Articles
Published 2022-04-28
Keywords
- anuran larvae,
- Dendropsophus elegans,
- Atlantic rainforest,
- tail loss,
- development
- feeding ...More
How to Cite
da Silva Martins, A. G., Rebouças, R., Santos, I., Rosa Domingos, A. H., & Toledo, L. F. (2022). Influence of tail injury on the development of Neotropical elegant treefrog tadpoles. Acta Herpetologica, 17(1), 13–20. https://doi.org/10.36253/a_h-11453
Funding data
-
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Grant numbers 001 -
Fundação de Amparo à Pesquisa do Estado de São Paulo
Grant numbers 2016/25358-3;2019/18335-5 -
Conselho Nacional de Desenvolvimento Científico e Tecnológico
Grant numbers 300896/2016-6;302834/2020-6
Abstract
Anuran larvae in aquatic environments are important prey items for several vertebrate and invertebrate species. Besides avoiding predation, there are some strategies that may reduce the physical damage in those tadpoles that survive the predation attempt. For example, the injured tadpole tail can regrow after a predator bite, but few studies have examined the consequences of such injury. We examined the consequences of three levels of injury to the tail and how this influenced development and feeding behavior of tadpoles of the Neotropical elegant treefrog, Dendropsophus elegans. We collected spawns and kept them in the laboratory until tadpoles reached Gosner’s stages 28 to 35. Then, they were separated in four experimental groups: individuals with tail trimmed in 30, 50 or 70 % of its length, and a control group, with no tail removing. We counted the days until metamorphosis, calculated the Scaled Mass Index (SMI) through weight and length of newly-metamorphosed, and evaluated the feeding frequency to evaluate the influence of tail amputation on them. We found that the time until metamorphosis was positively related to the extent of the amputation, but SMI and feeding behavior were not influenced. As the time to metamorphose is related to the survivorship chances of individuals: i.e., if the aquatic environment is with high density of predators, it would be advantageous to rapidly metamorphose out of the water. However, tail injury delays the metamorphose process, which could influence the survival of the individual.
References
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Blanco-Torres, A., Bonilla, M.A., Cagnolo, L. (2020): Habitat modification effects on anuran food webs in the Colombian tropical dry forest. Food Webs. 22: e00133. https://doi.org/10.1016/j.fooweb.2019.e00133
Both, C., Grant, T. (2012): Biological invasions and the acoustic niche: the effect of bullfrog calls on the acoustic signals of white-banded tree frogs. Biol lett. 8: 714-716.
Cabrera-Guzmán, E., Crossland, M.R., Shine, R. (2012): Predation on the eggs and larvae of invasive cane toads (Rhinella marina) by native aquatic invertebrates in tropical Australia. Biol Conserv. 153: 1-9. doi: 10.1016/j.biocon.2012.04.012
Crane, A.L., Chivers, D.P., Ferrari, M.C.O. (2018): Embryonic background risk promotes the survival of tadpoles facing surface predators. PLOS ONE. 13: e0193939. https://doi.org/10.1371/journal.pone.0193939
Crossland, M.R., Alford, R.A. (1998): Evaluation of the toxicity of eggs, hatchlings and tadpoles of the introduced toad Bufo marinus (Anura: Bufonidae) to native Australian aquatic predators. Aust J Ecol. 23: 129-137.
Crump, M.L., Vaira, M. (1991): Vulnerability of Pleurodema borelli tadpoles to an avian predator: Effect of body size and density. Herpetologica. 47: 316-321.
D’Heursel, A., Haddad, C.F.B. (1999): Unpalatability of Hyla semilineata tadpoles (Anura) to captive and free-ranging vertebrate predators. Ethol Ecol Evol. 11: 339-348.
Ding, G.-H., Lin, Z.-H., Wei, L. (2014): The compensatory effect of tail regeneration on swimming speed in larval Hoplobatrachus chinensis Osbeck, 1765 (Anura: Ranidae) after tail removal. Acta Herpetol. 9: 219-225.
