Advertisement

Evolutionary Ecology

, Volume 27, Issue 5, pp 831–845 | Cite as

Not all colors are equal: predation and color polytypism in the aposematic poison frog Oophaga pumilio

  • Robert H. Hegna
  • Ralph A. Saporito
  • Maureen A. Donnelly
Original Paper

Abstract

Aposematic organisms are not predicted to show high levels of warning signal diversity because they are expected to be under stabilizing selection to decrease costs of ‘educating’ predators about their unpalatability. However, systematic changes in warning signals (polytypism) can be expected if they represent adaptations to local predators. The aposematic strawberry poison frog (Oophaga pumilio) is red throughout its mainland distribution in Costa Rica and Panamá, but displays high levels of warning signal diversity in the Bocas del Toro Archipelago of Panamá. Both coloration and spot pattern vary in a polytypic sense. Sexual selection contributes to maintaining the polytypism, but little work has investigated the potential influence of predation. We used unspotted models of O. pumilio to determine if predation might help explain the color polytypism on Isla Colón in the Bocas del Toro Archipelago of Panamá. We tested whether attack rates differed among the red mainland morph, green/yellow Isla Colón morph, and the brown control. We found that frog color significantly predicted being attacked. The local green Isla Colón models were attacked more than foreign red or brown models. No difference in attack rate existed between red and brown control models. Our results suggest that the red mainland morph possesses a more effective warning signal, even when it is not the local morph. Honest signaling of unpalatability, neophobia, and the use of search images by local predators are potential explanations. Similarity of the brown model to other local poison frogs might explain the lower attack rate compared to previous work. The attack rate was lower on Isla Colón compared to mainland Costa Rica, which supports the hypothesis that less overall predation in the Bocas del Toro Archipelago may contribute to the overall warning signal diversity in O. pumilio there by relaxing selection for aposematic traits.

Keywords

Color polymorphism Conspicuous coloration Dendrobates pumilio Dendrobatidae Model experiment Bocas del Toro Honest signaling 

Notes

Acknowledgments

We thank the Smithsonian Tropical Research Institute (STRI) Bocas del Toro field station and the Institute for Tropical Ecology and Conservation (ITEC) for valuable logistical support. This work was completed with official permission from the Autoridad Nacional del Ambiente (ANAM permit number SE/A-68-08). Jonathan R. Hegna and Humberto Vlades provided assistance in field work preparations. Janna Goldrup’s work at ITEC contributed, in part, to the idea for this study. The manuscript was improved by helpful comments from Johanna Mappes, Craig Guyer, Mike Heithaus, Frank Hensley, Natalie Hyslop, Thomas R. Jones, Monica Isola, Seiichi Murasaki, A. Justin Nowakowski, Kelsey Reider, Janne Valkonen, Steven Whitfield, and the herpetology group at John Carroll University. The manuscript also benefitted from suggestions by editors John Endler and Manuel Leal, along with the anonymous reviewers. We thank Mikael Puurtinen for discussions about the implications of their numerical model. Kenneth G. Gerow graciously provided statistical consulting. Funding was provided by the American Society of Ichthyologists and Herpetologists, the Judith Parker Travel Fund, Organization for Tropical Studies, Greater Cincinnati Herpetological Society, and the Chicago Herpetological Society. A National Science Foundation Postdoctoral Research Fellowship partially supported RAS. This paper is contribution 237 to the program in Tropical Biology at Florida International University.

