Evolutionary Ecology

, Volume 27, Issue 4, pp 783–795 | Cite as

No evidence for differential survival or predation between sympatric color morphs of an aposematic poison frog

  • Corinne L. Richards-Zawacki
  • Justin Yeager
  • Henry P. S. Bart
Original Paper


Because variation in warning signals slows down the predator education process, aposematic theory predicts that animal warning signals should be monomorphic. Yet, warning color polytypisms are not uncommon in aposematic species. In cases where warning signal variants are separated geographically, adaptation to local predators could explain this variation. However, this cannot explain the persistence of sympatric polymorphisms in aposematic taxa. The strawberry poison frog (Oophaga pumilio) exhibits both allopatric and sympatric warning color variation in and around the Bocas del Toro archipelago of Panama. One explanation that has been proposed for the rapid diversification of O. pumilio coloration in this archipelago is low predation; if island populations have few predators, stabilizing selection would be relaxed opening the door for diversification via selection or genetic drift. Using a combination of mark-recapture and clay model studies, we tested for differences in survival and predation among sympatric red and yellow color morphs of O. pumilio from Bastimentos Island. We found no evidence for differential survival or predation in this population, despite the fact that one morph (red) is more common and widely distributed than the other (yellow). Even in an area of the island where the yellow morph is not found, predator attack rates were similar among morphs. Visual modeling suggests that yellow and red morphs are distinguishable and conspicuous against a variety of backgrounds and by viewers with different visual systems. Our results suggest that general avoidance by predators of red and yellow, both of which are typical warning colors used throughout the animal kingdom, may be contributing to the apparent stability of this polymorphism.


Color polymorphism Polytypism Aposematism Bocas del Toro Dendrobates pumilio Predation Survival 



We thank Narissa Bax, Sebastian Castillo, Ricardo Cossio, Anisha Devar, Deyvis Gonzalez, Eli Hornstein, Danny Lenger, Tom Richards, Becky Richards, Eric Rightley, Tracy Stetzinger, Geoff Zawacki and Amanda Zellmer for help with the mark-recapture study and to Anisha Devar for help with the predation experiment. The STRI provided logistical support for this project and we are particularly grateful to Gabriel Jacome and Plinio Gondola of the Bocas del Toro Field Station. This study was financially supported by short-term fellowships from STRI to CLRZ and JY, postdoctoral fellowships from the National Science Foundation (Award No. 0801165) and the University of California President’s office to CLRZ, and a Tulane Dean’s grant to HPSB. The Panamanian National Authority for the Environment (ANAM) provided research permission for this study. This work complied with IACUC protocols (University of Michigan No. 09765, Tulane University No. 0832 and STRI No. 2007-17-12-15-07).

Supplementary material

10682_2013_9636_MOESM1_ESM.docx (392 kb)
Supplementary material 1 (DOCX 392 kb)


