SITIO DE OVIPOSICIÓN, MORTALIDAD EN PUESTAS Y CUIDADO PARENTAL EN UNA POBLACIÓN COLOMBIANA DE LA RANA DE CRISTAL Hyalinobatrachium tatayoi (ANURA: CENTROLENIDAE)
DOI:
https://doi.org/10.22201/fc.25942158e.2025.4.1185Palabras clave:
Anfibios, Rana de cristal, sobrevivencia, depredación, progenieResumen
El conocimiento de la historia natural de las puestas en anuros es fundamental para comprender la alta diversidad de modos reproductivos y la ecología de sus poblaciones. En este estudio se documentó el sitio de oviposición, tamaño de puesta, y porcentajes y causas de mortalidad en puestas en una población colombiana de la rana de cristal Hyalinobatrachium tatayoi. Además, mediante experimentos de perturbación, se evaluó el nivel de compromiso (latencia de escape) de los parentales ante potenciales amenazas de depredación. Entre julio y diciembre de 2022 se realizaron muestreos aleatorios un transecto de 105 m de quebrada en un fragmento de bosque premontano de la cordillera Central de Colombia. Se registraron 337 puestas de tamaño variable, depositadas mayoritariamente en el envés de las hojas y a una altura promedio de 1.88 m. El porcentaje promedio de mortalidad en 53 puestas fue de 52.81 %, siendo desecación la principal causa de mortalidad. Dieciocho machos sobre puestas exhibieron mayor latencia de escape que cinco machos adyacentes a puestas y diecinueve machos sin puestas. El tamaño y ubicación de puestas es similar a lo registrado en otras poblaciones de H. tatayoi. Sin embargo, en una población de Panamá no se reportó cuidado parental ni mortalidad por desecación. Esto podría deberse a diferencias ambientales entre localidades que afectarían riesgos de desecación en puestas y la toma de decisiones por parte de machos parentales. Resultados de los experimentos de perturbación sugieren que los parentales están más dispuestos a arriesgarse que individuos sin crías ante posibles depredadores. Sin embargo, explicaciones alternas (e.g., estado fisiológico de los machos) no pueden descartarse. Con este estudio se contribuye al conocimiento de la historia natural y ecología de puestas y cuidado parental de H. tatayoi en poblaciones de Colombia a la vez que se resalta la importancia de estudios etológicos en diferentes poblaciones de una misma especie.
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Abràmoff, M. D., Magalhães, P. J., & Ram, S. J. (2004). Image processing with ImageJ. Biophotonics International, 11, 36–42.
Alonso-Álvarez, C., & Velando, A. (2012). Benefits and costs of parental care. En D. M. Kölliker (Ed.), The evolution of parental care (pp. 40–61). Oxford University Press.
Altig, R., & McDiarmid, R. W. (2007). Morphological diversity and evolution of egg and clutch structure in amphibians. Herpetological Monographs, 21, 1–32.
AmphibiaWeb. (2025). Teratohyla spinosa: Spiny Cochran frog. University of California, Berkeley. https://amphibiaweb.org/species/1799
Angiolani-Larrea, F. N., Valencia-Aguilar, A., Garrido-Priego, M., Peignier, M., Culebras, J., Jindiachi, L., Tinajero-Romero, J. G., Guayasamin, J. M., & Ringler, E. (2024). Is there a right place? The effect of oviposition site selection on offspring survival in a glassfrog. bioRxiv. 2024-08.
Arela-Jaramillo, A., Frenkel, C., Pazmiño-Armijos, G., & Carrión, J. C. (2023). Hyalinobatrachium tatayoi. En S. R. Ron, A. Merino-Viteri, & D. A. Ortiz (Eds.), Anfibios del Ecuador (Versión 2024.0). Museo de Zoología, Pontificia Universidad Católica del Ecuador. https://bioweb.bio/faunaweb/amphibiaweb/FichaEspecie/Hyalinobatrachium%20tatayoi
Barona-Cortés, E., & Mendoza-Henao, A. M. (2022). Hyalinobatrachium tatayoi. Catálogo de Anfibios y Reptiles de Colombia, 8, 43–54.
Basto-Riascos, M. C., López-Caro, J., & Vargas-Salinas, F. (2017). Reproductive ecology of the glass frog Espadarana prosoblepon (Anura: Centrolenidae) in an urban forest of the Central Andes of Colombia. Journal of Natural History, 51(43-44), 2535–2550.
