REPERTORIO DE SEÑALES ACÚSTICAS EN LA RANA DE CRISTAL Hyalinobatrachium tatayoi (ANURA: CENTROLENIDAE)

Maribel Rojas Montoya; Yelenny  López-Aguirre; Cristian  González-Acosta; Fernando Vargas-Salinas

doi:10.22201/fc.25942158e.2024.1.747

Autores/as

Maribel Rojas Montoya Grupo de Investigación en Evolución, Ecología y Conservación (EECO), Programa de Biología, Universidad del Quindío
Yelenny López-Aguirre
Cristian González-Acosta
Fernando Vargas-Salinas

DOI:

https://doi.org/10.22201/fc.25942158e.2024.1.747

Palabras clave:

Bioacústica, Comunicación acústica, Rana de cristal, Variación geográfica intraespecífica

Resumen

La comunicación acústica es la modalidad de comunicación más estudiada en anuros. No obstante, del repertorio de señales acústicas que se conoce para anuros, tradicionalmente se ha descrito el canto de anuncio, mientras que cantos de cortejo y de auxilio son menos conocidos. Dado que caracterizar las señales acústicas en anuros es útil para estudios de ecología, sistemática y evolución, y en la implementación de estrategias de manejo y conservación, en este estudio describimos tres tipos de canto en la rana de cristal Hyalinobatrachium tatayoi (Centrolenidae). Entre julio y diciembre de 2022 realizamos 21 salidas de campo nocturnas a una localidad en la vertiente occidental de la cordillera Central, en el departamento del Quindío, Colombia. Obtuvimos grabaciones de 407 cantos de anuncio emitidos por 21 machos, 230 cantos de cortejo emitidos por nueve machos, y ocho cantos de auxilio, dos emitidos por un macho y seis por una hembra. Nuestra descripción del canto de anuncio y cortejo, basada en 13 parámetros (siete espectrales, seis temporales), es la más detallada de las publicadas hasta la fecha para H. tatayoi. Además, proviene de una población que se encuentra separada de otras poblaciones para las cuales se han descrito estos cantos, por la presencia de dos cordilleras. Una comparación preliminar del canto de anuncio y de cortejo entre poblaciones de H. tatayoi permite visualizar poca variación geográfica intraespecífica en la frecuencia dominante y la duración del canto. Hasta la fecha, se conocen cuatro tipos de canto del repertorio de señales acústicas en H. tatayoi: canto de anuncio, canto de cortejo, canto de auxilio, y canto agonístico. Aunque no todos los parámetros de estos tipos de canto han sido cuantificados con el mismo nivel de detalle, H. tatayoi se convierte en una de las especies de Centrolenidae en que mejor se conoce su repertorio de señales acústicas.

Citas

Angulo, A., J.V. Rueda-Almonacid, J.V Rodríguez-Mahecha & E. La Marca. (Eds.). 2006. Técnicas de inventario y monitoreo para los anfibios de la región tropical andina. Conservación Internacional. Serie Manuales de Campo N2. Panamericana Formas e Impresos SA, Bogotá, Colombia.

Annibale, F.S., V.T. De Sousa, F.R. Da Silva & C.G. Murphy. 2020. Geographic variation in the acoustic signals of Dendropsophus nanus (Boulenger 1889) (Anura: Hylidae). Herpetologica 76:267-277.

Arcila-Pérez, L.F., J.A. Rios-Soto, O.S. Montilla, C.A. Londoño-Guarnizo, C. Gómez & F. Vargas-Salinas. 2017. Vocalizations and natural history in populations of a glassfrog assigned to Nymphargus griffithsi in Central Andes of Colombia. Herpetological Review 48:275-280.

Ashton, K.G. & C.R. Feldman. 2003. Bergmann's rule in nonavian reptiles: turtles follow it, lizards and snakes reverse it. Evolution 57:1151-1163.

Barona-Cortés, E. & A.M. Mendoza-Henao. 2022. Hyalinobatrachium tatayoi. Catálogo de anfibios y reptiles de Colombia 8:43-54.

