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Tadpole and advertisement call of Physalaemus erythros Caramaschi, Feio & Guimarães-Neto, 2003 (Amphibia, Anura, Leiuperidae) DÉLIO BAÊTA1, NASCIMENTO2
ANA
CAROLINA
CALIJORNE
LOURENÇO1
&
LUCIANA
BARRETO
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:
[email protected];
[email protected] 2 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:
[email protected]
Abstract We describe the tadpole and the advertisement call of Physalaemus erythros Caramaschi, Feio & Guimarães-Neto, 2003 from Parque Estadual do Itacolomi, Municipality of Ouro Preto, State of Minas Gerais, Brazil. Our data are compared with the information available for Physalaemus rupestris, the only species of the Physalaemus deimaticus species group with 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 & Guimarães-Neto, 2003 do Parque Estadual do Itacolomi, Município de Ouro Preto, Estado de Minas Gerais, Brasil. Os dados obtidos são comparados com as informações disponíveis para Physalaemus rupestris, a única espécie do grupo de Physalaemus 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 from southern Mexico to northern Argentina, 36 occurring in Brazil (Nascimento et al. 2005; Frost 2007). In the original description, Physalaemus erythros Caramaschi, Feio & Guimarães-Neto, 2003 was not included in any 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 and defined seven groups, allocating the three species mentioned in the P. deimaticus group. Species of this group occur in the mountains of the State of Minas Gerais, southeastern Brazil, and are endemic of their respective type 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 Parque Estadual do Itacolomi, Municipality of Ouro Preto (Caramaschi et al. 2003); and P. rupestris from Parque Estadual do Ibitipoca, Municipality of Lima Duarte (Caramaschi et al. 1991) (Fig. 1). Tadpole and advertise-
Accepted by M. Vences: 18 Sept.; published: 26 Oct. 2007
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ment call are known only for P. rupestris (Nascimento et al. 2001). Herein, we describe the tadpole and advertisement call of P. erythros.
FIGURE 1: Map showing the geographical distribution of the three species of thePhysalaemus deimaticus species group, 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 to Lagoa Seca (20º 25' S, 43º 29' W, 1600 m above sea level), at Parque Estadual do Itacolomi, Municipality of Ouro Preto, state of Minas Gerais, Brazil, on 19 January 2005. This locality is at the southernmost edge of the Serra do Espinhaço, a mountainous complex ranging from central Minas Gerais, southeastern Brazil, to northern 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 (following Gosner 1960) were fixed and preserved in 5% formalin and deposited at the herpetological collection of Museu de Ciências Naturais, at Pontifícia Universidade Católica de Minas Gerais (MCNAM 7345). Additional tadpoles were reared to allow specific identification but not preserved. Furthermore, identification is corroborated by the characteristic coloration of this tadpole (similar to the adult), unique among all other species found in the site of study. Measurements and terminology to describe tadpoles follows Altig & McDiarmid (1999). Measurements (in millimeters) were taken using a caliper and an ocular grid used with a stereo microscope. Vocalizations were recorded with a Sony TCM 5000 EV portable cassette recorder coupled to a Sennheiser K6/ME66 microphone set. Sonograms were analyzed with the softwares Avisoft-SASLab Light, ver-
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sion 3.74, and SoundRuler, version 0.9.4.1. Vocalizations were digitized and edited at a sampling frequency of 22050 kHz at 16 bit resolution, FFT width 256 points, overlap 50%, filter Hamming and 16bit resolution. Air and water temperatures were recorded with a digital thermometer to the nearest 0.5ºC. Description and terminology of acoustic parameters of advertisement calls follows Duellman & Trueb (1986).
Results Description of tadpole The following description is based on eight tadpoles at stages 37–39 (Gosner 1960). Body robust, elliptical in dorsal ventral and lateral views (Fig. 2A, B, C). Body length about 39% of total length; body height about 62% of body length and 86.4% of body width. Snout rounded in dorsal view and nearly rounded in lateral view. Eyes located dorsolaterally; its diameter about 11.6% of body length. Interorbital distance about 46.5% of body width. Nostrils nearly rounded, oriented dorsally, closer to the snout than to the eyes; nostrilsnout distance about 12.8% of body length. Nostril diameter about 11.1% of nostril-snout distance. Spiracle tubular-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 same plane of caudal musculature, slightly wider than ventral fin; dorsal and ventral fins slightly arched. Caudal musculature reaches tail tip, which is pointed. Oral disc ventral, laterally emarginated; its width approximately 35.8% of body width, with a wide dorsal gap, surrounded by a uniseriate row of papillaes, in alternated position. Upper jaw sheath ‘M’-shaped and lower sheath ‘V’-shaped, both with serrated edges. Labial tooth row 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 brown spots; fins with a few brown dots on the first third of the tail. Legs with dark brown transversal bars. Iris brown.
