D.R. (2002): Species of the World: an online reference. V2.21 (15 July 2002). Electronic database available at http://research.amnh.org/herpetology/amphibia/index.html Gosner, K.L. (1960): A simplified table for staging anuran embryos and larvae, with notes on identification. Herpetologica 16: 183-190. Heyer, W.R., Rand, A.S., Cruz, C.A.G., Peixoto, O.L., Nelson, C.E. (1990): Frogs of Boracéia. Arquivos de Zoologia 31: 231-410. Johnston, G.F., Altig, R. (1986): Identification characteristics of anuran tadpoles. Herpetological Review 17: 36- 37. Langone, J.A. (1989): Descripción de la larva de (Boulenger, 1883) (Amphibia, Anura, Leptodactylidae). Comunicaciones Zoologicas del Museo de Historia Natural de Montevideo 12: 1-11. Lynch, J.D. (1970): Systematic of the American leptodactylid frog genera , Eupemphix,and Physalaemus. Copeia 1970: 488-496. Perroti, M.G. (1997): The tadpole of Physalaemus cuqui Lobo, 1993 (Amphibia, Anura, Leptodactylidae). Amphibia-Reptilia 18: 427-432. Rossa-Feres, D.C., Jim, J. (1993): Tadpole of (Anura, Leptodactylidae). Copeia 1993: 566-569. Tárano, Z. (2001): Variation in male advertisement calls in the Neotropical frog Physalaemus enesefae. Copeia 2001: 1064-1072. Van Sluys, M. (1998): Geographic Distribution. Physalaemus aguirrei. Herpetological Review 29: 49. Weber, L.N., Carvalho-e-Silva, S.P. (2001): Descrição da larva de Physalaemus signifer (Girard, 1853) (Am- phibia, Anura, Leptodactylidae) e informações sobre a reprodução e a distribuição geográfica da espécie. Boletim do Museu Nacional, N.S., Zoologia 462:1-6. Wogel, H., Abrunhosa, P.A., Pombal, Jr., J.P. (2002): Atividade reprodutiva de Physalaemus signifer (Anura, Leptodactylidae) em ambiente temporário. Iheringia, Sér. Zool. 92: 57-70.

Received: February 25, 2003. Accepted: May 23, 2003.

Aspects of the ecology of a distinct population of Xenosaurus platyceps from Querétaro, México

Julio A. Lemos-Espinal1,GeoffreyR.Smith2,4, Royce E. Ballinger3

1 Laboratorio de Ecología, Unidad de Biología, Tecnología y Prototipos, Facultad de Estudios Superiores Iztacala (UNAM), Av. De Los Barrios No. 1, Los Reyes Iztacala, Tlalnepantla, Estado de México, C.P. 54090 México 2 Department of Biology, Denison University, Granville, Ohio 43023, USA 3 School of Biological Sciences, University of Nebraska, Lincoln, Nebraska 68588, USA 4 Corresponding author, e-mail: [email protected]

© Koninklijke Brill NV, Leiden, 2004 Amphibia-Reptilia 25: 204-210 Also available online - www.brill.nl