Barría, E.A., J. Ashcroft, A. De Gracia, A. Baules, M. Quiroz, M. Miranda, A. Batista & R.D. Fuentes. 2023. Agonistic behaviour in the White-spotted Glassfrog, Sachatamia albomaculata (Taylor, 1949), with a report of interspecific amplexus. Herpetology Notes 16:71-74.

Barros-Granados, A.A., J.L. Pérez-González, Guerra, R.O. & L.A. Rueda-Solano. 2023. New records of the lovely leaf frog Phyllomedusa venusta from Sierra Nevada de Santa Marta, Colombia with description of the female release call. The Herpetological Bulletin 166:14-17.

Baum, D.A. & D.S. Smith. 2012. Tree Thinking: an Introduction to Phylogenetic Biology. Greenwood Village, CO: Roberts. USA.

Berger-Tal, O. & D. Saltz. (Eds.). 2016. Conservation Behavior: Applying Behavioral Ecology to Wildlife Conservation and Management. Cambridge University Press, Cambridge, USA.

Bernal, X.E., C. Guarnizo & H. Lüddecke. 2005. Geographic variation in advertisement call and genetic structure of Colostethus palmatus (Anura, Dendrobatidae) from the Colombian Andes. Herpetologica 61:395-408.

The Cornell Lab of Ornithology. Research Program. 2011. Raven Pro: interactive sound analysis software (version 1.4). Ithaca (NY): The Cornell Lab of Ornithology. http://www.birds.cornell.edu/ raven.

Bolívar-G, W., T. Grant & L.A. Osorio. 1999. Combat behavior in Centrolene buckleyi and other centrolenid frogs. Alytes 16:77-83.

Boughman, J.W. 2002. How sensory drive can promote speciation. Trends in Ecology & Evolution 17:571-577.

Castroviejo-Fisher, S., José Ayarzagüena & C. Vila. 2007. A new species of Hyalinobatrachium (Centrolenidae: Anura) from Serrania de Perijá, Venezuela. Zootaxa 1441:51-62.

Chen, Z. & J.J. Wiens. 2020. The origins of acoustic communication in vertebrates. Nature Communication 11:369.

Clemmons, J.R. & R. Buchholz. 1997. Behavioral Approaches to Conservation in the Wild. Cambridge University Press, Cambridge, USA.

Cliff, N. 1988. The eigenvalues-greater-than-one rule and the reliability of components. Psychological Bulletin 103:276.

Delia, J., D.F. Cisneros-Heredia, J. Whitney & R. Murrieta-Galindo. 2010. Observations on the reproductive behavior of a Neotropical glassfrog, Hyalinobatrachium fleischmanni (Anura: Centrolenidae). South American Journal of Herpetology 5:1-12.

Duarte-Marín, S., K.J López-Molina & L.F. Arcila-Pérez. 2019. Defensive behavior in Hyloscirtus larinopygion Duellman, 1973 (Anura: Hylidae). Herpetology Notes 12:509-511.

Duarte-Marín, S., M. Rada, M. Rivera-Correa, V. Caorsi, E. Barona, G. González-Durán & F. Vargas-Salinas. 2022. Tic, Tii and Trii calls: advertisement call descriptions for eight glass frogs from Colombia and analysis of the structure of auditory signals in Centrolenidae. Bioacoustics 32:143-180.

Duellman, W.E. 2001. The Hylid frogs of Middle America. Natural History Museum of the University of Kansas, Ithaca, New York, USA.

Duellman, W.E. & L. Trueb. 1994. Biology of Amphibians. The Johns Hopkins University press, Baltimore, USA.

Escalona, M., P. Ivo Simões, A. Gonzalez-Voyer & S. Castroviejo-Fisher. 2019. Neotropical frogs and mating calls: The evolution of advertisement calls in glassfrogs. Journal of Evolutionary Biology 32:163-176.

Florez, G.A.P., A.F. Liévano-Bonilla, A.M. Mendoza-Henao & S. Duarte-Marín. 2023. The distress call and range extension of the Hermosas Robber frog, Pristimantis racemus (Anura: Strabomantidae). Revista Latinoamericana de Herpetología 6:23-31.

Foster, S. A. & J.A. Endler. (Eds.). 1999. Geographic Variation in Behavior: Perspectives on Evolutionary Mechanisms. Oxford University Press, England, U.K.

