Hydrobiologia

, Volume 583, Issue 1, pp 43–56 | Cite as

A comparative study of predator-induced phenotype in tadpoles across a pond permanency gradient

  • Alex Richter-Boix
  • Gustavo A. Llorente
  • Albert Montori
Primary Research Paper

Abstract

In a field survey the distribution of pond-breeding anuran species and their potential large predators was investigated along a freshwater habitat gradient, ranging from ephemeral pools to permanent ponds. In a laboratory experiment predator-induced plasticity was examined for all tadpole species to test whether the plastic response of ephemeral and temporary pond species differs from that of permanent pond species. Desiccation and predation pose conflicting demands; reduced activity lowers the risk of death by predation but increases the risk of death by desiccation. It was expected that species from time-constrained habitats would display a morphotype that would reduce vulnerability to invertebrate predators, thus allowing these species to maintain a high level of activity, whereas species from permanent ponds would avoid predation both morphologically and behaviourally. Species distribution and predator composition along the hydroperiod gradient differed. Variations between ephemeral and temporary ponds can be attributed to hydroperiod differences and the presence of large invertebrate predators in temporary ponds, whereas the contrasts between temporary and permanent ponds can only be attributed to the hydroperiod, since the presence and abundance of top predators are similar in both habitat types. With the exception of bufonids, all species showed predator-induced plasticity in agreement with previous studies. Tadpole species differed in the integration of the phenotypic traits measured, but differences observed between species could not be attributed only to habitat. Species from temporary habitats showed an expected response, with a low reduction of activity in comparison with the rest of the species. The lack of general patterns in the morphological changes suggests that species within the same habitat type did not converge on similar phenotypes, perhaps due to functional constraints on differences in microhabitat use in the water column.

Keywords

Behavioural plasticity Mediterranean area Morphological plasticity Phenotypic integration Predation risk gradient Spatial distribution Temporary pond Trade-offs 

