Abstract
Vocalization is a fundamental resource for anurans in processes such as territoriality and mating, with intra- and interspecific variation. These signals are modulated by the calls of other species and by the microclimate. In this study, we evaluated vocal activity patterns and their relationship with environmental variables in three artificial ponds in a fragment of tropical dry forest in northeastern Colombia. We propose that biotic and abiotic factors structure vocal activity; we predict that: 1) temporal overlap will tend to be lower between closely related species; 2) dominant frequency will act as a complementary axis of acoustic partitioning, modulating but not determining overlap patterns, and 3) vocal activity will depend on minimum thresholds of temperature and relative humidity, with variation in tolerance among species. We recorded activity during high- and low-precipitation seasons through continuous acoustic monitoring; we analyzed temporal overlap and applied multivariate clustering with temperature and humidity. We identified 13 species, ten of which showed predominantly nocturnal activity. In Dendropsophus and Leptodactylus, overlap was low, while among species with similar frequencies, it was variable. Vocal activity responded to temperature (>20 °C) and humidity (>75%) thresholds, with specific microclimatic ranges for each species. The results show temporal partitioning and a complementary role of dominant frequency, supporting our predictions and highlighting the value of acoustic monitoring for understanding coexistence and community structure in tropical dry forest artificial environments.
References
Agostinelli, C. & Lund, C. (2017). R package circular: Circular Statistics. Department of Environmental Sciences, Informatics and Statistics, Foscari University. https://cran.r-project.org/web/packages/circular/circular.pdf
Alonso, R., Rodríguez-Gómez, A., Estrada, A. R. (2001). Patrones de actividad acústica y trófica de machos cantores de Eleutherodactylus eileenae (Anura: Leptodactylidae). Revista española de herpetología, 15, 45-52. https://herpetologica.es/revista-espanola-de-herpetologia-15-2001/
Angulo, A., Rueda-Almonacid, J. V., Rodríguez-Mahecha, J. V., La Marca, E. (Eds.). (2006). Técnicas de inventario y monitoreo para los anfibios de la región tropical andina. Conservación Internacional.
Arrieta-García, D., Díaz, G., Ortiz, L. J., Acevedo, A. A. (2025). Acoustic ecology of anuran communities across Andean biomes: unveiling the soundscape of Northeastern Colombia. Bioacoustics, 34, 66-87. https://doi.org/10.1080/09524622.2025.2461527
Bioacoustic Research Program. (2025). Raven Pro: Interactive Sound Analysis Software (Version 1.6). Computer software, The Cornell Lab of Ornithology. http://www.birds.cornell.edu/raven
Boquimpani-Freitas, L., Marra, R. V., Van Sluys, M., Rocha, C. F. D. (2007). Temporal niche of acoustic activity in anurans: interspecific and seasonal variation in a neotropical assemblage from south-eastern Brazil. Amphibia-Reptilia, 28(2), 269-276. https://doi.org/10.1163/156853807780202422
Bovolon, J. P. & Toledo, L. F. (2024). Dendropsophus minutus repertoire complexity and its relationship with environmental traits. Bioacoustics, 33(4), 295-310. https://doi.org/10.1080/09524622.2024.2350718
Braga, H. S., Vieira, M. V., Silva, T. A., Protázio, A. S., Protazio, A. S. (2023). Acoustic partitioning explains the coexistence between two Physalaemus species (Anura, Leptodactylidae) in the Atlantic Forest in Eastern Bahia State, Brazil. Anais da Academia Brasileira de Ciências, 95(1), e20211348. https://doi.org/10.1590/0001-3765202320211348