Eterovick, P.C., Mendes, I.S., Kloh, J.S., Pinheiro, L.T., Václav, A.B.H.P., Santos,T., Gontijo, A.S.B. (2018): Tadpoles respond to background colour under threat. Scientific Reports. 8: 4085. https://doi.org/10.1038/s41598-018-22315-8
Figiel Jr, C.R., Semlitsch, R.D. (2011): Effects of nonlethal injury and habitat complexity on predation in tadpole populations. Can J Zool. 69: 830-834.
Fox, J., Weisberg, S. (2019): An R Companion to Applied Regression (Third). Sage. https://socialsciences.mcmaster.ca/jfox/Books/Companion/
Gherardi, F., Renai, B., Corti, C. (2001): Crayfish predation on tadpoles: A comparison between a native (Austropotamobius pallipes) and an alien species (Procambarus clarkii). Bulletin Français de la Pêche et de la Pisciculture. 361: 659-668.
Gontijo, A.S.B., Espanha, J., Eterovick, P.C. (2018): Is tadpole coloration adaptive against bird predation? Acta Ethol. 21: 69-79.
Gosner, K.L. (1960): A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica. 16: 183-190.
Hair, J.F., Anderson, R.E., Babin, B.J., Black, W.C. (2010): Multivariate data analysis: A global perspective (Vol. 7). Pearson.
Heyer, W.R., McDiarmid, R.W., Weigmann, D.L. (1975): Tadpoles, predation and pond habitats in the tropics. Biotropica. 7: 100-111. https://doi.org/10.2307/2989753
Hoff, K.V.S., Wassersug, R.J. (2000): Tadpole locomotion: axial movement and tail functions in a largely vertebraeless vertebrate. Am Zool. 40: 62-076.
Koch, N.M., Wilcoxen, T.E. (2019): The effects of tail damage on tadpole development and leaping ability after metamorphosis in Cuban tree frogs (Osteopilus septentrionalis). Bios. 89: 165-173.
McCollum, S.A., Leimberger, J.D. (1997): Predator-induced morphological changes in an amphibian: Predation by dragonflies affects tadpole shape and color. Oecologia. 109: 615-621.
Morgan, L.A., Buttemer, W. (1996): Predation by the non-native fish Gambusia holbrooki on small Litoria aurea and L. dentata tadpoles. Aust Zool. 30: 143-149.
Morin, P.J. (1981): Predatory salamanders reverse the outcome of competition among three species of anuran tadpoles. Science. 212: 1284-1286. doi: 10.1126/science.212.4500.1284
Morin, P.J. (1985): Predation intensity, prey survival and injury frequency in an amphibian predator-prey interaction. Copeia. 1985: 638-644. doi: 10.2307/1444755
Nunes, A.L., Cruz, M.J., Tejedo, M., Laurila, A., Rebelo, R. (2010): Nonlethal injury caused by an invasive alien predator and its consequences for an anuran tadpole. Basic and Appl Ecol. 11: 645-654.
Parichy, D.M., Kaplan, R.H. (1992): Developmental consequences of tail injury on larvae of the oriental fire-bellied toad, Bombina orientalis. Copeia. 1992: 129-137. https://doi.org/10.2307/1446544
R Core Team. (2021): R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. https://www.R-project.org/
Rebouças R, Castro I.M., Solé M. (2013): Diet of Haddadus binotatus (Spix, 1824)(Anura: Craugastoridae) in Brazilian Atlantic Rainforest, Bahia state. North-West J Zool. 9: 159-165.
Rebouças R, Solé M. (2015): Diet of Adenomera thomei (Almeida and Angulo, 2006)(Anura: Leptodactylidae) from a rubber tree plantation in southern Bahia, Brazil. Stud Neotrop Fauna E. 50: 73-79.
Sales, L.P., Rebouças, R., Toledo, L.F. (2021): Native range climate is insufficient to predict anuran invasive potential. Biol Invasions. doi: 10.1007/s10530-021-02528-1.
Segalla, M.V., Berneck, B., Caramaschi, U., Cruz, C.A.G., Garcia, P.C.A., Grant, T., Haddad, C.F.B., Lourenço, A.C.C., Mangia, S., Mott, T., Nascimento, L., Toledo, L. F., Werneck, F., Langone, J.A. (2021): List of Brazilian Amphibians. Herpetologia Brasileira. 10: 121-216. https://doi.org/10.5281/zenodo.4716176
Semlitsch, R.D. (1990): Effects of body size, sibship, and tail injury on the susceptibility of tadpoles to dragonfly predation. Can J Zool. 68: 1027-1030.
