Journal of Chemical Ecology

, Volume 42, Issue 4, pp 329–338

Variation in Chemical Defense Among Natural Populations of Common Toad, Bufo bufo, Tadpoles: the Role of Environmental Factors

  • Veronika Bókony
  • Ágnes M. Móricz
  • Zsófia Tóth
  • Zoltán Gál
  • Anikó Kurali
  • Zsanett Mikó
  • Katalin Pásztor
  • Márk Szederkényi
  • Zoltán Tóth
  • János Ujszegi
  • Bálint Üveges
  • Dániel Krüzselyi
  • Robert J. Capon
  • Herbert Hoi
  • Attila Hettyey
Article

Abstract

Defensive toxins are widespread in nature, yet we know little about how various environmental factors shape the evolution of chemical defense, especially in vertebrates. In this study we investigated the natural variation in the amount and composition of bufadienolide toxins, and the relative importance of ecological factors in predicting that variation, in larvae of the common toad, Bufo bufo, an amphibian that produces toxins de novo. We found that tadpoles’ toxin content varied markedly among populations, and the number of compounds per tadpole also differed between two geographical regions. The most consistent predictor of toxicity was the strength of competition, indicating that tadpoles produced more compounds and larger amounts of toxins when coexisting with more competitors. Additionally, tadpoles tended to contain larger concentrations of bufadienolides in ponds that were less prone to desiccation, suggesting that the costs of toxin production can only be afforded by tadpoles that do not need to drastically speed up their development. Interestingly, this trade-off was not alleviated by higher food abundance, as periphyton biomass had negligible effect on chemical defense. Even more surprisingly, we found no evidence that higher predation risk enhances chemical defenses, suggesting that low predictability of predation risk and high mortality cost of low toxicity might select for constitutive expression of chemical defense irrespective of the actual level of predation risk. Our findings highlight that the variation in chemical defense may be influenced by environmental heterogeneity in both the need for, and constraints on, toxicity as predicted by optimal defense theory.

Keywords

Amphibian toxins Bufadienolides Geographical variation Aquatic community Pond permanence 

Supplementary material

10886_2016_690_MOESM1_ESM.kml (13 kb)
Supplementary 1(KML 13 kb)
10886_2016_690_MOESM2_ESM.xlsx (53 kb)
Supplementary 2(XLSX 53 kb)
10886_2016_690_MOESM3_ESM.docx (472 kb)
Supplementary 3(DOCX 472 kb)

