Avoiding Predation: The Importance of Chemical and Visual Cues in Poison Frog Reproductive Behaviour

  • Lisa M. Schulte
  • Rainer Schulte
  • Stefan Lötters
Chapter

Abstract

The detection of biological signals is especially important in ­predator–prey systems. Anuran amphibians have evolved a remarkable diversity of defense strategies against predators, but the most risk-free is the prevention of a possible danger. This is valid for the protection of offspring as well. The neotropical poison frog Ranitomeya variabilis deposits both eggs and tadpoles in phytotelmata. The ­exploitation of these small pools is advantageous as it lowers the risk of offspring ­predation compared to larger water bodies. Nonetheless, there are potential predators in these pools as well. We analysed how the parent frogs avoid conspecific ­cannibalistic tadpoles and damselfly larvae of the species Microstigma rotundatum. We compared the use of chemical and visual cues and show that R. variabilis avoids conspecific tadpoles for the deposition of its offspring using chemical cues, while visual tadpole models alone were not avoided by the frogs. Damselfly larvae in contrast were avoided when present, but could not be detected by chemical cues alone. We suggest that the invertebrate predators mask their chemical cues, forcing the frogs to use other senses to detect them.

Keywords

Clay Cage Assimilation Polypropylene Detritus 

Notes

Acknowledgements

We thank M. Mayer and E. Rudolf for field assistance, A. Holmes for proofreading our manuscript and O. Finke for the identification of the damselfly larvae. Asociación de Productores de Ranas Venenosas, Progreso (ASPRAVEP) allowed us to use their field station. Research permits were obtained from the Ministry of Agriculture (DGFFS) in Lima, Peru (Authorization No. 0204-2010-AG-DGFFS-DGFFS and 0200-2011-AG-DGFFS-DGFFS). Part of this research was funded with grants from the ‘Forschungsfonds’ of Trier University (to S. Lötters), the ‘Studienstiftung des deutschen Volkes’ (to L. M. Schulte) and the ‘Deutsche Forschungsgemeinschaft’ to S. Lötters, M. Veith and W. Brack (LO 1681/1-1).

