The advertisement call of Proceratophrys cristiceps and a different advertisement call of Leptodactylus ocellatus are described, and the advertisement call of Leptodactylus troglodytes is redescribed. Power spectrums, audiospectrograms, and waveforms are presented. Vocalizations were recorded in municipalities of Feira de Santana and Mangue Seco, State of Bahia, Brazil. Aspects related to taxonomy from vocalization of species are discussed.São descritos os cantos de anúncio de Proceratophrys cristiceps e um diferente canto de anúncio de Leptodactylus ocellatus, bem como é redescrito o canto de anúncio de Leptodactylus troglodytes. Espectrogramas, sonogramas e oscilogramas das vocalizações são apresentados. As gravações foram realizadas nos municípios de Feira de Santana e Mangue Seco, Estado da Bahia, Brasil. São discutidos aspectos taxonômicos a partir das vocalizações

Juncá, Flora Acuña

Nunes, Ivan

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1 Submitted on September 27, 2005. Accepted on March 23, 2006.2 Museu Nacional/UFRJ, Departamento de Vertebrados. Quinta da Boa Vista, São Cristóvão, 20940-040, Rio de Janeiro, RJ, Brasil. E-mail: ivan.nunes@yahoo.com.br.3 Universidade Estadual de Feira de Santana, Departamento de Ciências Biológicas, Laboratório de Animais Peçonhentos e Herpetologia. Campus Universitário,Avenida Universitária, 44031-460, Feira de Santana, BA, Brasil. E-mail: fjunca@uefs.br.Arquivos do Museu Nacional, Rio de Janeiro, v.64, n.2, p.151-157, abr./jun.2006ISSN 0365-4508ADVERTISEMENT CALLS OF THREE LEPTODACTYLID FROGSIN THE STATE OF BAHIA, NORTHEASTERN BRAZIL (AMPHIBIA, ANURA,LEPTODACTYLIDAE), WITH CONSIDERATIONS ON THEIR TAXONOMIC STATUS 1(With 9 figures)IVAN NUNES 2FLORA ACUÑA JUNCÁ 3ABSTRACT: The advertisement call of Proceratophrys cristiceps and a different advertisement call ofLeptodactylus ocellatus are described, and the advertisement call of Leptodactylus troglodytes is redescribed.Power spectrums, audiospectrograms, and waveforms are presented. Vocalizations were recorded inmunicipalities of Feira de Santana and Mangue Seco, State of Bahia, Brazil. Aspects related to taxonomyfrom vocalization of species are discussed.Key words: Proceratophrys cristiceps. Leptodactylus ocellatus. Leptodactylus troglodytes. Vocalization. Taxonomy.RESUMO: Canto de anúncio de três espécies da família Leptodactylidae no Estado da Bahia, Nordeste doBrasil (Amphibia, Anura, Leptodactylidae), com considerações sobre suas posições taxonômicas.São descritos os cantos de anúncio de Proceratophrys cristiceps e um diferente canto de anúncio deLeptodactylus ocellatus, bem como é redescrito o canto de anúncio de Leptodactylus troglodytes.Espectrogramas, sonogramas e oscilogramas das vocalizações são apresentados. As gravações foram realizadasnos municípios de Feira de Santana e Mangue Seco, Estado da Bahia, Brasil. São discutidos aspectostaxonômicos a partir das vocalizações.Palavras-chave: Proceratophrys cristiceps. Leptodactylus ocellatus. Leptodactylus troglodytes. Vocalização. Taxonomia.INTRODUCTIONAnuran advertisement calls are generally species-specific (GERHARDT, 1988) and their specificitypromotes a species isolating mechanism thatcharacterizes it as an important taxonomiccharacter (DUELLMAN & TRUEB, 