References

  1. Alves-Costa CP, Lopes AV (2001) Using artificial fruits to evaluate fruit selection by birds in the field. Biotropica 33:713–717Google Scholar
  2. Anderson RP, Charles O, Handley JR (2002) Dwarfism in insular sloths: biogeography, selection, and evolutionary rate. Evolution 56:1045–1058PubMedGoogle Scholar
  3. Aoki M, Izawa E, Koga K, Yanagihara S, Matsushima T (2000) Accurate visual memory of colors in controlling the pecking behavior of quail chicks. Zool Sci 17:1053–1059PubMedCrossRefGoogle Scholar
  4. Aronsson M, Gamberale-Stille G (2008) Domestic chicks primarily attend to colour, not pattern, when learning an aposematic coloration. Anim Behav 75:417–423CrossRefGoogle Scholar
  5. Blough P (1992) Detectability and choice during visual search: joint effects of sequential priming and discriminability. Learn Behav 20:293–300CrossRefGoogle Scholar
  6. Blount JD, Speed MP, Ruxton GD, Stephens PA (2009) Warning displays may function as honest signals of toxicity. Proc R Soc Lond B 276:871–877Google Scholar
  7. Bond AB, Riley DA (1991) Searching image in the pigeon: a test of three hypothetical mechanisms. Ethology 87:203–224CrossRefGoogle Scholar
  8. Branham M, Wenzel JW (2003) The origin of photic behavior and the evolution of sexual communication in fireflies (Coleoptera: Lampyridae). Cladistics 19:1–22CrossRefGoogle Scholar
  9. Brodie ED III (1993) Differential avoidance of coral snake banded patterns by free-ranging avian predators in Costa Rica. Evolution 47:227–235CrossRefGoogle Scholar
  10. Brower LP, Brower VZJ, Stiles FG, Croze HJ, Hower AS (1964) Mimicry: differential advantage of color patterns in the natural environment. Science 144:183PubMedCrossRefGoogle Scholar
  11. Brown JL, Maan ME, Cummings ME, Summers K (2010) Evidence for selection on coloration in a Panamánian poison frog: a coalescent-based approach. J Biogeogr 37:891–901CrossRefGoogle Scholar
  12. Chouteau M, Angers B (2012) Wright’s shifting balance theory and the diversification of aposematic signals. PLoS ONE 7:e34028PubMedCrossRefGoogle Scholar
  13. Cook LM, Brower LP, Alcock J (1969) An attempt to verify mimetic advantage in a neotropical environment. Evolution 23:339–345CrossRefGoogle Scholar
  14. Cortesi F, Cheney KL (2010) Conspicuousness is correlated with toxicity in marine opisthobranchs. J Evol Biol 23:1509–1518PubMedCrossRefGoogle Scholar
  15. Cuthill IC, Stevens M, Sheppard J, Maddocks T, Parraga CA, Troscianko TS (2005) Disruptive coloration and background pattern matching. Nature 434:72–74PubMedCrossRefGoogle Scholar
  16. Daly JW, Myers CW (1967) Toxicity of Panamánian poison frogs (Dendrobates): some biological and chemical aspects. Science 156:970–973PubMedCrossRefGoogle Scholar
  17. Darst CR, Cummings ME, Cannatella DC (2006) A mechanism for diversity in warning signals: conspicuousness versus toxicity in poison frogs. Proc Natl Acad Sci USA 103:5852–5857PubMedCrossRefGoogle Scholar
  18. Endler JA (1993) The color of light in forests and its implications. Ecol Monogr 63:1–27CrossRefGoogle Scholar
  19. Endler JA, Mappes J (2004) Predator mixes and the conspicuousness of aposematic signals. Am Nat 163:532–547PubMedCrossRefGoogle Scholar
  20. Exnerová A, Landova E, Stys P, Fuchs R, Prokopova M, Cehlarikova P (2003) Reactions of passerine birds to aposematic and non-aposematic firebugs (Pyrrhocoris apterus; Heteroptera). Biol J Linn Soc 78:517–525CrossRefGoogle Scholar
  21. Gittleman JL, Harvey PH (1980) Why are distasteful prey not cryptic? Nature 286:149–150CrossRefGoogle Scholar
  22. Grant T, Frost DR, Caldwell JP, Gagliardo RON, Haddad CFB, Kok PJR, 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 299:1–262CrossRefGoogle Scholar
  23. Hegna RH (2009) Aposematism in the strawberry poison frog Oophaga pumilio: The effect of pattern, color, and frog density on predation. Thesis, Florida International UniversityGoogle Scholar