References

  1. Arbuckle K, Brockhurst M, Speed MP (2013) Does chemical defence increase niche space? A phylogenetic comparative analysis of the Musteloidea. Evol Ecol 27:863–881CrossRefGoogle Scholar
  2. Barlow A, Pook CE, Harrison RA, Wüster W (2009) Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution. Proc R Soc B 276:2443–2449CrossRefPubMedPubMedCentralGoogle Scholar
  3. Benard MF, Fordyce JA (2003) Are induced defenses costly? Consequences of predator-induced defenses in western toads, Bufo boreas. Ecology 84:68–78CrossRefGoogle Scholar
  4. Brodie ED (2009) Toxins and venoms. Curr Biol 19:R931–R935CrossRefPubMedGoogle Scholar
  5. Brossman KH, Carlson BE, Stokes AN, Langkilde T (2014) Eastern newt (Notophthalmus viridescens) larvae alter morphological but not chemical defenses in response to predator cues. Can J Zool 92:279–283CrossRefGoogle Scholar
  6. Crossland MR, Alford RA (1998) Evaluation of the toxicity of eggs, hatchlings and tadpoles of the introduced toad Bufo marinus (Anura: Bufonidae) to native Australian aquatic predators. Aust J Ecol 23:129–137CrossRefGoogle Scholar
  7. Crossland MR, Shine R (2012) Embryonic exposure to conspecific chemicals suppresses cane toad growth and survival. Biol Lett 8:226–229CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cunha Filhoa GA, Schwartz CA, Resck IS, Murta MM, Lemos SS, Castro MS, Kyaw C, Pires OR Jr, Leite JRS (2005) Antimicrobial activity of the bufadienolides marinobufagin and telocinobufagin isolated as major components from skin secretion of the toad Bufo rubescens. Toxicon 45:777–782CrossRefGoogle Scholar
  9. Daly JW (1995) The chemistry of poisons in amphibian skin. Proc Natl Acad Sci U S A 92:9–13CrossRefPubMedPubMedCentralGoogle Scholar
  10. Darst CR, Menéndez-Guerrero PA, Coloma LA, Cannatella DC (2005) Evolution of dietary specialization and chemical defense in poison frogs (Dendrobatidae): a comparative analysis. Am Nat 165:56–69CrossRefPubMedGoogle Scholar
  11. Fordyce JA, Nice CC, Shapiro AM (2006) A novel trade-off of insect diapause affecting a sequestered chemical defense. Oecologia 149:101–106CrossRefPubMedGoogle Scholar
  12. Fritz RS, Simms EL (1992) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  13. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  14. Groner ML, Rollins-Smith LA, Reinert LK, Hempel J, Bier ME, Relyea RA (2014) Interactive effects of competition and predator cues on immune responses of leopard frogs at metamorphosis. J Exp Biol 217:351–358CrossRefPubMedGoogle Scholar
  15. Gunzburger MS, Travis J (2005) Critical literature review of the evidence for unpalatability of amphibian eggs and larvae. J Herpetol 39:547–57CrossRefGoogle Scholar
  16. Hagman M, Hayes RA, Capon RJ, Shine R (2009) Alarm cues experienced by cane toad tadpoles affect post-metamorphic morphology and chemical defences. Funct Ecol 23:126–132CrossRefGoogle Scholar
  17. Hanifin CT, Brodie ED III, Brodie ED Jr (2003) Tetrodotoxin levels in eggs of the rough-skin newt, Taricha granulosa, are correlated with female toxicity. J Chem Ecol 29:1729–1739CrossRefPubMedGoogle Scholar
  18. Hayes RA, Crossland MR, Hagman M, Capon RJ, Shine R (2009a) Ontogenetic variation in the chemical defences of cane toads (Bufo marinus): toxin profiles and effects on predators. J Chem Ecol 35:391–399CrossRefPubMedGoogle Scholar
  19. Hayes RA, Piggott AM, Dalle K, Capon RJ (2009b) Microbial biotransformation as a source of chemical diversity in cane toad steroid toxins. Bioorg Med Chem Lett 19:1790–1792CrossRefPubMedGoogle Scholar
  20. Henrikson B-I (1990) Predation on amphibian eggs and tadpoles by common predators in acidified lakes. Holarct Ecol 13:201–206Google Scholar
  21. 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 24:1007–1019CrossRefPubMedGoogle Scholar
  22. Hettyey A, Tóth Z, Van Buskirk J (2014) Inducible chemical defences in animals. Oikos 123:1025–1028Google Scholar
  23. Krebs CJ (1999) Ecological methodology, 2nd ed. Addison-Wesley Educational Publishers, IncGoogle Scholar
