[en] The hydroperiod of breeding habitats imposes a strong selection on amphibians and pond-breeding species usually exhibit a high degree of plasticity in the duration of larval period. However, the potential for phenotypic plasticity in fast developing species was investigated only in a small number of anurans, and the specific response to environmental cues such as low water versus decreasing water level, as well as the effects of such cues on particular developmental stages, are even less understood. In this context, we investigated the plastic response to pond desiccation in a neotropical species (Ceratophrys stolzmanni) by raising tadpoles in three water level treatments: constant high, constant low and decreasing. The growth rates were the highest reported for amphibian tadpoles (up to 0.3g/day) and the time to metamorphosis was short in all treatments, with the fastest developing tadpole metamorphosing in only 16 days after egg deposition. Individuals from the constant high water level treatment had a higher growth rate than those in the other two treatments, whereas decreasing and constant low water levels had similar effects on development, speeding up metamorphosis. In turn, this involved a cost as these tadpoles had a lower body size and mass at metamorphosis than the ones raised in constant high water levels. The final stages of metamorphosis, when tadpoles are the most vulnerable, were shorter in tadpoles exposed to a decreasing water level, allowing them to leave water quickly. Our experiment demonstrates that phenotypic plasticity is maintained even in environments devoid of permanent aquatic habitats. Ceratophryd tadpoles are able to shorten their developmental time when they perceive a risk of desiccation and react similarly to cues coming from the two unfavorable water conditions showing their adaptation to ephemeral and unpredictable breeding habitats.
Research Center/Unit :
AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Disciplines :
Zoology Aquatic sciences & oceanology Animal production & animal husbandry
F.R.S.-FNRS - Fonds de la Recherche Scientifique WBI - Wallonie-Bruxelles International SENESCYT - Secretaría de Educación Superior Ciencia Tecnología e Innovación CCCDI-UEFISCDI
Altwegg, R. & Reyer, H.-U. (2003). Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57, 872–882.
Angulo, A., Coloma, L.A., Ron, S. & Cisneros-Heredia, D. (2004). Ceratophrys stolzmanni. The IUCN Red List of Threatened Species 2004: e.T56341A11464974.
Babbitt, K.J. & Meshaka, W.E. Jr (2000). Benefits of eating conspecifics: effects of background diet on survival and metamorphosis in the Cuban treefrog (Osteopilus septentrionalis). Copeia 2000, 469–474.
Brady, L.D. & Griffiths, R.A. (2000). Developmental responses to pond desiccation in tadpoles of the British anuran amphibians (Bufo bufo, B. calamita and Rana temporaria). J. Zool. Lond. 252, 61–69.
Cabrera-Guzmán, E., Crossland, M.R., Brown, G.P. & Shine, R. (2013). Larger body size at metamorphosis enhances survival, growth and performance of young cane toads (Rhinella marina). PLoS One 8, e70121.
Charbonnier, J.F. & Vonesh, J.R. (2015). Consequences of life history switch point plasticity for juvenile morphology and locomotion in the Túngara frog. PeerJ 3, e1268.
Crump, M.L. (1989). Effect of habitat drying on developmental time and size at metamorphosis in Hyla pseudopuma. Copeia 1989, 794–797.
Denoël, M. (2003). How do paedomorphic newts cope with lake drying? Ecography 26, 405–410.
Denver, R.J. (1997). Proximate mechanisms of phenotypic plasticity in amphibian metamorphosis. Am. Zool. 37, 172–184.
Denver, R.J., Mirhadi, N. & Phillips, M. (1998). Adaptive plasticity in amphibian metamorphosis: response of Scaphiopus hammondii tadpoles to habitat desiccation. Ecology 79, 1859–1872.
Downie, J.R., Bryce, R. & Smith, J. (2004). Metamorphic duration: an under-studied variable in frog life histories. Biol. J. Linn. Soc. 83, 261–272.
Espinosa, C.I., de la Cruz, M., Jara-Guerrero, A., Gusmán, E. & Escudero, A. (2016). The effects of individual tree species on species diversity in a tropical dry forest change throughout ontogeny. Ecography 39, 329–337.
Fabrezi, M. (2011). Heterochrony in growth and development in anurans from the Chaco of South America. Evol. Biol. 38, 390–411.
Fabrezi, M., Quinzio, S.I., Goldberg, J., Cruz, J.C., Pereyra, M.C. & Wassersug, R.J. (2016). Developmental changes and novelties in ceratophryid frogs. EvoDevo 7, 1–16.
Fan, X.-L., Lin, Z.-H. & Wei, J. (2014). Effects of hydroperiod duration on developmental plasticity in tiger frog (Hoplobatrachus chinensis) tadpoles. Zool. Res. 35, 124–131.
Goater, C.P. (1994). Growth and survival of postmetamorphic toads: interactions among larval history, density, and parasitism. Ecology 75, 2264–2274.
Gómez-Mestre, I. & Buchholz, D.R. (2006). Developmental plasticity mirrors differences among taxa in spadefoot toads linking plasticity and diversity. Proc. Natl Acad. Sci. USA 103, 19021–19026.
Gómez-Mestre, I., Kulkarni, S. & Buchholz, D.R. (2013). Mechanisms and consequences of developmental acceleration in tadpoles responding to pond drying. PLoS One 8, e84266.
Gosner, K.L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183–190.
Grözinger, F., Thein, J., Feldhaar, H. & Rödel, M.-O. (2014). Giants, dwarfs and the environment – metamorphic trait plasticity in the common frog. PLoS One 9, e89982.