  24. Hegna RH, Saporito RA, Gerow KG, Donnelly MA (2011) Contrasting colors of an aposematic poison frog do not affect predation. Ann Zool Fenn 48:29–38CrossRefGoogle Scholar
  25. Joron M, Mallet JLB (1998) Diversity in mimicry: paradox or paradigm? Trends Ecol Evol 13:461–466PubMedCrossRefGoogle Scholar
  26. Lindstedt C, Eager H, Ihalainen E, Kahilainen A, Stevens M, Mappes J (2011) Direction and strength of selection by predators for the color of the aposematic wood tiger moth. Behav Ecol 22:580–587CrossRefGoogle Scholar
  27. Lindström L, Alatalo RV, Lyytinen A, Mappes J (2001) Strong antiapostatic selection against novel rare aposematic prey. Proc Natl Acad Sci USA 98:9181–9184PubMedCrossRefGoogle Scholar
  28. Maan ME, Cummings ME (2008) Female preferences for aposematic signal components in a polymorphic poison frog. Evolution 62:2334–2345PubMedCrossRefGoogle Scholar
  29. Maan ME, Cummings ME (2012) Poison frog colors are honest signals of toxicity, particularly for bird predators. Am Nat 179:E1–E14PubMedCrossRefGoogle Scholar
  30. Mallet J, Barton NH (1989) Strong natural selection in a warning-color hybrid zone. Evolution 43:421–431CrossRefGoogle Scholar
  31. Mappes J, Alatalo RV (1997) Effects of novelty and gregariousness in survival of aposematic prey. Behav Ecol 8:174–177CrossRefGoogle Scholar
  32. Mappes J, Marples N, Endler JA (2005) The complex business of survival by aposematism. Trends Ecol Evol 20:598–603PubMedCrossRefGoogle Scholar
  33. Marples NM, Roper TJ, Harper DGC (1998) Responses of wild birds to novel prey: evidence of dietary conservatism. Oikos 83:161–165CrossRefGoogle Scholar
  34. Myers CW, Daly JW (1983) Dart-poison frogs. Sci Am 248:120–133PubMedCrossRefGoogle Scholar
  35. Nokelainen O, Hegna RH, Reudler JH, Lindstedt C, Mappes J (2012) Trade-off between warning signal efficacy and mating success in the wood tiger moth. Proc R Soc Lond B 279:257–265Google Scholar
  36. Noonan BP, Comeault AA (2009) The role of predator selection on polymorphic aposematic poison frogs. Biol Lett 5:51–54PubMedCrossRefGoogle Scholar
  37. Osorio D, Vorobyev M (2005) Photoreceptor spectral sensitivities in terrestrial animals: adaptations for luminance and colour vision. Proc R Soc Lond B 272:1745–1752Google Scholar
  38. Poulin B, Lefebvre G, Ibanez R, Jaramillo C, Hernandez C, Rand AS (2001) Avian predation upon lizards and frogs in a neotropical forest understorey. J Trop Ecol 17:21–40CrossRefGoogle Scholar
  39. Poulton EB (1890) The Colours of animals: their meaning and use especially considered in the case of insects. Kegan Paul, Trench, Trübner, & Co. Ltd., LondonGoogle Scholar
  40. Przeczek K, Mueller C, Vamosi SM (2008) The evolution of aposematism is accompanied by increased diversification. Integr Zool 3:149–156PubMedCrossRefGoogle Scholar
  41. Punzalan D, Rodd FH, Hughes KA (2005) Perceptual processes and the maintenance of polymorphism through frequency-dependent predation. Evol Ecol 19:303–320CrossRefGoogle Scholar
  42. Puurtinen M, Kaitala V (2006) Conditions for the spread of conspicuous warning signals: a numerical model with novel insights. Evolution 60:2246–2256PubMedGoogle Scholar
  43. Reid PJ, Shettleworth SJ (1992) Detection of cryptic prey: search image or search rate? J Exp Psychol Anim Behav Process 18:273–286PubMedCrossRefGoogle Scholar
  44. Reynolds RG, Fitzpatrick BM (2007) Assortative mating in poison-dart frogs based on an ecologically important trait. Evolution 61:2253–2259PubMedCrossRefGoogle Scholar
  45. Roper TJ (1990) Responses of domestic chicks to artificially coloured insect prey: effects of previous experience and background colour. Anim Behav 39:466–473CrossRefGoogle Scholar
  46. Roper TJ, Wistow R (1986) Aposematic colouration and avoidance learning in chicks. Q J Exp Psychol Sect B Comp Physiol Psychol 38:141–149Google Scholar