Bates, D., Martin, M., Ben, B., & Walker, S. (2023). Lme4: Linear Mixed-Effects Models Using Eigen and S4 (Versión 1.1-35.1). https://cran.r-project.org/web/packages/lme4/lme4.pdf
Bolívar-García, W., Gómez-Figueroa, A., & Blanco Torres, A. (2019). Ecología Trófica. En Ecología Trófica (pp. 209–248). Editorial UPTC.
Bravo-Valencia, L., & Delia, J. (2016). Maternal care in a glassfrog: care function and commitment to offspring in Ikakogi tayrona. Behavioral Ecology and Sociobiology, 70(1), 41–48.
Brooks, M. E., Kristensen, K., van Benthem, K. J., Magnusson, A., Berg, C. W., Nielsen, A., Skaug, H. J., Maechler, M., & Bolker, B. M. (2017). glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal, 9(2), 378–400. https://journal.r-project.org/archive/2017/RJ-2017-066/index.html
Burrowes, P. A. (2000). Parental care and sexual selection in the Puerto Rican cave-dwelling frog, Eleutherodactylus cooki. Herpetologica, 56(3), 375–386.
Cabanzo-Olarte, L. C., Ramírez-Pinilla, M. P., & Serrano-Cardozo, V. H. (2013). Oviposition, site preference, and evaluation of male clutch attendance in Espadarana andina (Anura: Centrolenidae). Journal of Herpetology, 47(2), 314–320.
Carvajal-Castro, J. D., López-Aguirre, Y., Ospina-L, A. M., Santos, J. C., Rojas, B., & Vargas-Salinas, F. (2020). Much more than a clasp: evolutionary patterns of amplexus diversity in anurans. Biological Journal of the Linnean Society, 129(3), 652–663.
Castroviejo-Fisher, S., Ayarzagüena, J., & Vilà, C. (2007). A new species of Hyalinobatrachium (Centrolenidae: Anura) from Serranía de Perijá Venezuela. Zootaxa, 1441(1), 51–62.
Chaves-Acuña, W., Salazar-Zúñiga, J. A., & Chaves, G. (2020). Egg clutch survival under prolonged paternal care in a glass frog, Hyalinobatrachium talamancae. Copeia, 108(3), 514–521.
Cisneros-Heredia, D. F., & McDiarmid, R. W. (2007). Revision of the characters of Centrolenidae (Amphibia: Anura: Athesphatanura), with comments on its taxonomy and the description of new taxa of glassfrogs. Zootaxa, 1572(1), 1–82.
Clutton-Brock, T. H. (1991). The evolution of parental care. Princeton University Press.
Consolmagno, R. C., Requena, G. S., Machado, G., & Brasileiro, C. A. (2016). Costs and benefits of temporary egg desertion in a rocky shore frog with male-only care. Behavioral Ecology and Sociobiology, 70(5), 785–795.
Crump, M. L. (1984). Ontogenetic changes in vulnerability of a tropical frog (Hyla plebeja) to predation. Copeia, 1984(3), 657–663.
Crump, M. L. (1995). Parental care. En H. Heatwole & B. K. Sullivan (Eds.), Amphibian Biology (pp. 518–56). Surrey Beatty & Sons Pty Ltd.
Crump, M. L. (1996). Parental care among the Amphibia. En J. S. Rosenblatt & C. T. Snowdon (Eds.), Parental Care: Evolution, Mechanisms, and Adaptive Significance (pp. 109–144). Elsevier.
Crump, M. L. (2015). Anuran reproductive modes: evolving perspectives. Journal of Herpetology, 49(1), 1–16.
Delia, J., Bravo-Valencia, L., & McDiarmid, R. W. (2017b). Notes on paternal behavior in Hyalinobatrachium glassfrogs (Anura: Centrolenidae). Phyllomedusa: Journal of Herpetology, 16(1), 101–107.
Delia, J., Bravo-Valencia, L., & Warkentin, K. M. (2017a). Patterns of parental care in Neotropical glassfrogs: fieldwork alters hypotheses of sex-role evolution. Journal of Evolutionary Biology, 30(5), 898–914.