References

  1. Binckley CA, Resetarits WJ Jr (2003) Functional equivalence of none-lethal effects: generalized fish avoidance determines distribution of gray treefrog, Hyla chrysoscelis, larvae. Oikos 102:623–629CrossRefGoogle Scholar
  2. Bradbury JW, Vehrencamp S (1998) The principles of animal communication. Sinauer Associates, SunderlandGoogle Scholar
  3. Brodie ED, Brodie ED Jr (1999) Predator-prey arms races. Bioscience 49:557–568CrossRefGoogle Scholar
  4. Brönmark C, Hansson LA (2000) Chemical communication in aquatic systems: an introduction. Oikos 88:103–109CrossRefGoogle Scholar
  5. Brown JL, Morales V, Summers K (2008a) Divergence in parental care, habitat selection and larval life history between two species of Peruvian poison frogs: an experimental analysis. J Evol Biol 21:1534–1543PubMedCrossRefGoogle Scholar
  6. Brown JL, Twomey E, Morales V, Summers K (2008b) Phytotelm size in relation to parental care and mating strategies in two species of Peruvian poison frogs. Behaviour 145:1139–1165CrossRefGoogle Scholar
  7. Brown JL, Morales V, Summers K (2009) Home range size and location in relation to reproductive resources in poison frogs (Dendrobatidae): a Monte Carlo approach using GIS data. Anim Behav 77:547–554CrossRefGoogle Scholar
  8. Brust DG (1993) Maternal brood care by Dendrobates pumilio: a frog that feeds its young. J Herpetol 27:96–98CrossRefGoogle Scholar
  9. Caldwell JP, de Araújo MC (1998) Cannibalistic interactions resulting from indiscriminate predatory behavior in tadpoles of poison frogs (Anura: Dendrobatidae). Biotropica 30:92–103CrossRefGoogle Scholar
  10. Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595PubMedCrossRefGoogle Scholar
  11. Chivers DP, Mirza RS (2001) Importance of predator diet cues in responses of larval wood frogs to fish and invertebrate predators. J Chem Ecol 27:45–51PubMedCrossRefGoogle Scholar
  12. Cooper WE, Caldwell JP, Vitt LJ (2009) Conspicuousness and vestigial escape behaviour by two dendrobatid frogs, Dendrobates auratus and Oophaga pumilio. Behaviour 146:325–349CrossRefGoogle Scholar
  13. Darst CR, Cummings ME (2006) Predator learning favours mimicry of a less-toxic model in poison frogs. Nature 440:208–211PubMedCrossRefGoogle Scholar
  14. Duellman WE, Trueb L (1986) Biology of amphibians. Johns Hopkins University Press, New YorkGoogle Scholar
  15. Edmunds M (1974) Defence in animals: a survey of anti-predator defences. Longman, New YorkGoogle Scholar
  16. Eklöv P (2000) Chemical cues from multiple predator-prey interactions induce changes in behavior and growth of anuran larvae. Oecologia 123:192–199CrossRefGoogle Scholar
  17. Ewert JP (1974) The neural basis of visually guided behavior. Sci Am 230:34–42PubMedCrossRefGoogle Scholar
  18. Ferland-Raymond B, Murray DL (2008) Predator diet and prey adaptive responses: can tadpoles distinguish between predators feeding on congeneric vs. conspecific prey? Can J Zool 86:1329–1336CrossRefGoogle Scholar
  19. Ferland-Raymond B, March RE, Metcalfe CD, Murray DL (2010) Prey detection of aquatic predators: assessing the identity of chemical cues eliciting prey behavioral plasticity. Biochem Syst Ecol 38:169–177CrossRefGoogle Scholar
  20. Ferrari MCO, Chivers DP (2010) The ghost of predation future: threat-sensitive and temporal assessment of risk by embryonic woodfrogs. Behav Ecol Sociobiol 64:549–555CrossRefGoogle Scholar
  21. Ferrari MCO, Messier F, Chivers DP (2007) Degradation of chemical alarm cues under natural conditions: risk assessment by larval woodfrogs. Chemoecology 17:263–266CrossRefGoogle Scholar
  22. Fisher RA (1922) On the interpretation of X2 from contingency tables, and the calculation of P. J Roy Stat Soc Ser A (Stat Soc) 85:87–94CrossRefGoogle Scholar
