Herpetology Notes, volume 10: 27-29 (2017) (published online on 27 January 2017)

Description of the distress call in and the post-amplexus vocal display in savagei (Anura: Centrolenidae)

Julián Rios-Soto1,*, Ana María Ospina-L.1, María Camila Basto-Riascos1, Jhulyana López-Caro1 and Fernando Vargas-Salinas1

One of the most frequent modalities in anuran the advertisement call (Wells, 2007). This latter type communication is the use of auditory signals (Gerhardt of call has been reported and described just for some and Huber, 2002). Different types of calls have been glassfrogs species: H. fleishmanni (Greer and Wells, classified according to the context in which they are 1980); E. prosoblepon (Jacobson ,1985); N. grandisonae emitted, of which the advertisement call is the most (Hutter et al., 2013) and Centrolene savagei (Vargas- conspicuous and therefore the most studied anuran Salinas et al., 2014). signal (Wells, 2007). The diversity and importance of other call types is still vastly understudied, and a better Distress call in Espadarana prosoblepon comprehension of anuran auditory signals relies on Espadarana prosoblepon is a glassfrog whose males the observation of the behaviour during which they are quite territorial and exhibit aggressive social are emitted (Wells, 1977; Gerhardt, 1992). Here, we interactions; they hang venter-to-venter and keep their describe the distress call of Espadarana prosoblepon, and the post-amplexus vocal display of Centrolene humeral spines interlocked in the other male’s axial savagei, two species of glassfrogs with populations in region (Krohn and Voyles, 2014). On May 20 of 2015 Colombia. (20:10 hours) we observed an aggressive interaction between two males of this species (Fig. 1A) at the The family Centrolenidae is a Neotropical group of stream “La Aldana” located in the Botanical Garden of composed of approximately 150 species (Frost et the Universidad del Quindío, municipality of Armenia, al., 2016). Males of some glassfrogs exhibit aggressive western slope of the Central Andes of Colombia interactions and it includes the defence of territory, calling (4º32’40”N; 75º46’13”W; altitude: 1500 m). The two and oviposition sites: Hyalinobatrachium fleishmanni males were hanging by their toes in the fronds of a (Greer and Wells, 1980); Espadarana prosoblepon fern at 2.10 m above the water level; they were in an (Jacobson, 1985); Nymphargus grandisonae (Hutter upside-down and venter-to-venter grappling position. et al., 2013). However, the auditory signals used in Both males had a similar size: snout-vent length of such interactions have only been described in some 27.1 mm and 28.2 mm. The larger male was grasping species (e.g. Centrolene buckleyi: Bolivar et al., 1999; the smaller male and dangling with his legs free and Centrolene lynchi: Dautel et al., 2011 and Nymphargus emitted a distress call approximately every 10 minutes, grandisonae: Hutter et al., 2013). On the other hand, possibly as a result of the agitation and pain caused by in some anurans, males were observed to alter their the fight. The interaction lasted for 139 minutes and behaviour when females are close, including the ended when the defeated male fell onto a leaf below. emission of courtship calls which are quite distinct from The winning male went up to a fern frond beam and began to produce advertisement calls. We recorded wounds of the phalanges and dorsum of both males. We also recorded one distress call with a Nikon COOLPIX

1 Programa de Biología, Facultad de Ciencias Básicas y P520 digital camera and analysed it after extracting the Tecnologías, Universidad del Quindío, Armenia, Colombia. sound from the video in WAV format. The call analysis * Corresponding author e-mail: [email protected] was performed in Raven Pro 1.4 (Bioacustics Research 28 Julián Rios-Soto et al.

Figure 1. Aggressive interaction in the glassfrog Espadarana prosoblepon (A) (the defeated males is marked with an arrow), Oscillogram (B) and spectrogram (C) of the distress call emitted by the defeated male.