Delia, J., Bravo-Valencia, L., & Warkentin, K. M. (2020). The evolution of extended parental care in glassfrogs: Do egg clutch phenotypes mediate coevolution between the sexes? Ecological Monographs, 90(4), e01411.
Delia, J., Cisneros-Heredia, D. F., Whitney, J., & Murrieta-Galindo, R. (2010). Observations on the reproductive behavior of a Neotropical glassfrog, Hyalinobatrachium fleischmanni (Anura: Centrolenidae). South American Journal of Herpetology, 5(1), 1–12.
Delia, J., Ramírez-Bautista, A., & Summers, K. (2013). Parents adjust care in response to weather conditions and egg dehydration in a Neotropic glass frog. Behavioral Ecology and Sociobiology, 67(4), 557–569.
Díaz-Ricaurte, J. C., Guevara-Molina, E. C., & Serrano, F. (2019). Oviposition site preference and reproductive ecology of Teratohyla midas (Anura: Centrolenidae) in the Colombian Amazon. Journal of Natural History, 53(31-32), 1811–1822.
Duellman, W. E., & True, L. (1986). Biology of Amphibians. McGraw Hill.
Endler, J. A. (2025). What should we be doing as Behavioural Ecologists? Behavioral Ecology, araf029.
Escalona, S. M. D., Simões, P. I., Gonzalez-Voyer, A., & Castroviejo-Fisher, S. (2019). Neotropical frogs and mating songs: The evolution of advertisement calls in glassfrogs. Journal of Evolutionary Biology, 32(2), 163–176.
Fischer, E. K., & O'Connell, L. A. (2020). Hormonal and neural correlates of care in active versus observing poison frog parents. Hormones and Behavior, 120, 104696.
Fischer, E. K., Roland, A. B., Moskowitz, N. A., Tapia, E. E., Summers, K., Coloma, L. A., & O'Connell, L. A. (2019). The neural basis of tadpole transport in poison frogs. Proceedings of the Royal Society B: Biological Sciences, 286(1907), 20191084.
Foster, S. A., & Endler, J. A. (1999). Geographic Variation in Behavior. Oxford University Press.
Fowler, M. A., & Williams, T. D. (2017). A physiological signature of the cost of reproduction associated with parental care. The American Naturalist, 190(6), 762–773.
Friard, O., & Gamba, M. (2024). BORIS: Behavioral Observation Research Interactive Software (Versión 9.2.1) [Software]. https://www.boris.unito.it/
Frid, A., & Dill, M. (2002). Human-caused disturbance stimuli as a form of predation risk. Conservation Ecology, 6(1), 11.
Garrido-Priego, M., Tószeghi, M., Angiolani-Larrea, F. N., Valencia-Aguilar, A., Bégué, L., Núñez, R., & Warkentin, K. M. (2024). Clutch attendance and call parameters are linked to mating success in a glassfrog with paternal care. Behavioral Ecology, 35(6), arae078.
Ghalambor, C. K., & Martin, T. E. (2001). Fecundity-survival trade-offs and parental risk-taking in birds. Science, 292(5516), 494–497.
Gilbert, J. D., & Manica, A. (2015). The evolution of parental care in insects: a test of current hypotheses. Evolution, 69(5), 1255–1270.
Gomez-Mestre, I., Pyron, R. A., & Wiens, J. J. (2012). Phylogenetic analyses reveal unexpected patterns in the evolution of reproductive modes in frogs. Evolution, 66(12), 3687–3700.
Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16(3), 183–190.
Greer, B. J., & Wells, K. D. (1980). Territorial and reproductive behavior of the tropical American frog Centrolenella fleischmanni. Herpetologica, 36(4), 318–326.
Gross, M. R. (2005). The evolution of parental care. The Quarterly Review of Biology, 80(1), 37–45.
Guayasamin, J. M., Castroviejo-Fisher, S., Ayarzagüena, J., Trueb, L., & Vilà, C. (2008). Phylogenetic relationships of glassfrogs (Centrolenidae) based on mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution, 48(2), 574–595.
Guayasamin, J. M., Castroviejo-Fisher, S., Trueb, L., Ayarzagüena, J., Rada, M., & Vilà, C. (2009). Phylogenetic systematics of Glassfrogs (Amphibia: Centrolenidae) and their sister taxon Allophryne ruthveni. Zootaxa, 2100(1), 1–97.