  23. Forester DC, Wisnieski A (1991) The significance of airborne olfactory cues to the recognition of home area by the dart-poison frog Dendrobates pumilio. J Herpetol 25:502–504CrossRefGoogle Scholar
  24. Gomez D, Richardson C, Lengagne T, Plenet S, Joly P, Léna JP, Théry M (2009) The role of ­nocturnal vision in mate choice: females prefer conspicuous males in the European tree frog (Hyla arborea). Proc R Soc B 276:2351–2358PubMedCrossRefGoogle Scholar
  25. Gotelli NJ, Ellison AM (2004) A primer of ecological statistics. Sinauer Associates, SunderlandGoogle Scholar
  26. Haberl W, Wilkinson JW (1997) A note on the Unkenreflex and similar defensive postures in Rana temporaria (Anura, Amphibia). Herpetol Bull 61:16–20Google Scholar
  27. Hamer R, Lemckert FL, Banks PB (2011) Adult frogs are sensitive to the predation risks of olfactory communication. Biol Lett 7:361–363PubMedCrossRefGoogle Scholar
  28. Hart S (1996) The language of animals. Hentry Holt and Company, New YorkGoogle Scholar
  29. Hasson O (1991) Pursuit-deterrent signals: communication between prey and predator. Trends Ecol Evol 6:325–329PubMedCrossRefGoogle Scholar
  30. Hettyey A, Vincze K, Zsarnóczai S, Hoi H, Laurila A (2011) Costs and benefits of defences induced by predators differing in dangerousness. J Evol Biol 24:1007–1019PubMedCrossRefGoogle Scholar
  31. Hews DK (1988) Alarm response in larval western toads, Bufo boreas: release of larval chemicals by a natural predator and its effect on predator capture efficiency. Anim Behav 36:125–133CrossRefGoogle Scholar
  32. Hödl W, Amézquita A, Ryan MJ (2001) Visual signaling in anuran amphibians. In: Ryan MJ (ed) Anuran communication. Smithsonian Press, Washington, pp 121–141Google Scholar
  33. Hopey ME, Petranka JW (1994) Restriction of wood frogs to fish-free habitats: how important is adult choice? Copeia 1994:1023–1025CrossRefGoogle Scholar
  34. Ingle DJ, Hoff KS (1990) Visually elicited evasive behavior in frogs. Bioscience 40:284–291CrossRefGoogle Scholar
  35. Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394Google Scholar
  36. Lannoo MJ, Townsend DS, Wassersug RJ (1987) Larval life in the leaves: arboreal tadpole types, with special attention to the morphology, ecology, and behavior of the oophagous Osteopilus brunneaus (Hylidae) larva. Fieldiana (Zool) 38:1–31Google Scholar
  37. Laurila A, Kujasalo J, Ranta E (1997) Different antipredator behaviour in two anuran tadpoles: effects of predator diet. Behav Ecol Sociobiol 40:329–336CrossRefGoogle Scholar
  38. Laurila A, Kujasalo J, Ranta E (1998) Predator-induced changes in life history in two anuran tadpoles: effects of predator diet. Oikos 83:307–317CrossRefGoogle Scholar
  39. Lehtinen RM, Lannoo MJ, Wassersug RJ (2004) Phytotelm-breeding anurans: past, present, and future research. Misc Publ Mus Zool Univ Mich 193:1–10Google Scholar
  40. Lenzi-Mattos R, Antoniazzi MM, Haddad CFB, Tambourgi DV, Rodrigues MT, Jared C (2005) The inguinal macroglands of the frog Physalaemus nattereri (Leptodactylidae): structure, toxic secretion and relationship with deimatic behaviour. J Zool 266:385–394CrossRefGoogle Scholar
  41. Lötters S, Jungfer K-H, Henkel F-W, Schmidt W (2007) Poison frogs: biology, species & captive husbandry. Chimaira, FrankfurtGoogle Scholar
  42. Marchisin A, Anderson JD (1978) Strategies employed by frogs and toads (Amphibia, Anura) to avoid predation by snakes (Reptilia, Serpentes). J Herpetol 12:151–155CrossRefGoogle Scholar
  43. Martins M (1989) Deimatic behavior in Pleurodema brachyops. J Herpetol 23:305–307CrossRefGoogle Scholar
  44. McDiamond RW, Altig R (1999) Tadpoles: the biology of anuran larvae. University of Chicago Press, ChicagoGoogle Scholar
