, Volume 173, Issue 1, pp 117–127 | Cite as

Food availability determines the response to pond desiccation in anuran tadpoles

  • Urtzi Enriquez-UrzelaiEmail author
  • Olatz San Sebastián
  • Núria Garriga
  • Gustavo A. Llorente
Population ecology - Original research


Food availability and pond desiccation are two of the most studied factors that condition amphibian metamorphosis. It is well known that, when food is abundant, organisms undergo metamorphosis early and when they are relatively large. The capability of anurans to accelerate their developmental rate in response to desiccation is also common knowledge. These two variables must act together in nature, since we know that, as a pond dries, the per capita resources decrease. We conduct an experiment to evaluate the effects of desiccation and food availability separately and in combination in tadpoles of the painted frog (Discoglossus pictus). We demonstrate that food deprivation leads to slow growth rates, which delay metamorphosis and produce smaller size and weight. The capability to accelerate metamorphosis when facing a drying pond is also confirmed, but, nevertheless, with factor interaction (when the pool is drying and resources are scarce) the capacity to respond to desiccation is lost. In addition, slow drying rates are shown to be stressful situations, but not enough to provoke a shortening of the larval period; in fact, the larval period becomes longer. We also demonstrate that the interaction of these factors changes the allometric relationship of different parts of the hind limb, which has implications for the biomechanics of jumping. Due to low mortality rates and an adequate response to both environmental factors, we expect D. pictus to have a great invasive potential in its new Mediterranean distribution area, where lots of temporary and ephemeral ponds are present.


Phenotypic plasticity Development Metamorphosis Feeding restriction Drying 



We thank the Departament de Medi Ambient i Habitatge of the Generalitat de Catalunya for their support and permission to collect clutches. We also thank Marc Franch for providing the clutches for this study. B. Bolker provided helpful statistical consultation. Francesc Oliva (Departament d’Estadística), Ross Alford (handling editor) and two anonymous reviewers gave helpful comments on the manuscript.