Guerra V, Llusia D, Gambale PG, et al. Abràmoff, M.D., P. J. Magalhães & S. J. Ram. 2004. Image processing with ImageJ. Biophotonics international 11:36-42.
Guerra, V., Llusia, D., Gambale, P. G., Vasconcelos, A., Gualda-Barros, J., & Campos, L. A. (2018). The advertisement calls of Brazilian anurans: historical review, current knowledge and future directions. PLoS ONE, 13(1), e0191691.
Guevara-Molina, E. C., Gomes, F. R., & Warkentin, K. M. (2022). Heat-induced hatching of red-eyed treefrog embryos: hydration and clutch structure increase behavioral thermal tolerance. Integrative Organismal Biology, 4(1), obac041.
Hartig, F. (2022). DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models (R package version 0.4.6). https://CRAN.R-project.org/package=DHARMa
Hawley, T. J. (2006). Embryonic development and mortality in Hyalinobatrachium pulveratum (Anura: Centrolenidae) of south-western Costa Rica. Journal of Tropical Ecology, 22(6), 731–734.
Hernández, J. C., Mejía, A. G., & Samper, D. (1996). Los Andes del Quindío: Introducción a la historia natural. Diego Samper Ediciones.
Jacobson, S. K. (1985). Reproductive behavior and male mating success in two species of glass frogs (Centrolenidae). Herpetologica, 41(4), 396–404.
Jones, J. C., & Reynolds, J. D. (1999). Costs of egg ventilation for male common gobies breeding in conditions of low dissolved oxygen. Animal Behaviour, 57(1), 181–188.
Kubicki, B. (2004). Rediscovery of Hyalinobatrachium chirripoi (Anura: Centrolenidae) in southeastern Costa Rica. Revista de Biología Tropical, 52(1), 277–280.
Kusrini, M. D., Rowley, J. J., Khairunnisa, L. R., Shea, G. M., & Altig, R. (2015). The reproductive biology and larvae of the first tadpole-bearing frog, Limnonectes larvaepartus. PLoS ONE, 10(1), e116154.
Kvarnemo, C. (2010). Parental care. En D. F. Westneat & C. W. Fox (Eds.), Evolutionary behavioural ecology (pp. 451–467). Oxford University Press.
Lehtinen, R. M., Green, S. E., & Pringle, J. L. (2014). Impacts of paternal care and seasonal change on offspring survival: A multiseason experimental study of a Caribbean Frog. Ethology, 120(4), 400–409.
Lenth, R. V. (2023). emmeans: Estimated marginal means, aka least-squares means (R package version 1.8.8). https://CRAN.R-project.org/package=emmeans
Li, Y., Cohen, J. M., & Rohr, J. R. (2013). Review and synthesis of the effects of climate change on amphibians. Integrative Zoology, 8(2), 145–161.
Licht, L. E., & Grant, K. P. (1997). The effects of ultraviolet radiation on the biology of amphibians. American Zoologist, 37(2), 137–145.
Lima, S. L. (2009). Predators and the breeding bird: behavioral and reproductive flexibility under the risk of predation. Biological Reviews, 84(4), 485–513.
López-Bedoya, P. A., Gutiérrez-Cárdenas, P. D. A., Cardona-Galvis, E. A., Edwards, F. A., Edwards, D. P., Blanco-Torres, A., & Urbina-Cardona, J. N. (2024). Knowledge shortfalls on amphibian diets in Colombia: Future trends and challenges. Austral Ecology, 49(10), e13600.
Marco, A., Lizana, M., Álvarez, A., & Blaustein, A. R. (2001). Egg-wrapping behaviour protects newt embryos from UV radiation. Animal Behaviour, 61(3), 639–644.
Márquez-García, M., Correa-Solis, M., Sallaberry, M., & Méndez, M. A. (2009). Effects of pond drying on morphological and life-history traits in the anuran Rhinella spinulosa (Anura: Bufonidae). Evolutionary Ecology Research, 11(5), 803–815.
McDiarmid, R. W. (1978). Evolution of parental care in frogs. En G. M. Burghard & M. Bekoff (Eds.), The development of behavior: Comparative and evolutionary aspects (pp. 127–147). NY Garland Press.
