Evolutionary Ecology

, Volume 25, Issue 5, pp 993–1015 | Cite as

Behavioural elements reflect phenotypic colour divergence in a poison frog

Original Paper


The coexistence of both aposematic and cryptic morphs as different anti-predator strategies within a species seems to be an unusual phenomenon in nature. The strawberry poison frog, Oophaga pumilio, shows an astonishing colour diversity among populations in western Panama. In this study we selected a red and a green colour morph from two Panamanian islands (Isla Solarte and Isla Colón) for behavioural observations and measurements of conspicuousness. We found that red frogs were more visible to both conspecific frogs and potential predators than green frogs. Interestingly the difference in conspicuousness was most pronounced at the substrate that males used as principal calling places. Red males were more active and spent more time foraging than green males, which spent more time hidden. The association between conspicuousness of colouration and behaviour results in a more aposematic and a more cryptic anti-predator strategy. This is the first study which links differences in conspicuousness between animals on their natural backgrounds to differences in foraging as well as anti-predator behaviour and discusses the results in light of previous findings of toxicity analyses and potential costs and benefits of aposematism. To this end, our study adds a novel perspective for explaining extreme colour diversity between populations within an initially aposematic species.


Aposematism Crypsis Colour diversity Anti-predator strategy Oophaga pumilio Poison frog 



We thank Martine Maan, Adolfo Amezquita, Corinna Dreher and two anonymous referees who provided helpful insights on the manuscript. Rüdiger Brüning and Sönke von den Berg helped with figure preparation. We are especially grateful to Thomas Cronin from the University of Maryland who provided the sensitivity spectra for the photoreceptors of strawberry poison frogs and Nathan Hart from the University of Queensland who provided sensitivity spectra for the photoreceptors of blue tits.