  24. Licht LE (1967) Growth inhibition in crowded tadpoles: intraspecific and interspecific effects. Ecology 48:736–745CrossRefGoogle Scholar
  25. Ligabue-Braun R, Carlini CR (2015) Poisonous birds: a timely review. Toxicon 99:102–108CrossRefPubMedGoogle Scholar
  26. Marquis O, Saglio P, Neveu A (2004) Effects of predators and conspecific chemical cues on the swimming activity of Rana temporaria and Bufo bufo tadpoles. Arch Hydrobiol 160:153–170CrossRefGoogle Scholar
  27. McCall AC, Fordyce JA (2010) Can optimal defence theory be used to predict the distribution of plant chemical defences? J Ecol 98:985–992CrossRefGoogle Scholar
  28. McClintock JB, Baker BJ (2001) Marine chemical ecology. CRC Press, Boca RatonCrossRefGoogle Scholar
  29. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  30. Reading CJ, Loman J, Madsen T (1991) Breeding pond fidelity in the common toad, Bufo bufo. J Zool (Lond) 225:201–211CrossRefGoogle Scholar
  31. Relyea RA (2002) Local population differences in phenotypic plasticity: predator-induced changes in wood frog tadpoles. Ecol Monogr 72:77–93CrossRefGoogle Scholar
  32. Richter-Boix A, Llorente GA, Montori A (2007) A comparative study of predator-induced phenotype in tadpoles across a pond permanency gradient. Hydrobiologia 583:43–56CrossRefGoogle Scholar
  33. Richter-Boix A, Tejedo M, Rezende EL (2011) Evolution and plasticity of anuran larval development in response to desiccation. A comparative analysis. Ecol Evol 1:15–25CrossRefPubMedPubMedCentralGoogle Scholar
  34. Sultan SE, Spencer HG (2002) Metapopulation structure favors plasticity over local adaptation. Am Nat 160:271–283CrossRefPubMedGoogle Scholar
  35. Tempone AG, Carvalho PD, Lebrun I, Sartorelli P, Taniwaki NN, de Andrade HF Jr, Antoniazzi MM, Jared C (2008) Antileishmanial and antitrypanosomal activity of bufadienolides isolated from the toad Rhinella jimi parotoid macrogland secretion. Toxicon 52:13–21CrossRefPubMedGoogle Scholar
  36. Van Buskirk J (2002) A comparative test of the adaptive plasticity hypothesis: relationships between habitat and phenotype in anuran larvae. Am Nat 160:87–102CrossRefPubMedGoogle Scholar
  37. Van Buskirk J, Arioli M (2005) Habitat specialization and adaptive phenotypic divergence of anuran populations. J Evol Biol 18:596–608CrossRefPubMedGoogle Scholar
  38. Van Buskirk J, Schmidt BR (2000) Predator-induced phenotypic plasticity in larval newts: trade-offs, selection, and variation in nature. Ecology 81:3009–3028CrossRefGoogle Scholar
  39. Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  40. Woodhams DC, Rollins-Smith LA, Carey C, Reinert L, Tyler MJ, Alford RA (2006) Population trends associated with skin peptide defenses against chytridiomycosis in Australian frogs. Oecologia 146:531–540CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Veronika Bókony
    • 1
  • Ágnes M. Móricz
    • 2
  • Zsófia Tóth
    • 3
  • Zoltán Gál
    • 1
    • 4
  • Anikó Kurali
    • 1
  • Zsanett Mikó
    • 1
  • Katalin Pásztor
    • 1
  • Márk Szederkényi
    • 1
    • 5
  • Zoltán Tóth
    • 1
  • János Ujszegi
    • 1
  • Bálint Üveges
    • 1
    • 5
  • Dániel Krüzselyi
    • 2
  • Robert J. Capon
    • 6
  • Herbert Hoi
    • 5
  • Attila Hettyey
    • 1
  1. 1.Lendület Evolutionary Ecology Research Group, Plant Protection Institute, Centre for Agricultural ResearchHungarian Academy of SciencesBudapestHungary
  2. 2.Department of Pathophysiology, Plant Protection Institute, Centre for Agricultural ResearchHungarian Academy of SciencesBudapestHungary
  3. 3.Department of Evolutionary Zoology and Human BiologyUniversity of DebrecenDebrecenHungary
  4. 4.Agricultural Biotechnology Institute, NARICGödöllőHungary
  5. 5.Department of Integrative Biology and Evolution, Konrad Lorenz Institute of EthologyUniversity of Veterinary MedicineViennaAustria
  6. 6.Institute for Molecular BioscienceUniversity of QueenslandSt LuciaAustralia

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