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.
Similar content being viewed by others
References
Arbuckle K, Brockhurst M, Speed MP (2013) Does chemical defence increase niche space? A phylogenetic comparative analysis of the Musteloidea. Evol Ecol 27:863–881
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 276:2443–2449
Benard MF, Fordyce JA (2003) Are induced defenses costly? Consequences of predator-induced defenses in western toads, Bufo boreas. Ecology 84:68–78
Brodie ED (2009) Toxins and venoms. Curr Biol 19:R931–R935
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 92:279–283
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 23:129–137
Crossland MR, Shine R (2012) Embryonic exposure to conspecific chemicals suppresses cane toad growth and survival. Biol Lett 8:226–229
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 45:777–782
Daly JW (1995) The chemistry of poisons in amphibian skin. Proc Natl Acad Sci U S A 92:9–13
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 165:56–69
Fordyce JA, Nice CC, Shapiro AM (2006) A novel trade-off of insect diapause affecting a sequestered chemical defense. Oecologia 149:101–106
Fritz RS, Simms EL (1992) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. University of Chicago Press, Chicago
Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190
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 217:351–358
Gunzburger MS, Travis J (2005) Critical literature review of the evidence for unpalatability of amphibian eggs and larvae. J Herpetol 39:547–57
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 23:126–132
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 29:1729–1739
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 35:391–399
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 19:1790–1792
Henrikson B-I (1990) Predation on amphibian eggs and tadpoles by common predators in acidified lakes. Holarct Ecol 13:201–206
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 24:1007–1019
Hettyey A, Tóth Z, Van Buskirk J (2014) Inducible chemical defences in animals. Oikos 123:1025–1028
Krebs CJ (1999) Ecological methodology, 2nd ed. Addison-Wesley Educational Publishers, Inc
Licht LE (1967) Growth inhibition in crowded tadpoles: intraspecific and interspecific effects. Ecology 48:736–745
Ligabue-Braun R, Carlini CR (2015) Poisonous birds: a timely review. Toxicon 99:102–108
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 160:153–170
McCall AC, Fordyce JA (2010) Can optimal defence theory be used to predict the distribution of plant chemical defences? J Ecol 98:985–992
McClintock JB, Baker BJ (2001) Marine chemical ecology. CRC Press, Boca Raton
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Reading CJ, Loman J, Madsen T (1991) Breeding pond fidelity in the common toad, Bufo bufo. J Zool (Lond) 225:201–211
Relyea RA (2002) Local population differences in phenotypic plasticity: predator-induced changes in wood frog tadpoles. Ecol Monogr 72:77–93
Richter-Boix A, Llorente GA, Montori A (2007) A comparative study of predator-induced phenotype in tadpoles across a pond permanency gradient. Hydrobiologia 583:43–56
Richter-Boix A, Tejedo M, Rezende EL (2011) Evolution and plasticity of anuran larval development in response to desiccation. A comparative analysis. Ecol Evol 1:15–25
Sultan SE, Spencer HG (2002) Metapopulation structure favors plasticity over local adaptation. Am Nat 160:271–283
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 52:13–21
Van Buskirk J (2002) A comparative test of the adaptive plasticity hypothesis: relationships between habitat and phenotype in anuran larvae. Am Nat 160:87–102
Van Buskirk J, Arioli M (2005) Habitat specialization and adaptive phenotypic divergence of anuran populations. J Evol Biol 18:596–608
Van Buskirk J, Schmidt BR (2000) Predator-induced phenotypic plasticity in larval newts: trade-offs, selection, and variation in nature. Ecology 81:3009–3028
Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, Chicago
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 146:531–540
Acknowledgments
We thank Kutyó L. Jókai and Gábor Fera for help in the field, the Pilisi Parkerdő Zrt. for allowing us to use their forestry roads, and Edina Simon for help with the lab measurements of periphyton biomass. The Közép-Duna-Völgyi KTVF issued the permission to conduct the present study (KTF:603–3/2014). Financial support was provided by the ‘Lendület’ programme of the Hungarian Academy of Sciences (MTA, LP2012-24/2012), an FP7 Marie Curie Career Integration Grant (PCIG13-GA-2013–631722), and a Sparkling Science Project of the Federal Ministry of Science and Research, Austria (BMWF, SPA 04/171). During the study, Z. T. was supported by the MTA postdoctoral research programme (SZ-029/2013) and the Hungarian Scientific Research Fund (OTKA, PD108938). During write-up, V.B. was supported by the Bolyai Fellowship of the Hungarian Academy of Sciences.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary 1
(KML 13 kb)
Supplementary 2
(XLSX 53 kb)
Supplementary 3
(DOCX 472 kb)
Rights and permissions
About this article
Cite this article
Bókony, V., Móricz, Á.M., Tóth, Z. et al. Variation in Chemical Defense Among Natural Populations of Common Toad, Bufo bufo, Tadpoles: the Role of Environmental Factors. J Chem Ecol 42, 329–338 (2016). https://doi.org/10.1007/s10886-016-0690-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-016-0690-2