Program, 2011) with a Blackman algorithm and a interrupted amplexus once or twice and reinitiated window size of 256. calling activity. We recorded two of those calls emitted The distress call consisted of two short “beep” notes by a male with a digital recorder (Marantz PMD661) and with amplitude and frequency modulation; the former a unidirectional microphone (Sennheisser K6/ME 66). beep lasted 47 ms and the latter one lasted 51 ms (Fig. The recording files were analysed using the software 1B); the dominant frequency of the former beep was Raven Pro 1.4 (Bioacustics Research Program, 2011) 5350.7 Hz, while in the latter beep was 5684.8 Hz (Fig. with a Blackman algorithm and a windows size of 256. 1C). Hedman and Hughley (2015) mention that the The post-amplexus vocal display in Centrolene fighting between males of E. prosoblepon includes calls, savagei included two types of auditory signals (Fig. but we are the first to measure temporal and spectral call 2). One type of signal consisted of one note similar features. to a “beep”, which lasted on average 11 ± 6 ms and whose mean dominant frequency was 5684.8 ± 0.0 Hz Post-amplexus vocal display in Centrolene savagei (N= 2). This signal is similar to the advertisement call Males of Centrolene savagei exhibit a reproductive described by Díaz-Gutiérrez et al. (2013). The second behaviour which includes the formation of amplexus type of signal was composed by a unique note with 31 after a courtship display; nevertheless, in some cases ± 0.7 pulses. Each pulse lasted on average 7.2 ± 1 ms an interruption of the amplexus by the amplectant male, and was followed by short silent intervals of 3.1 ± 0.7 which then begins to vocalize again, has been recorded ms on average; the mean call duration was 156 ± 28.2 (Vargas-Salinas et al., 2014). In March 2016, we ms and the mean dominant frequency was 5871.2 ± observed three interrupted amplexi in a population of C. 101.8 Hz (N=2). The temporal structure of this signal is savagei located at the stream “El Bosque”, residential similar to the courtship call emitted before the amplexus “La Aldea”, municipality of Circasia, western slope formation by a male of C. savagei in a population of of the Central Andes of Colombia (4º38’1.7”N, Western Andes of Colombia (Vargas-Salinas et al., 75º37’21.8”W; altitude: 1749 m). In two cases, we 2014). These authors were the first to report an anuran recorded that males, without any apparent reasons, male temporarily interrupting amplexus for vocalizing, Distress call in Espadarana prosoblepon and vocal display in Centrolene savagei 29

Dautel, N., Maldonado, A.L.S., Abuza, R., Imba, H., Griffin, K., Guayasamin, J.M. (2011): Advertisement and combat calls of the glass Centrolene lynchi (Anura: Centrolenidae), with notes on combat and reproductive behavior. Phyllomedusa 10: 31-43. Frost, D.R. (2016): Species of the World: an Online Reference. Version 6.0 Available at: http: http://research.amnh. org/vz/herpetology/amphibia/. Last accessed on 2 February 2016. Gerhardt, H.C. (1992): Multiple messages in acoustic signals. Seminars in Neuroscience 4: 391-400. Gerhardt, H.C., Huber, F. (2002): Acoustic communication in insects and anurans. Common problems and diverse solutions. Chicago, University of Chicago Press. Greer, B.J., Wells, K.D. (1980): Territorial and reproductive behavior of the tropical American frog Centrolenella fleischmanni. Herpetologica 36: 318-326. Hedman, H.D., Hughey, M.C. (2015): Body size, humeral spine size, and aggressive interactions in the emerald , Espadarana prosoblepon (Anura: Centrolenidae) in Costa Rica. Mesoamerican Herpetology 2: 500-508. Figure 2. Oscillogram (A), spectrogram (B) and power Hutter, C.R., Esobar-Lasso, S., Rojas-Morales, J.A., Gutiérrez- spectrum (C) of the auditory signals emitted during a post- Cárdenas, P.D.A., Imba, H., Guayasamín, J.M. (2013): The amplexus vocal display in the glassfrog Centrolene savagei. territoriality, vocalizations, and aggressive interactions of the red-spotted glassfrog, Nymphargus grandisonae, Cochran & Goin 1970 (Anura: Centrolenidae). Journal of Natural History 47: 3011-3032. Jacobson, S.K. (1985): Reproductive behavior and male but this study is the first in which temporal and spectral mating success in two species of glass frogs (Centrolenidae). features were measured for this type of post-amplexus Herpetologica 41: 396-404. vocal display. Krohn, A.R., Voyles, J.A. (2014): A short note on the use of humeral spines in combat in Espadarana prosoblepon (Anura: Centrolenidae). Alytes 31: 83-85. Acknowledgements. We thank Sebastian Vera, Baladev Sánchez, Vargas-Salinas, F., Quintero-Ángel, A., Osorio-Domínguez, D., Carlos Gómez, Sebastian Duarte, Andres Grisales, Juliana Rojas-Morales, J.A., Escobar-Lasso, S., Gutiérrez-Cárdenas, González and Daniela Ospina for their support in fieldwork. We P.D.A., Amézquita, A. (2014): Breeding and parental behaviour also thank Carlos Londoño for his help in extracting sound from in the glass frog Centrolene savagei (Anura: Centrolenidae). video recordings. Valuable commentaries by Marco Rada and Journal of Natural History 48: 1-17. Iris Starnberger improved previous versions of this manuscript. Wells, K.D. (1977): The courtship of frogs. In: The Reproductive We acknowledge the foundation IdeaWild for the donation biology of , p. 233–262. Taylor, D., Guttman, S., of equipment for fieldwork. Finally, we thank the Centro de Eds., New York: Plenum. Estudios e Investigaciones en Biodiversidad y Biotecnología de la Wells, K.D. (2007): The ecology and behavior of amphibians. Universidad del Quindío (CIBUQ), Ricardo Ospina, and Adriana Chicago, University of Chicago Press. Vanegas for providing permits to access the study areas.

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