  1. Alford RA, Harris RN (1988) Effects of larval growth history on anuran metamorphosis. Am Nat 131(1):91–106CrossRefGoogle Scholar
  2. Barbadillo LJ, Lacomba JI, Pérez-Mellado V, Sancho V, López-Jurado LF (1999) Anfibios y reptiles de la Peninsula Iberica, Baleares y Canarias. Planeta, BarcelonaGoogle Scholar
  3. Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst 35:651–673CrossRefGoogle Scholar
  4. Berven KA (1981) Mate choice in the wood frog Rana sylvatica. Evolution 35:707–722CrossRefGoogle Scholar
  5. Bolker B, Phillips C (2011) Package “cpcbp”. Available from
  6. Brodeur JC, Svartz G, Perez-Coll CS, Marino DJG, Herkovits J (2009) Comparative susceptibility to atrazine of three developmental stages of Rhinella arenarum and influence on metamorphosis: non-monotonous acceleration of the time to climax and delayed tail resorption. Aquat Toxicol 91:161–170PubMedCrossRefGoogle Scholar
  7. Choi IH, Park K (1996) Variations in the take-off velocity of anuran amphibians: relation to morphology, muscle contractile function and enzyme activity. Comp Biochem Physiol 113A:393–400CrossRefGoogle Scholar
  8. Choi IH, Shim JH, Ricklefts RE (2003) Morphometric relationships of take-off speed in anuran amphibians. J Exp Zool A Comp Exp Biol 299:99–102PubMedCrossRefGoogle Scholar
  9. Day T, Rowe L (2002) Developmental thresholds and the evolution of reaction norms for age and size at life-history transitions. Am Nat 159:338–350PubMedCrossRefGoogle Scholar
  10. Denver RJ, Mirhadi N, Phillips M (1998) Adaptive plasticity in amphibian metamorphosis: response of Scaphiopus hammondii tadpoles to habitat desiccation. Ecology 79:1859–1872Google Scholar
  11. Flury B (1988) Common principal components and related multivariate models. Wiley, New YorkGoogle Scholar
  12. Franch M, Llorente GA, Montori A, Richter-Boix A, Carranza S (2007) Discovery of an introduced population of Discoglossus pictus beyond its known distributional range. Herpetol Rev 38:356–359Google Scholar
  13. Geniez P, Cheylan M (1987) Atlas de distribution des reptiles et des amphibiens du Languedoc-Roussillon. Laboratoire de Biogéographie et Ecologie des Vertébrés, MontpellierGoogle Scholar
  14. Gervasi SS, Foufopoulos J (2008) Costs of plasticity: responses to desiccation decrease post-metamorphic immune function in a pond-breeding amphibian. Funct Ecol 22:100–108Google Scholar
  15. Goater CP (1994) Growth and survival of postmetamorphic toads: interactions among larval history, density and parasitism. Ecology 75:2264–2274CrossRefGoogle Scholar
  16. Gomez-Mestre I, Saccoccio VL, Iijima T, Collins EM, Rosenthal GG, Warkentin KM (2010) The shape of things to come: linking developmental plasticity to post-metamorphic morphology in anurans. J Evol Biol 23:1364–1373PubMedCrossRefGoogle Scholar
  17. Gosner KL (1960) A simplified table for staging anuran embryos larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  18. Gotthard K, Sören N (1995) Adaptive plasticity and plasticity as an adaptation: a selective review of plasticity in animal morphology and life history. Oikos 74:3–17CrossRefGoogle Scholar
  19. Handrigan GR, Wassersug RJ (2007) The anuran Bauplan: a review on the adaptive, developmental, and genetic underpinnings of frog and tadpole morphology. Biol Rev 82:1–25PubMedCrossRefGoogle Scholar
  20. Harris RN (1999) The anuran tadpole: evolution and maintenance. In: McDiarmid RW, Altig R (eds) Tadpoles. The biology of anuran larvae. University of Chicago Press, Chicago, pp 279–294Google Scholar
  21. Hensley FR (1993) Ontogenetic loss of phenotypic plasticity of age at metamorphosis in tadpoles. Ecology 74:2405–2412CrossRefGoogle Scholar
  22. Hourdry J, Beaumont A (1985) Les métamorphoses des amphibiens. Masson, ParisGoogle Scholar
  23. Huxley JS (1932) Problems of relative growth. Lincoln MacVeagh Dial, New YorkGoogle Scholar
  24. James RS, Wilson RS (2008) Explosive jumping: extreme morphological and physiological specializations of Australian rocket frogs. Physiol Biochem Zool 81(2):176–185PubMedCrossRefGoogle Scholar
  25. Kulkarni SS, Gomez-Mestre I, Moskalik CL, Storz BL, Buchholz DR (2011) Evolutionary reduction of developmental plasticity in desert spadefoot toads. J Evol Biol 24:2445–2455PubMedCrossRefGoogle Scholar
  26. Laurila A, Pakkasmaa S, Crochet PA, Merilä J (2002) Predator-induced plasticity in early life history and morphology in two anuran amphibians. Oecologia 132:524–530CrossRefGoogle Scholar