Cañas, J. S., Toro-Gómez, M. P., Sugai, L. S. M., Benítez-Restrepo, H. D., Rudas, J., Posso-Bautista, B., Toledo, L. F., Dena, S., Domingos, A. H. R., de Souza, F. L., Neckel-Oliveira, S., da Rosa, A., Carvalho-Rocha, V., Bernardy, J. V., Sugai, J. L. M. M., dos Santos, C. E., Bastos, R. P., Llusia, D., Ulloa, J. S. (2023). A dataset for benchmarking neotropical anuran calls identification in passive acoustic monitoring. Scientific Data, 10(1), 771. https://doi.org/10.1038/s41597-023-02666-2
Carrillo-Fajardo, M., Rivera-Díaz, O., Sánchez-Montaño, R. (2007). Caracterización florística y estructural del bosque seco tropical del Cerro Tasajero, San José de Cúcuta (Norte de Santander), Colombia. Actualidades biológicas, 29, 55-73. https://doi.org/10.17533/udea.acbi.329348
Carvajal-Castro, J. D. & Vargas-Salinas, F. (2016). Stream noise, habitat filtering, and the phenotypic and phylogenetic structure of Neotropical anuran assemblages. Evolutionary Ecology, 30(3), 451-469. https://doi.org/10.1007/s10682-016-9817-8
Charif, R. A., Waack, A. M., Strickman, L. M. (2010). Raven Pro 1.4 User’s Manual. Cornell Lab of Ornithology. http://www.birds.cornell.edu/raven
Chhaya, V., Lahiri, S., Jagan, M. A., Mohan, R., Pathaw, N. A., Krishnan, A. (2021). Community bioacoustics: Studying acoustic community structure for ecological and conservation insights. Frontiers in Ecology and Evolution, 9, 706445. https://doi.org/10.3389/fevo.2021.706445
de Lira, A. B., Alquezar, R. D., Giozza, A. P., dos Santos Campos, E. R., Cardoso, A. G. T., Brandão, R. A. (2020). Acoustic space partition by four Hylidae in an open habitat in Central Brazil. Heringeriana, 14(2), 65-80. https://doi.org/10.17648/heringeriana.v14i2.917916
Duarte, M. H., Caliari, E. P., Viana, Y. P., Nascimento, L. B. (2019). A natural orchestra: How are anuran choruses formed in artificial ponds in southeast Brazil? Amphibia-Reptilia, 40(3), 373-382. https://doi.org/10.1163/15685381-20191146
Gerhardt, H. C. & Huber, F. (2002). Acoustic communication in insects and anurans: Common problems and diverse solutions. University of Chicago Press. https://doi.org/10.1046/j.1365-3032.2002.00308.x
Gingras, B., Böckle, M., Herbst, C. T., Fitch, W. T. (2013). Call acoustics reflect body size across four clades of anurans. Journal of Zoology, 289(2), 143-150.
Goutte, S., Dubois, A., Howard, S. D., Márquez R., Rowley, J. J. L., Dehling, J. M., Grandcolas, P., Xiong, R. C., Legendre, F. (2018). How the environment shapes animal signals: A test of the acoustic adaptation hypothesis in frogs. Journal of Evolutionary Biology, 31, 148-158. https://doi.org/10.1111/jeb.13210
Hernández-Hernández, J. C., Chávez, C., List, R. (2018). Diversidad y patrones de actividad de mamíferos medianos y grandes en la Reserva de la Biosfera La Encrucijada, Chiapas, México. Revista de Biología Tropical, 66(2), 634-646. https://doi.org/10.15517/rbt.v66i2.33395
Hoffmann, E. P., Cavanough, K. L., Mitchell, N. J. (2021). Low desiccation and thermal tolerance constrains a terrestrial amphibian to a rare and disappearing microclimate niche. Conservation Physiology, 9(1), coab027. https://doi.org/10.1093/conphys/coab027
Köhler, J., Jansen, M., Rodríguez, A., Kok, P. J. R., Toledo, L. F., Emmrich, M., Glaw, F., Haddad, C. F. B, Rödel, M. O., Vences, M. (2017). The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa, 4251(1), 1-124. https://doi.org/10.11646/zootaxa.4251.1.1
Krause, B. L. (1993). The niche hypothesis: A virtual symphony of animal sounds, the origins of musical expression and the health of habitats. Soundscape Newsl, 6, 6-10.