Mendoza, A. M., Bolívar-García, W., Vázquez-Domínguez, E., Ibáñez, R., & Olea, G. P. (2019). The role of Central American barriers in shaping the evolutionary history of the northernmost glassfrog, Hyalinobatrachium fleischmanni (Anura: Centrolenidae). PeerJ, 7, e6115.
Mendoza-Henao, A. M., Arias, E., Townsend, J. H., & Parra-Olea, G. (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(5), 464–484.
Montilla, S. O., Arcila-Pérez, L. F., Toro-Gómez, M. P., Vargas-Salinas, F., & Rada, M. (2023). A multidisciplinary approach reveals a new species of glassfrog from Colombia (Anura: Centrolenidae: Nymphargus). Zootaxa, 5271(1), 1–48.
Morrison, C., & Hero, J. M. (2003). Geographic variation in life-history characteristics of amphibians: a review. Journal of Animal Ecology, 72(2), 270–279.
Neckel-Oliveira, S. (2004). Effects of landscape change on clutches of Phyllomedusa tarsius, a neotropical treefrog. Biological Conservation, 118(1), 109–116.
Nokhbatolfoghahai, M., Pollock, C. J., & Downie, J. R. (2015). Oviposition and development in the glass frog Hyalinobatrachium orientale (Anura: Centrolenidae). Phyllomedusa: Journal of Herpetology, 14(1), 3–17.
Noronha, J. D. C. D., & Rodrigues, D. D. J. (2018). Reproductive behaviour of the glass frog Hyalinobatrachium cappellei (Anura: Centrolenidae) in the Southern Amazon. Journal of Natural History, 52(3-4), 207–224.
Nunes-de-Almeida, C. H. L., Haddad, C. F. B., & Toledo, L. F. (2021). A revised classification of the amphibian reproductive modes. Salamandra, 57(4), 413–427.
Ortiz-Ross, X., Thompson, M. E., Salicetti-Nelson, E., Vargas-Ramírez, O., & Donnelly, M. A. (2020). Oviposition site selection in three glass frog species. Copeia, 108(2), 333–340.
Ospina-L, A. M., Navarro-Salcedo, P., Rios-Soto, J. A., Duarte-Marín, S., & Vargas-Salinas, F. (2020). Temporal patterns, benefits, and defensive behaviors associated with male parental care in the glassfrog Centrolene savagei. Ethology Ecology & Evolution, 32(2), 162–174.
Ospina-L, A. M., Rios-Soto, J. A., & Vargas-Salinas, F. (2017). Size, endurance, or parental care performance? Male–male competition, female choice, and non-random mating pattern in the glassfrog Centrolene savagei. Copeia, 105(3), 575–583.
Poo, S., & Bickford, D. P. (2013). The adaptive significance of egg attendance in a south-east Asian tree frog. Ethology, 119(8), 671–679.
R Development Core Team. (2023). R: A Language and Environment for Statistical Computing (Versión 4.3.0). https://www.r-project.org/
Rada, M., Dos Santos Dias, P. H., Pérez-Gonzalez, J. L., Anganoy-Criollo, M., Rueda-Solano, L. A., Pinto-E, M. A., Mejía Quintero, L., Vargas-Salinas, F., & Grant, T. (2019). The poverty of adult morphology: Bioacoustics, genetics, and internal tadpole morphology reveal a new species of glassfrog (Anura: Centrolenidae: Ikakogi) from the Sierra Nevada de Santa Marta, Colombia. PLoS ONE, 14(4), e0215349.
Ringler, E., Rojas, B., Stynoski, J. L., & Schulte, L. M. (2023). What amphibians can teach us about the evolution of parental care. Annual Review of Ecology, Evolution, and Systematics, 54, 43–62.
Rios-Soto, J. A., Ospina-L, A. M., & Vargas-Salinas, F. (2017). The advertisement call and notes of the reproductive ecology of the glassfrog “Centrolene” quindianum (Anura: Centrolenidae). South American Journal of Herpetology, 12(2), 117–127.
Rojas-Montoya, M., López-Aguirre, Y., González-Acosta, C., & Vargas-Salinas, F. (2024a). Comportamiento reproductivo de la rana de cristal Hyalinobatrachium tatayoi (Anura: Centrolenidae) en una población de los Andes colombianos. Revista Latinoamericana de Herpetología, 7(1), e945–995.