Frost, D.R. 2024. Amphibian species of the world: an online reference. Version 6.1 electronic database. American Museum of Natural History, New York. Available from https://amphibiansoftheworld.amnh.org.

Gerhardt, H.C. & F. Huber. 2002. Acoustic Communication in Insects and Anurans: Common Problems and Diverse Solutions. University of Chicago Press, Chicago, USA.

Gillooly, J.F. & A.G. Ophir. 2010. The energetic basis of acoustic communication. Proceedings of the Royal Society B: Biological Sciences 277:1325–1331.

Gingras, B., M. Boeckle, C.T. Herbst & W.T. Fitch. 2013. Call acoustics reflect body size across four clades of anurans. Journal of Zoology 289:143-150.

Gosling, L.M. & W.J. Sutherland (Eds.). 2000. Behavior and conservation. Cambridge University Press, Cambridge, USA.

Greer, B.J. & K.D. Wells. 1980. Territorial and reproductive behavior of the tropical American frog Centrolenella fleischmanni. Herpetologica 36:318-326.

Guayasamin, J.M., R.M. Brunner, A. Valencia-Aguilar, D. Franco-Mena, E. Ringler, A.M. Armijos, C. Morochz, L. Bustamante, R.J. Maynard & J. Culebras, J. 2022. Two new glassfrogs (Centrolenidae: Hyalinobatrachium) from Ecuador, with comments on the endangered biodiversity of the Andes. PeerJ 10:e13109.

Guerra, V., D. Llusia, P.G. Gambale, A.R. De Morais, R. Márquez & R.P. Bastos. 2018. The advertisement calls of Brazilian anurans: Historical review, current knowledge and future directions. PLoS ONE 13:e0191691.

Guerra, V., D. Llusia, P.G. Gambale, A.R.D. Morais, R. Márquez & R.P. Bastos. 2018. The advertisement calls of Brazilian anurans: Historical review, current knowledge and future directions. PLoS One, 13:e0191691.

Hedman, H.D. & M.C. Hughey. 2015. Body size, humeral spine size, and aggressive interactions in the emerald glass frog, Espadarana prosoblepon (Anura: Centrolenidae) in Costa Rica. Mesoamerican Herpetology 2:500-508.

Heyer, W.R., M.A. Donnell, R.W. McDiarmid, L.C. Hayek & M.S. Foster. 1994. Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians. Smithsonian Institution Press, Washington, D.C, USA.

Hödl, W. & G. Gollmann. 1986. Distress calls in Neotropical frogs. Amphibia-Reptilia 7:11-21.

Hütter, C.R., S. Esobar-Lasso., J.A. Rojas-Morales., P.D.A. Gutiérrez-Cárdena., H. Imb. & J.M. Guayasamin. 2013. The territoriality, vocalizations and aggressive interactions of the red-spotted glassfrog, Nymphargus grandisonae, Cochran and Goin, 1970 (Anura: Centrolenidae). Journal of Natural History 47:3011-3032.

Ibáñez, D.R., A.S. Rand & C.A Jaramillo. 1999. Los anfibios del Monumento Natural Barro Colorado, Parque Nacional Soberanía y áreas adyacentes. Editorial Mizrachi and Pujol, Panamá.

IBM Corp. Released. 2019. IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY: IBM Corp.

Irwin, D.E., S. Bensch & T.D Price. 2001. Speciation in a ring. Nature 409:333-337.

Jacobson, S.K. 1985. Reproductive behavior and male mating success in two species of glass frogs (Centrolenidae). Herpetologica 41:396-404.

Köhler, J., M. Jansen, A. Rodríguez, P.J. Kok, L.F. Toledo, M. Emmrich, F. Glaw, C.F.B. Haddad, M.O. Rödel & M. Vences. 2017. The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa 4251:1-124.

Lee, J.C. 1996. The Amphibians and Reptiles of the Yucatan Peninsula. Ithaca. Cornell University Press, New York, USA.

Lescure, J. & C. Marty. 2000. Atlas des Amphibiens de Guyane. Museum national d'histoire naturelle, Paris.

López, C., M. Quispe, A. Villalón, M.L. Concha, M. Penna & N.A. Velásquez. 2020. Geographic variation in the laryngeal morphology of aG widely distributed South-American anuran: behavioural and evolutionary implications. Zoological Journal of the Linnean Society 190:140-148.

