COMPORTAMIENTO REPRODUCTIVO DE LA RANA DE CRISTAL Hyalinobatrachium tatayoi (ANURA: CENTROLENIDAE) EN UNA POBLACIÓN DE LOS ANDES COLOMBIANOS
DOI:
https://doi.org/10.22201/fc.25942158e.2024.3.945Palabras clave:
Anuros, Comportamiento animal, rana de cristal, selección sexual, Variación geografica intraespecíficaResumen
Monitoreamos el comportamiento reproductivo de la rana de cristal Hyalinobatrachium tatayoi en una población de la cordillera Central de Colombia. Describimos el sitio de canto de los machos, el comportamiento de cortejo, amplexo, oviposición y el patrón de apareo. Además, comparamos nuestros resultados con los obtenidos en un estudio similar realizado hace 30 años en una población de Panamá. Durante 21 salidas de campo realizadas entre julio y diciembre de 2022, registramos 85 machos y 89 hembras desde el suelo hasta alturas mayores a los 5 m. En H. tatayoi, los machos cantan desde el envés o el haz de hojas y el cortejo dura más de 30 min; cuando un macho atrae una hembra, empieza a emitir cantos de anuncio y cortejo mientras que ella se mueve a su alrededor o incluso lo toca en varias ocasiones con sus extremidades y cuerpo. Durante el cortejo, el macho no intenta forzar el amplexo. El amplexo es axilar y el macho cubre con su cuerpo los huevos pocos minutos después de la oviposición. El éxito de apareo de los machos se incrementó con el número de noches que ellos estuvieron activos en su territorio, pero no se relacionó con su tamaño corporal ni con la altura promedio del sustrato en el cual fue registrado. Este es un resultado recurrente en estudios de comportamiento reproductivo en Centrolenidae. Futuros estudios son necesarios para determinar si las hembras, o incluso los machos, discriminan entre potenciales parejas. Al comparar nuestros resultados con los obtenidos en la población panameña estudiada previamente, no detectamos variación geográfica intraespecífica en el comportamiento reproductivo de H. tatayoi.
Citas
Amézquita, A. & W. Hödl. 2004. How, when, and where to perform visual displays: the case of the Amazonian frog Hyla parviceps. Herpetologica 60:420-429.
Arak, A. 1983. Male-male competition and mate choice in anuran amphibians. Pp. 181-210. En P. Bateson (Ed.). Mate choice. Cambridge University Press, New York, New York, USA.
Arcila-Pérez, L.F., J.A. Rios-Soto, S.O. Montilla, C.A. Londoño-Guarnizo, C. Gómez & F. Vargas-Salinas. 2017. Vocalization and natural history in populations of a glassfrog assigned to Nymphargus griffithsi in the Central Andes of Colombia. Herpetological Review 48:275-280.
Baraquet, M., N.E. Salas & I.E. Di Tada. 2007. Variación geográfica en el canto de advertencia de Hypsiboas pulchellus (Anura, Hylidae) en Argentina. Revista Española de Herpetología 21:107-118.
Barnett, J.B., C. Michalis, H.M. Anderson, B.L. McEwen, J. Yeager, J.N. Pruitt, N.E. Scott-Samuel & I.C. Cuthill. 2020. Imperfect transparency and camouflage in glass frogs. Proceedings of the National Academy of Sciences 117:12885-12890.
Barona-Cortés, E. & A.M. Mendoza-Henao. 2022. Hyalinobatrachium tatayoi. Catálogo de anfibios y reptiles de Colombia 8:43-54.
Basto-Riascos, M.C., J. López-Caro & F. Vargas-Salinas. 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 51:2535-2550.
Bates, D., M. Martin, B. Ben & S. Walker. 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 [Consultado en febrero 2024]
Bateson, P. 1983. Mate choice. Cambridge University Press, New York, New York, USA.
Bernal, X.E., A.S. Rand & M.J. Ryan. 2006. Acoustic preferences and localization performance of blood-sucking flies (Corethrella coquillett) to tungara frog calls. Behavioral Ecology 17:709-715.
Bevier, C.R. 2016. Physiological and biochemical correlates of calling behavior in anurans with different calling strategies. Pp. 63-79. En D.V. de Andrade, C.R. Bevier & J.E. de Carvalho (Eds.), Amphibian and Reptile Adaptations to the Environment: Interplay Between Physiology and Behavior. CRC Press Taylor & Fracis Group, Florida, USA.