  27. Leips J, Travis J (1994) Metamorphic responses to changing food levels in two species of hylid frogs. Ecology 75(5):1345–1356CrossRefGoogle Scholar
  28. Leips J, Mcmanus MG, Travis J (2000) Response of treefrog larvae to drying ponds: comparing temporary and permanent pond breeders. Ecology 81:2997–3008CrossRefGoogle Scholar
  29. Lind MI, Persbo F, Johansson F (2008) Pool desiccation and developmental thresholds in the common frog, Rana temporaria. Proc R Soc Lond B 275:1073–1080CrossRefGoogle Scholar
  30. Llewelyn J, Phillips BL, Alford RA, Schwarzkopf L, Shine R (2010) Locomotor performance in an invasive species: cane toads from the invasion front have greater endurance, but not speed, compared to conspecifics from a long-colonised area. Oecologia 162:343–348PubMedCrossRefGoogle Scholar
  31. Llorente GA, Montori A, Santos X, Carretero MA (1995) Atlas dels amfibis i reptils de Catalunya i Andorra. El Brau, BarcelonaGoogle Scholar
  32. Llorente GA, Montori A, Santos X, Carretero MA (1997) Discoglossus pictus. In: Pleguezuelos JM (ed) Distribución y biogeografía de los anfibios y reptiles en España y Portugal. Asociación Herpetológica Española—Universidad de Granada, Granada, pp 137–139Google Scholar
  33. Llorente GA, Montori A, Santos X, Carretero MA (2001) Discoglossus pictus (Otth 1837). Sapillo pintojo mediterráneo. In: Pleguezuelos JM, Márquez R, Lizana M (eds) Atlas y libro rojo de los anfibios y reptiles de España. Ministerio de Medio Ambiente, Madrid, pp 91–93Google Scholar
  34. Loman J, Claesson D (2003) Plastic response to pond drying in tadpoles Rana temporaria: tests of cost models. Evol Ecol Res 5:179–194Google Scholar
  35. Márquez-García M, Correa-Solis M, Sallaberry M, Méndez MA (2009) Effects of pond drying on morphological and life-history traits in the anuran Rhinella spinulosa (Anura: Bufonidae). Evol Ecol Res 11:803–815Google Scholar
  36. Martínez-Solano Í (2009) Sapillo pintojo mediterráneo—Discoglossus pictus Otth 1837. In: Salvador A, Martínez-Solano Í (eds) Enciclopedia virtual de los vertebrados españoles. Museo Nacional de Ciencias Naturales, Madrid, pp 1–13.
  37. McCoy MW (2007) Conspecific density determines the magnitude and character of predator-induced phenotype. Oecologia 153:871–878PubMedCrossRefGoogle Scholar
  38. McCoy MW, Bolker BM, Osenberg CW, Miner BG, Vonesh JR (2006) Size correction: comparing morphological traits among populations and environments. Oecologia 148:547–554PubMedCrossRefGoogle Scholar
  39. Merilä J, Laurila A, Lindgren B (2004) Variation in the degree and costs of adaptive phenotypic plasticity among Rana temporaria populations. J Evol Biol 17:1132–1140PubMedCrossRefGoogle Scholar
  40. Morey S, Reznick D (2000) A comparative analysis of plasticity in larval development in three species of spadefoot toads. Ecology 81:1736–1749CrossRefGoogle Scholar
  41. Morey SR, Reznick D (2004) The relationship between habitat permanence and larval development in California spadefoot toads: field and laboratory comparisons of developmental plasticity. Oikos 104:172–190CrossRefGoogle Scholar
  42. Newman RA (1989) Developmental plasticity of Scaphiopus couchii tadpoles in an unpredictable environment. Ecology 70:1775–1787CrossRefGoogle Scholar
  43. Newman RA (1992) Adaptive plasticity in amphibian metamorphosis. Bioscience 42:671–678CrossRefGoogle Scholar
  44. Newman RA (1998) Ecological constraints on amphibian metamorphosis: interactions of temperature and larval density with responses to changing food level. Oecologia 115:9–16CrossRefGoogle Scholar
  45. Newman RA, Dunham AE (1994) Size at metamorphosis and water loss in a desert anuran (Scaphiopus couchii). Copeia 1994:372–381CrossRefGoogle Scholar
  46. Plaistow SJ, Lapsley CT, Beckerman AP, Benton TG (2004) Age and size at maturity: sex, environmental variability and developmental thresholds. Proc R Soc Lond B 271:919–924CrossRefGoogle Scholar
  47. Pujol-Buxó E, San-Sebastián O, Garriga N, Llorente GA (2012) How does the invasive/native nature of species influence tadpoles’ plastic responses to predators? Oikos. doi: 10.1111/j.1600-0706.2012.20617.x Google Scholar
  48. R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  49. Richter-Boix A, Llorente GA, Montori A (2004) Responses to competition effects of two anuran tadpoles according to life-history traits. Oikos 106:39–50CrossRefGoogle Scholar
  50. Richter-Boix A, Llorente GA, Montori A (2006) Effects of phenotypic plasticity on post-metamorphic traits during pre-metamorphic stages in the anuran Pelodytes punctatus. Evol Ecol Res 8:309–320Google Scholar
