SALAMANDRA 51(2) 103–110 30 JuneNotes 2015 on ProceratophrysISSN 0036–3375 caramaschii Advertisement call, colour variation, natural history, and geographic distribution of Proceratophrys caramaschii (Anura: Odontophrynidae) Ivan Nunes1, Daniel Loebmann2, Carlos Alberto G. Cruz1 & Célio F. B. Haddad3 1) Universidade Federal do Rio de Janeiro, Museu Nacional, Departamento de Vertebrados, 20940-040 Rio de Janeiro, RJ, Brazil 2) Universidade Federal do Rio Grande, Instituto de Ciências Biológicas, Laboratório de Vertebrados, 96203-900 Rio Grande, RS, Brazil 3) Universidade Estadual Paulista “Júlio de Mesquita Filho”, Instituto de Biociências, Departamento de Zoologia, 13506-900 Rio Claro, SP, Brazil Corresponding author: Ivan Nunes, e-mail: [email protected] Manuscript received: 17 May 2014 Accepted: 21 August 2014 by Jörn Köhler Abstract. Proceratophrys caramaschii was described only from a single locality in Mucuripe, Fortaleza municipality, Ceará state, Brazil. The discovery of a new population of this poorly known species facilitated the collection of new data re- garding colour in life, vocalization, habitat, and geographic distribution. It has a much wider distribution than formerly thought, is considerably variable in its colour pattern, and its reproductive strategy is strongly associated with the begin- ning of the rainy season. Males call from the ground and hidden in vegetation. The advertisement call is a short trill of notes. Further data is necessary to evaluate the threat status of this species. Key words. Amphibia, Anura, Proceratophrys, antiphonal call, colour variation, biology, Caatinga Domain. Introduction Proceratophrys caramaschii was recently described by Cruz et al. (2012) based on 39 specimens from Mucuripe, The genus Proceratophrys Miranda-Ribeiro current- Fortaleza municipality, coast of Ceará state. The authors ly comprises 40 species that are distributed throughout stated that the known distribution was restricted to the Brazil, northeastern Argentina, and Paraguay (see Frost type locality, and were unable to provide additional bio- 2014). Among them, the Proceratophrys cristiceps species logical information on this species (e.g., advertisement call group is composed of species lacking palpebral append- and natural history). ages and postocular swellings, and inhabiting mainly sea- While investigating the anurofauna in a transition zone sonally dry open environments (Cerrado and Caatinga between Caatinga (dry savannah) and forest formation, in domains) of Brazil (Giaretta et al. 2000). Fifteen spe- the Complexo do Planalto da Ibiapaba, Ceará state, Bra- cies are currently included in this taxonomic group (sensu zil (see Loebmann & Haddad 2010), two of us (DL and Brandão et al. 2013): Proceratophrys aridus Cruz, Nunes CFBH) discovered a population that was previously as- & Juncá, P. bagnio Brandão, Caramaschi, Vaz-Silva & signed as P. cristiceps, but in fact represents P. caramaschii. Campos, P. branti Brandão, Caramaschi, Vaz-Silva & Herein, we present recently gathered data pertaining to Campos, P. caramaschii Cruz, Nunes & Juncá, P. carranca P. caramaschii from this population. Godinho, Moura, Lacerda & Feio, P. concavi tympanum Giaretta, Bernarde & Kokubum, P. cristiceps (Müller), P. cururu Eterovick & Sazima, P. dibernardoi Brandão, Materials and methods Caramaschi, Vaz-Silva & Campos, P. goyana (Miran- da-Ribeiro), P. huntingtoni Ávila, Pansonato & Strüss- The acronyms used in the text are CFBH Célio( F. B. mann, P. moratoi (Jim & Caramaschi), P. rotundi palpebra Haddad Collection, Departamento de Zoologia, I.B., Martins & Giaretta, P. strussmannae Ávila, Kawashi- Universidade Estadual Paulista, Rio Claro, SP, Brazil), DL ta-Ribeiro & Morais, and P. vielliardi Martins & Gia- (Daniel Loebmann sound recordings, stored at the De- retta. partamento de Zoologia, I.B., Universidade Estadual Pau- © 2015 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Mannheim, Germany All articles available online at http://www.salamandra-journal.com 103 Ivan Nunes et al. lista, Rio Claro, SP, Brazil), and NHMB (Naturhistorisches dio-spectrograms, and power spectra were obtained using Museum, Basel, Switzerland). The diagnosis of the species SoundRuler v. 0.9.6.0 (Gridi-Papp 2007), with a changed follows Cruz et al. (2012), Brandão et al. (2013), and our Fast Fourier Transform length (FFT) of 256. The following new data provided. descriptions are based on the advertisement calls of three We found calling males of Proceratophrys caramaschii in males. The records DL 001, 002 and 003 represent single disturbed areas of a relict moist forest in the municipalities calling males, and DL 004 males calling antiphonally. of Ubajara (03°49’ S, 40°55’ W, 857 m above sea level), and Viçosa do Ceará (03°34’ S, 41°04’ W, 340 m a.s.l.; WGS84 datum), both in Ceará state, Brazil, between February of Results 2007 and January of 2008. We recorded advertisement calls emitted by males using a Sony cassette tape recorder The specimens were identified upon the presence of the (TCM-150) with an external directional microphone, Yoga following traits (according to Cruz et al. [2012], with the (HT 81 Boom), positioned at a maximum distance of 3 m to addition of character states referring to the eyelids accord- the calling males. The resulting sound files were deposited ing to Brandão et al. [2013], and SVL data of this study): in the CFBH Sound Library (DL 001 [8 February 2007], medium size (adult males SVL 42.7–56.3 mm, adult fe- DL 002 [28 February 2007], DL 003 [22 January 2008], males 53.8–68.3 mm); snout rounded in dorsal view, obtuse DL 004 [28 January 2008]), and voucher specimens stored in profile view; HL/HW 78–86%; tympanum concealed; in the CFBH Amphibian Collection (CFBH 16102, 16109, anterior and posterior eyelid tubercles not differentiated; 16112–16114, 16119, 16120, 16125, 16126, 16131, 23455–23462, one transverse crest of interocular tubercles; canthal crests 23756–23762). The recorded calling individuals were not poorly defined; frontoparietal crest developed; outer meta- collected. carpal tubercle divided into two oval sections, with the in- We digitalized the vocalization recordings using a PC ner one being larger than the external one; webbing formu- desktop equipped with a sound card, Creative Sound Blast- la I 1‑2 II 2+‑3 III 2+‑4‑ IV 4‑2 V; inner metacarpal tubercle er Audigy 2 ZS (sampling frequency of 44.1 kHz and sam- elongated; a few large blotches on the venter. ple size of 16 bits). Advertisement calls were analysed using Raven Pro 1.4 software (Charif et al. 2010), with Fast Fou- Advertisement call: The advertisement call of isolated males rier Transform length (FFT) = 1024, Frame = 100, Over- (Fig. 1) comprises one multipulsed note with 33 to 59 pulses lap = 60, and window function flap top. Waveforms, au- (mean 45 ± 9.19; n = 3 males, 45 calls); call duration 0.41 to Ampl Ampl (Pa) Time (s) Frequency Frequency (kHz) Time (s) Amplitude Frequency (kHz) Figure 1. Wave form (top) and spectrogram (middle) of the advertisement call and power spectrum of the pulse (bottom) with a higher amplitude of a single male of Proceratophrys caramaschii. Recorded in the municipality of Viçosa do Ceará, Ceará state, Brazil. DL 003, 22 January 2008, air temperature not recorded. 104 Notes on Proceratophrys caramaschii 0.74 s (mean 0.57 ± 0.11; n = 3 males, 45 calls); call interval isolated males (77.50 to 79.85 pulses/s, mean 78.14 ± 0.71; 0.50 to 1.94 s (mean 0.93 ± 0.43; n = 3 males, 42 intervals); n = 1 male B, 15 calls). The antiphonal call interval of male rate of pulse emission 78.56 to 81.82 pulses/s (mean 80.01 ± A ranges from 0.44 to 0.77 s (mean 0.54 ± 0.09; n = 1 male 0.86; n = 3 males, 45 calls); pulse duration 0.006 to 0.009 s A, 15 intervals). The call interval of male B was not meas- (mean 0.0088 ± 0.0007; n = 3 males, 6 calls, 360 pulses); ured, because it would start just before the end or just be- and pulse interval 0.001 to 0.007 s (mean 0.0048 ± 0.0011; fore the beginning of the call of male A, with little over- n = 3 males, 6 calls, 354 intervals). The dominant frequen- lap, which renders it difficult to pick the exact beginning or cy has two bandwidths, with the most common lying at end of the call. The remarkable difference between the calls 0.86 kHz (87% of 30 calls of 3 males). The other bandwidth of male A and male B is the division of the acoustic space is present at 1.03 kHz (13% of 30 calls of 3 males). The call by different dominant frequencies used by each male, with has a descendant amplitude modulation, with the first male A occupying the frequency bandwidth of 0.86 kHz pulse being much higher than the last one, and does not and male B that of 1.03 kHz. exhibit frequency modulation; the pulses have descendant amplitudes and frequency modulations. Colour variation in life: Regarding the variation of the dor- Antiphonal calls (Fig. 2) were emitted in “call and re- sal colouration pattern, P. caramaschii may be classified sponse” style, with partial overlapping between calls. The as a highly polychromatic species (see some examples in advertisement call of male A has the same temporal pa- Fig. 3). The dorsal colour pattern is marbled with several rameters as those of single calling males. The call of male B shades of brown on a cream background. The cream back- is slightly different in that it exhibits a lower range of pulse ground and the light brown tones may have a reddish hue. emissions while still overlapping with those of male A or The mid-dorsal region, internal to the limits of a spear- Ampl Ampl (Pa) Time (s) Frequency Frequency (kHz) Time (s) Amplitude Amplitude Frequency (kHz) Frequency (kHz) Figure 2. Wave form (top) and spectrogram (middle) of the advertisement calls and power spectrum (bottom) of the pulse with a higher amplitude of Pro ceratophrys caramaschii in antiphonal interaction.