Rojas-Montoya, M., López-Aguirre, Y., González-Acosta, C., & Vargas-Salinas, F. (2024b). Repertorio de señales acústicas en la rana de cristal Hyalinobatrachium tatayoi (Anura: Centrolenidae). Revista Latinoamericana de Herpetología, 7(1), e747–760.
Rojas-Morales, J. A., & Escobar-Lasso, S. (2013). Notes on the natural history of three glass frogs species (Anura: Centrolenidae) from the Andean Central Cordillera of Colombia. Boletín Científico. Centro de Museos. Museo de Historia Natural, 17(1), 127–140.
Rojas-Runjaic, F. J., Infante-Rivero, E. E., & Cabello, P. (2012). New records and distribution extensions of centrolenid frogs for Venezuela. Check List, 8(4), 819–825.
Royle, N. J., Smiseth, P. T., & Kölliker, M. (2012). The evolution of parental care. Oxford University Press.
Salazar-Nicholls, M. J., & Del Pino, E. M. (2015). Early development of the glass frogs Hyalinobatrachium fleischmanni and Espadarana callistomma (Anura: Centrolenidae) from cleavage to tadpole hatching. Amphibian & Reptile Conservation, 8(1), 89–106.
Salgado, A. L., & Guayasamin, J. M. (2018). Parental care and reproductive behavior of the minute dappled glassfrog (Centrolenidae: Centrolene peristictum). South American Journal of Herpetology, 13(3), 211–219.
Santana, E. M., Mendoza-Henao, A. M., & Goyes Vallejos, J. (2025). The ‘silent’ half: diversity, function and the critical knowledge gap on female frog vocalizations. Proceedings of the Royal Society B: Biological Sciences, 292(20250454).
Savage, J. M. (2002). The amphibians and reptiles of Costa Rica: A herpetofauna between two continents, between two seas. University of Chicago Press.
Schlippe Justicia, L., Fouilloux, C. A., & Rojas, B. (2023). Poison frog social behaviour under global change: Potential impacts and future challenges. Acta Ethologica, 26(3), 151–166.
Schulte, L. M., Ringler, E., Rojas, B., & Stynoski, J. L. (2020). Developments in Amphibian parental care research: history, present advances, and future perspectives. Herpetological Monographs, 34(1), 71–97.
Shidemantle, G., May, D., Melnick-Kelley, Q., Crane, K., & Hua, J. (2019). The effect of intensified illuminance and artificial light at night on fitness and susceptibility to abiotic and biotic stressors. Environmental Pollution, 251, 600–608.
Smithsonian Tropical Research Institute. (2024). Smithsonian Tropical Research Institute. https://biogeodb.stri.si.edu/physical_monitoring/research/barrocolorado
Toledo, L. F. (2005). Predation of juvenile and adult anurans by invertebrates: current knowledge and perspectives. Herpetological Review, 36(4), 395–399.
Touchon, J. C., & Warkentin, K. M. (2008). Reproductive mode plasticity: aquatic and terrestrial oviposition in a treefrog. Proceedings of the National Academy of Sciences of the United States of America, 105(19), 7495–7499.
Touchon, J. C., & Warkentin, K. M. (2010). Short- and long-term effects of the abiotic egg environment on viability, development and vulnerability to predators of a Neotropical anuran. Functional Ecology, 24(3), 566–575.
Townsend, D. S., Stewart, M. M., & Pough, F. H. (1984). Male parental care and its adaptive significance in a neotropical frog. Animal Behaviour, 32(2), 421–431.
Valencia-Aguilar, A., Castro-Herrera, F., & Ramírez-Pinilla, M. P. (2012). Microhabitats for oviposition and male clutch attendance in Hyalinobatrachium aureoguttatum (Anura: Centrolenidae). Copeia, 2012(4), 722–731.
Valencia-Aguilar, A., Guayasamin, J. M., & Prado, C. P. (2021). Alloparental care in glassfrogs: males care for unrelated clutches only when associated with their own. Scientific Reports, 11(1), 1386.
Valencia-Aguilar, A., Ringler, E., Lüpold, S., Guayasamin, J. M., & Prado, C. P. (2024). Evolutionary trade-offs between testes size and parenting in Neotropical glassfrogs. Proceedings of the Royal Society B: Biological Sciences, 291(20240054), 20240054.
Valencia-Aguilar, A., Rodrigues, D. D. J., & Prado, C. P. (2020). Male care status influences the risk-taking decisions in a glassfrog. Behavioral Ecology and Sociobiology, 74(7), 84.
