, Volume 141, Issue 1, pp 139–147 | Cite as

Induced defences in an endangered amphibian in response to an introduced snake predator

  • Robin D. Moore
  • Richard A. Griffiths
  • Cliona M. O’Brien
  • Adam Murphy
  • David Jay
Conservation Ecology


Introduced species have contributed significantly to the extinction of endemic species on islands. They also create new selection pressures on their prey that may result in modified life history strategies. Introduced viperine snakes (Natrix maura) have been implicated in the decline of the endemic midwife toad of Mallorca (Alytes muletensis). A comparison of A. muletensis tadpoles in natural pools with and without snakes showed that those populations subject to snake predation possessed longer tails with narrower tail fins but deeper tail muscles. Field and laboratory experiments showed that these changes in tail morphology could be induced by chemical and tactile cues from snakes. Populations of tadpoles that were subject to snake predation also displayed clear bimodal size-frequency distributions, with intermediate-sized tadpoles missing from the pools completely. Tadpoles in pools frequented by snakes developed faster in relation to their body size than those in pools without snakes. Variation in morphology between toad populations may therefore be caused by a combination of size-selective predation and tadpole plasticity. The results of this study indicate that the introduction of alien species can result in selection for induced defences, which may facilitate coexistence between predator and prey under certain conditions.


Alien species Alytes muletensis Amphibian declines Natrix maura Predator-prey interactions 



This work was carried out with the co-operation of La Consellaria de Medi Ambient and Associació per la Recuperació del Ferreret. We thank V. Muñoz, F. Kraaijeveld-Smit, A. Román, C. Zayas and R. Barber for logistical support in the field. B. Schmidt and P. Gregory provided helpful comments on earlier drafts of the manuscript. The work was supported by the Durrell Institute of Conservation and Ecology and NERC.


