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Coloration in the polymorphic frog Oophaga pumilio associates with level of aggressiveness in intraspecific and interspecific behavioral interactions

Abstract

Intraspecific morphological variation may correspond to behavioral variation that helps determine the nature of species interactions. Color variation among populations of variably toxic organisms has been shown to associate with alternative anti-predator behaviors. However, the effects of these alternative behavioral tendencies on the outcomes of interspecific interactions other than predator–prey remain largely unexplored. We investigated how coloration and body size variation in Oophaga pumilio, one of the most phenotypically diverse amphibians known, associated with territorial aggressiveness and how this association influenced the outcome of agonistic male–male interactions with conspecifics and heterospecifics of two sympatric species (Andinobates claudiae and Phyllobates lugubris). Irrespective of body size, resident frogs from more conspicuous, red-colored O. pumilio populations responded to same-morph conspecifics and P. lugubris more quickly and exhibited more aggressive behaviors and more energetically expensive behaviors than resident frogs from green populations under these same treatments. Furthermore, red-colored resident frogs dominated most of the interactions in which they were involved, whereas green residents dominated only a few of the interactions, despite their status as residents. Because conspecific and heterospecific intruders did not behave more aggressively toward red resident frogs, aggressiveness of red residents does not appear to be a response to higher aggression being directed toward them. These results suggest that coloration in O. pumilio is a good indicator of aggressiveness that associates with the outcome of intraspecific and some interspecific behavioral male–male interactions, providing support for a positive association among anti-predator traits, agonistic behavior, and dominance in both intraspecific and interspecific, intraguild interactions.

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References

  1. Adams DC (2004) Character displacement via aggressive interference in Appalachian salamanders. Ecology 85:2664–2670

    Article  Google Scholar 

  2. Anderson CN, Grether GF (2010) Interspecific aggression and character displacement of competitor recognition in Hetaerina damselflies. Proc R Soc Lond B 277:549–555

    Article  Google Scholar 

  3. Bastiaans E, Morinaga G, Gaytan JGC, Marshall JC, Sinervo B (2013) Male aggression varies with throat color in 2 distinct populations of the mesquite lizard. Behav Ecol 24:968–981

    Article  Google Scholar 

  4. Baugh JR, Forester DC (1994) Prior residence effect in the dart-poison frog, Dendrobates pumilio. Behaviour 131:207–224

    Article  Google Scholar 

  5. Bee MA (2003) A test of the “dear enemy effect” in the strawberry dart-poison frog (Dendrobates pumilio). Behav Ecol Sociobiol 54:601–610

    Article  Google Scholar 

  6. Bernays EA, Singer M (2002) Contrasted foraging tactics in two species of polyphagous caterpillars. Acta Zool Hung 48:117–135

    Google Scholar 

  7. Blomberg SP, Garland T Jr, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–45

    PubMed  Article  Google Scholar 

  8. Brown JL, Maan ME, Cummings ME, Summers K (2010) Evidence for selection on coloration in a Panamanian poison frog: a coalescent-based approach. J Biogeogr 37:891–901

    Article  Google Scholar 

  9. Cohen J (1988) Statistical power analyses for the behavioral sciences, 2nd edn. Erlbaum, Hillsdale

    Google Scholar 

  10. Crothers LR, Cummings ME (2013) Warning signal brightness variation: sexual selection may work under the radar of natural selection in populations of a polytypic poison frog. Am Nat 181:E116–E124

    PubMed  Article  Google Scholar 

  11. Crothers LR, Cummings ME (2015) A multifunctional warning signal behaves as an agonistic status signal in a poison frog. Behav Ecol 26:560–568

    Article  Google Scholar 

  12. Crothers LR, Gering E, Cummings ME (2011) Aposematic signal variation predicts male-male interactions in a polymorphic poison frog. Evolution 65:599–605

    PubMed  Article  Google Scholar 

  13. Daly JW, Myers CW (1967) Toxicity of Panamanian poison frogs (Dendrobates): some biological and chemical aspects. Science 156:970–973

    PubMed  Article  CAS  Google Scholar 

  14. Dijkstra PD, Groothuis TG (2011) Male-male competition as a force in evolutionary diversification: evidence in haplochromine cichlid fish. Int J Evol Biol 2011:689254

    PubMed  PubMed Central  Article  Google Scholar 

  15. Dijkstra PD, Seehausen O, Groothuis TGG (2005) Direct male-male competition can facilitate invasion of new colour types in Lake Victoria cichlids. Behav Ecol Sociobiol 58:136–143