  1. Anderson RP, Handley CO (2001) A new species of three-toed sloth (Mammalia: Xenarthra) from Panama, with a review of the genus Bradypus. Proc Biol Soc Wash 114:1–33Google Scholar
  2. Bernays EA, Singer M (2002) Contrasted foraging in two species of polyphagous caterpillars. Acta Zool Academ Sci Hung 48:117–135Google Scholar
  3. Bezzerides AL, McGraw KJ, Parker RS, Hussein J (2007) Elytra color as signal of chemical defense in the Asian ladybird beetle Harmonia axyridis. Behav Ecol Sociobiol 61:1401–1408CrossRefGoogle Scholar
  4. Brodie ED (1989) Genetic correlations between morphology and anti-predator behaviour in natural populations of the garter snake Thamnophis ordinoides. Nature 342:542–543PubMedCrossRefGoogle Scholar
  5. Caldwell JP (1996) The evolution of myrmecophagy and its correlates in poison frogs (family Dendrobatidae). J Zool Lond 240:75–101CrossRefGoogle Scholar
  6. Chamberlain NL, Hill R, Kapan DD, Gilbert LE, Kronforst MR (2009) Polymorphic butterfly reveals the missing link in ecological speciation. Science 326:847–850PubMedCrossRefGoogle Scholar
  7. Chiao C-C, Vorobyev M, Cronin TW, Osorio D (2000) Spectral tuning of dichromats to natural scenes. Vis Res 40:3257–3271PubMedCrossRefGoogle Scholar
  8. Cooper WE, Avalos A (2010) Escape decisions by the syntopic congeners Sceloporus jarrovii and S. virgatus: Comparative effects of perch height and of predator approach speed, persistence and direction of turning. J Herpetol 44:425–430CrossRefGoogle Scholar
  9. Cooper WE, Caldwell JP, Vitt LJ (2009) Risk assessment and withdrawal behaviour by two species of aposematic poison frogs, Dendrobates auratus and Oophaga pumilio, on forest trails. Ethology 115:311–320CrossRefGoogle Scholar
  10. Cummings ME, Jordao JM, Cronin TW, Oliveira RF (2008) Visual ecology of the fiddler crab, Uca tangeri: effects of sex, viewer and background on conspicuousness. Anim Behav 75:175–188CrossRefGoogle Scholar
  11. Curio E (1970) Validity of the selective coefficient of a behaviour trait in hawkmoth larvae. Nature 228:382PubMedCrossRefGoogle Scholar
  12. Cuthill IC, Bennett ATD, Partridge JC, Maier EJ (1999) Plumage reflectance and the objective assessment of avian sexual dichromatism. Am Nat 160:183–200CrossRefGoogle Scholar
  13. Daly JW, Myers CW (1967) Toxicity of Panamanian poison frogs (Dendrobates): some biological and chemical aspects. Science 156:970–973PubMedCrossRefGoogle Scholar
  14. Endler JA (1990) On the measurement and classification of colour in studies of animal colour pattern. Biol J Linn Soc 41:315–352CrossRefGoogle Scholar
  15. Grant T, Frost DR, Caldwell JP, Gagliardo R, Haddad CFB, Kok PRJ, Means DB, Noonan BP, Schargel WE, Wheeler WC (2006) Phylogenetic systematics of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bull Am Mus Nat Hist 299:6–262CrossRefGoogle Scholar
  16. Hagemann S, Pröhl H (2007) Mitochondrial paraphyly in a polymorphic poison frog species (Dendrobatidae; D. pumilio). Mol Phyl Evol 45:740–747CrossRefGoogle Scholar
  17. Hart NS (2001a) Variations in cone photoreceptor abundance and the visual ecology of birds. J Comp Physiol A 187:685–698PubMedCrossRefGoogle Scholar
  18. Hart NS (2001b) The visual ecology of avian photoreceptors. Prog Retinal Eye Res 20:281–322CrossRefGoogle Scholar
  19. Hart NS, Partridge JC, Cuthill IC (1998) Visual pigments, oil droplets and cone photorezeptor distribution in the European Starling (Sturnus vulgaris). J Exp Biol 201:1433–1446PubMedGoogle Scholar
  20. Hart NS, Partridge JC, Cuthill IC, Bennett ATD (2000) Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L.) and the Blackbird (Turdus merula L.). J Comp Physiol A 186:375–387PubMedCrossRefGoogle Scholar
  21. Hoekstra HE, Hirschmann RJ, Bundey RA, Insel PA, Crossland JP (2006) A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313:101–104PubMedCrossRefGoogle Scholar
  22. Jackson JF, Ingram W III, Campbell HW (1976) The dorsal pigmentation pattern of snakes as an anti-predator strategy: a multivariate approach. Am Nat 110:1029–1053CrossRefGoogle Scholar
  23. Jiggins CD (2008) Ecological speciation in mimetic butterflies. Bioscience 58:541–547CrossRefGoogle Scholar