Bolívar-G, W., T. Grant & L.A. Osorio. 1999. Combat behavior in Centrolene buckleyi and other centrolenid frogs. Alytes 16:77-83.
Bravo-Valencia, L. & J. Delia. 2016. Maternal care in a glassfrog: care function and commitment to offspring in Ikakogi tayrona. Behavioral Ecology and Sociobiology 70:41-48.
Brunetti, A.E., C. Taboada & J. Faivovich. 2014. The reproductive biology of Hypsiboas punctatus (Anura: Hylidae) male territoriality and the possible role of different signals during female choice. Salamandra 50:215-224.
Byrne, P.G., J.D. Gaitan-Espitia & A.J. Silla. 2019. Genetic benefits of extreme sequential polyandry in a terrestrial-breeding frog. Evolution 73:1972-1985.
Byrne, P.G. & J.D. Roberts. 2012. Evolutionary causes and consequences of sequential polyandry in anuran amphibians. Biological Reviews 87:209-228.
Cardozo-Urdaneta, A.C. & C. Señaris. 2010. Vocalización y biología reproductiva de las ranas de cristal Hyalinobatrachium pallidum y Centrolene daidaleum (Anura; Centrolenidae) en la sierra de Perijá; Venezuela. Memoria de la Fundación La Salle de Ciencias Naturales 70:87-106.
Carvajal-Castro, J.D., Y. López-Aguirre, A.M. Ospina-L, J.C. Santos, B. Rojas & F. Vargas-Salinas. 2020. Much more than a clasp: evolutionary patterns of amplexus diversity in anurans. Biological Journal of the Linnean Society 129:652-663.
Castroviejo-Fisher, S., J. Ayarzagüena & C. Vila. 2007. A new species of Hyalinobatrachium (Centrolenidae: Anura) from Serranía de Perijá, Venezuela. Zootaxa 1441:51-62.
Castroviejo-Fisher, S., J.M. Guayasamin, A. Gonzalez-Voyer, C. Vilà & M. Ebach. 2014. Neotropical diversification seen through glassfrogs. Journal of Biogeography 41:66-80.
Castroviejo-Fisher, S., C. Vila, J. Ayarzagueena, M. Blanc & R. Ernst. 2011. Species diversity of Hyalinobatrachium glassfrogs (Amphibia: Centrolenidae) from the Guiana Shield, with the description of two new species. Zootaxa 3132:1-55.
Cisneros-Heredia, D.F. & R.W. McDiarmid. 2007. Revision of the characters of Centrolenidae (Amphibia: Anura: Athesphatanura), with comments on its taxonomy and the description of new taxa of glassfrogs. Zootaxa 1572:1-82.
Coyne, J.A. & H.A. Orr. 2004. Speciation: a catalogue and critique of species concepts. Pp. 272-292. En A. Rosenberg & R. Arp (Eds.). Philosophy of biology: an anthology. Wiley-Blackwell, West Sussex, UK.
Crawford, A.J. & A. Paz. 2017. Recolección de tejidos biológicos para análisis genéticos en anfibios. Pp. 1-33. En M.A. González & H. Arenas-Castro (Eds.). Recolección de tejidos biológicos para análisis genéticos. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt. Bogotá, Colombia.
Davies, N.B. & T.R. Halliday. 1977. Optimal mate selection in the toad Bufo bufo. Nature 269:56-58.
Delia, J., A. Ramirez-Bautista & K. Summers. 2013. Parents adjust care in response to weather conditions and egg dehydration in a Neotropic glass frog. Behavioral Ecology and Sociobiology 67:557-569.
Delia, J., A. Ramirez-Bautista & K. Summers. 2014. Glassfrog embryos hatch early after parental desertion. Proceedings of the Royal Society B: Biological Sciences 281:20133237.
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.
Delia, J., L. Bravo-Valencia & K.M. Warkentin. 2017. Patterns of parental care in Neotropical glassfrogs: fieldwork alters hypotheses of sex-role evolution. Journal of Evolutionary Biology 30:898-914.
Delia, J., L. Bravo-Valencia & K.M. Warkentin. 2020. The evolution of extended parental care in glassfrogs: Do egg clutch phenotypes mediate coevolution between the sexes? Ecological Monographs 90:3-e01411.