    Article  Google Scholar 

  16. Dijkstra PD, van Dijk S, Groothuis TGG, Pierotti MER, Seehausen O (2009) Behavioral dominance between female color morphs of a Lake Victoria cichlid fish. Behav Ecol 20:593–600

    Article  Google Scholar 

  17. Donnelly MA (1989) Demographic effects of reproductive resource supplementation in a territorial frog, Dendrobates pumilio. Ecol Monogr 59:207–221

    Article  Google Scholar 

  18. Dreher CE, Cummings ME, Proehl H (2015) An analysis of predator selection to affect aposematic coloration in a poison frog species. PLoS One 10, e0130571

    PubMed  PubMed Central  Article  Google Scholar 

  19. Duckworth RA, Badyaev AV (2007) Coupling of dispersal and aggression facilitates the rapid range expansion of a passerine bird. Proc Natl Acad Sci U S A 104:15017–15022

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  20. Dugas MB, Halbrook SR, Killius AM, Sol JF, Richards‐Zawacki CL (2015) Colour and escape behaviour in polymorphic populations of an aposematic poison frog. Ethology 121:813–822

    Article  Google Scholar 

  21. Evans MR, Norris K (1996) The importance of carotenoids in signalling during aggressive interactions between male firemouth cichlids (Cichlasoma meeki). Behav Ecol 7:1–6

    Article  Google Scholar 

  22. Forester D, Cover J, Wisnieski A (1993) The influence of time of residency on the tenacity of territorial defense by the dart-poison frog Dendrobates pumilio. Herpetologica 49:94–99

    Google Scholar 

  23. Gehara M, Summers K, Brown JL (2013) Population expansion, isolation and selection: novel insights on the evolution of color diversity in the strawberry poison frog. Evol Ecol 27:797–824

    Article  Google Scholar 

  24. Grant JB (2007) Ontogenetic colour change and the evolution of aposematism: a case study in panic moth caterpillars. J Anim Ecol 76:439–447

    PubMed  Article  Google Scholar 

  25. Grether GF, Anderson CN, Drury JP, Kirschel ANG, Losin N, Okamoto K, Peiman KS (2013) The evolutionary consequences of interspecific aggression. Ann N Y Acad Sci 1289:48–68

    PubMed  Article  Google Scholar 

  26. Healey M, Uller T, Olsson M (2007) Seeing red: morph-specific contest success and survival rates in a colour-polymorphic agamid lizard. Anim Behav 74:337–341

    Article  Google Scholar 

  27. Hegna RH, Saporito RA, Donnelly MA (2013) Not all colors are equal: predation and color polytypism in the aposematic poison frog Oophaga pumilio. Evol Ecol 27:831–845

    Article  Google Scholar 

  28. Heying H (2004) Reproductive limitation by oviposition site in a treehole breeding Madagascan poison frog (Mantella laevigata). Misc Publ Mus Zool Univ Mich 193:23–30

    Google Scholar 

  29. Hödl W, Amézquita A (2001) Visual signaling in anuran amphibians. In: Ryan MJ (ed) Anuran communication. Smithsonian Institute Press, Washington, pp 121–141

    Google Scholar 

  30. Hover EL (1985) Differences in aggressive-behavior between two throat color morphs in a lizard, Urosaurus ornatus. Copeia 1985:933–940

    Article  Google Scholar 

  31. Hsu Y, Earley RL, Wolf LL (2006) Modulation of aggressive behaviour by fighting experience: mechanisms and contest outcomes. Biol Rev Camb Philos 81:33–74

    Article  Google Scholar 

  32. Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983–997

    PubMed  Article  CAS  Google Scholar 

  33. Laiolo P (2012) Interspecific interactions drive cultural co-evolution and acoustic convergence in syntopic species. J Anim Ecol 81:594–604

    PubMed  Article  Google Scholar 

  34. Lehtonen TK, McCrary JK, Meyer A (2010) Territorial aggression can be sensitive to the status of heterospecific intruders. Behav Process 84:598–601

    Article  Google Scholar 

  35. Lieberman SS (1986) Ecology of the leaf litter herpetofauna of a neotropical rain forest: La Selva, Costa Rica. Acta Zool Mex 15:1–72

    Google Scholar 

  36. Lötters S, Jungfer KH, Henkel FW, Schmidt W (2007) Poison frogs, biology, species & captive husbandry. In: Edition Chimaira & Serpents Tale. Frankfurt am Main, Germany

    Google Scholar 

  37. Maan ME, Cummings ME (2008) Female preferences for aposematic signal components in a polymorphic poison frog. Evolution 62:2334–2345