  24. Jiggins CD, Naisbit RE, Coe RL, Mallet J (2001) Reproductive isolation caused by colour pattern mimicry. Nature 411:302–305PubMedCrossRefGoogle Scholar
  25. Joron M, Mallet JLB (1998) Diversity in mimicry: paradox or paradigm. Trends Ecol Evol 13:461–466PubMedCrossRefGoogle Scholar
  26. Lehner PN (1979) Handbook of ethological methods. Garland STPM Press, New York, LondonGoogle Scholar
  27. Lindquist N, Hay ME (1996) Palatability and chemical defense of marine invertebrate larvae. Ecol Monogr 66:431–450CrossRefGoogle Scholar
  28. Livezey BC, Zusi RL (2007) Higher order phylogeny of modern birds. Zool J Linn Soc London 149:1–95CrossRefGoogle Scholar
  29. Maan ME, Cummings ME (2008) Female preferences for aposematic signal components in a polymorphic poison frog. Evolution 62:2334–2345PubMedCrossRefGoogle Scholar
  30. Maan ME, Cummings ME (2009) Sexual dimorphism and directional sexual selection on aposematic signals in a poison frog. Proc Natl Acad Sci USA 105:19072–19077CrossRefGoogle Scholar
  31. Mappes J, Marples N, Endler JA (2005) The complex business of survival by aposematism. Trends Ecol Evol 20:598–603PubMedCrossRefGoogle Scholar
  32. Marples NM, Vanveelen W, Brakefield PM (1994) The relative importance of color, taste and smell in the protection of an aposematic insect Coccinella septempunctata. Anim Behav 48:967–974CrossRefGoogle Scholar
  33. Master TL (1999) Predation by Rufous Motmot on black-and-green poison dart frog. Wilson Bull 111:439–440Google Scholar
  34. Merilaita S, Tullberg B (2005) Constrained camouflage facilitates the evolution of conspicuous warning colouration. Evolution 59:38–45PubMedGoogle Scholar
  35. Mochida K (2009) A parallel geographical mosaic of morphological and behavioural aposematic traits of the newt, Cynops pyrrhogaster (Urodela: Salamandridae). Biol J Linn Soc 97:613–622CrossRefGoogle Scholar
  36. Muñoz AG, Salazar C, Castano J, Jiggins CD, Linares M (2010) Multiple sources of reproductive isolation in a bimodal butterfly hybrid zone. J Evol Biol 23:1312–1320PubMedCrossRefGoogle Scholar
  37. Myers CW, Daly JW (1983) Dart-poison frogs. Sci Am 248(Feb):96–105Google Scholar
  38. Osorio D, Miklosi A, Gonda Z (1999) Visual ecology and perception of colouration patterns by domestic chicks. Evol Ecol 13:673–689CrossRefGoogle Scholar
  39. Pough FH, Taigen TL (1990) Metabolic correlates of the foraging and social behaviour of dart-poison frogs. Anim Behav 39:145–155CrossRefGoogle Scholar
  40. Poulton EB (1890) The colours of animals: their meaning and use especially considered in the case of insects. Kegan Paul, Trench, Trubner and Co. Ltd, London, UKGoogle Scholar
  41. Pröhl H, Hödl W (1999) Parental investment, potential reproductive rates and mating system in the strawberry dart-poison frog Dendrobates pumilio. Behav Ecol Sociobiol 46:215–220CrossRefGoogle Scholar
  42. Reynolds RG, Fitzpatrick BM (2007) Assortative mating in poison-dart frogs based on an ecologically important trait. Evolution 61:2253–2259PubMedCrossRefGoogle Scholar
  43. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  44. Rosenblum EB (2006) Convergent evolution and divergent selection in lizards at the white sands ecotone. Am Nat 167:1–15PubMedCrossRefGoogle Scholar
  45. Ruxton GD, Sherratt TN, Speed M (2004) Avoiding attack. The evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, Oxford, UKGoogle Scholar
  46. Ruxton GD, Speed MP, Broom M (2009) Identifying the ecological conditions that select for intermediate levels of aposematic signalling. Evol Ecol 23:491–501CrossRefGoogle Scholar
  47. Santos JC, Coloma LA, Cannatella DC (2003) Multiple, recurring origins of aposematism and diet specialization in poison frogs. Proc Natl Acad Sci USA 100:12792–12797PubMedCrossRefGoogle Scholar
  48. Saporito RA, Garraffo HM, Donnelly MA, Edwards AL, Longino JT, Daly JW (2004) Formicine ants: an arthropod source for the pumiliotoxin alkaloids of dendrobatid poison frogs. Proc Natl Acad Sci USA 101:8045–8050PubMedCrossRefGoogle Scholar
  49. Saporito RA, Donnelly MA, Jain P, Garraffo HM, Spande TF, Daly JW (2007a) Spatial and temporal patterns of alkaloid variation in the poison frog Oopahaga pumilio in Costa Rica and Panama over 30 years. Toxicon 50:757–778PubMedCrossRefGoogle Scholar