Márquez, R., Llusia, D., Beltrán, J. F. (2014). Aplicación de la bioacústica al seguimiento de anfibios. Boletín de la Asociación Herpetológica Española, 25(4), 52-58. http://hdl.handle.net/10261/132973
Martínez-Medina, D., Acevedo-Charry, O., Medellín-Becerra, S., Rodríguez-Fuentes, J., López-Casas, S., Muñoz-Duque, S., Rivera-Correa, M., López-Aguirre, Y., Vargas-Salinas, F., Laverde-R., O., Rodríguez-Posada, M. E. (2021). Estado, desarrollo y tendencias de los estudios en acústica de la fauna en Colombia. Biota colombiana, 22(1), 7-25. https://doi.org/10.21068/c2021.v22n01a01
McGill, R., Tukey, J. W., Larsen, W. A. (1978). Variations of box plots. The American statistician, 32, 12–16. https://doi.org/10.2307/2683468
Mejía-Cepeda, N., Murillo-García, Ó., Bolívar-García, W. (2024). Acústica de un ensamblaje de anuros del valle geográfico del río Cauca, Colombia. Revista de Biología Tropical, 72(1). https://doi.org/10.15517/rev.biol.trop..v72i1.55782
Narins, P. M., Feng, A. S., Fay, R. R., Popper, A. N. (Eds.). (2006). Hearing and sound communication in amphibians. Springer. https://doi.org/10.1007/978-0-387-47796-1
Navas, C. A. (1996). Implications of microhabitat selection and patterns of activity on the thermal ecology of high elevation neotropical anurans. Oecologia, 108, 617-626. https://doi.org/10.1007/BF00329034
OcenAudio Team. (2025). Ocenaudio – easy, fast and powerful audio editor. Ocen Framework. https://www.ocenaudio.com/whatis
Oseen, K. L. & Wassersug, R. J. (2002). Environmental factors influencing calling in sympatric anurans. Oecologia, 133, 616-625. https://doi.org/10.1007/s00442-002-1067-5
Oyamaguchi, H. M., Vo, P., Grewal, K., Do, R., Erwin, E., Jeong, N., Tse, K., Chen, C., Miyake, C., Lin, A., Gridi‐Papp, M. (2018). Thermal sensitivity of a Neotropical amphibian (Engystomops pustulosus) and its vulnerability to climate change. Biotropica, 50(2), 326-337. https://doi.org/10.1111/btp.12519
Revell, L. J., Harmon, L. J., Collar, D. C. (2008). Phylogenetic signal, evolutionary process, and rate. Systematic biology, 57(4), 591-601. https://doi.org/10.1080/10635150802302427
Ridout, M. S. & Linkie, M. (2009). Estimating overlap of daily activity patterns from camera trap data. Journal of Agricultural, Biological, and Environmental Statistics, 14, 322-337. https://doi.org/10.1198/jabes.2009.08038
Rivera-Correa, M., Ospina-L, A. M., Rojas-Montoya, M., Venegas-Valencia, K., Rueda-Solano, L. A., Gutiérrez-Cárdenas, P. D. A., Vargas-Salinas, F. (2021). Cantos de las ranas y los sapos de Colombia: estado actual del conocimiento y perspectivas de investigación en ecoacústica. Neotropical biodiversity, 7(1), 350-363. https://doi.org/10.1080/23766808.2021.1957651
Rojas-Morales, J. A., La Marca, E., Ramírez-Chaves, H. E. (2021). Advertisement call of a population of the nurse frog Leucostethus fraterdanieli (Anura: Dendrobatidae), with notes on its natural history. Biota colombiana, 22(1), 122-132. http://doi.org/10.21068/c2021.v22n01a08
RStudio Team. (2024). RStudio: Integrated Development Environment for R (Versión 2024.09.0). Posit PBC. https://posit.co/download/rstudio-desktop/
Ryan, M. J. (1983). Sexual selection and communication in a Neotropical frog, Physalaemus pustulosus. Evolution, 37(2), 261-272. https://doi.org/10.2307/2408335
Ryan, M. J. & Rand, A. S. (2003). Sexual selection in female perceptual space: How female túngara frogs perceive and respond to complex mating calls. Evolution, 57(11), 2608–2618. https://doi.org/10.1111/j.0014-3820.2003.tb01504.x
Saldaña, I., Cadavid, A., Gómez, D. (2019). Abundancia relativa y patrones de actividad de Didelphis marsupialis en un área periurbana de Medellín, Colombia. Revista MVZ Córdoba, 24(3), 7366-7371. https://doi.org/10.21897/rmvz.1352
Sánchez-Porras, R., Brenes-Cambronero, L., Chavarría-Esquivel, K., Mejías-Vásquez, Y. (2021). Abundancia relativa, diversidad y patrones de actividad de mamíferos terrestres medianos y grandes, sendero Pájaro Sombrilla, Reserva Biológica Alberto Manuel Brenes, Alajuela, Costa Rica. Pensamiento Actual, 21(36). https://doi.org/10.15517/pa.v21i36.47014
Santana, O. F. (1991). El análisis de cluster: aplicación, interpretación y validación. Papers: revista de sociologia, 37, 65-76. https://doi.org/10.5565/rev/papers/v37n0.1596
Seefeld, K. & Linder, E. (2007). Statistics using R with biological examples. Durham: University of New Hampshire.