1986). For example,the morphologies of some closely related speciesof frogs are indistinguishable, but theiradvertisement calls differ from each other (seeHEYER et al., 1996; HADDAD & POMBAL, 1998; HADDAD& SAZIMA, 2004).Leptodactylidae is a large family of frogs with ageographical distribution ranging from southernUSA and Antilles to southern South America(FROST, 2004). The subfamilies Leptodactylinae andCeratophryinae have a lot of not well-delimitedspecies, and vocalizations (mainly advertisementcalls) have been used to solve the relationshipsamong them (HEYER, 1978; HEYER et al., 1996; KWET& FAIVOVICH, 2001; HEYER & JUNCÁ, 2003).The purpose of our study is to describe theadvertisement call of Proceratophrys cristiceps(Müller, 1883), describe a different advertisementcall of Leptodactylus ocellatus (Linnaeus, 1758),redescribe the advertisement call of  L. troglodytesLutz, 1926, and discuss the contribution of call datato understanding their respective taxonomic status.MATERIAL AND METHODSRecordings of advertisement calls of two specimensof Proceratophrys cristiceps and one specimen ofLeptodactylus ocellatus were obtained during asurvey of anurans in Serra São José (semidecidualforest), Municipality of Feira de Santana, Bahia,Brazil. Recordings of advertisement calls of twospecimens of Leptodactylus troglodytes wereobtained during a survey of anurans in theMunicipality of Mangue Seco (Atlantic Forest),Bahia, Brazil.The vocalizations were recorded in the field with a152                                        I.NUNES & F.A.JUNCÁArq. Mus. Nac., Rio de Janeiro, v.64, n.2, p.151-157, abr./jun.2006SONY WM-D6 Digital Audio Tape (DAT) and a SONYECM-MS907 Electret Condenser Microphone.Advertisement calls were analyzed using Canary 1.2.4software (CHARIF et al., 1995). The calls were digitizedat a sample rate of 44.1 Hz, and sample size of 16bits. Call classification and acoustic parametersterminology follows DUELLMAN & TRUEB (1986), JUNCÁ(1999), and LITTLEJOHN (2001). Temporal parameterswere measured from the waveform. Dominantfrequency was determined using the spectrumanalysis in Canary with settings of spectrum analysisresolution filter band-width 174.85 Hz, frame length1.024 points, grid resolution time 1.451ms, overlap93.75%, grid resolution frequency 43.07 Hz, FFT size1.024 points, window function hamming, amplitudelogarithmic, clipping level–80 dB. Call amplitudemodulation and frequency modulation were evaluatedfrom visual inspection of wave form andaudioespectrogram displays, respectively.RESULTSThe summary of the acoustic parameters of theadvertisement calls described below is presentedin table 1.Proceratophrys cristiceps(Figs.1-3)The advertisement call comprises one multipulsednote (  x̄   = 57 ±6 pulses; N = 29) (Fig.1). Call durationranges from 0.52 to 0.79s ( x̄  = 0.66 ±0.05s; N = 29)and call interval ranges from 0.84 to 37.83s (x̄  =4.47±7.65s; N = 28). The pulse rate ranges from 87.43to 91.85 pulses/s ( x̄  = 89.54 ±1.20 pulses/s; N =28). The call has not a frequency modulation (Fig.2).Because the narrow band filter analyses, figure 2shows artifacts that could be misleading interpretedas an harmonic structure (VIELLIARD, 1993). Thedominant frequency ranges from 0.90 to 0.99 kHz( x̄  = 0.94 ±0.02 kHz; N = 