  1. Arntzen JW, García-Paris M (1995) Morphological and allozyme studies of midwife toads (genus Alytes), including the description of two new taxa from Spain. Contrib Zool 65:5–34Google Scholar
  2. Babbit KJ, Tanner GW (1998) Effects of cover and predator size on survival and development of Rana utricularia tadpoles. Oecologia 114:258–262CrossRefGoogle Scholar
  3. Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, CambridgeGoogle Scholar
  4. Bradford DF (1991) Mass mortality and extinction in a high-elevation population of Rana muscosa. J Herpetol 25:174–177Google Scholar
  5. Brodie ED Jr, Formanowicz D Jr (1983) Prey size preferences of predators: differential vulnerability of larval anurans. Herpetologica 39:67–75Google Scholar
  6. Brönmark C, Miner JG (1992) Predator-induced phenotypical change in body morphology in crucian carp. Science 258:1348–1350Google Scholar
  7. Buley KR, García G (1997) Recovery programme for the Mallorcan midwife toad. Dodo 33:80–90Google Scholar
  8. Bush SL (1993) Courtship and male parental care in the Mallorcan midwife toad (Alytes muletensis). PhD Thesis, University of East Anglia, NorwichGoogle Scholar
  9. Bush SL (1994) Good news for the Mallorcan midwife toad. Froglog 10:3Google Scholar
  10. Cambar R, Martin S (1959) Table chronologique du déveleopment embryonnaire et larvaire du crapaud accoucher (Alytes obstetricans Laur.). Actes Soc Linn Bord 98:3–33Google Scholar
  11. Case TJ, Bolger DT (1991) The role of introduced species in shaping the distribution and abundance of island reptiles. Evol Ecol 5:272–290Google Scholar
  12. Chivers DP, Wildy EL, Kiesecker JM, Blaustein AR (2001) Avoidance response of juvenile Pacific treefrogs to chemical cues of introduced bullfrogs. J Chem Ecol 27:1667–1676CrossRefPubMedGoogle Scholar
  13. Clark CW, Harvell CD (1992) Inducible defenses and the allocation of resources: a minimal model. Am Nat 139:521–539CrossRefGoogle Scholar
  14. Crump ML, Viara M (1991) Vulnerability of Pleurodema borelliu tadpoles to an avian predator: effect of body size and density. Herpetologica 47:316–321Google Scholar
  15. Diamond J (1989) Overview of recent extinctions. In: Western D, Pearl M (eds) Conservation for the twenty-first century. Oxford University Press, New York, pp 37–41Google Scholar
  16. Dodson SI (1989) Predator-induced reaction norms. Bioscience 39:447–452Google Scholar
  17. Drost CA, Fellers GM (1996) Collapse of a regional frog fauna in the Yosemite area of the California Sierra Nevada, USA. Conserv Biol 10:414–425CrossRefGoogle Scholar
  18. Fellers GM, Drost CA (1993) Disappearance of the cascades frog Rana cascadae at the southern end of its range, California, USA. Biol Conserv 65:177–181CrossRefGoogle Scholar
  19. Forsman A (1996) Body size and net energy gain in gape-limited predators: a model. J Herpetol 30:307–319Google Scholar
  20. Forsman A, Lindell LE (1993) The advantage of a big head: swallowing performance in adders, Vipera berus. Funct Ecol 7:183–189Google Scholar
  21. Fritts TH, Rodda GH (1998) The role of introduced species in the degradation of island ecosystems: a case history of Guam. Annu Rev Ecol Syst 29:113–140CrossRefGoogle Scholar
  22. Gotthard K, Nylin S (1995) Adaptive plasticity and plasticity as an adaptation: a selective review of plasticity in animal morphology and life history. Oikos 74:3–17Google Scholar
  23. Griffiths RA (1997) Temporary ponds as amphibian habitats. Aq Conserv Mar Fresh Ecosyst 7:119–126CrossRefGoogle Scholar
  24. Griffiths RA, Beebee T (1992) Decline and fall of the amphibians. New Sci 134:25–29Google Scholar
  25. Griffiths RA, Schley L, Sharp PE, Dennis JL, Romàn A (1998) Behavioural responses of Mallorcan midwife toad tadpoles to natural and unnatural snake predators. Anim Behav 55:207–214CrossRefPubMedGoogle Scholar
  26. Hamer AJ, Lane SJ, Mahony MJ (2002) The role of introduced mosquitofish (Gambusia holbrooki) in excluding the native green and golden bell frog (Litoria aurea) from original habitats in south-eastern Australia. Oecologia 132:445–452CrossRefGoogle Scholar
  27. Hayes MP, Jennings MR (1986) Decline of ranid frog species in western North America: are bullfrogs (Rana catesbeiana) responsible? J Herpetol 20:490–509Google Scholar