Kupferberg, S.J. (1997). The role of larval diet in anuran metamorphosis. Am. Zool. 37, 146–159.
Laugen, A.T., Laurila, A. & Merilä, J. (2002). Maternal and genetic contributions to geographical variation in Rana temporaria larval life-history traits. Biol. J. Linn. Soc. 76, 61–70.
Laurila, A. & Kujasalo, J. (1999). Habitat duration, predation risk and phenotypic plasticity in common frog (Rana temporaria) tadpoles. J. Anim. Ecol. 68, 1123–1132.
Loman, J. (2002). Microevolution and maternal effects on tadpole Rana temporaria growth and development rate. J. Zool. Lond. 257, 93–99.
Merilä, J., Laurila, A., Laugen, A.T., Rasanen, K. & Pahkala, M. (2000). Plasticity in age and size at metamorphosis in Rana temporaria: comparison of high and low latitude populations. Ecography 23, 457–465.
Michimae, H. & Emura, T. (2012). Correlated evolution of phenotypic plasticity in metamorphic timing. J. Evol. Biol. 25, 1331–1339.
Morey, S. & Reznick, D. (2000). A comparative analysis of plasticity in larval development in three species of spadefoot toads. Ecology 81, 1736–1749.
Morey, S. & Reznick, D. (2001). Effects of larval density on postmetamorphic spadefoot toads (Spea hammondii). Ecology 82, 510–522.
Morey, S.R. & Reznick, D.N. (2004). The relationship between habitat permanence and larval development in California spadefoot toads: field and laboratory comparisons of developmental plasticity. Oikos 104, 172–190.
Newman, R.A. (1998). Ecological constraints on amphibian metamorphosis: interactions of temperature and larval density with responses to changing food level. Oecologia 115, 9–16.
Orizaola, G., Dahl, E., Nicieza, A.G. & Laurila, A. (2013). Larval life history and anti-predator strategies are affected by breeding phenology in an amphibian. Oecologia 171, 873–881.
Ortiz, D.A., Almeida-Reinoso, D. & Coloma, L.A. (2013). Notes on husbandry, reproduction and development in the Pacific horned frog Ceratophrys stolzmanni (Anura: Ceratophryidae), with comments on its amplexus. Int. Zoo Yearb. 47, 151–162.
Padilla, D.K. & Adolph, S.C. (1996). Plastic inducible morphologies are not always adaptive: the importance of time delays in a stochastic environment. Evol. Ecol. 10, 105–117.
Perotti, M., Jara, F. & Úbeda, C. (2011). Adaptive plasticity of life-history traits to pond drying in three species of Patagonian anurans. Evol. Ecol. Res. 13, 415–429.
Quinzio, S.I., Fabrezi, M. & Faivovich, J. (2006). Redescription of the tadpole of Chacoprys pierottii (Vellard, 1984) (Anura, Ceratophrydae). S. Am. J. Herpetol. 1, 202–209.
Richter-Boix, A., Tejedo, M. & Rezende, E.L. (2011). Evolution and plasticity of anuran larval development in response to desiccation. A comparative analysis. Ecol. Evol. 1, 15–25.
Rowe, L. & Ludwig, D. (1991). Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72, 413–427.
Rudolf, V.H.W. & Rödel, M.-O. (2007). Phenotypic plasticity and optimal timing of metamorphosis under uncertain time constraints. Evol. Ecol. 21, 121–142.
Schalk, C.M., Montaña, C.G., Klemish, J.L. & Wild, E.R. (2014). On the diet of the frogs of the Ceratophryidae: synopsis and new contributions. S. Am. J. Herpetol. 9, 90–105.
Semlitsch, R.D. & Caldwell, J.P. (1982). Effects of density of growth, metamorphosis, and survivorship in tadpoles of Scaphiopus holbrooki. Ecology 63, 905–911.
Stearns, S.C. & Koella, J.C. (1986). The evolution of phenotypic plasticity in life-history traits: predictions of reaction norms for age and size at maturity. Evolution 40, 893–913.
Székely, P., Tudor, M. & Cogălniceanu, D. (2010). Effect of habitat drying on the development of the Eastern spadefoot toad (Pelobates syriacus) tadpoles. Amphibia-Reptilia 31, 425–434.
Tarvin, R.D., Silva Bermúdez, C., Briggs, V.S. & Warkentin, K.M. (2015). Carry-over effects of size at metamorphosis in red-eyed treefrogs: higher survival but slower growth of larger metamorphs. Biotropica 47, 218–226.
Urban, M.C., Richardson, J.L. & Freidenfelds, N.A. (2014). Plasticity and genetic adaptation mediate amphibian and reptile responses to climate change. Evol. Appl. 7, 88–103.
Van Buskirk, J. & Saxer, G. (2001). Delayed costs of an induced defense in tadpoles? Morphology, hopping, and development rate at metamorphosis. Evolution 55, 821–829.
Walsh, P.T. (2010). Anuran life history plasticity: variable practice in determining the end-point of larval development. Amphibia-Reptilia 31, 157–167.
Walsh, P.T., Downie, J.R. & Monaghan, P. (2008). Plasticity of the duration of metamorphosis in the African clawed toad. J. Zool., Lond. 274, 143–149.
Wassersug, R.J. & Sperry, D.G. (1977). The relationships of locomotion to differential predation on Pseudacris triseriata (Anura: Hylidae). Ecology 58, 830–839.
Wells, K.D. (2010). The ecology and behavior of amphibians. Chicago: University of Chicago Press.
Werner, E.E. (1986). Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. Am. Nat. 128, 319–341.