29) (Fig.3). The specimenswere found at night, calling on the ground near atemporary stream.Leptodactylus ocellatus(Figs.4-6)The advertisement call consists of one multipulsednote ( x̄ = 11 ±1 pulses; N = 68) frequently repeated(Fig.4). Call duration ranges from 0.28 to 0.39s ( x̄ =0.34 ±0.02s; N = 68) and call interval ranges from0.50 to 2.82s (1.2 ±0.52; N = 57). The call has anascendant amplitude modulation (Fig.4) and do notpresent a frequency modulation (Fig.5). The dominantfrequency ranges from 0.34 to 0.39 kHz ( x̄ = 0.35±0.02 kHz; N=28) (Fig.6). The specimen was found atnight, calling in the water (from a permanent pond).Leptodactylus troglodytes(Figs.7-9)The advertisement call consists of a tonal single note(Fig.7). Call duration mean is 0.06 ±0.01s (N = 163)and call interval ranges from 0.18 to 1.59s ( x̄  = 0.48±0.18s; N = 162). The call has an ascendantfrequency modulation (Fig.8). The dominantfrequency mean is 3.28 ±0.06 kHz (N = 163) (Fig.9).The specimens were found at night, calling hiddenon rocks and dense vegetation.Table 1. Acoustic parameters of the advertisement call of Leptodactylus ocellatus, Leptodactylus troglodytes, andProceratophrys cristiceps. The results are presented as mean ± standard deviation (amplitude).ACOUSTIC PARAMETERS Leptodactylus ocellatus Leptodactylus troglodytes Proceratophrys cristiceps Call duration (s)  0.34 ± 0.02 (0.28 – 0.39) 0.06 ± 0.01 (0.05 – 0.07) 0.66 ± 0.05 (0.52 – 0.79) Interval between calls (s)  1.20 ± 0.52 (0.50 – 2.82) 0.48 ± 0.18 (0.18 – 1.59) 4.47 ± 7.65 (0.84 – 37.83) Number of notes  1  1  1  Number of pulses  10.88 ± 0.77 (9 – 12) - 57,46 ± 6,02 (46 – 69) Dominant frequency (kHz)  0.35 ± 0.02 (0.34 – 0.39) 3.28 ± 0.06 (3.20 – 3.39) 0.94 ± 0.02 (0.90 – 0.99) Physical structure of call pulsed pulsed pulsed Frequency Modulation - ascendent - N (analyzed calls/ ) 68 / 1 163 / 2 29 / 2                                      ADVERTISEMENT CALLS OF THREE LEPTODACTYLID FROGS IN THE STATE OF BAHIA                               153Arq. Mus. Nac., Rio de Janeiro, v.64, n.2, p.151-157, abr./jun.2006132Advertisement call of Proceratophrys cristiceps, recorded 29/XI/2004. Air temperature 21ºC and water temperature 24ºC:fig.1- wave form; fig.2- audiospectrogram; fig.3- power spectrum.154                                        I.NUNES & F.A.JUNCÁArq. Mus. Nac., Rio de Janeiro, v.64, n.2, p.151-157, abr./jun.2006Advertisement call of Leptodactylus ocellatus, recorded 29/XI/2004. Air temperature 21ºC and water temperature 24ºC:fig.4- wave form; fig.5- audiospectrogram; fig.6- power spectrum.465                                     ADVERTISEMENT CALLS OF THREE LEPTODACTYLID FROGS IN THE STATE OF BAHIA                               155Arq. Mus. Nac., Rio de Janeiro, v.64, n.2, p.151-157, abr./jun.2006Advertisement call of Leptodactylus troglodytes, recorded 21/IV/1998. Air temperature 20ºC: fig.7- wave form (7a =compacted view of amplitude structure; scale bar = 0.04s); fig.8- audiospectrogram (8a = compacted view of frequencystructure; scale bar = 0.04s); fig.9- power spectrum.798156                                        I.NUNES & F.A.JUNCÁArq. Mus. Nac., Rio de Janeiro, v.64, n.2, p.151-157, abr./jun.2006DISCUSSIONThe advertisement call of Proceratophrys cristicepspresents differences