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TERM OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website site is prohibited. TABLE 1. Range, mean and standard deviation (SD) of measurements (mm) of tadpoles assigned to Physalaemus erythros (n=8, stages 37−39). 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
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
Nostril diameter
In preservative, the color pattern is the same as in life with the following exceptions: the reddish blotch on lateral surfaces became cream, and the iris became black.
Description of the advertisement call Calls 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 a flooded floor under a rocky formation on the edge of a temporary pool. The mean air temperature was 18°C and water temperature was 20°C. In that night, males emitted continually one type of vocalization, which we define 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=63 calls), 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 History Calling 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 to vocalize at the sunset and were observed calling with half of the body submerged in the water, on sheltered sites (e.g. holes made by the steps of other animals or crevices among rocks). During heavy rains calling activity 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
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September 2004, and the other within a flooded rock crevice, observed in December 2005. Tadpoles were collected 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 monthly monitoring anurans in this location, we never observed any others species in the hole where the tapoles was collected (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 advertisement call of Physalaemus erythros; recorded at Ouro Preto, Minas Gerais, Brazil on 10 October 2006, 7:38 PM. Air temperature 18ºC, water temperature 20ºC. Calls recorded from unvouchered specimen.
Discussion The tadpole of Physalaemus erythros exhibits important morphological differences compared to the tadpoles of P. rupestris (see Nascimento et al. 2001). Tadpoles of P. erythros are distinguished from P. rupestris by the labial 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 from the 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 reddish blotch coloration from the lateral side of head (under the eyes) and flanks, extending to the ventral surface (this regions is transparent in. in P. rupestris). This conspicuous reddish blotch is similar to the red blotches observed in some regions of the body of the adults of P. erythros and is an important diagnostic for this 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 only one male, we observed this species vocalizing in many opportunities. Adults collected on these occasions are listed in appendix and were deposited in herpetologicals collections of Laboratório de Zoologia de Vertebrados 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 males were 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 males of P. erythros. In contrast to prolonged-breeders, a vocal repertoire compound for one or two types of vocalizations is commonly observed in explosive-breeders (Wells 1977; Arak 1983), due, probably, the brevity of the reproductive period in these species and great number of clustered males, where vocal interactions among individuals seem not be so important. This brevity or clumping reflects a limited or absent of vocal interactions between males and females and between males in short or long distance, factors that can be responsible by 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 be an explosive-breeder, nevertheless, considering that its call activity is related to the beginning of the rainy seasons, this specific condition could shorten its reproductive period and, consequently, restrict vocal interactions among individuals. Nascimento et al. (2001) did not associate each of the two types of calls observed in P. rupestris to a specific social context. The advertisement call of P. erythros is distinguished from the first call of P. rupestris by the 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 by the dominant frequency (1.03-1.52 in P. erythros; 1.55-1.72kHz in P. rupestris); and call duration (0.04-0.07s in P. erythros; 0.10-0.16 in P. rupestris)
Acknowledgements We thank Leandro O. Drummond, Tiago L. Pezzuti, Vinícius S. Monteiro (Universidade Federal de Ouro Preto - UFOP) and Aristides S. Guimarães-Neto (IBAMA) for field assistance; Mirele C. Brant for the line drawings; Bruno V.S. Pimenta (Museu Nacional, Rio de Janeiro), Jörn Köhler and Henrique Wogel for critically reading the manuscript and suggestions; Instituto Estadual de Florestas de Minas Gerais (IEF-MG) and Alberto V.M. Mattos, the director of Parque Estadual do Itacolomi, for the permission to collect in this conservation area; Délio Baêta and Ana Carolina Calijorne Lourenço thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the fellowships granted (procs. 130993/2007-7 and 130995/20070); Luciana Barreto Nascimento thanks Fundo de Incentivo à Pesquisa (FIP/PUC Minas) for the fellowship granted.