Semlitsch, R.D., Gibbons, J.W. (1988): Fish predation in size-structured populations of treefrog tadpoles. Oecologia. 75: 321-326. https://doi.org/10.1007/BF00376932
Smith, D.C., van Buskirk, J. (1995): Phenotypic design, plasticity, and ecological performance in two tadpole species. Am Nat. 145: 211-233.
Toledo, L.F., Ribeiro, R.S., Haddad, C.F.B. (2007): Anurans as prey: an exploratory analysis and size relationships between predators and their prey. J Zool. 271: 170-177.
Touchon, J.C., Wojdak, J.M. (2014): Plastic hatching timing by red-eyed treefrog embryos interacts with larval predator identity and sublethal predation to affect prey morphology but not performance. PLOS ONE 9: e100623. doi: 10.1371/journal.pone.0100623
Üveges, B., Szederkényi, M., Mahr, K., Móricz, Á.M., Krüzselyi, D., Bókony, V., Hoi, H., Hettyey, A. (2019): Chemical defense of toad tadpoles under risk by four predator species. Ecol Evol. 9: 6287-6299.
van Buskirk, J., Anderwald, P., Lüpold, S., Reinhardt, L., Schuler, H. (2003): The lure effect, tadpole tail shape, and the target of dragonfly strikes. J Herpetol. 37: 420-424.
van Buskirk, J., Arioli, M. (2002): Dosage response of an induced defense: how sensitive are tadpoles to predation risk? Ecology 83: 1580-1585. doi: https://doi.org/10.1890/0012-9658(2002)083[1580:DROAID]2.0.CO;2
van Buskirk, J., McCollum, S.A. (2000a): Functional mechanisms of an inducible defence in tadpoles: morphology and behaviour influence mortality risk from predation. J Evol Biol. 13: 336-347.
van Buskirk, J., McCollum, S.A. (2000b): Influence of tail shape on tadpole swimming performance. J Exp Biol. 203: 2149-2158.
Watkins, T.B. (2015): Predator-mediated selection on burst swimming performance in tadpoles of the pacific tree frog, Pseudacris regilla. Physiol Biochem Zool. 69: 154-167.
Wilbur, H.M., Semlitsch, R.D. (1990): Ecological consequences of tail injury in Rana tadpoles. Copeia. 1990: 18-24. https://doi.org/10.2307/1445817
Zamora-Camacho, F.J., Aragón, P. (2019): Failed predator attacks have detrimental effects on antipredatory capabilities through developmental plasticity in Pelobates cultripes toads. Funct Ecol. 33: 846-854.
Zamora-Camacho, F.J., Cortés-Manzaneque, S., Aragón, P. (2019): Simulated predation pressure in Pelobates cultripes tadpoles modulates morphology at the metamorphic stage. Curr Zool. 65: 651-656.
Blanco-Torres, A., Bonilla, M.A., Cagnolo, L. (2020): Habitat modification effects on anuran food webs in the Colombian tropical dry forest. Food Webs. 22: e00133. https://doi.org/10.1016/j.fooweb.2019.e00133
Both, C., Grant, T. (2012): Biological invasions and the acoustic niche: the effect of bullfrog calls on the acoustic signals of white-banded tree frogs. Biol lett. 8: 714-716.
Cabrera-Guzmán, E., Crossland, M.R., Shine, R. (2012): Predation on the eggs and larvae of invasive cane toads (Rhinella marina) by native aquatic invertebrates in tropical Australia. Biol Conserv. 153: 1-9. doi: 10.1016/j.biocon.2012.04.012
Crane, A.L., Chivers, D.P., Ferrari, M.C.O. (2018): Embryonic background risk promotes the survival of tadpoles facing surface predators. PLOS ONE. 13: e0193939. https://doi.org/10.1371/journal.pone.0193939
Crossland, M.R., Alford, R.A. (1998): Evaluation of the toxicity of eggs, hatchlings and tadpoles of the introduced toad Bufo marinus (Anura: Bufonidae) to native Australian aquatic predators. Aust J Ecol. 23: 129-137.