from the known vocalizationsof other species of Proceratophrys: P. avelinoi (KWET& BALDO, 2003), P. bigibbosa (KWET & FAIVOVICH, 2001),P. boiei (HEYER et al., 1990), P. brauni (KWET &FAIVOVICH, 2001), P. cururu (ETEROVICK & SAZIMA, 1998),and P. moehringi (WEYGOLDT & PEIXOTO, 1985). Thenumber of pulses of the advertisement call of P.cristiceps ( x̄  = 57) is greater than for P. avelinoi ( x̄  =38), P. bigibbosa ( x̄  = 42), P. boiei (30-35), P. brauni(x̄  = 26), P. cururu (40), and less than for P. moehringi(140). The call duration of P. cristiceps ( x̄  = 0.66 s) islonger than in P. avelinoi ( x̄  = 0.54 s) and shorterthan in P. bigibbosa (1.6-1.9s), P. boiei (0.7-0.8 s), P.brauni (0.7-0.9 s), P. cururu (1.2 s), and P. moehringi(3.5-4.0 s). The pulse rate of P. cristiceps ( x̄  = 89.54pulses/s) is faster than in P. avelinoi ( x̄  = 68.7 pulses/s),P. bigibbosa ( x̄  = 25.1 pulses/s), P. boiei (45 pulses/s),P. brauni ( x̄   = 37.5 pulses/s), P. cururu (45 pulses/s),and P. moehringi (33-40 pulses/s). The dominantfrequency of P. cristiceps ( x̄ = 0.94 kHz) is lower thanin P. avelinoi (x̄  = 1.60 kHz), P. bigibbosa (1.05kHz), and P. brauni (1.35 kHz), and higher thanin P. boiei (0.6 kHz), P. cururu (0.9 kHz), and P.moehringi (0.45 kHz).The advertisement call of Leptodactylus ocellatusfrom Serra São José, Bahia, Brazil is different fromthe advertisement call of L. ocellatus from EntreRios, Argentine, available in “Catalogue of the voicesof argentine amphibians” (STRANECK et al.,  1993).Both calls consisted of a repeated note, but theadvertisement call of Entre Rios is tonal, while fromBahia is multipulsed. The dominant frequency ofthe population here studied ( x̄ = 0.35 kHz) seemssimilar to the argentine population (amplitudefrequency of call ranges from 0.2 to 0.4 kHz). Thedistinct structure of the call (multipulsed x tonal)observed may indicate that called species L.ocellatus represents a complex of species.The advertisement call of Leptodactylus troglodyteswas described from one locality in the State of Bahia(Municipality of Andaraí) by HEYER (1978). Thedominant frequency of the advertisement call ofLeptodactylus troglodytes from Mangue Seco (3.20-3.39 kHz) is quite similar to that of L. troglodytesfrom Andaraí (2.60-3.20 kHz), as is the callduration ( x̄  = 0.06s from Mangue Seco and 0.04sfrom Andaraí). These results lead us to concludethat the two populations of Leptodactylustroglodytes from Mangue Seco and Andaraírepresent the same species.ACKNOWLEDGMENTSWe thank Prof. W. Ronald Heyer (SmithsonianInstitution, USA) for critically reading andimproving the manuscript. A.Santana, E.Mercês,D.Andrade, F.Lima, F.Casal, M.Borba,M.C.Carneiro, and R.Santiago (UEFS) for help inthe fieldwork. Prof. A.Kwet (SMNS, Germany) andProf. W. Ronald Heyer for reprints. Prof. C.A.G.Cruz(MNRJ) by indicating pertinent bibliography.Universidade Estadual de Feira de Santana (UEFS)and Fundação de Amparo à Pesquisa do Estado daBahia (FAPESB) supported our work. UEFSprovided a graduate grant to I.Nunes.REFERENCESCHARIF, R.A.; MITCHELL, S. & CLARK, C.W., 1995.Canary 1.2 user’s manual. Ithaca, New York: CornellLaboratory of Ornithology. 229p.DUELLMAN, W.E. & TRUEB L., 1986. Biology ofamphibians. New York, St. Louis, San Francisco:McGraw-Hill Book Company. 