  28. Hemmer H, Alcover JA (eds) (1984) Historia biologica del ferreret. Editorial Moll, Palma de MallorcaGoogle Scholar
  29. de Jong G (1995) Phenotypic plasticity as a product of selection in a variable environment. Am Nat 145:493–512CrossRefGoogle Scholar
  30. Kats LB, Ferrer RP (2003) Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Divers Distrib 9:99–110CrossRefGoogle Scholar
  31. Kats LB, Petranka JW, Sih A (1988) Antipredator defenses and the persistence of amphibian larvae with fishes. Ecology 69:1865–1870Google Scholar
  32. Kiesecker JM, Blaustein AR (1997) Population differences in responses of red-legged frogs (Rana aurora) to introduced bullfrogs. Ecology 78:1752–1760Google Scholar
  33. Kupferberg SJ (1997) The role of larval diet in anuran metamorphosis. Am Zool 37:146–159Google Scholar
  34. Lawler SP (1989) Behavioural responses to predators and predation risk in four species of larval anurans. Anim Behav 38:1039–1047Google Scholar
  35. Lawler SP, Hero JM (1997) Palatability of Bufo marinus tadpoles to a predatory fish decreases with development. Wildl Res 24:327–334Google Scholar
  36. Lawler SP, Dritz D, Strange T, Holyoak M (1999) Effects of introduced mosquitofish and bullfrogs on the threatened Californian red-legged frog. Conserv Biol 13:613–622CrossRefGoogle Scholar
  37. Lea J, Dyson M, Halliday T (2002) The effects of cohort structure and density on larval growth and development in Alytes muletensis: implications for conservation. Herpetol J 12:155–164Google Scholar
  38. Lefcort H (1998) Adaptive, chemically mediated fright response in southern toad (Bufo terrestris) tadpoles. Copeia 1998:445–450Google Scholar
  39. McCollum SA, Leimberger JD (1997) Predator-induced morphological changes in an amphibian: predation by dragonflies affects tadpole shape and colour. Oecologia 109:615–621CrossRefGoogle Scholar
  40. McCollum SA, Van Buskirk J (1996) Costs and benefits of a predator-induced polyphenism in the gray tree frog, Hyla chrysocelis. Evolution 50:583–593Google Scholar
  41. Mehta RS (2003) Prey-handling behaviour of hatchling Elaphe helena (Colubridae). Herpetologica 59:469–474Google Scholar
  42. Moore RD (2002) The impact of introduced predators on the Mallorcan midwife toad (Alytes muletensis). PhD Thesis, University of Kent, CanterburyGoogle Scholar
  43. Moore RD, Griffiths RA, Romàn A (2004) Distribution of the Mallorcan midwife toad (Alytes muletensis) in relation to landscape topography and introduced predators. Biol Conserv 116:327–332CrossRefGoogle Scholar
  44. Moran NA (1992) The evolutionary maintenance of alternative phenotypes. Am Nat 139:971–989CrossRefGoogle Scholar
  45. O’Brien CM (2000) Plasticity and induced defences in tadpoles: the effects of an introduced predator on the Mallorcan midwife toad (Alytes muletensis). MSc Dissertation, University of Kent, CanterburyGoogle Scholar
  46. Pearl CA, Adams MJ, Schuytema GS, Nebeker AV (2003) Behavioral responses of anuran larvae to chemical cues of native and introduced predators in the Pacific northwestern United States. J Herpetol 37:572–576Google Scholar
  47. Peckarsky BL, Taylor BW, McIntosh AR, McPeek MA, Lytle DA (2001) Variation in mayfly size at metamorphosis as a development response to the risk of predation. Ecology 82:740–757Google Scholar
  48. Petranka JW, Kats LB, Sih A (1987) Predator-prey interactions among fish and larval amphibians: use of chemical cues to detect predatory fish. Anim Behav 35:420–425Google Scholar
  49. Relyea RA (2000) Trait-mediated indirect effects in larval anurans: reversing competitive outcomes with the threat of predation. Ecology 81:2278–2289Google Scholar
  50. Relyea RA (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:523–540Google Scholar
  51. Rodda GH, Fritts TH (1992) The impact of the introduction of the colubrid snake Boiga irregularis on Guam lizards. J Herpetol 26:166–174Google Scholar
  52. Rodriguez-Robles JA (2002) Feeding ecology of North American gopher snakes (Pituophis catenifer, Colubridae). Biol J Linn Soc 77:165–183CrossRefGoogle Scholar