References Altig, R. & McDiarmid, R.W. (1999) Body plan: development and morphology. In: McDiarmid, & Altig, R. (Eds.), Tadpoles: The Biology of Anuran Larvae, The University of Chicago Press, Chicago, pp. 24−51. Arak, A. (1983) Male-male competition and mate choice in anuran amphibians. In: Bateson, P. (Ed.), Mate Choice, Cambridge University Press, Cambridge, pp. 181-210. Caramaschi, U., Carcerelli, L.C.C. & Feio, R.N. (1991) A new species of Physalaemus (Anura: Leptodactylidae) from Minas Gerais, Southeastern Brazil. Herpetologica, 47, 148−151. Caramaschi, U., Feio, R.N. & Guimarães-Neto, A.S. (2004) A new, brightly colored species of Physalaemus (Anura: Leptodactylidae) from Minas Gerais, Southeastern Brazil. Herpetologica, 59, 519−524. Caramaschi, U., Cruz, C.A.G. & Feio, R. (2006) A new species of Phyllomedusa Wagler, 1830 from the state of Minas Gerais, Brazil (Amphibia; Anura; Hylidae). Boletim do Museu Nacional, Nova Série, Zoologia, 524, 1−8. Drummond, L.O. (2006). Distribuição espacial e temporal de anfíbios anuros em uma lagoa temporária no Parque Estadual do Itacolomi. Universidade Federal de Ouro Preto, Ouro Preto, 46 pp.
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TERM OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website site is prohibited. Duellman, W.E. & Trueb, L. (1986) Biology of Amphibians, The Johns Hopkins University Press, Baltimore, 670 pp. Eterovick, P.C. & Sazima, I. (2004) Anfíbios da Serra do Cipó, FUMARC, Belo Horizonte, 155 pp. Frost, D. R. (2007) Amphibian Species of the World: an Online Reference. Version 5.0 (1 February, 2007). Electronic Database accessible at http://research.amnh.org/herpetology/amphibia/index.php. American Museum of Natural History, New York, USA. (access on 09 April 2007) Gosner, K.L. (1960) A simplified table for staging anuran embryo and larvae with notes on identification. Herpetologica, 16, 183−190. Hartmann, M.T.; Hartmann, P.A. & Haddad, C.F.B. (2006) Repertório vocal de Hylodes phyllodes (Amphibia, Anura, Hylodidae). Papéis Avulsos de Zoologia, 46, 203−209. Nascimento, L.B., Caramaschi, U. & Cruz, C.A.G. (2005) Taxonomic review of the species groups of the genus Physalaemus Fitzinger, 1826 with revalidation of the genera Engystomops Jimenez-de-La-Espada, 1872 and Euphemphix Steindachner, 1863 (Amphibia, Anura, Leptodactylidae). Arquivos do Museu Nacional, 63, 297−320. Nascimento, L.B., Carvalho Jr, R.R., Wogel, H., Fernandes, D.S. & Feio, R.N. (2001) Reprodução e descrição do girino de Physalaemus rupestris Caramaschi, Carcerelli & Feio, 1991 (Amphibia, Anura, Leptodactylidae). Boletim do Museu Nacional, Nova Série, Zoologia, 450, 1-10. Pedralli, G., Guimarães-Neto, A.S. & Teixeira, M.C.B. 2001. Diversidade de anfíbios na região de Ouro Preto. Ciência Hoje 30,70–73. Pimenta, B.V.S., Cruz, C.A.G. & Silvano, D.L. (2005) A new species of the genus Physalaemus Fitzinger, 1826 (Anura, Leptodactylidae) from the Atlantic Rain Forest of southern Bahia, Brazil. Amphibia-Repitilia, 26, 201-210. Pimenta, B.V.S. & Cruz, C.A.G. (2004) The tadpole and advertisement call of Physalaemus aguirrei Bokermann, 1966 (Amphibia, Anura, Leptodactylidae). Amphibia-Reptilia, 25, 197−204. Prado, G.M.; Bilate, M. & Wogel, H. (2007) Call diversity of Leptodactylus natalensis Lutz, 1930 (Anura; Leptodactylidae). Papéis Avulsos de Zoologia, 47, 97−103. Sazima, I. & Caramaschi, U. (1986) Descrição de Physalaemus deimaticus, sp. n., e observações sobre comportamento deimático em Physalaemus nattereri (Steidn.) (Anura, Leptodactylidae). Revista de Biologia, 13, 91−101. Toledo, L.F. & Haddad, C.F.B. (2005) Acoustic repertoire and calling behavior of Scinax fuscomarginatus (Anura, Hylidae). Journal of Herpetology, 39, 455-461. Wells, K.D. (1977) The social behavior of anuran amphibians. Animal Behaviour, 25, 666−693.
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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 Calijorne Lourenço, Délio Baêta, Leandro Oliveira Drummond and Renato Neves Feio on 06 October 2004; LZV 547A, collected 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 Délio Baêta and Ana Carolina Calijorne Lourenço, on 10 October 2006.
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