Crump, M.L., Vaira, M. (1991): Vulnerability of Pleurodema borelli tadpoles to an avian predator: Effect of body size and density. Herpetologica. 47: 316-321.
D’Heursel, A., Haddad, C.F.B. (1999): Unpalatability of Hyla semilineata tadpoles (Anura) to captive and free-ranging vertebrate predators. Ethol Ecol Evol. 11: 339-348.
Ding, G.-H., Lin, Z.-H., Wei, L. (2014): The compensatory effect of tail regeneration on swimming speed in larval Hoplobatrachus chinensis Osbeck, 1765 (Anura: Ranidae) after tail removal. Acta Herpetol. 9: 219-225.
Eterovick, P.C., Mendes, I.S., Kloh, J.S., Pinheiro, L.T., Václav, A.B.H.P., Santos,T., Gontijo, A.S.B. (2018): Tadpoles respond to background colour under threat. Scientific Reports. 8: 4085. https://doi.org/10.1038/s41598-018-22315-8
Figiel Jr, C.R., Semlitsch, R.D. (2011): Effects of nonlethal injury and habitat complexity on predation in tadpole populations. Can J Zool. 69: 830-834.
Fox, J., Weisberg, S. (2019): An R Companion to Applied Regression (Third). Sage. https://socialsciences.mcmaster.ca/jfox/Books/Companion/
Gherardi, F., Renai, B., Corti, C. (2001): Crayfish predation on tadpoles: A comparison between a native (Austropotamobius pallipes) and an alien species (Procambarus clarkii). Bulletin Français de la Pêche et de la Pisciculture. 361: 659-668.
Gontijo, A.S.B., Espanha, J., Eterovick, P.C. (2018): Is tadpole coloration adaptive against bird predation? Acta Ethol. 21: 69-79.
Gosner, K.L. (1960): A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica. 16: 183-190.
Hair, J.F., Anderson, R.E., Babin, B.J., Black, W.C. (2010): Multivariate data analysis: A global perspective (Vol. 7). Pearson.
Heyer, W.R., McDiarmid, R.W., Weigmann, D.L. (1975): Tadpoles, predation and pond habitats in the tropics. Biotropica. 7: 100-111. https://doi.org/10.2307/2989753
Hoff, K.V.S., Wassersug, R.J. (2000): Tadpole locomotion: axial movement and tail functions in a largely vertebraeless vertebrate. Am Zool. 40: 62-076.
Koch, N.M., Wilcoxen, T.E. (2019): The effects of tail damage on tadpole development and leaping ability after metamorphosis in Cuban tree frogs (Osteopilus septentrionalis). Bios. 89: 165-173.
McCollum, S.A., Leimberger, J.D. (1997): Predator-induced morphological changes in an amphibian: Predation by dragonflies affects tadpole shape and color. Oecologia. 109: 615-621.
Morgan, L.A., Buttemer, W. (1996): Predation by the non-native fish Gambusia holbrooki on small Litoria aurea and L. dentata tadpoles. Aust Zool. 30: 143-149.
Morin, P.J. (1981): Predatory salamanders reverse the outcome of competition among three species of anuran tadpoles. Science. 212: 1284-1286. doi: 10.1126/science.212.4500.1284
Morin, P.J. (1985): Predation intensity, prey survival and injury frequency in an amphibian predator-prey interaction. Copeia. 1985: 638-644. doi: 10.2307/1444755
Nunes, A.L., Cruz, M.J., Tejedo, M., Laurila, A., Rebelo, R. (2010): Nonlethal injury caused by an invasive alien predator and its consequences for an anuran tadpole. Basic and Appl Ecol. 11: 645-654.
Parichy, D.M., Kaplan, R.H. (1992): Developmental consequences of tail injury on larvae of the oriental fire-bellied toad, Bombina orientalis. Copeia. 1992: 129-137. https://doi.org/10.2307/1446544
R Core Team. (2021): R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. https://www.R-project.org/
Rebouças R, Castro I.M., Solé M. (2013): Diet of Haddadus binotatus (Spix, 1824)(Anura: Craugastoridae) in Brazilian Atlantic Rainforest, Bahia state. North-West J Zool. 9: 159-165.