  45. McDiarmid RW, Gorzula S (1989) Aspects of the reproductive ecology and behavior of the tepui toads, genus Oreophrynella (Anura, Bufonidae). Copeia 2:445–451CrossRefGoogle Scholar
  46. Murray DL, Roth JD, Wirsing AJ (2004) Predation risk avoidance by terrestrial amphibians: the role of prey experience and vulnerability to native and exotic predators. Ethology 110:635–647CrossRefGoogle Scholar
  47. Narins PM, Hödl W, Grabul DS (2003) Bimodal signal requisite for agonistic behavior in a dart-poison frog, Epipedobates femoralis. Proc Natl Acad Sci U S A 100:577PubMedCrossRefGoogle Scholar
  48. Narins PM, Grabul DS, Soma KK, Gaucher P, Hödl W (2005) Cross-modal integration in a dart-poison frog. Proc Natl Acad Sci U S A 102:2425PubMedCrossRefGoogle Scholar
  49. Osorio D, Srinivasan MV (1991) Camouflage by edge enhancement in animal coloration patterns and its implications for visual mechanisms. Proc R Soc B 244:81–85PubMedCrossRefGoogle Scholar
  50. Pearl CA, Cervantes M, Chan M, Ho U, Shoji R, Thomas EO (2000) Evidence for a mate-attracting chemosignal in the dwarf African clawed frog Hymenochirus. Horm Behav 38:67–74PubMedCrossRefGoogle Scholar
  51. Pearson K (1956) On the theory of contingency and its relation to association and normal ­correlation; On the general theory of skew correlation and non-linear regression. In: Pearson ES (Ed) Karl Pearson’s early statistical papers. Cambridge University Press, Cambridge, pp 443–475Google Scholar
  52. Petranka J, Hayes L (1998) Chemically mediated avoidance of a predatory odonate (Anaxjunius) by American toad (Bufo americanus) and wood frog (Ranasylvatica) tadpoles. Behav Ecol Sociobiol 42:263–271CrossRefGoogle Scholar
  53. Petranka JW, Hopey ME, Jennings BT, Baird SD, Boone SJ (1994) Breeding habitat segregation of wood frogs and American toads: the role of interspecific tadpole predation and adult choice. Copeia 1994:691–697CrossRefGoogle Scholar
  54. Poelman EH, Dicke M (2007) Offering offspring as food to cannibals: oviposition strategies of Amazonian poison frogs (Dendrobates ventrimaculatus). Evol Ecol 21:215–227CrossRefGoogle Scholar
  55. Pramuk JB, Hiler BI (1999) An investigation of obligate oophagy of Dendrobates pumilio ­tadpoles. Herpetol Rev 30:219–220Google Scholar
  56. Prates I, Antoniazzi MM, Sciani JM, Pimenta DC, Toledo LF, Haddad CFB, Jared C (2011) Skin glands, poison and mimicry in dendrobatid and leptodactylid amphibians. J Morphol 273(3):279–90PubMedCrossRefGoogle Scholar
  57. Pröhl H, Ostrowski T (2011) Behavioural elements reflect phenotypic colour divergence in a poison frog. Evol Ecol 25:1–23CrossRefGoogle Scholar
  58. Resetarits WJ Jr, Wilbur HM (1989) Choice of oviposition site by Hyla chrysoscelis: role of predators and competitors. Ecology 70:220–228CrossRefGoogle Scholar
  59. Richards-Zawacki CL, Cummings ME (2010) Intraspecific reproductive character displacement in a polymorphic poison dart frog, Dendrobates pumilio. Evolution 65:259–267PubMedCrossRefGoogle Scholar
  60. Rieger JF, Binckley CA, Resetarits WJ Jr (2004) Larval performance and oviposition site preference along a predation gradient. Ecology 85:2094–2099CrossRefGoogle Scholar
  61. Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals, and mimicry. Oxford University Press, OxfordCrossRefGoogle Scholar
  62. Sachs L (1974) Angewandte Statistik: Planung und Auswertung—Methoden und Modelle. Springer, BerlinCrossRefGoogle Scholar
  63. Saenz D, Johnson JB, Adams CK, Dayton GH (2003) Accelerated hatching of southern leopard frog (Rana sphenocephala) eggs in response to the presence of a crayfish (Procambarus nigrocinctus) predator. Copeia 2003:646–649CrossRefGoogle Scholar