References

  1. Altwegg, R., 2002. Predator-induced life-history plasticity under time constraints in pool frogs. Ecology 83: 2542–2551.CrossRefGoogle Scholar
  2. Anholt, B. R. & E. E. Werner, 1995. Interaction between food availability and predation mortality mediated by activity. Ecology 76: 2235–2239.CrossRefGoogle Scholar
  3. Anholt, B. R., D. K. Skelly & E. E. Werner, 1996. Factors modifying antipredator behaviour in larval toads. Herpetologica 52: 301–313.Google Scholar
  4. Anholt, B. R., E. E. Werner & D. K. Skelly, 2000. Effect of food and predators on the activity of four larval ranid frogs. Ecology 81: 3509–3521.CrossRefGoogle Scholar
  5. Babbitt, K. J., J. B. Matthew & T. L. Tarr, 2003. Patterns of larval amphibian distribution along a wetland hydroperiod gradient. Canadian Journal of Zoology 81: 1539–1552.CrossRefGoogle Scholar
  6. Bookstein, F. L., 1991. Morphometrics Tool for Landmark Data: Geometry and Biology. Cambridge University Press, Cambridge.Google Scholar
  7. Bridges, C. M., 2002. Tadpoles balance foraging and predator avoidance: effects of predation, pond drying, and hunger. Journal of Herpetology 36: 627–634.Google Scholar
  8. Chovanec, A., 1992. The influence of tadpole swimming behaviour on predation by dragonfly nymphs. Amphibia-Reptilia 13: 341–349.Google Scholar
  9. Cronin, J. T. & J. Travis, 1986. Size-limited predation on larval Rana aerolata (Anura: Ranidae) by two species of backswimmers (Heteroptera: Notonectidae). Herpetologica 42: 171–174 .Google Scholar
  10. DeWitt, T. J. & S. M. Scheiner, 2004. Phenotypic Plasticity: Functional and Conceptual Approaches. Oxford University Press, New York, USA.Google Scholar
  11. Díaz-Paniagua, C., 1987a. Estudio en cautividad de la actividad alimenticia de las larvas de siete especies de anuros. Revista Española de Herpetología 2: 189–197.Google Scholar
  12. Díaz-Paniagua, C., 1987b. Tadpole distribution in relation to vegetal heterogeneity in temporary ponds. Herpetological Journal 1: 167–169.Google Scholar
  13. Eklöv, P. & C. Halvarsson, 2000. The trade-off between foraging activity and predation risk for Rana temporaria in different food environments. Canadian Journal of Zoology 78: 734–739.CrossRefGoogle Scholar
  14. Felsenstein, J., 1985. Phylogenies and the comparative method. American Naturalist 125: 1–13.CrossRefGoogle Scholar
  15. Gunzburger, M. S. & J. Travis, 2004. Evaluating predation pressure on green treefrog larvae across a habitat gradient. Oecologia 140: 422–429.PubMedCrossRefGoogle Scholar
  16. Laurila, A. & J. Kujasalo, 1999. Habitat duration, predation risk and phenotypic plasticity in common frog (Rana temporaria) tadpoles. Journal of Animal Ecology 68: 1123–1132.CrossRefGoogle Scholar
  17. Lardner, B., 2000. Morphological and life history responses to predators in larvae of seven anurans. Oikos 88: 169–180.CrossRefGoogle Scholar
  18. Loy, A., M. Corti & L. F. Marcus, 1993. Landmarks data: size and shape analysis in systematics. A case study on old world talpidae (Mammalia, Insectivora). In Marcus, L. F., E. Bello & A. García-Valdecasas (eds), Contributions to Morphometrics. Monografías del Museo Nacional de Ciencias Naturales, Madrid, 215–239.Google Scholar
  19. McCollum, S. A. & J. D. Leimberger, 1997. Predator-induced morphological changes in an amphibian: predation by dragonflies affects tadpole shape and color. Oecologia 109: 612–615.CrossRefGoogle Scholar
  20. Reeve, J. & E. Abouheif, 2003. Phylogenetic Independence. Version 2.0, Department of Biology, McGill University. Distributed freely by the authors on request.Google Scholar
  21. Relyea, R.A., 2002. Cost of phenotypic plasticity. American Naturalist 159: 272–282.CrossRefGoogle Scholar
  22. Relyea, R. A. 2004. Integrating phenotypic plasticity when death is on the line: insights from predator–prey systems. In Pigliucci, M. & K. Preston (eds), Phenotypic Integration: Studying the Ecology and Evolution of Complex Phenotypes. Oxford University Press, New York, USA.Google Scholar
  23. Relyea, R. A. & E. E. Werner, 1999. Quantifying the relation between predator-induced behavior and growth performance in larval anurans. Ecology 80: 2117–2124.CrossRefGoogle Scholar
  24. Relyea, R. A. & E. E. Werner, 2000. Morphological plasticity in four larval anurans distributed along an environmental gradient. Copeia 2000: 178–190.CrossRefGoogle Scholar
  25. Richardson, J. M. L., 2001a. The relative roles of adaptation and phylogeny in determination of larval traits in diversifying anuran lineages. American Naturalist 157: 282–299.CrossRefGoogle Scholar
  26. Richardson, J. M. L., 2001b. A comparative study of activity levels in larval anurans and response to the presence of different predators. Behavioural Ecology 12: 51–58.Google Scholar
  27. Richardson, J. M. L., 2002a. A comparative study of phenotypic traits related to resource utilization in anuran communities. Evolutionary Ecology 16: 101–122.CrossRefGoogle Scholar
  28. Richardson, J. M. L., 2002b. Burst swim speed in tadpoles inhabiting ponds with different top predators. Evolutionary Ecology Research 4: 627–642.Google Scholar