Rebouças R, Solé M. (2015): Diet of Adenomera thomei (Almeida and Angulo, 2006)(Anura: Leptodactylidae) from a rubber tree plantation in southern Bahia, Brazil. Stud Neotrop Fauna E. 50: 73-79.
Sales, L.P., Rebouças, R., Toledo, L.F. (2021): Native range climate is insufficient to predict anuran invasive potential. Biol Invasions. doi: 10.1007/s10530-021-02528-1.
Segalla, M.V., Berneck, B., Caramaschi, U., Cruz, C.A.G., Garcia, P.C.A., Grant, T., Haddad, C.F.B., Lourenço, A.C.C., Mangia, S., Mott, T., Nascimento, L., Toledo, L. F., Werneck, F., Langone, J.A. (2021): List of Brazilian Amphibians. Herpetologia Brasileira. 10: 121-216. https://doi.org/10.5281/zenodo.4716176
Semlitsch, R.D. (1990): Effects of body size, sibship, and tail injury on the susceptibility of tadpoles to dragonfly predation. Can J Zool. 68: 1027-1030.
Semlitsch, R.D., Gibbons, J.W. (1988): Fish predation in size-structured populations of treefrog tadpoles. Oecologia. 75: 321-326. https://doi.org/10.1007/BF00376932
Smith, D.C., van Buskirk, J. (1995): Phenotypic design, plasticity, and ecological performance in two tadpole species. Am Nat. 145: 211-233.
Toledo, L.F., Ribeiro, R.S., Haddad, C.F.B. (2007): Anurans as prey: an exploratory analysis and size relationships between predators and their prey. J Zool. 271: 170-177.
Touchon, J.C., Wojdak, J.M. (2014): Plastic hatching timing by red-eyed treefrog embryos interacts with larval predator identity and sublethal predation to affect prey morphology but not performance. PLOS ONE 9: e100623. doi: 10.1371/journal.pone.0100623
Üveges, B., Szederkényi, M., Mahr, K., Móricz, Á.M., Krüzselyi, D., Bókony, V., Hoi, H., Hettyey, A. (2019): Chemical defense of toad tadpoles under risk by four predator species. Ecol Evol. 9: 6287-6299.
van Buskirk, J., Anderwald, P., Lüpold, S., Reinhardt, L., Schuler, H. (2003): The lure effect, tadpole tail shape, and the target of dragonfly strikes. J Herpetol. 37: 420-424.
van Buskirk, J., Arioli, M. (2002): Dosage response of an induced defense: how sensitive are tadpoles to predation risk? Ecology 83: 1580-1585. doi: https://doi.org/10.1890/0012-9658(2002)083[1580:DROAID]2.0.CO;2
van Buskirk, J., McCollum, S.A. (2000a): Functional mechanisms of an inducible defence in tadpoles: morphology and behaviour influence mortality risk from predation. J Evol Biol. 13: 336-347.
van Buskirk, J., McCollum, S.A. (2000b): Influence of tail shape on tadpole swimming performance. J Exp Biol. 203: 2149-2158.
Watkins, T.B. (2015): Predator-mediated selection on burst swimming performance in tadpoles of the pacific tree frog, Pseudacris regilla. Physiol Biochem Zool. 69: 154-167.
Wilbur, H.M., Semlitsch, R.D. (1990): Ecological consequences of tail injury in Rana tadpoles. Copeia. 1990: 18-24. https://doi.org/10.2307/1445817
Zamora-Camacho, F.J., Aragón, P. (2019): Failed predator attacks have detrimental effects on antipredatory capabilities through developmental plasticity in Pelobates cultripes toads. Funct Ecol. 33: 846-854.
Zamora-Camacho, F.J., Cortés-Manzaneque, S., Aragón, P. (2019): Simulated predation pressure in Pelobates cultripes tadpoles modulates morphology at the metamorphic stage. Curr Zool. 65: 651-656.