670p.ETEROVICK, P.C. & SAZIMA, I., 1998. New species ofProceratophrys (Anura: Leptodactylidae) fromsoutheastern Brazil. Copeia, 1998(1):159-164.GERHARDT, H.C., 1988. Acoustic properties used in callrecognition by frogs and toads. In: FRITZSCH, B.M.; RYAN,M.J.; WILCZYNSKI, W.; HETHERINGTON, T.E. &WALKOWIAK, W. (Eds.) The evolution of the amphibianauditory system. New York: JohnWiley & Sons. p.455-483.HADDAD, C.F.B. & POMBAL JR., J.P., 1998. Redescriptionof Physalaemus spiniger (Anura: Leptodactylidae) anddescription of two new reproductive modes. Journal ofHerpetology, 32(4):557-565.HADDAD, C.F.B. & SAZIMA, I., 2004. A new species ofPhysalaemus (Amphibia; Leptodactylidae) from the Atlanticforest in southeastern Brazil. Zootaxa, 479:1-12.HEYER, W.R., 1978. Systematics of the fuscus group ofthe frog genus Leptodactylus (Amphibia, Leptodactylidae).Bulletin of Los Angeles County Museum of NaturalHistory, 29:1-85.HEYER, W.R. & JUNCÁ, F.A., 2003. Leptodactyluscaatingae, a new species of frog from eastern Brazil(Amphibia: Anura: Leptodactylidae). Proceedings of theBiological Society of Washington, 116(2):317-329.HEYER, W.R.; GARCIA-LOPEZ, J.M. & CARDOSO,A.J., 1996. Advertisement call variation in theLeptodactylus mystaceus species complex (Amphibia:Leptodactylidae) with description of a new siblingsspecies. Amphibia-Reptilia, 17(1):7-31.                                     ADVERTISEMENT CALLS OF THREE LEPTODACTYLID FROGS IN THE STATE OF BAHIA                               157Arq. Mus. Nac., Rio de Janeiro, v.64, n.2, p.151-157, abr./jun.2006HEYER, W.R.; RAND, A.S.; CRUZ, C.A.G.; PEIXOTO, O.L.& NELSON, C.E., 1990. Frogs of Boracéia. Arquivos deZoologia, 31(4):231-410.JUNCÁ, F.A., 1999. Sucesso reprodutivo e seleção sexualem Colostethus stepheni. São Paulo. 103p. Tese(Doutorado em Zoologia). Programa de Pós-graduação emCiências Biológicas – Zoologia, IB-USP.KWET, A. & BALDO, D. 2003. Advertisement call of theleptodactylid frog Proceratophrys avelinoi. Amphibia-Reptilia, 24(1):104-107.KWET, A. & FAIVOVICH, J., 2001. Proceratophrysbigibbosa species group (Anura: Leptodactylidae), withdescription of a new species. Copeia, 2001(1):203-215.LITTLEJOHN, M.J., 2001. Patterns of differentiation intemporal properties of acoustic signals of anurans. In:RYAN, M.J. (Ed.) Anuran communication. Washington:Smithsonian Institution Press. p.102-120.STRANECK, R.; OLMEDO, E.V. & CARRIZO, G.R., 1993.Catalogo de voces de anfibios argentinos. Parte 1.Buenos Aires: Ediciones L.O.L.A. 131p.VIELLIARD, J., 1993. “Side-bands” artefact and digitalsound processing. Bioacustics, 5(2):159-162.WEYGOLDT, P. & PEIXOTO, O.L., 1985. A new species ofhorned toad (Proceratophrys) from Espírito Santo, Brazil(Amphibia: Salientia: Leptodactylidae). SenckenbergianaBiologica, 66(1/3):1-8.

Canto de anúncio de três espécies da família Leptodactylidae no Estado da Bahia, Nordeste do Brasil (Amphibia, Anura, Leptodactylidae), com considerações sobre suas posições taxonômicas

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Canto de anúncio de três espécies da família Leptodactylidae no Estado da Bahia, Nordeste do Brasil (Amphibia, Anura, Leptodactylidae), com considerações sobre suas posições taxonômicas

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