Lott, D.F. 1984. Intraspecific variation in the social systems of wild vertebrates. Behavior 88:266-325.

Meiri, S. & T. Dayan. 2003. On the validity of Bergmann’s rule. Journal of Biogeography 30:331-351.

Mendoza-Henao, A.M., E. Arias, J.H. Townsend & G. Parra-Olea. 2020. Phylogeny-based species delimitation and integrative taxonomic revision of the Hyalinobatrachium fleischmanni species complex, with resurrection of H. viridissimum (Taylor, 1942). Systematics and Biodiversity 18:464-484.

Mendoza-Henao, A.M., K.R. Zamudio, J.M. Guayasamin, M. Escalona & G. Parra-Olea. 2022. Enviroment rather than character displacement explains call evolution in glassfrogs. Evolution 77:355-369

Mittelbach, G.G. & B.J. McGill. 2019. Community Ecology. Oxford University Press, England, U.K.

Montilla, S.O., L.F. Arcila-Pérez, M.P. Toro-Gómez, F. Vargas-Salinas & M. Rada. 2023. A multidisciplinary approach reveals a new species of glassfrog from Colombia (Anura: Centrolenidae: Nymphargus). Zootaxa 5271:1-48.

Morrison, C. & J.M. Hero. 2003. Geographic variation in life‐history characteristics of amphibians: a review. Journal of Animal Ecology 72:270-279.

Narins, P.M. & A.S. Feng. 2006. Hearing and Sound Communication in Amphibians: Prologue and Prognostication. Springer New York, USA.

Narins, P.M. & S.L. Smith. 1986. Clinal variation in anuran advertisement calls: basis for acoustic isolation?. Behavioral Ecology and Sociobiology 19:135-141.

Narins, P.M. & S.L. Smith. 1986. Clinal variation in anuran advertisement calls: basis for acoustic isolation? Behavioral Ecology and Sociobiology 19:135-141.

Owen, P.C. & J.K. Tucker. 2006. Courtship calls and behavior in two species of chorus frogs, genus Pseudacris (Anura: Hylidae). Copeia 2006:137-144.

Peres-Neto, P.R., D.A. Jackson & K.M. Somers. 2005. How many principal components? Stopping rules for determining the number of non-trivial axes revisited. Computational Statistics Data Analysis 49:974-997.

Pisso-Florez, G.A., A.F. Liévano-Bonilla, A.M. Mendoza-Henao & S. Duarte-Marín. 2023. The distress call and range extension of the Hermosas Robber frog, Pristimantis racemus (Anura: Strabomantidae). Revista Latinoamericana de Herpetología 6:23-31.

Pough, F.H., R.M. Andrews, M.L. Crump, A.H. Savitzky, K.D. Wells & M.C. Bradley. 2016. Herpetology, 4th Edition. Sinauer Associates is an imprint of Oxford University Press, USA.

R Development Core Team. 2023. R: A Language and Environment for Statistical Computing.

Rios-Soto, J., A.M. Ospina-L, M.C. Basto-Riascos, J. López-Caro & F. Vargas-Salinas. 2017. Description of the distress call in Espadarana prosoblepon and the post-amplexus vocal display in Centrolene savagei (Anura: Centrolenidae). Herpetology Notes 10:27-29.

Rivera-Correa, M., A.M. Ospina-L, M. Rojas-Montoya, K. Venegas-Valencia, L.A. Rueda-Solano, P.D.A. Gutiérrez-Cárdenas & F. Vargas-Salinas. 2021. Cantos de las ranas y los sapos de Colombia: estado actual del conocimiento y perspectivas de investigación en ecoacústica. Neotropical Biodiversity 7:350-363.

Rojas-Runjaic, F.J.M. & P. Cabello. 2011. Centrolene daidaleum (Ruiz-Carranza & Lynch, 1991) (Anura, Centrolenidae): a glassfrog with primitive and derived combat behavior. Zootaxa 2011:60-64

Rosen, M. & R.E. Lemon. 1974. The vocal behavior of spring peepers, Hyla crucifer. Copeia 940-950.