  29. Richter-Boix, A., G. A. Llorente & A. Montori, 2006a. A comparative analysis of the adaptive developmental plasticity hypothesis in six Mediterranean anuran species along a pond permanency gradient. Evolutionary Ecology Research 8: 1139–1154.Google Scholar
  30. Richter-Boix, A., G. A. Llorente & A. Montori, 2006b. Breeding phenology of an amphibian community in a Mediterranean area. Amphibia-Reptilia 27: 544–559.CrossRefGoogle Scholar
  31. Richter-Boix, A., G. A. Llorente & A. Montori, 2007. Hierarchical competition in pond-breeding anuran larvae in a Mediterranean area. Amphibia-Reptilia 28: in press.Google Scholar
  32. Rohlf, F. J., 2001. Thin-Plate Spline (TPS) Software. Free available on:http://life.bio.sunysb.edu/morph/ (last modified October 31, 2005).
  33. Schaffer, H. B., R. A. Alford, B. D. Woodward, S. J. Richards, R. G. Altig & C. Gascon, 1994. Quantitative sampling of amphibian larvae. In Heyer, W. R., 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, 130–141.Google Scholar
  34. Schlichting, C. & M. Pigliucci, 1998. Phenotypic Evolution: A Reaction Norm Perspective. Sinauer, Sunderland, 400 pp.Google Scholar
  35. Schneider, D. W. & T. M. Frost, 1996. Habitat duration and community structure in temporary ponds. Journal of the North American Benthological Society 15: 64–86.CrossRefGoogle Scholar
  36. Skelly, D. K., 1994. Activity level and the susceptibility of anuran larvae to predation. Animal Behaviour 47: 465–468.CrossRefGoogle Scholar
  37. Skelly, D. K., 1995. A behavioural trade-off and its consequences for the distribution of Pseudacris treefrog larvae. Ecology 76: 150–164.CrossRefGoogle Scholar
  38. Skelly, D. K., 1996. Pond drying, predators, and the distribution of Pseudacris treefrog tadpoles. Copeia 1996: 599–605.CrossRefGoogle Scholar
  39. Skelly, D. K. & E. E. Werner, 1990. Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology 71: 2313–2322.CrossRefGoogle Scholar
  40. Snodgrass, J. W., A. L. Bryan & J. Burger, 2000. Development of expectations of larval amphibian assemblage structure in southeastern depression wetlands. Ecological Applications 10: 1219–1229.CrossRefGoogle Scholar
  41. Stocks, R. & M. A. McPeek, 2003. Predators and life histories shape Lestes damselfly assemblages along a freshwater habitat gradient. Ecology 84: 1576–1587.Google Scholar
  42. Teplitsky, C., S. Plénet & P. Joly, 2005. Cost and limits of dosage response to predation risk: to what extent can tadpoles invest in anti-predator morphology? Oecologia 145: 364–370.PubMedCrossRefGoogle Scholar
  43. Travis, J., W. H. Keen & J. Juilianna, 1985. The role of relative body size in a predator–prey relationship between dragonfly naiads and larval anurans. Oikos 45: 59–65.CrossRefGoogle Scholar
  44. Van Buskirk, J., 2000. The cost of an inducible defense in anuran larvae. Evolution 81: 2813–2821.Google Scholar
  45. Van Buskirk, J., 2002. A comparative test of the adaptive plasticity hypothesis: relationships between habitat and phenotype in anuran larvae. American Naturalist 160: 87–102.CrossRefGoogle Scholar
  46. Van Buskirk, J., 2003. Habitat partitioning in European and North American pond-breeding frogs and toads. Diversity and Distributions 9: 399–410.CrossRefGoogle Scholar
  47. Van Buskirk, J. & M. Arioli, 2005. Habitat specialization and adaptive phenotypic divergence of anuran populations. Journal of Evolutionary Biology 18: 596–608.PubMedCrossRefGoogle Scholar
  48. Van Buskirk, J. & R. A. Relyea, 1998. Natural selection for phenotypic plasticity: predator-induced responses in tadpoles. Biological Journal of the Linnean Society 65: 301–328.CrossRefGoogle Scholar
  49. Van Buskirk, J., S. A. McCollum & E. E. Werner, 1997. Natural selection for environmentally-induced phenotypes in tadpoles. Evolution 52: 1983–1992.CrossRefGoogle Scholar
  50. Via, S., R. Gomulkiewicz, G. De Jong, S. Scheiner, C. D. Schlichting & P. H. Van Tienderen, 1995. Adaptive phenotypic plasticity: consensus and controversy. Trends in Ecology and Evolution 10: 212–217.CrossRefGoogle Scholar
  51. Watt, P. J., S. F. Nottingham & S. Young, 1997. Toad tadpole aggregation behaviour: evidence for a predator avoidance function. Animal Behaviour 54: 865–872.PubMedCrossRefGoogle Scholar
  52. Wellborn, G. A., D. K. Skelly & E. E. Werner, 1996. Mechanism creating community structure across a freshwater habitat gradient. Annual Review in Ecology and Systematics 27: 337–363.CrossRefGoogle Scholar
  53. Werner, E. E. & M. A. McPeek, 1994. Direct and indirect effects of predators on two anuran species along an environmental gradient. Ecology 75: 1368–1382.CrossRefGoogle Scholar
  54. Wilbur, H. M., 1997. Experimental ecology of food webs: complex systems in temporary ponds. Ecology 78: 2279–2302.CrossRefGoogle Scholar
  55. Woodward, B. D., 1983. Predator–prey interactions and breeding-pond use of temporary-pond species in a desert anuran community. Ecology 64: 1549–1555.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Alex Richter-Boix
    • 1
  • Gustavo A. Llorente
    • 1
  • Albert Montori
    • 1
  1. 1.Departament Biologia Animal, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain

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