  1. Anderson DR, Burnham KP (2002) Avoiding pitfalls when using information-theoretic methods. J Wildl Manage 66:912–918Google Scholar
  2. Brodie ED III (1993) Differential avoidance of coral snake banded patterns by free-ranging avian predators in Costa Rica. Evolution 47:227–235CrossRefGoogle Scholar
  3. Brown JL, Twomey E, Amézquita A, De Souza MB, Caldwell JP, Lötters S, Von May R, Melo-Sampaio PR, Mejía-Vargas D, Perez-Pena P, Pepper M, Poelman EH, Sanchez-Rodriguez M, Summers K (2011) A taxonomic revision of the Neotropical poison frog genus Ranitomeya (Amphibia: Dendrobatidae). Zootaxa 3083:1–120Google Scholar
  4. Chouteau M, Angers B (2011) The role of predators in maintaining the geographic organization of aposematic signals. Am Nat 178:810–817PubMedCrossRefGoogle Scholar
  5. Chouteau M, Angers B (2012) Wright’s shifting balance theory and the diversification of aposematic signals. PLoS ONE 7:e34028PubMedCrossRefGoogle Scholar
  6. Chouteau M, Summers K, Morales V, Angers B (2011) Advergence in Müllerian mimicry: the case of the poison dart frogs of Northern Peru revisited. Biol Lett 7:796–800PubMedCrossRefGoogle Scholar
  7. Cummings ME, Jordão 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
  8. Daly JW, Myers CW (1967) Toxicity of Panamanian poison frogs (Dendrobates): some biological and chemical aspects. Science 156:970–973PubMedCrossRefGoogle Scholar
  9. Endler JA, Mielke PW (2005) Comparing entire colour patterns as birds see them. Biol J Linn Soc 86:405–431CrossRefGoogle Scholar
  10. Gomez D (2006) AVICOL, a program to analyse spectrometric data. Available from Accessed Sept 2012
  11. Gray HM, Christy JH (2000) Predation by the grapsid crab, Armastes angustum (Smith, 1870), on tadpoles of the green poison frog, Dendrobates auratus Girard, 1855. Crustaceana 73:1023–1025CrossRefGoogle Scholar
  12. Hart NS, Vorobyev M (2005) Modeling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors. J Comp Physiol A 191:381–392CrossRefGoogle Scholar
  13. Hegna RH, Saporito RA, Gerow KG, Donnelly MA (2011) Contrasting colors of an aposematic poison frog do not affect predation. Ann Zool Fennici 48:29–38CrossRefGoogle Scholar
  14. Hegna RH, Saporito RA, Donnelly MA (2012) Not all colors are equal: predation and color polytypism in the aposematic poison frog Oophaga pumilio. Evol Ecol Online First. doi: 10.1007/s10682-012-9605-z Google Scholar
  15. Hemmi JM, Marshall J, Pix W, Vorobyev M, Zeil J (2006) The variable colours of the fiddler crab Uca vomeris and their relation to background and predation. J Exp Biol 209:4140–4153PubMedCrossRefGoogle Scholar
  16. Jordão JM, Cronin TW, Oliveira RF (2007) Spectral sensitivity of four species of fiddler crabs (Uca pugnax, Uca pugilator, Uca vomeris and Uca tangeri) measured by in situ microspectrophotometry. J Exp Biol 210:447–453PubMedCrossRefGoogle Scholar
  17. Joron M, Mallet J (1998) Diversity in mimicry: paradox or paradigm? Trends Ecol Evol 13:461–466PubMedCrossRefGoogle Scholar
  18. Kalmus H, Maynard Smith S (1966) Some evolutionary consequences of pegmatypic mating systems (imprinting). Am Nat 100:619–635CrossRefGoogle Scholar
  19. Maan ME, Cummings ME (2008) Female preferences for aposematic signal components in a polymorphic poison frog. Evolution 62:2334–2345PubMedCrossRefGoogle Scholar
  20. Maan ME, Cummings ME (2009) Sexual dimorphism and directional sexual selection on aposematic signals in a poison frog. Proc Natl Acad Sci USA 106:19072–19077PubMedCrossRefGoogle Scholar
  21. Maan ME, Cummings ME (2012) Poison frog colors are honest signals of toxicity, particularly for bird predators. Am Nat 179:E1–E14PubMedCrossRefGoogle Scholar
  22. Mappes J, Alatalo RV (1997) Effects of novelty and gregariousness in survival of aposematic prey. Behav Ecol 8:174–177CrossRefGoogle Scholar
  23. Mappes J, Marples N, Endler J (2005) The complex business of survival by aposematism. Trends Ecol Evol 20:598–603PubMedCrossRefGoogle Scholar
  24. Marples NM, Roper TJ, Harper DGC (1998) Responses of wild birds to novel prey: evidence of dietary conservatism. Oikos 83:161–165CrossRefGoogle Scholar