Rueda-Solano, L.A., J.L. Pérez-González, M. Rivera-Correa & F. Vargas-Salinas. 2020. Acoustic signal diversity in the harlequin toad Atelopus laetissimus (Anura: Bufonidae). Copeia 108:503-513.

Ryan, M.J. 1988. Constraints and patterns in the evolution of anuran acoustic communication. Pp. 637-677. En: B. Fritzsch (Ed.), The evolution of the amphibian auditory system. John Wiley & Sons, USA.

Ryan, M.J. & W. Wilczynski. 1991. Evolution of intraspecific variation in the advertisement call of a cricket frog (Acris crepitans Hylidae). Biological Journal of the Linnean Society 44:249-272.

Santana, D.J., V.G. Orrico, V.D.A. São-Pedro & R.N. Feio. 2013. Distress call of Hypsiboas leucocheilus (Caramaschi and Niemeyer, 2003) (Anura, Hylidae). Herpetology Notes 6:289-293.

Schneider, H. & U. Sinsch. 2007. Contributions of Bioacoustics to the taxonomy of the Anura. Pp 2893-2933. En: H. Heatwole & M. Tyler (Eds.), Amphibian Biology Volume 7. Surrey Beatty & Sons, Australia.

Seehausen, O., Y. Terai, I.S. Magalhaes, K.L. Carleton, H.D.J. Mrosso, R. Miyagi, I. van der Sluijs, M.V. Schneider, M.E. Maan, H. Tachida, H. Imai & N. Okada. 2008. Speciation through sensory drive in cichlid fish. Nature 455:620-626.

Sueur, J., T. Aubin & C. Simonis. 2008. Seewave, a free modular tool for sound analysis and synthesis. Bioacoustics 18:213-226.

Tessarolo, G., N.M. Maciel, A. Ribeiro Morais & R.P. Bastos. 2016. Geographic variation in advertisement calls among populations of Dendropsophus cruzi (Anura: Hylidae). The Herpetological Journal 26:219-227.

Toledo, L.F., C. Fernando & B. Haddad. 2009. Defensive vocalizations of Neotropical anurans. South American Journal of Herpetology 4:25-42.

Toledo, L.F., I.A. Martins, D.P. Bruschi, M.A. Passos, C. Alexandre & C.F. Haddad. 2014. The anuran calling repertoire in the light of social context. Acta Ethologica 18:87-99.

Tonini, J.F.R., D.B. Provete, N.M. Maciel, A.R. Morais, S. Goutte, L.F. Toledo & R.A. Pyron. 2020. Allometric escape from acoustic constraints is rare for frog calls. Ecology and Evolution 10:3686-3695.

Vargas-Salinas, F. & A. Amézquita. 2014. Abiotic noise, call frequency, and stream-breeding anuran assemblages. Evolutionary Ecology 28:341-359.

Vargas-Salinas, F., A. Dorado-Correa & A. Amézquita. 2014. Microclimate and stream noise predict geographic divergence in the auditory signal of a threatened poison frog. Biotropica 46:748-755.

Vargas‐Salinas, F., A. Dorado‐Correa & A. Amézquita. 2014. Microclimate and stream noise predict geographic divergence in the auditory signal of a threatened poison frog. Biotropica 46:748-755.

Vitt, L.J. & J.P Caldwell. 2014. Herpetology. An Introductory Biology of Amphibians and Reptiles, 4th Edition. Elsevier Inc.

Vitt, L.J. 2013. Walking the natural-history trail. Herpetologica 69:105-117.

Wells, K.D. & J.J. Schwartz. 1982. The effect of vegetation on the propagation of calls in the neotropical frog Centrolenella fleischmanni. Herpetologica 38:449-455.

Wells, K.D. 2007. The Ecology and Behavior of Amphibians, University of Chicago Press, Chicago, USA.

Wilczynski, W. & M.J. Ryan. 1999. Geographic variation in animal communication systems. Pp. 234-261. En S.A. Foster, S.A. & J.A. Endler (Eds.), Geographic Variation in Behavior. Oxford University Press, England, U.K.

Wilkins, M.R., N. Seddon & R.J. Safran. 2013. Evolutionary divergence in acoustic signals: causes and consequences. Trends in Ecology & Evolution 28:156-166.