Donnelly, M.A., C. Guyer, E.J. Juterbock & R.A. Alford. 1994. Pp. 277–284. Techniques for marking amphibians. En W. R. Heyer, M. A. Donnelly, R. W. McDiarmid, L. C. Hayek, M. S. Foster (Eds.), Measuring and monitoring biological diversity: Standard methods for amphibians. Smithsonian Institution Press, Washington D.C., USA.
Duarte-Marín, S., M. Rada, M. Rivera-Correa, V. Caorsi, E. Barona, G. González-Durán & F. Vargas-Salinas. 2022. Tic, Tii and Trii calls: the advertisement call for eight glass frogs from Colombia and analysis of the structure of auditory signals in Centrolenidae. Bioacoustics 32:143-180.
Dyson, M.L., S. Peter Henzi, T.R. Halliday & L. Barrett. 1998. Success breeds success in mating male reed frogs (Hyperolius marmoratus). Proceedings of the Royal Society of London. Series B: Biological Sciences 265:1417-1421.
Escalona, S.M.D., P. Ivo Simões, A. Gonzalez‐Voyer & S. Castroviejo‐Fisher. 2019. Neotropical frogs and mating songs: the evolution of advertisement calls in glassfrogs. Journal of Evolutionary Biology 32:163-176.
Evans, J.P. & A.E. Magurran. 2000. Multiple benefits of multiple mating in guppies. Proceedings of the National Academy of Sciences 97:10074-10076.
Fan, X.L., Z.H. Lin & X. Ji. 2013. Male size does not correlate with fertilization success in two bufonid toads that show size-assortative mating. Current Zoology 59:740-746.
Ferner, J.W. 2010. Measuring and marking post-metamorphic amphibians. Pp. 123-141. En C.K. Dodd (Ed.). Amphibian ecology and conservation: A handbook of techniques, Oxford University Press, UK.
Forsman, A. & M. Hagman. 2006. Calling is a honest indicator of paternal genetic quality in poison frogs. Evolution 60:2148-2157.
Friedl, T.W. & G.M. Klump. 2005. Sexual selection in the lek-breeding European treefrog: body size, chorus attendance, random mating and good genes. Animal Behaviour 70:1141-1154.
Frost, D.R. 2024. Amphibian species of the world: an online reference. American Museum of Natural History, New York. Version 6.1. https://amphibiansoftheworld.amnh.org [Consultado en febrero 2024]
Gerhardt, H.C. & F. Huber. 2002. Acoustic communication in insects and anurans: common problems and diverse solutions. University of Chicago Press, Chicago, USA.
Gómez-Murcia, D.A., M.M. Bedoya-Ospina, L.F. Arcila-Pérez & F. Vargas-Salinas. 2023. Nothing like home: Most males of Espadarana prosoblepon (Anura: Centrolenidae) exhibit homing to calling sites despite the availability of alternative suitable sites for calling and mating. Ethology Ecology & Evolution 1-16.
González-Acosta, C., A. Amézquita & F. Vargas-Salinas. 2023 (in press). Variation in the advertisement call of the poison frog Andinobates bombetes relates with geographic distance between populations, but not with divergence in warning coloration. Studies on Neotropical Fauna and Environment.
Gosner, K.L. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183-190.
Goutte, S. 2023. Acoustic Communication in Anurans. Pp. 193-218. En G. Moreno-Rueda & M. Comas (Eds.). Evolutionary Ecology of Amphibians. CRC Press, Abingdon, UK.
Goyes Vallejos, J., J. Gómez, A.D. Hernández-Figueroa, R. Vera & D.M. Green. 2021. Fertilization success suggests random pairing in frogs with regard to body size. Behavioral Ecology and Sociobiology 75:1-8.
Goyes Vallejos, J., K. Ramirez-Soto. 2020. Causes of embryonic mortality in Espadarana prosoblepon (Anura: Centrolenidae) from Costa Rica. Phyllomedusa 19:83-92.
Grafe, U.T. 1997. Costs and benefits of mate choice in the lek-breeding reed frog, Hyperolius marmoratus. Animal Behaviour 53:1103-1117.
Greer, B.J. & K.D. Wells. 1980. Territorial and reproductive behavior of the tropical American frog Centrolenella fleischmanni. Herpetologica 36:318-326.