  64. Schulte LM, Yeager J, Schulte R, Veith M, Werner P, Beck LA, Lötters S (2011) The smell of success: choice of larval rearing sites by means of chemical cues in a Peruvian poison frog. Anim Behav 81:1147–1154CrossRefGoogle Scholar
  65. Smith GR, Burgett AA, Temple KG, Sparks KA, Winter KE (2008) The ability of three species of tadpoles to differentiate among potential fish predators. Ethology 114:701–710CrossRefGoogle Scholar
  66. Spieler M, Linsenmair KE (1997) Choice of optimal oviposition sites by Hoplobatrachus occipitalis (Anura: Ranidae) in an unpredictable and patchy environment. Oecologia 109:184–199CrossRefGoogle Scholar
  67. Stauffer HP, Semlitsch RD (1993) Effects of visual, chemical and tactile cues of fish on the behavioral-responses of tadpoles. Anim Behav 46:355–364CrossRefGoogle Scholar
  68. Stevens M, Merilaita S (2009) Animal camouflage: current issues and new perspectives. Philos Trans R Soc Lond Ser B Biol Sci 364:423–427CrossRefGoogle Scholar
  69. Summers K (1999) The effects of cannibalism on Amazonian poison frog egg and tadpole deposition and survivorship in Heliconia axil pools. Oecologia 119:557–564CrossRefGoogle Scholar
  70. Summers K, Symula R, Clough M, Cronin T (1999) Visual mate choice in poison frogs. Proc R Soc Lond Ser B Biol Sci 266:2141–2145CrossRefGoogle Scholar
  71. Takahara T, Kohmatsu Y, Yamaoka R (2008) Predator-avoidance behavior in anuran tadpoles: a new bioassay for characterization of water-soluble cues. Hydrobiologia 607:123–130CrossRefGoogle Scholar
  72. Takahashi M (2007) Oviposition site selection: pesticide avoidance by gray treefrogs. Environ Toxicol Chem 26:1476–1480PubMedCrossRefGoogle Scholar
  73. Teixeira RL, Mili PSM, Rödder D (2006) Ecology of anurans inhabiting bromeliads in a saxicolous habitat of southeastern Brazil. Salamandra 42:155Google Scholar
  74. Toledo RC, Jared C (1995) Cutaneous granular glands and amphibian venoms. Comp Biochem Physiol Physiol 111:1–29CrossRefGoogle Scholar
  75. Toledo LF, Fernando C, Haddad B (2009) Defensive vocalizations of neotropical anurans. South Am J Herpetol 4:25–42CrossRefGoogle Scholar
  76. Toledo LF, Sazima I, Haddad CFB (2011) Behavioural defences of anurans: an overview. Ethol Ecol Evol 23:1–25CrossRefGoogle Scholar
  77. Townend J (2002) Practical statistics for environmental and biological scientists. Wiley, ChichesterGoogle Scholar
  78. Varga L (1928) Ein interessanter Biotop der Biocönose von Wasserorganismen. Biol Zentralbl 48:143–162Google Scholar
  79. Williams DA (1976) Improved likelihood ratio tests for complete contingency tables. Biometrika 63:33CrossRefGoogle Scholar
  80. Williams CR, Brodie ED Jr, Tyler MJ, Walker SJ (2000) Antipredator mechanisms of Australian frogs. J Herpetol 34:431–443CrossRefGoogle Scholar
  81. Wilson EO (1970) Chemical communication within animal species. In: Sondheimer E, Simeone JB (eds) Chemical ecology. Academic, New York, pp 133–155Google Scholar
  82. Wirsing AJ, Roth JD, Murray DL (2005) Can prey use dietary cues to distinguish predators? A test involving three terrestrial amphibians. Herpetologica 61:104–110CrossRefGoogle Scholar
  83. Wissinger S, McGrady J (1993) Intraguild predation and competition between larval dragonflies: direct and indirect effects on shared prey. Ecology 74:207–218CrossRefGoogle Scholar
  84. Woolf B (1957) The log likelihood ratio test (the G-test); methods and tables for tests of heterogeneity in contingency tables. Ann Hum Genet 21:397–409PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Lisa M. Schulte
    • 1
  • Rainer Schulte
    • 2
  • Stefan Lötters
    • 1
  1. 1.Department of BiogeographyTrier UniversityTrierGermany
  2. 2.Instituto de Investigación Biológica de las Cordilleras Orientales—INIBICOTarapotoPeru

Personalised recommendations