  50. Saporito RA, Donnnelly MA, Norton RA, Garraffo HM, Spande TF, Daly JW (2007b) Oribatid mites as a major dietary source for alkaloids in poison frogs. Proc Natl Acad Sci USA 104:8885–8890PubMedCrossRefGoogle Scholar
  51. Saporito RA, Zuercher R, Roberts M, Gerow K, Donnelly M (2007c) Experimental evidence for Aposematism in the Dendrobatid Poison Frog Oophaga pumilio. Copeia 4:1006–1011CrossRefGoogle Scholar
  52. Savage JM (2002) The amphibians and reptiles of Costa Rica. University Chicago Press, ChicagoGoogle Scholar
  53. Siddiqi A, Cronin TW, Loew ER, Vorobyev M, Summers K (2004) Interspecific and intraspecific views of color signals in the Strawberry Poison Frog Dendrobates pumilio. J Exp Biol 207:2471–2485PubMedCrossRefGoogle Scholar
  54. Speed MP, Ruxton GD (2005) Aposematism: what should our starting point be? Proc R Soc B 272:431–438PubMedCrossRefGoogle Scholar
  55. Speed MP, Ruxton GD (2007) How bright and now nasty: explaining diversity in warning signal strength. Evolution 61:623–635PubMedCrossRefGoogle Scholar
  56. Stamp NE, Wilkens RT (1993) On the cryptic side of life: being unapparent to enemies and the consequences for foraging and growth in caterpillars. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman and Hall, New York, pp 283–330Google Scholar
  57. Stankovich T, Blumstein DT (2005) Fear in animals: a meta-analysis and review of risk assessment. Proc R Soc B 272:2627–2634CrossRefGoogle Scholar
  58. Staudt K, Meneses Ospina S, Mebs D, Pröhl H (2010) Foraging behaviour and territoriality of the strawberry poison frog (Oophaga pumilio) in dependence of the presence of ants. Amphibia Reptilia 31:217–227CrossRefGoogle Scholar
  59. Stuart-Fox DM, Moussalli A, Marshall NJ, Owens IPF (2003) Conspicuous males suffer higher predation risk: visual modelling and experimental evidence from lizards. Anim Behav 66:541–550CrossRefGoogle Scholar
  60. Summers K, Clough M (2001) The evolution of coloration and toxicity in the poison frog family (Dendrobatidae). Proc Natl Acad Sci USA 98:6227–6232PubMedCrossRefGoogle Scholar
  61. Summers K, Bermingham E, Weigt L, McCafferty S, Dahlstrom L (1997) Phenotypic and genetic divergence in three species of dart-poison frogs with contrasting parental behavior. J Hered 88:8–13PubMedGoogle Scholar
  62. Summers K, Symula R, Clough M, Cronin T (1999) Visual mate choice in poison frogs. Proc R Soc Lond B 266:2141–2145CrossRefGoogle Scholar
  63. Summers K, Cronin TW, Kennedy T (2003) Variation in spectral reflectance among populations of Dendrobates pumilio, the strawberry poison frog, in the Bocas del Toro Archipelago, Panama. J Biogeogr 30:35–53CrossRefGoogle Scholar
  64. Sword GA (2002) A role for phenotypic plasticity in the evolution of aposematism. Proc R Soc Lond B 269:1639–1644CrossRefGoogle Scholar
  65. Théry M, Debut M, Gomez D, Casas J (2004) Specific color sensitivities of prey and predator explain camouflage in different visual systems. Behav Ecol 16:25–29CrossRefGoogle Scholar
  66. Toft CA (1995) Evolution of diet specialization in poison dart frogs. Herpetologica 51:202–216Google Scholar
  67. Vorobyev M, Osorio D (1998) Receptor noise as a determinant of receptor thresholds. Proc R Soc Lond B 265:351–358CrossRefGoogle Scholar
  68. Vorobyev M, Osorio D, Bennett ATD, Marshall NJ, Cuthill IC (1998) Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A 183:621–633PubMedCrossRefGoogle Scholar
  69. Wallace AR (1889) Darwinism–an exposition of the theory of natural selection with some of its applications. MacMillan & Co., London, UKGoogle Scholar
  70. Wang IJ, Shaffer HB (2008) Rapid color evolution in an aposematic species: a phylogenetic analysis of color variation in the strikingly polymorphic strawberry poison-dart frog. Evolution 62:2742–2759PubMedCrossRefGoogle Scholar
  71. Wells KD (2007) The ecology and behaviour of amphibians. University of Chicago Press, Chicago and LondonGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Institute of ZoologyUniversity of Veterinary Medicine of HannoverHannoverGermany

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