Sierra-Ramírez, N. & Péfaur, J. (2022). Uso del Hábitat y Estructura Estacional de una Comunidad de Anuros de los Andes Venezolanos. Acta Biologica Venezuelica, 42(2), 131-148.
Straughan, I. R. & Heyer, W. R. (1976). A functional analysis of the mating calls of the Neotropical frog genera of the Leptodactylus complex (Amphibia, Leptodactylidae). Papéis Avulsos de Zoologia, 29(23), 221–245. http://hdl.handle.net/10088/4580
Suárez, F., Bonilla, S., Martínez, E., Galindo-T, R., Sánchez, L. R. (2004). Aporte al manejo de los bosques secos del área metropolitana de Cúcuta. Corporación Autónoma Regional de la Frontera Nororiental (Corponor). Sistema de Parques Nacionales Naturales de Colombia, San José de Cúcuta, Colombia. https://corponor.gov.co/areasnaturalesestrategicas/descargas/bst_Aporte_al_Manejo_de_los_Bosques_Secos_del_AM_Cucuta_2004.pdf
Sugai, L. S., Silva, T. S., Llusia, D., Siqueira, T. (2021). Drivers of assemblage‐wide calling activity in tropical anurans and the role of temporal resolution. Journal of Animal Ecology, 90(3), 673-684. https://doi.org/10.1111/1365-2656.13399
Tapia, C. E. F. & Cevallos, K. L. F. (2021). Pruebas para comprobar la normalidad de datos en procesos productivos: Anderson-Darling, Ryan-Joiner, Shapiro-Wilk y Kolmogórov-Smirnov. Societas, 23(2), 83-106. https://www.revistas.up.ac.pa/index.php/societas/article/view/2302
Turriago, J. L., Tejedo, M., Hoyos, J. M., Camacho, A., Bernal, M. H. (2023). The time course of acclimation of critical thermal maxima is modulated by the magnitude of temperature change and thermal daily fluctuations. Journal of Thermal Biology, 114, 103545. https://doi.org/10.1016/j.jtherbio.2023.103545
Valetti, J. A., Salas, N. E., Martino, A. L. (2013). Bioacoustic of the advertisement call of Ceratophrys cranwelli (Anura: Ceratophryidae). Revista de Biología Tropical, 61(1), 273-280. https://www.scielo.sa.cr/scielo.php?pid=S0034-77442013000100022&script=sci_abstract
Vasconcelos, T. da S., Rossa-Feres, D. de C. (2008). Habitat heterogeneity and use of physical and acoustic space in anuran communities in Southeastern Brazil. Phyllomedusa: Journal of Herpetology, 7(2), 127-142. https://doi.org/10.11606/issn.2316-9079.v7i2p127-142
Villanueva-Rivera, L. J. (2014). Eleutherodactylus frogs show frequency but no temporal partitioning: implications for the acoustic niche hypothesis. PeerJ, 2, e496. https://doi.org/10.7717/peerj.496
Wells, K. (2007). The Ecology and Behavior of Amphibians. Chicago: University of Chicago Press. https://doi.org/10.7208/9780226893334
Wickham, H. (2011). ggplot2. Wiley interdisciplinary reviews: computational statistics, 3(2), 180-85.
Yasumiba, K., Alford, R. A., Schwarzkopf, L. (2015). Why do male and female cane toads, Rhinella marina, respond differently to advertisement calls? Animal Behaviour, 109, 141-147. https://doi.org/10.1016/j.anbehav.2015.08.015
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Copyright (c) -1 Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales