Herpetology Notes, volume 13: 805-808 (2020) (published online on 05 October 2020)

An unidentified call emission by boticariana Giaretta and Aguiar, 1998

Edelcio Muscat1, Daniel Rodrigues Stuginski1, Matheus de Toledo Moroti1,2,*, and Luís Felipe Toledo3

There is a lack of information about the natural history combining the morphological characteristics of the of thousands of species (Toledo et al., 2014). species’ description (Giaretta and Aguiar, 1998). It is Several factors limit the acquisition of basic natural also the only species of Megaelosia that occurs at the history data, such as species rarity, cryptic behaviour, or study site (Muscat et al., 2020). We here describe these absence of audible vocalisations (Gaston and Blackburn, vocalisations and discuss their possible function. 1994; Verdade et al., 2008; Toledo et al., 2014). Rare The recordings were made during regular field surveys species generally have small geographical ranges, low carried out by the Projeto Dacnis research team in the tolerance to changes in habitat, small populations, Reserva das Araucárias, sub-district of São Francisco or even a combination of all these traits (Rabinowitz, Xavier, Municipality of São José dos Campos, São 1981). species of the genus Megaelosia fit all Paulo State, Brazil. All calls were made when one of us these criteria, with almost no data available on their (E.M.) handled the by their hind limbs. All frogs natural history (see Giaretta and Aguiar, 1998; Alves emitted the vocalisation with mouth closed while trying and Toledo, 2017; Augusto-Alves et al., 2018). All to escape. We did not observe any vocal sac expansion. Megaelosia species inhabit fast-flowing streams in These calls were recorded with a smartphone (Moto X4 the Brazilian Atlantic Forest and the vast majority are and QuickVoice recorder application), approximately considered mute, as they have never been reported to 5 cm from the frogs. Recordings were made at a produce acoustic signals (Augusto-Alves et al., 2018). sample rate of 44 kHz and a sample size of 16 bits of The exception is M. boticariana. Giaretta and Aguiar resolution in .wav format. All sound analyses were (1998) reported, but did not record, a weak vocalisation performed in Raven Pro 1.4 (Bioacoustics Research emitted by three different specimens of M. boticariana Program, Cornell Lab of Ornithology). We filtered out during handling. all the sounds below 200 Hz to decrease environmental In recent field samplings we were able to witness sound interference. Raven Pro configurations adopted and record the same behaviour displayed by three were: 55% brightness, 75% contrast, and both DFT unvouchered specimens of M. boticariana (two adults size and window size of 256, Hann window, and 50% and one juvenile) of undetermined sex, due to lack overlapping. We measured the following acoustic of sexual structures. We identified the species by parameters: call duration; note duration; interval between notes; note number per call; pulse number per note; peak of dominant frequency (peak frequency function in Raven); minimum frequency (frequency 5% function in Raven); maximum frequency (frequency 95% function in Raven); and frequency bandwidth (BW 1 Projeto Dacnis, Ubatuba and São Francisco Xavier, São Paulo 90% function in Raven). We measured all temporal 11680-000 Brazil. parameters directly from the oscillogram, the spectral 2 Pós-graduação em Ecologia e Conservação, Instituto de parameters from the spectrogram, and we followed Biociências, Universidade Federal do Mato Grosso do Sul, bioacoustic terminology and definitions presented by Campo Grande, Mato Grosso do Sul 79070-900 Brazil. Köhler et al. (2017). These recordings are deposited at 3 Laboratório de História Natural de Anfíbios Brasileiros, Departamento de Biologia , Instituto de Biologia, Fonoteca Neotropical Jacques Vielliard (FNJV), Museu Universidade Estadual de Campinas, Campinas, São Paulo de Zoologia “Prof. Adão José Cardoso”, Universidade 13083-862 Brazil. Estadual de Campinas, Campinas, Brazil: FNJV 44967- * Corresponding author. E-mail: [email protected] 71. 806 Edelcio Muscat et al.

Megaelosia boticariana (Fig. 1) calls were mostly low in amplitude and composed of 1 to 6 notes with total call duration between 29 and 569 ms. These notes were variable in structure. Some notes were not pulsed and some were pulsed, with varying durations, from very short click sounds (Fig. 2A), to longer notes having up to 40 pulses (Fig. 2B-D). Note duration ranged from 2 to 237 ms, and the interval between notes from 7 to 66 ms. Frequency also varied: some notes had only one frequency band (Fig. 2A), other notes had multiple frequency bands (Fig. 2B-D). Dominant frequency, maximum frequency, and frequency bandwidth were also variable due to the presence of high-pitched frequency pulses in some notes (Table 1). Although we recorded Figure 1. Specimen of Megaelosia boticariana found in calls with a smartphone, which does not have the same Reserva das Araucárias (-22.903024, -46.018145, WGS-84), recording quality as other devices, it provides the same sub-district of São Francisco Xavier, Municipality of São José dominant frequency as other recorders and also contains dos Campos, São Paulo State, Brazil.

Figure 2. Megaelosia boticariana call variation: a one-pulse note (A), a multi-pulsed note (B), a note with poorly defined pulses and more than one frequency band (C), and a long and pulsed note with high-pitched frequencies (D). An unidentified call emission by Megaelosia boticariana 807 sufficient quality information to extract the parameters Release calls are vocalisations used by frogs of both we used to presently describe the call (see Köhler et al., sexes, when the amplexus is not desired by the amplected 2017). These high-pitched frequencies sounded like a individual (Toledo et al., 2015). Release calls can also click in the beginning, middle, or end of the note (Fig. be emitted during human handling, especially when the 1D). Although we did not measure the sound pressure frog is held by the flanks. However, because the calls level, the calls were weak, probably inaudible beyond a reported here were also emitted by non-amplected frogs distance of 1 m in a quiet environment (it would be even and with no human manipulation (both M. boticariana less at the stream margins). Moreover, one of us (E.M.) and M. goeldii), it is unlikely that these are release heard a vocalisation, similar to those recorded, during calls. Another possibility is that these vocalisations are a nocturnal field survey near the rocks where we found defensive calls. Distress calls are the most common the other M. boticariana specimens. However, we were defensive call, generally emitted when frogs are seized unable to locate the specimen that made the call. by their predators (or humans), and function to distract or Our report is the first analysis of sound recordings of intimidate predators (Hödl and Gollmann, 1986; Toledo specimens of the genus Megaelosia. Giaretta and Aguiar et al., 2015). However, distress calls are loud, high- (1998) described the sound emission of M. boticariana pitched and emitted with mouths wide open (Toledo et as a “weak vocalisation when the frogs were handled al., 2015). The vocalisations recorded by us were weak in field”. A call was also heard for M. goeldii during a (too weak to scare predators), mostly composed of field survey in July 2006: a weak, low-pitched sound low frequencies, and produced with the mouth closed. was emitted by an adult M. goeldii inside a rock crevice Therefore, they do not match with the distress call on a stream bank (A.M.P.T. Carvalho-e-Silva and characteristics (Toledo et al., 2015). Finally, alarm calls V.G.D. Orrico, pers. comm.). These other descriptions are another type of defensive call emitted while the frog are similar to our observations. They are weak sounds, is fleeing or when the frog is being preyed on (Toledo emitted either during handling or, possibly, while et al., 2015; Köhler et al., 2017). These calls have the fleeing. Thus, we consider they are the same type of function of alerting nearby conspecifics (Leary and call. Megaelosia boticariana is a nocturnal species Razafindratsita, 1998). Alarm calls are rarely recorded, found under rocks and fallen branches in the stream but they seem to be employed particularly by species (Muscat et al., 2020). The sounds we heard in the field that rely on escaping into the water (e.g., Lithobates were almost inaudible, since they were emitted close to catesbeianus; Cooper Jr., 2011). Although specimens of a fast-flowing and noisy stream. all species of the genus Megaelosia live by the water

Table 1. Call measurements of the Megaelosia boticariana vocalisation. Table 1. Call measurements of the Megaelosia boticariana vocalisation.

Acoustic parameters Specimen 1 Specimen 2 Specimen 3 Call 1 Call 2 Call 3 Call 4 Call 5

Call duration (ms) 125 29 157 569 237 Notes/call 6 1 2 3 1 Note duration 9.83 ± 11.02 29 70.00 ± 96.16 116.67 ± 28.94 237 (2 – 25) – (2 – 138) (98 – 150) – Pulses/note 1.67±2.16 0 – 14.67 ± 13.05 44 (0 – 6) – (0 – 1) (0 – 25) – Dominant frequency (kHz) 1.52 ± 0.13 1.72 2.58 ± 1.70 5.28 ± 6.61 11.71 (1.38 – 1.72) – (1.38 – 3.79) (1.38 – 12.92) – Minimum frequency (kHz) 1.03 ± 0.22 1.21 0.86 ± 0.49 0.80 ± 0.26 0.69 (0.86 – 1.38) – (0.52 – 1.21) (0.52 – 1.03) – Maximum frequency (kHz) 4.62 ± 3.62 4.82 9.74 ± 1.36 11.65 ± 7.17 19.98 (1.72 – 11.37) – (8.78 – 10.70) (4.82 – 19.12) – Frequency bandwidth (kHz) 3.59 ± 3.70 3.61 8.89 ± 1.85 10.86 ± 7.08 19.29 (0.34 – 10.34) – (7.58 – 10.20) (3.96 – 18.11) – Internote duration (ms) 13.00 ± 6.48 – 17 33.00 ± 30.11 – (7 – 24) – – (7.00 – 66.00) –

1

808 Edelcio Muscat et al. and usually escape jumping into streams (E. Muscat, Gaston, K.J., Blackburn, T.M. (1994): Are newly described bird pers. obs.), a call with an alarm function should be loud species small-bodied? Letters 2: 16–20. enough to be heard by nearby conspecifics, which does Giaretta, A.A., Aguiar Jr, O. (1998): A new species of Megaelosia from the Mantiqueira Range, Southeastern Brazil. Journal of not seem to be the case. Herpetology 32: 80–83. According to Augusto-Alves et al. (2018) M. apuana Hödl, W., Gollmann, G. (1986): Distress class in Neotropical frogs. is mute and has visual communication and aggressive Amphibia-Reptilia 7: 11–21 interactions with conspecifics. Visual signalling is also Muscat, E., Stuginski, D., Nunes, I., Martins, I., Augusto-Alves, present in some species of torrent frogs, such as those of G., Toledo, L.F., Moroti, M.T. (2020): Update on the geographic the genus (de Sá et al., 2016). However, we do distribution of three poorly known frog species in the Mantiqueira not have more information about visual communication mountain range. Herpetology Notes 13: 573–577. Köhler, J., Jansen, M., Rodríguez, A., Kok, P.J.R., Toledo, L.F., in Megaelosia boticariana. Another possibility of Emmrich, M., et al. (2017): The use of bioacoustics in anuran communication is underwater vocalisation (Zheng et : theory, terminology, methods and recommendations al., 2011; Brunetti et al., 2017). Yet, this behaviour in for best practice. Zootaxa 4251: 1–124. anurans is restricted to calm streams (Brunetti et al., Leary C.J., Razafindratsita, V.R. (1998): Attempt predation 2017), not noisy and fast as the one Megaelosia spp. on a hylid frog, Phrynohyas venulosa, by an indigo snake, inhabit. Based on our current knowledge, we cannot Drymarchon corais, and the response of conspecific frogs to assign a specific role to the vocalisations we presently distress calls. Amphibia-Reptilia 19: 442–446. Rabinowitz, D. (1981): Seven forms of rarity: In: The Biological describe. Aspects of Rare Plant Conservation, p. 205–217. Synge, H., Ed., Chichester, West Sussex, England, John Wiley & Sons Ltd. Acknowledgments. We thank Projeto Dacnis for the support, Toledo, L.F., Becker, C.G., Haddad, C.F.B., Zamudio, K.R. (2014): Elsie K. Rotenberg for the English revision and suggestions to Rarity as an indicator of endangerment in Neotropical frogs. improve this manuscript, Renata de Albuquerque Pinheiro and Biological Conservation 179: 54–62. Patrícia Pupo do Prado for allowing us to carry out our research Toledo, L.F., Martins, I.A., Bruschi, D.P., Passos, M.A., Alexandre, in their property “Reserva das Araucárias” and for always C., Haddad, C.F.B. (2015): The anuran calling repertoire in the supporting our studies. We thank Ana Maria P. T. Carvalho- light of social context. Acta Ethologica 18: 87–99. e-Silva and V.G.D. Orrico for the valuable information on M. Verdade, V.K., Rodrigues, M.T., Cassimiro, J., Pavan, D., Liou, goeldii. LFT thanks Fundação de Amparo à Pesquisa do Estado N., Lange, M.C. (2008): Advertisement call, vocal activity, de São Paulo (Process n. 2016/25358-3) and Conselho Nacional and geographic distribution of Brachycephalus hermogenesi de Desenvolvimento Científico e Tecnológico (Process n. (Giaretta and Sawaya, 1998) (Anura, Brachycephalidae). 300896/2016-6) for a grant and a fellowship. MTM is grateful Journal of Herpetology 42: 542–549. to Coordenação de Aperfeiçoamento de Pessoal de Nível Zheng, Y., Dingqi, R.A.O., Murphy, R.W., Xiaomao, Z. (2011): Superior for its scholarship. We thank Instituto Chico Mendes Reproductive behavior and underwater calls in the emei de Conservação da Biodiversidade/Sistema de Autorização e mustache toad, Leptobrachium boringii. Asian Herpetological Informação em Biodiversidade for the licenses granted (Process Research 2: 199–215. n. 27745–19).

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