Van Dijk, D. E. (1971). Anuran ecology in relation particularly to oviposition and development out of water. African Zoology, 6(1), 119–132.
Van Grunsven, R. H., Creemers, R., Joosten, K., Donners, M., & Veenendaal, E. M. (2017). Behaviour of migrating toads under artificial lights differs from other phases of their life cycle. Amphibia-Reptilia, 38(1), 49–55.
Vargas-Salinas, F., Londoño-Guarnizo, C. A., Duarte-Marín, S., Torres-Suárez, O. L., & Amézquita, A. (2024). Uncoupled evolutionary patterns in spectral and temporal components of acoustic signals in anurans associated with streams. Ethology, 130(6), e13510.
Vargas-Salinas, F., Muñoz-Ávila, J. A., & Morales-Puentes, M. E. (2019). Biología de los anfibios y reptiles en el bosque seco tropical del norte de Colombia. Editorial UPTC.
Vargas-Salinas, F., Quintero-Ángel, A., Osorio-Domínguez, D., Rojas-Morales, J. A., Escobar-Lasso, S., Gutiérrez-Cárdenas, P. D. A., Rivera-Correa, M., & Amézquita, A. (2014). Breeding and parental behavior in the glassfrog Centrolene savagei. Journal of Natural History, 48(27-28), 1689–1705.
Villa, J. (1977). A symbiotic relationship between frog (Amphibia, Anura, Centrolenidae) and fly larvae (Drosophilidae). Journal of Herpetology, 11(3), 317–322.
Villa, J. (1984). Biology of a neotropical glass frog, Centrolenella fleischmanni (Boettger), with special reference to its frogfly associates. Milwaukee Public Museum Contributions in Biology and Geology, 55.
Villegas-Mora, D., Muñoz-Acevedo, S., Guevara-Molina, E. C., & Vargas-Salinas, F. (2020). Phenology and mortality of embryos in a Colombian population of Nymphargus grandisonae (Centrolenidae). Phyllomedusa, 19(2), 225–241.
Vitt, L. J., & Caldwell, J. P. (2013). Herpetology: An introductory biology of amphibians and reptiles. Academic Press.
Vockenhuber, E. A., Hödl, W., & Amézquita, A. (2009). Glassy fathers do matter: Egg attendance enhances embryonic survivorship in the glass frog Hyalinobatrachium valerioi. Journal of Herpetology, 43(2), 340–344.
Vockenhuber, E. A., Hödl, W., & Karpfen, U. (2008). Reproductive behaviour of the glass frog Hyalinobatrachium valerioi (Anura: Centrolenidae) at the tropical stream Quebrada Negra (La Gamba, Costa Rica). Stapfia, 88, 335–348.
Ward, R. J. S., Cotter, S. C., & Kilner, R. M. (2009). Current brood size and residual reproductive value predict offspring desertion in the burying beetle Nicrophorus vespilloides. Behavioral Ecology, 20(6), 1274–1281.
Warkentin, K. M. (2011). Environmentally cued hatching across taxa: embryos respond to risk and opportunity. Integrative and Comparative Biology, 51(1), 14–25.
Warne, R. W., & Catenazzi, A. (2016). Pouch brooding marsupial frogs transfer nutrients to developing embryos. Biology Letters, 12(10), 20160673.
Weather Spark. (2023). Weather Spark: Climate and Average Weather Year Round in La Tebaida, Colombia (Data base). https://weatherspark.com/y/22438/Average-Weather-in-La-Tebaida-Colombia-Year-Round
Wells, K. D. (2007). The Ecology and Behavior of Amphibians. University of Chicago Press.
Weygoldt, P. (1987). Evolution of parental care in dart poison frogs (Amphibia: Anura: Dendrobatidae). Journal of Zoological Systematics and Evolutionary Research, 25(1), 51–67.
Wickramasinghe, D. D., Oseen, K. L., Kotagama, S. J., & Wassersug, R. J. (2004). The terrestrial breeding biology of the ranid rock frog Nannophrys ceylonensis. Behaviour, 141(7), 899–913.
Worldclim. (2023). Global climate and weather (Versión 2.1). https://www.worldclim.org/
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Derechos de autor 2025 Revista Latinoamericana de Herpetología
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