Guevara-Molina, S.C. & F. Vargas-Salinas 2014. Nymphargus grandisonae (Anura: Centrolenidae). Reproductive behaviour. Herpetological Bulletin 128:29-30.
Halliday, T. & M. Tejedo. 1995. Intrasexual selection and alternative mating behavior. Pp. 419-468. En H. Heatwole (Ed.). Amphibian biology: Social behaviour, Surrey Beatty, Chipping Norton, Australia.
Howard, D.H. 1978. The influence of male-defended oviposition sites on early embryo mortality in bullfrogs. Ecology 59:789-798.
Hütter, C.R., S. Escobar-Lasso, J.A. Rojas-Morales, P.D.A. Gutiérrez-Cárdenas, H. Imba & J.M. Guayasamin. 2013a. 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.
Hütter, C.R., J.M. Guayasamin, J.J. Wiens & A. Mooers. 2013b. Explaining Andean megadiversity: the evolutionary and ecological causes of glassfrog elevational richness patterns. Ecology Letters 16:1135-1144.
IBM Corp. Released. 2019. IBM SPSS Statistics for Windows.Version 26.0. https://www.ibm.com/es-es/products/spss-statistics [Consultado en enero 2024]
Jacobson, S.K. 1985. Reproductive behavior and male mating success in two species of glass frogs (Centrolenidae). Herpetologica 41:396-404.
Krohn, A.R. & J. Voyles. 2014. A short note on the use of humeral spines in combat in Espadarana prosoblepon (Anura: Centrolenidae). Alytes 31:83-85.
Kubicki, B. 2007. Ranas de vidrio de Costa Rica. Glass frogs of Costa Rica. Santo Domingo de Heredia: Editorial INBio. Santo Domingo, Heredia, Costa Rica.
Llusia, D., R. Márquez, J.F. Beltrán, C. Moreira & J.P. Do Amaral. 2013. Environmental and social determinants of anuran lekking behavior: intraspecific variation in populations at thermal extremes. Behavioral Ecology and Sociobiology 67:493-511.
Luyten, P.H. & N.R. Liley. 1985. Geographic variation in the sexual behaviour of the guppy, Poecilia reticulata (Peters). Behaviour 95:164-179.
Mangold, A., K.Trenkwalder, M. Ringler, W. Höld & E. Ringler. 2015. Low reproductive skew despite high male-biased operational sex ratio in a glass frog with paternal care. BMC Evolutionary Biology 15:1-13.
McCaffery, R. & K. Lips. 2013. Survival and abundance in males of the glass frog Espadarana (Centrolene) prosoblepon in central Panama. Journal of Herpetology 47:162-168.
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. Environment rather than character displacement explains call evolution in glassfrogs. Evolution 7:355-369.
Meuche, I., O. Brusa, K.E. Linsenmair, A. Keller & H. Pröhl. 2013. Only distance matters–non-choosy females in a poison frog population. Frontiers in zoology 10:1-16.
Montilla, S.O., L.F. Arcila-Pérez, M.P. Toro-Gómez, F. Vargas-Salinas & M. Rada. 2023. 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.
Navarro-Salcedo, P., L.F. Arcila-Pérez, J.L. González-Pérez, L.A. Rueda-Solano, M. Rada & F. Vargas-Salinas. 2022. Sex difference in homing: males but not females return home despite offspring mortality in Ikakogi tayrona, a glassfrog with prolonged maternal care. Behavioral Ecology and Sociobiology 76:1-13.
Navarro-Salcedo, P., S. Duarte-Marín, M. Rada & F. Vargas-Salinas 2021. Parental status is related to homing motivation in males of the glassfrog Centrolene savagei. Ethology Ecology and Evolution 33:528-542.
Noronha, J.D.C.D. & D.D.J. Rodrigues. 2018. Reproductive behaviour of the glass frog Hyalinobatrachium cappellei (Anura: Centrolenidae) in the Southern Amazon. Journal of Natural History 52:207-224.
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 108:333 -340.
Ospina-L, A.M., J.A. Rios-Soto & F. Vargas-Salinas. 2017. Size, endurance or parental care performance? Male-male competition, female choice, and non-random mating pattern in the glassfrog Centrolene savagei. Copeia 105:575-583.