    PubMed  Article  Google Scholar 

  38. Maan ME, Cummings ME (2009) Sexual dimorphism and directional sexual selection on aposematic signals in a poison frog. Proc Natl Acad Sci U S A 106:19072–19077

    PubMed  PubMed Central  Article  Google Scholar 

  39. Maan ME, Cummings ME (2012) Poison frog colors are honest signals of toxicity, particularly for bird predators. Am Nat 179:E1–E14

    PubMed  Article  Google Scholar 

  40. Merilaita S, Tullberg BS (2005) Constrained camouflage facilitates the evolution of conspicuous warning coloration. Evolution 59:38–45

    PubMed  Article  Google Scholar 

  41. Mikami OK, Kawata M (2004) Does interspecific territoriality reflect the intensity of ecological interactions? A theoretical model for interspecific territoriality. Evol Ecol Res 6:765–775

    Google Scholar 

  42. Mochida K (2009) A parallel geographical mosaic of morphological and behavioural aposematic traits of the newt, Cynops pyrrhogaster (Urodela: Salamandridae). Biol J Linn Soc 97:613–622

    Article  Google Scholar 

  43. Peiman KS, Robinson BW (2007) Heterospecific aggression and adaptive divergence in brook stickleback (Culaea inconstans). Evolution 61:1327–1338

    PubMed  Article  CAS  Google Scholar 

  44. Peiman KS, Robinson BW (2010) Ecology and evolution of resource-related heterospecific aggression. Q Rev Biol 85:133–158

    PubMed  Article  Google Scholar 

  45. Pigliucci M (2003) Phenotypic integration: studying the ecology and evolution of complex phenotypes. Ecol Lett 6:265–272

    Article  Google Scholar 

  46. Pröhl H (1997) Territorial behaviour of the strawberry poison-dart frog, Dendrobates pumilio. Amphibia-Reptilia 18:437–442

    Article  Google Scholar 

  47. Pröhl H, Berke O (2001) Spatial distributions of male and female strawberry poison frogs and their relation to female reproductive resources. Oecologia 129:534–542

    PubMed  Article  Google Scholar 

  48. Pröhl H, Hagemann S, Karsch J, Höbel G (2007) Geographic variation in male sexual signals in strawberry poison frogs (Dendrobates pumilio). Ethology 113:825–837

    Article  Google Scholar 

  49. Pröhl H, Ostrowski T (2011) Behavioural elements reflect phenotypic colour divergence in a poison frog. Evol Ecol 25:993–1015

    Article  Google Scholar 

  50. Prudic KL, Skemp AK, Papaj DR (2007) Aposematic coloration, luminance contrast, and the benefits of conspicuousness. Behav Ecol 18:41–46

    Article  Google Scholar 

  51. Pryke SR, Astheimer LB, Buttemer WA, Griffith SC (2007) Frequency-dependent physiological trade-offs between competing colour morphs. Biol Lett 3:494–497

    PubMed  PubMed Central  Article  Google Scholar 

  52. Pryke SR, Griffith SC (2006) Red dominates black: agonistic signalling among head morphs in the colour polymorphic Gouldian finch. Proc R Soc Lond B 273:949–957

    Article  Google Scholar 

  53. Reynolds RG, Fitzpatrick BM (2007) Assortative mating in poison-dart frogs based on an ecologically important trait. Evolution 61:2253–2259

    PubMed  Article  Google Scholar 

  54. Richards-Zawacki CL, Cummings ME (2010) Intraspecific reproductive character displacement in a polymorphic poison dart frog, Dendrobates pumilio. Evolution 65:259–267

    PubMed  Article  Google Scholar 

  55. Robinson SK, Terborgh J (1995) Interspecific aggression and habitat selection by Amazonian birds. J Anim Ecol 64:1–11

    Article  Google Scholar 

  56. Rojas B, Devillechabrolle J, Endler JA (2014) Paradox lost: variable colour-pattern geometry is associated with differences in movement in aposematic frogs. Biol Lett 10:20140193

    PubMed Central  Article  Google Scholar 

  57. Rudh A, Breed MF, Qvarnstrom A (2013) Does aggression and explorative behaviour decrease with lost warning coloration? Biol J Linn Soc 108:116–126

    Article  Google Scholar 

  58. 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 65:1271–1282

    PubMed  Article  Google Scholar 

  59. 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 16:4284–4294

    PubMed  Article  CAS  Google Scholar 

  60. Sacchi R, Pupin F, Gentilli A, Rubolini D, Scali S, Fasola M, Galeotti P (2009) Male-male combats in a polymorphic lizard: residency and size, but not color, affect fighting rules and contest outcome. Aggress Behav 35:274–283