  47. Rowland HM, Ihalainen E, Lindström L, Mappes J, Speed MP (2007) Co-mimics have a mutualistic relationship despite unequal defences. Nature 448:64PubMedCrossRefGoogle Scholar
  48. Rudh A, Rogell B, Hoglund J (2007) Non-gradual variation in colour morphs of the strawberry poison frog Dendrobates pumilio: genetic and geographical isolation suggest a role for selection in maintaining polymorphism. Mol Ecol 16:4284–4294PubMedCrossRefGoogle Scholar
  49. Rudh A, Rogell B, Håstad O, Qvarnström A (2011) Rapid population divergence linked with co-variation between coloration and sexual display in strawberry poison frogs. Evolution 65:1271–1282PubMedCrossRefGoogle Scholar
  50. Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, New YorkCrossRefGoogle Scholar
  51. 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
  52. Saporito RA, Donnelly MA, Jain P, Garraffo HM, Spande TF, Daly JW (2007a) Spatial and temporal patterns of alkaloid variation in the poison frog Oophaga pumilio in Costa Rica and Panamá over 30 years. Toxicon 50:757–778Google Scholar
  53. Saporito RA, Zuercher R, Roberts M, Gerow KG, Donnelly MA (2007b) Experimental evidence for aposematism in the dendrobatid poison frog Oophaga pumilio. Copeia 2007:1006–1011Google Scholar
  54. Savage JM (2002) The amphibians and reptiles of Costa Rica: a herpetofauna between two continents, between two seas. University of Chicago Press, ChicagoGoogle Scholar
  55. Schuler W, Roper TJ (1992) Responses to warning coloration in avian predators. Adv Stud Behav 21:111–146CrossRefGoogle Scholar
  56. 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
  57. Skelhorn J (2011) Colour biases are a question of conspecifics’ taste. Anim Behav 81:825–829CrossRefGoogle Scholar
  58. Smith SM (1975) Innate recognition of coral snake pattern by a possible avian predator. Science 187:759–760PubMedCrossRefGoogle Scholar
  59. Speed MP, Ruxton GD (2005) Aposematism: what should our starting point be? Proc R Soc Lond B 272:431–438Google Scholar
  60. Summers K, Bermingham E, Weigt L, McCafferty S, Dahistrom L (1997) Phenotypic and genetic divergence in three species of dart-poison frogs with contrasting parental behavior. J Hered 88:8–13PubMedCrossRefGoogle Scholar
  61. 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, Panamá. J Biogeogr 30:35–53CrossRefGoogle Scholar
  62. 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
  63. Valkonen JK, Nokelainen O, Mappes J (2011) Antipredatory function of head shape for vipers and their mimics. PLoS ONE 6:e22272PubMedCrossRefGoogle Scholar
  64. Waldbauer G, Sternburg J (1975) Saturniid moths as mimics: an alternative interpretation of attempts to demonstrate mimetic advantage in nature. Evolution 29:650–658CrossRefGoogle Scholar
  65. Wang IJ (2011) Inversely related aposematic traits: reduced conspicuousness evolves with increased toxicity in a polymorphic poison-dart frog. Evolution 65:1637–1649PubMedCrossRefGoogle Scholar
  66. 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
  67. Wang IJ, Summers K (2010) Genetic structure is correlated with phenotypic divergence rather than geographic isolation in the highly polymorphic strawberry poison-dart frog. Mol Ecol 19:447–458PubMedCrossRefGoogle Scholar
  68. Wheelwright NT, Janson CH (1985) Colors of fruit displays of bird-dispersed plants in two tropical forests. Am Nat 126:777–799CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Robert H. Hegna
    • 1
    • 3
  • Ralph A. Saporito
    • 2
  • Maureen A. Donnelly
    • 1
  1. 1.College of Arts and SciencesFlorida International UniversityMiamiUSA
  2. 2.Department of BiologyJohn Carroll UniversityUniversity HeightsUSA
  3. 3.Centre of Excellence in Biological Interactions, Department of Biology and Environmental ScienceUniversity of JyväskyläJyväskyläFinland

Personalised recommendations