  25. Noonan BP, Comeault AA (2009) The role of predator selection on polymorphic aposematic poison frogs. Biol Lett 5:51–54PubMedCrossRefGoogle Scholar
  26. Poulton EB (1890) The colours of animals. Kegan Paul, Trench, Trübner and Co. Ltd., LondonGoogle Scholar
  27. Pröhl H, Berke O (2001) Spatial distributions of male and female strawberry poison frogs and their relation to female reproductive resources. Oecologia 129:534–542Google Scholar
  28. Pröhl H, Ostrowski T (2011) Behavioural elements reflect phenotypic colour divergence in a poison frog. Evol Ecol 25:993–1015Google Scholar
  29. Przeczek K, Mueller C, Vamosi SM (2008) The evolution of aposematism is accompanied by increased diversification. Integr Zool 3:149–156PubMedCrossRefGoogle Scholar
  30. Reynolds RG, Fitzpatrick BM (2007) Assortative mating in poison-dart frogs based on an ecologically important trait. Evolution 61:2253–2259PubMedCrossRefGoogle Scholar
  31. Richards-Zawacki CL, Cummings ME (2011) Intraspecific reproductive character displacement in a polymorphic poison dart frog, Dendrobates pumilio. Evolution 65:259–267PubMedCrossRefGoogle Scholar
  32. Richards-Zawacki CL, Wang IJ, Summers K (2012) Mate choice and the genetic basis for colour variation in a polymorphic dart frog: inferences from a wild pedigree. Mol Ecol 21:3879–3892PubMedCrossRefGoogle Scholar
  33. Rudh A, Rogell B, Hastad O, Qvarnstrom A (2011) Rapid population divergence linked with co-variation between coloration and sexual display in strawberry poison frogs. Evolution 65:1271–1282Google Scholar
  34. Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, New YorkCrossRefGoogle Scholar
  35. Ruxton GD, Franks DW, Balogh ACV, Leimar O, Van Baalen M (2008) Evolutionary implications of the form of predator generalization for aposematic signals and mimicry in prey. Evolution 62:2913–2921PubMedCrossRefGoogle Scholar
  36. Saporito RA, Donnelly MA, Garraffo HM, Spande TF, Daly JW (2006) Geographic and seasonal variation in alkaloid-based chemical defenses of Dendrobates pumilio from Bocas del Toro, Panama. J Chem Ecol 32:795–814PubMedCrossRefGoogle Scholar
  37. Saporito RA, Zuercher R, Roberts M, Gerow KG, Donnelly MA (2007) Experimental evidence for aposematism in the dendrobatid poison frog Oophaga pumilio. Copeia 2007:1006–1011CrossRefGoogle Scholar
  38. Schuler W, Roper TJ (1992) Responses to warning coloration in avian predators. Adv Stud Behav 21:111–146CrossRefGoogle Scholar
  39. Seiger MB (1967) A computer simulation study of the influence of imprinting on population structure. Am Nat 101:47–57CrossRefGoogle Scholar
  40. 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
  41. Skelhorn J (2011) Colour biases are a question of conspecifics’ taste. Anim Behav 81:825–829CrossRefGoogle Scholar
  42. Smith SM (1975) Innate recognition of coral snake pattern by a possible avian predator. Science 187:759–760PubMedCrossRefGoogle Scholar
  43. 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 88:8–13PubMedCrossRefGoogle Scholar
  44. Summers K, Symula R, Clough M, Cronin T (1999) Visual mate choice in poison frogs. Proc R Soc Lond B 266:2141–2145CrossRefGoogle Scholar
  45. Tazzyman SJ, Iwasa Y (2010) Sexual selection can increase the effect of random genetic drift: a quantitative genetic model of polymorphism in Oophaga pumilio, the strawberry poison-dart frog. Evolution 64:1719–1728PubMedCrossRefGoogle Scholar
  46. Verzijden MN, Lachlan RF, Servedio MR (2005) Female mate-choice behavior and sympatric speciation. Evolution 59:2097–2108PubMedGoogle Scholar
  47. Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc Lond B 265:351–358CrossRefGoogle Scholar
  48. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:120–139CrossRefGoogle Scholar
  49. Yeager J, Wooten C, Summers K (2011) A new technique for the production of large numbers of clay models for field studies of predation. Herpetol Rev 42:357–359Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Corinne L. Richards-Zawacki
    • 1
    • 2
  • Justin Yeager
    • 1
  • Henry P. S. Bart
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyTulane UniversityNew OrleansUSA
  2. 2.Smithsonian Tropical Research InstitutePanamaRepublica de Panama

Personalised recommendations