Ospina-L, A.M., P.A. Navarro-Salcedo, J.A. Rios-Soto, S. Duarte-Marín & F. Vargas-Salinas. 2020. Temporal patterns, benefits, and defensive behaviours associated with male parental care in the glassfrog Centrolene savagei. Ethology Ecology and Evolution 32:162-174.
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.
Parker, G.A. 1982. Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. Journal of theoretical biology 96:281-294.
Pettitt, B.A., G.R. Bourne & M.A. Bee. 2020. Females prefer the calls of better fathers in a Neotropical frog with biparental care. Behavioral Ecology 31:152-163.
Pough, F.H., W.E. Magnusson, M.J. Ryan, K.D. Wells & T.L. Taigen. 1992. Behavioral energetics. Pp. 395-436. En E. Feder, W. W. Burggren (Eds.). Environmental Physiology of the Amphibians. University of Chicago Press, Chicago, USA.
Prado-Sañudo, M.L., A. Giraldo & W. Bolivar-Garcia. 2018. Parental attendance and site selection of Centrolene savagei (Ruiz and Lynch 1991) in the western and central Andes of Colombia. Herpetology Notes 11:293-299.
Pröhl, H. 2003. Variation in male calling behaviour and relation to male mating success in the strawberry poison frog (Dendrobates pumilio). Ethology 109:273-290.
Pröhl, H., S. Hagemann, J. Karsch & G. Hobel. 2007. Geographic variation in male sexual signals in strawberry poison frogs (Dendrobates pumilio). Ethology 113:825-837.
R Development Core Team. 2023. R: A Language and Environment for Statistical Computing. Versión 4.3.0. https://www.r-project.org/ [Consultado en febrero 2024].
Rada, M., P.H. Dos Santos-Dias, J.L. Pérez-González, L.A. Rueda-Solano, M. Anganoy-Criollo, M.A. Pinto, L.R. Mejía-Quintero, F. Vargas-Salinas & T. Grant 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:e0215349.
Rios-Soto, J., A.M. Ospina-L & F. Vargas-Salinas. 2017a. The advertisement call and notes of the reproductive ecology of the glassfrog “Centrolene” quindianum (Anura: Centrolenidae). South American Journal of Herpetology 12:117-127.
Rios-Soto, J., A.M. Ospina-L, M.C. Basto-Riascos, J. López-Caro & F. Vargas-Salinas. 2017b. Description of the distress call in Espadarana prosoblepon and the post-amplexus vocal display in Centrolene savagei (Anura: Centrolenidae). Herpetology Notes 10:27-29.
Robertson, J.G.M. 1990. Female choice increases fertilization success in the Australian frog, Uperoleia laevigata. Animal Behavior 39:639-645.
Rojas-Montoya, M., Y. López-Aguirre, C. González-Acosta & F. Vargas-Salinas. 2024. Repertorio de señales acústicas en la rana de cristal Hyalinobatrachium tatayoi (Anura: Centrolenidae). Revista Latinoamericana de Herpetología 7:747-60.
Rosenthal, G.G. 2017. Mate choice: the evolution of sexual decision making from microbes to humans. Princeton University Press, Princeton, New Jersey, USA.
Salazar-Nicholls, M.J. & E.M Del Pino. 2015. Early development of the glass frogs Hyalinobatrachium fleischmanni and Espadarana callistomma (Anura: Centrolenidae) from cleavage to tadpole hatching. Amphibian & Reptile Conservation 8:89-106.
Schlupp, I. 2021. Male choice, female competition, and female ornaments in sexual selection. Oxford University Press, Oxford, Oxfordshire, UK.
Schulte, L.M., A. Martel, R. Cruz-Elizalde, A. Ramírez-Bautista & F. Bossuyt. 2021. Love bites: male frogs (Plectrohyla, Hylidae) use teeth scratching to deliver sodefrin precursor-like factors to females during amplexus. Frontiers in Zoology 18:1-14.
Silverstone, P.A. 1973. Observations on the behavior and ecology of a colombian poison-arrow frog the kõkoé-Pá (Dendrobates histrionicus Berthold). Herpetologica 29:295-301.
Souza, J.R., I.L. Kaefer & A.P. Lima. 2021. Calling activity determines male mating success in a territorial frog with parental care. Ethology 127:359-365.
Sullivan, B.K., M.J. Ryan & P.A. Verrell. 1995. Female choice and mating system structure. Pp. 469-517. En H. Heatwole (Ed.), Amphibian Biology: Social behaviour, Surrey Beatty, Chipping Norton, Australia.