    PubMed  Article  Google Scholar 

  61. SAS Institute I (2003) SAS/STAT user’s guide Release 91 SAS Institute. Cary, North Carolina

    Google Scholar 

  62. Savage JM (2002) The amphibians and reptiles of Costa Rica: a herpetofauna between two continents, between two seas. University of Chicago Press, Chicago

    Google Scholar 

  63. Seehausen O, Schluter D (2004) Male-male competition and nuptial-colour displacement as a diversifying force in Lake Victoria cichlid fishes. Proc R Soc Lond B 271:1345–1353

    Article  Google Scholar 

  64. 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 207:2471–2485

    PubMed  Article  Google Scholar 

  65. Sinervo B, Lively CM (1996) The rock-paper-scissors game and the evolution of alternative male strategies. Nature 380:240–243

    Article  CAS  Google Scholar 

  66. Sinervo B, Miles DB, Frankino WA, Klukowski M, DeNardo DF (2000) Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards. Horm Behav 38:222–233

    PubMed  Article  CAS  Google Scholar 

  67. Speed MP, Brockhurst MA, Ruxton GD (2010) The dual benefits of aposematism: predator avoidance and enhanced resource collection. Evolution 64:1622–1633

    PubMed  Article  Google Scholar 

  68. Stamp NE, Wilkens RT (1993) On the cryptic side of life: being unapparent to enemies and the consequences for foraging and growth of caterpillars. In: Caterpillars: ecological and evolutionary constraints on foraging. Chapman & Hall, New York, pp 283–330

  69. Summers K, Symula R, Clough M, Cronin T (1999) Visual mate choice in poison frogs. Proc R Soc Lond B 266:2141–2145

    Article  CAS  Google Scholar 

  70. 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 64:1719–1728

    PubMed  Article  Google Scholar 

  71. Toft CA (1980) Feeding ecology of thirteen syntopic species of anurans in a seasonal tropical environment. Oecologia 45:131–141

    Article  Google Scholar 

  72. 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 62:2742–2759

    PubMed  Article  CAS  Google Scholar 

  73. Wilczynski W, Lynch KS, O’Bryant EL (2005) Current research in amphibians: studies integrating endocrinology, behavior, and neurobiology. Horm Behav 48:440–450

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  74. Willink B, Brenes-Mora E, Bolanos F, Proehl H (2013) Not everything is black and white: color and behavioral variation reveal a continuum between cryptic and aposematic strategies in a polymorphic poison frog. Evolution 67:2783–2794

    PubMed  Google Scholar 

  75. Wong S, Parada H, Narins PM (2009) Heterospecific acoustic interference: effects on calling in the frog Oophaga pumilio in Nicaragua. Biotropica 41:74–80

    PubMed  PubMed Central  Article  Google Scholar 

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Acknowledgments

We are grateful to M. Caldwell, J. Cronin, J. Davis, B. Elderd, C. Richards-Zawacki, and R. Stevens for their helpful suggestions during the development and execution of this study. Many thanks to C. Richards-Zawacki for providing equipment and to L. Freeborn for providing information about frog localities. For their assistance in the field, we thank D. Gonzales, C. Harris, M. Alvarez, and A. Cuervo. The Smithsonian Tropical Research Institute provided logistical support, and we especially thank G. Jacome, P. Gondola, C. Jaramillo, and the Bocas del Toro Research Station staff. We thank M. Dugas, K. Hovanes, M. Klock, J. Touchon, A. Stuckert, K. Summers, members of the Richards-Zawaki Lab, and two anonymous reviewers for their comments on drafts of the manuscript and D. Blouin for providing statistical advice. This study was supported by the Sigma Xi Chapter of Louisiana State University and by two grants from the Louisiana Environmental and Education Commission from the Louisiana Department of Wildlife and Fisheries.

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Correspondence to Sandra P. Galeano.

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All applicable international, national, and institutional guidelines for the care and use of animals were followed. Experiments reported in this article comply with the current laws of Panama (ANAM permit No. SC/A-41-12). All procedures performed were in accordance with the ethical standards of Louisiana State University (IACUC No. 13-006) and the Smithsonian Tropical Research Institute (IACUC No. 2012-1015-2015).

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Communicated by K. Summers

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Galeano, S.P., Harms, K.E. Coloration in the polymorphic frog Oophaga pumilio associates with level of aggressiveness in intraspecific and interspecific behavioral interactions. Behav Ecol Sociobiol 70, 83–97 (2016). https://doi.org/10.1007/s00265-015-2027-5

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Keywords

  • Agonistic interactions
  • Aposematism
  • Body size
  • Conspicuousness
  • Dominance
  • Dendrobatidae