  53. Román A (2002) Recompte de les poblacions naturals i introduïdes de ferreret (Alytes muletensis) en totes les localitats (2001). Government of the Balearic Islands, Palma de MallorcaGoogle Scholar
  54. Román A, Mayol J (1997) Documents tècnics de conservació. La recuperación del ferreret, Alytes muletensis. Proyecto life ferreret, Government of the Balearic Islands, Palma de MallorcaGoogle Scholar
  55. Savidge JA (1987) Extinction of an island forest avifauna by an introduced snake. Ecology 68:660–668Google Scholar
  56. Scheiner SM (1993) Genetics and evolution of phenotypic plasticity. Annu Rev Ecol Syst 24:35–68CrossRefGoogle Scholar
  57. Schley L, Griffiths RA (1998) Midwife toads (Alytes muletensis) avoid chemical cues from snakes (Natrix maura). J Herpetol 32:72–574Google Scholar
  58. Schley L, Griffiths RA, Romàn A (1998) Activity patterns and microhabitat selection of Mallorcan midwife toad (Alytes muletensis) tadpoles in natural torrent pools. Amphibia Reptilia 19:143–151Google Scholar
  59. Semlitsch RD, Gavasso S (1992) Behavioural responses of Bufo bufo and Bufo calamita tadpoles to chemical cues of vertebrate and invertebrate predators. Ethol Ecol Evol 4:165–173Google Scholar
  60. Semlitsch RD, Gibbons JW (1988) Fish predation in size-structured populations of treefrog tadpoles. Oecologia 75:321–326Google Scholar
  61. Shine R (1991) Intersexual dietary divergence and the evolution of sexual dimorphism in snakes. Am Nat 138:103–122CrossRefGoogle Scholar
  62. Skelly DK (2002) Experimental venue and estimation of interaction strength. Ecology 83:2097–2101Google Scholar
  63. Skelly DK, Kiesecker JM (2001) Venue and outcome in ecological experiments: manipulations of larval anurans. Oikos 94:198–208Google Scholar
  64. Skelly DK, Werner EE (1990) Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology 71:2313–2322Google Scholar
  65. Smith DC, Van Buskirk J (1995) Phenotypic design, plasticity and ecological performance in two tadpole species. Am Nat 145:211–233CrossRefGoogle Scholar
  66. Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. Freeman, New YorkGoogle Scholar
  67. Tejedo M (1993) Size-dependent vulnerability and behavioural responses of tadpoles of two anuran species to beetle larvae predators. Herpetologica 49:287–294Google Scholar
  68. Teplitsky C, Plenet S, Joly P (2003) Tadpoles’ responses to risk of fish introduction. Oecologia 134:270–277PubMedGoogle Scholar
  69. Thompson JD (1991) Phenotypic plasticity as a component of evolutionary change. Trends Ecol Evol 6:246–249CrossRefGoogle Scholar
  70. Tollrian R, Harvell CD (1999) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, N.J.Google Scholar
  71. Tonge SJ (1986) Collecting the Mallorcan midwife toad. Oryx 20:74–78Google Scholar
  72. Tonge SJ, Bloxam QMC (1991) The breeding programme for the Mallorcan midwife toad Alytes muletensis at the Jersey Wildlife Preservation Trust. Dodo 27:146–156Google Scholar
  73. Van Buskirk J (2000) The costs of an inducible defense in anuran larvae. Ecology 81:2813–2821Google Scholar
  74. Van Buskirk J, McCollum SA (1999) Plasticity and selection explain variation in tadpole phenotype between ponds with different predator composition. Oikos 85:31–39Google Scholar
  75. Van Buskirk J, McCollum SA (2000) Functional mechanisms of an inducible defense in tadpoles: morphology and behaviour influence mortality risk from predation. J Evol Biol 13:336–347CrossRefGoogle Scholar
  76. Van Buskirk J, Relyea RA (1998) Selection for phenotypic plasticity in Rana sylvatica tadpoles. Biol J Linn Soc 65:301–328CrossRefGoogle Scholar
  77. Van Buskirk J, Schmidt BR (2000) Predator-induced phenotypic plasticity in larval newts: trade-offs, selection, and variation in nature. Ecology 81:3009–3028Google Scholar
  78. Wilbur HM (1988) Interactions between growing predators and growing prey. In: Ebenmann B, Persson L (eds) Size-structured populations: ecology and evolution. Springer, Berlin Heidelberg New York, pp 157–172Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Robin D. Moore
    • 1
  • Richard A. Griffiths
    • 1
  • Cliona M. O’Brien
    • 1
  • Adam Murphy
    • 1
  • David Jay
    • 1
  1. 1.The Durrell Institute of Conservation and EcologyUniversity of KentCanterburyUK

Personalised recommendations