Taboada, C., J. Delia, M. Chen, C. Ma, X. Peng, X. Zhu, L. Jiang, T. Vu, Q. Zhou & J. Yao. 2022. Glassfrogs conceal blood in their liver to maintain transparency. Science 378:1315-1320.
Torres-Gastello, C.P., J. Suárez-Segovia & D.F. Cisneros-Heredia. 2007. Cochranella erminea, a new species of Centrolenidae (Amphibia: Anura: Athesphatanura) from Amazonian Peru. Journal of the National Museum (Prague), Natural History Series 176:1-12.
Townsend, D.S. & M.M. Stewart. 1986. Courtship and mating behavior of a Puerto Rican frog, Eleutherodactylus coqui. Herpetologica 42:165-170.
Valencia-Aguilar, A., E. Ringler, S. Lüpold, J.M. Guayasamin & C.P.A. Prado. 2024. Evolutionary trade-offs between testes size and parenting in Neotropical glassfrogs. Proceedings of the Royal Society B 291:20240054.
Valencia-Aguilar, A., J.M. Guayasamin & C.P. Prado 2021. Alloparental care in glassfrogs: males care for unrelated clutches only when associated with their own. Scientific Reports 11:1386.
Valencia-Aguilar, A., K.R. Zamudio, C.F. Haddad, S.M. Bogdanowicz & C.P. Prado. 2020. Show me you care: female mate choice based on egg attendance rather than male or territorial traits. Behavioral Ecology 31:1054-1064.
Vargas-Salinas, F., A. Quintero-Ángel, D. Osorio-Domínguez, J.A. Rojas-Morales, S. Escobar-Lasso, P.D.A. Gutiérrez-Cárdenas, M. Rivera-Correa & A. Amézquita. 2014. Breeding and parental behavior in the glassfrog Centrolene savagei. Journal of Natural History 48:1689-1705.
Velásquez, N.A. 2014. Geographic variation in acoustic communication in anurans and its neuroethological implications. Journal of Physiology-Paris 108:167-173.
Villegas-Mora, D., S. Muñoz-Acevedo, E.C. Guevara-Molina & F. Vargas-Salinas. 2020. Phenology and mortality of embryos in a Colombian population of Nymphargus grandisonae (Centrolenidae). Phyllomedusa 19:225-241.
Vockenhuber, E.A, W. Hödl & A. Amézquita. 2009. Glassy Fathers Do Matter: Egg Attendance Enhances Embryonic Survivorship in the Glass Frog Hyalinobatrachium valerioi. Journal of Herpetology 43:340-344.
Vockenhuber, E.A., W. Hödl & U. Karpfen. 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.
Wells, K.D. 2007. The Ecology and Behavior of Amphibians, University of Chicago Press, Chicago, USA.
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. 2001. The energetics of calling frogs. Pp. 45-60. En M.J. Ryan (Ed.). Anuran communication. Smithsonian Institution Press, Washington D.C, USA.
Whitlock, M.C. & D. Schulter 2014. The analysis of biological data. Second edition. Roberts and Company Publisher, Greenwood Village, Colorado, USA.
Wilczynski, W. & M.J. Ryan. 1999. Geographic variation in animal communication systems. Pp. 234-261. En S.A. Foster & J.A. Endler (Eds.). Geographic variation in behavior. Oxford University Press, New York, New York, USA.
Zamudio, R.K., R.C. Bell, R.C. Nali. C.F.B. Haddad & C.P.A. Prado. 2016. Polyandry, Predation, and the Evolution of Frog Reproductive Modes. The American Naturalist 188:S41-S61.
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 [Consultado diciembre 2023]
Worldclim. 2023. Global climate and weather. Versión 2.1. https://www.worldclim.org/ [Consultado en diciembre 2023]
Zina, J. & C.F. Haddad. 2005. Reproductive activity and vocalizations of Leptodactylus labyrinthicus (Anura: Leptodactylidae) in southeastern Brazil. Biota Neotropica 5:119-129.
Descargas
Publicado
Cómo citar
Número
Sección
Licencia
Derechos de autor 2024 Revista Latinoamericana de Herpetología
Esta obra está bajo una licencia internacional Creative Commons Atribución-NoComercial-CompartirIgual 4.0.