  51. Richter-Boix A, Garriga N, Montori A, Franch M, San Sebastian O, Villero D, Llorente GA (2012) Effects of the non-native amphibian species Discoglossus pictus on the recipient amphibian community: niche overlap, competition and community organization. Biol Invasions. doi: 10.1007/s10530-012-0328-4 Google Scholar
  52. Rose CS (2005) Integrating ecology and developmental biology to explain the timing of frog metamorphosis. Trends Ecol Evol 20:129–135PubMedCrossRefGoogle Scholar
  53. Rowe L, Ludwig D (1991) Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72:413–427CrossRefGoogle Scholar
  54. Rudolf VHW, Rödel M-O (2007) Phenotypic plasticity and optimal timing of metamorphosis under uncertain time constraints. Evol Ecol 21:121–142CrossRefGoogle Scholar
  55. Salvador A, García París M (2001) Anfibios españoles. Identificación, historia natural y Distribución. Esfagnos, Talavera de la ReinaGoogle Scholar
  56. Savage RM (1952) Ecological, physiological and anatomical observations on some species of anuran tadpoles. Proc Zool Soc Lond 122:467–514Google Scholar
  57. Savage RM (1962) The ecology and life history of the common frog: Rana temporaria temporaria. Hafner, New YorkGoogle Scholar
  58. Semlitsch RD (1987) Paedomorphosis in Ambystoma talpoideum: effects of density, food, and pond drying. Ecology 68:994–1002CrossRefGoogle Scholar
  59. Smith DC (1987) Adult recruitment in chorus frog: effects of size and date at metamorphosis. Ecology 68:344–350CrossRefGoogle Scholar
  60. Tejedo M, Reques R (1994) Plasticity in metamorphic traits of natterjack tadpoles: the interactive effects of density and pond duration. Oikos 71:295–304CrossRefGoogle Scholar
  61. Touchon JC, Warkentin KM (2011) Thermally contingent plasticity: temperature alters expression of predator-induced colour and morphology in a neotropical treefrog tadpole. J Anim Ecol 80:79–88PubMedCrossRefGoogle Scholar
  62. Travis J (1984) Anuran size at metamorphosis: experimental test of a model based on intraspecific competition. Ecology 65:1155–1160CrossRefGoogle Scholar
  63. Van Buskirk J, Saxer G (2001) Delayed costs of an induced defense in tadpoles? Morphology, hopping, and development rate at metamorphosis. Evol Int J Org Evol 55:821–829CrossRefGoogle Scholar
  64. Walton M (1988) Relationships among metabolic, locomotory, and field measures of organismal performance in the fowler’s toad (Bufo woodhousei fowleri). Physiol Zool 61:107–118Google Scholar
  65. Wassersug RJ, Sperry DG (1977) The relationship of locomotion to differential predation on Pseudacris triseriata (Anura: Hylidae). Ecology 58:830–839CrossRefGoogle Scholar
  66. Watkins TB (2001) A quantitative genetic test of adaptive decoupling across metamorphosis for locomotor and life-history traits in the pacific tree frog, Hyla regilla. Evol Int J Org Evol 55:1668–1677Google Scholar
  67. Wells KD (2007) Complex life cycles and the ecology of amphibian metamorphosis. In: Wells KD (ed) The ecology and behavior of amphibians. University of Chicago Press, Chicago, pp 599–644CrossRefGoogle Scholar
  68. Werner EE (1986) Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. Am Nat 128:319–341CrossRefGoogle Scholar
  69. Wilbur HM (1977) Propagule size, number, and dispersion patterns in Ambystoma and Rana sylvatica. Am Nat 111:43–68CrossRefGoogle Scholar
  70. Wilbur HM (1980) Complex life cycles. Ann Rev Ecol Syst 11:67–93CrossRefGoogle Scholar
  71. Wilbur HM (1987) Regulation of structure in complex systems: experimental temporary pond communities. Ecology 68:1437–1452CrossRefGoogle Scholar
  72. Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis: nonnormal distributions of competitive ability reflect selection for facultative metamorphosis. Science 182:1305–1314PubMedCrossRefGoogle Scholar
  73. Zug GR (1972) Anuran locomotion: structure and function. I. Preliminary observations on relation between jumping and osteometrics of appendicular and postaxial skeleton. Copeia 4:613–624CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Urtzi Enriquez-Urzelai
    • 1
    Email author
  • Olatz San Sebastián
    • 1
    • 2
  • Núria Garriga
    • 1
  • Gustavo A. Llorente
    • 1
  1. 1.Departament de Biologia Animal, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain
  2. 2.Departamento de HerpetologíaAranzadi Zientzia Elkartea-Sociedad de Ciencias AranzadiDonostia-San SebastiánSpain

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