Skip to main content
SpringerLink
Log in

The effect of cyanogenic glucosides and their breakdown products on predation by domestic chicks

  • Original Article
  • Published:
Chemoecology Aims and scope Submit manuscript

Abstract

Cyanogenic insects release cyanide and other breakdown products that are thought to make them unpalatable to predators. Cyanogenic lepidopterans such as Heliconius butterflies and Zygaena moths are rejected by vertebrate predators, but the role played by these compounds in predator deterrence is poorly explored. Here I report tests undertook with captive domestic chicks (Gallus gallus) to evaluate the effect of cyanoglucosides, linamarin and prunasin and their breakdown products. In insects as well as plants, cyanoglucosides are enzymatically broken down when the tissue is disrupted as in the case of a predator attack. The aliphatic linamarin releases cyanide and acetone upon breakdown, while prunasin is an aromatic cyanoglucoside that releases cyanide and benzaldehyde. Using concentrations that mimicked the concentration of Heliconius butterflies, I ran trials with naïve chicks by offering palatable prey laced with chemicals resulting from cyanoglucoside breakdown. I categorized prey acceptance and compared the behavior of the predators towards test and control prey. Prey coated with cyanide and benzaldehyde were rejected by the birds, while acetone elicited some avoidance behavior. Intact cyanoglucosides were not rejected by the predators presumably because of fast ingestion time or lack of enzymes to break it down. Rejection of cyanide-laced prey confirms the protective nature of cyanoglucosides against a vertebrate predator. The rejection of the pungent but not toxic benzaldehyde and the potential effect of acetone suggest that cyanoglucosides could be detected via smell as well by taste. These results provide support for cyanoglucosides as defensive chemicals of aposematic lepidopterans and related arthropods.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Arias M, Mappes J, Théry M, Llaurens V (2016) Inter-species variation in unpalatability does not explain polymorphism in a mimetic species. Evol Ecol 30:395–409

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Boyden TC (1976) Butterfly palatability and mimicry: experiments with Ameiva lizards. Evolution 30:73–81

    Article  PubMed  Google Scholar 

  • Brower LP (1984) Chemical defence in butterflies. In: Vane-Wright RI, Ackery PR (eds) The biology of butterflies. Academic Press, London, pp 109–134

    Google Scholar 

  • Brower LP, Brower JVZ, Collins CT (1963) Experimental studies on mimicry. 7. Relative palatability and Mullerian mimicry among Neotropical butterflies of the subfamily Heliconiinae. Zoologica 48:65–84

    Google Scholar 

  • Brückner A, Raspotnig G, Wehner K, Meusinger R, Norton RA, Heethoff M (2017) Storage and release of hydrogen cyanide in a chelicerate (Oribatula tibialis). Proc Natl Acad Sci (USA) 114:3469–3472

    Article  Google Scholar 

  • Cardoso MZ, Gilbert LE (2013) Pollen feeding, resource allocation and the evolution of chemical defence in passion vine butterflies. J Evol Biol 26:1254–1260

    Article  CAS  PubMed  Google Scholar 

  • Castro ECP, Zagrobelny M, Cardoso MZ, Bak S (2018) The arms race between heliconiine butterflies and Passiflora plants—new insights in an ancient subject. Biol Rev 93:555–573

    Article  PubMed  Google Scholar 

  • Castro ECP, Zagrobelny M, Zurano JP, Cardoso MZ, Feyereisen R, Bak S (2019) Sequestration and biosynthesis of cyanogenic glucosides in passion vine butterflies and consequences for the diversification of their host plants. Ecol Evol 9:5079–5093

    Article  Google Scholar 

  • Chai P (1986) Field observations and feeding experiments on the responses of rufous-tailed jacamars (Galbula ruficauda) to free-flying butterflies in a tropical rainforest. Biol J Linn Soc 29:161–189

    Article  Google Scholar 

  • Chai P (1990) Relationships between visual characteristics of rainforest butterflies and responses of a specialized insectivorous bird. In: Wickstein M (ed) Adaptive coloration in invertebrates. Texas A&M Press, Texas, pp 31–60

    Google Scholar 

  • Chouteau M, Dezeure J, Sherratt TN, Llaurens V (2019) Similar predator aversion for natural prey with diverse toxicity levels. Anim Behav 153:49–59

    Article  Google Scholar 

  • Davis RH, Nahrstedt A (1981) Linamarin and lotaustralin as the source of cyanide in Zygaena filipendulae L. (Lepidoptera). Biochem Physiol B 64:395–397

    Google Scholar 

  • Engler-Chaouat HS, Gilbert LE (2007) De novo synthesis vs. sequestration: negatively correlated metabolic traits and the evolution of host plant specialization in cyanogenic butterflies. J Chem Ecol 33:25–42

    Article  CAS  PubMed  Google Scholar 

  • Jørgensen K, Bak S, Busk PK, Sorensen C, Olsen CR, Kaerlas JP, Moller BL (2005) Cassava plants with a depleted cyanogenic glucoside content in leaves and tubers. Distribution of cyanogenic glucosides, their site of synthesis and transport, and blockage of the biosynthesis by RNA interference technology. Plant Physiol 139:363–374

    Article  PubMed  PubMed Central  Google Scholar 

  • Langham G (2004) Specialized avian predators repeatedly attack novel color morphs of Heliconius butterflies. Evolution 58:2783–2787

    Article  PubMed  Google Scholar 

  • Muhtasib H, Evans DL (1987) Linamarin and histamine in the defense of adult Zygaena filipendulae. J Chem Ecol 13:133–142

    Article  CAS  PubMed  Google Scholar 

  • Nahrstedt A (1988) Cyanogenesis and the role of cyanogenic compounds in insects. In: Everud D, Harnett S (eds) Cyanide compounds in biology. Wiley, Chichester, pp 131–150

    Google Scholar 

  • Nahrstedt A, Davis RH (1983) Occurrence, variation and biosynthesis of the cyanogenic glucosides linamarin and lotaustralin in species of the Heliconiini (Insecta: Lepidoptera). Comp Biochem Physiol 75B:65–73

    CAS  Google Scholar 

  • Pentzold S, Jensen MK, Matthes A, Olsen CE, Petersen BL, Clausen H, Møller BL, Bak S, Zagrobelny M (2017) Spatial separation of the cyanogenic ß-glucosidase ZfBGD2 and cyanogenic glucosides in the haemolymph of Zygaena larvae facilitates cyanide release. R Soc Open Sci 4:170262

    Article  PubMed  PubMed Central  Google Scholar 

  • Peterson SC (1986) Breakdown products of cyanogenesis: repellency and toxicity to predatory ants. Naturwissenschaften 73:627–628

    Article  CAS  Google Scholar 

  • Pinheiro CEG, Campos VC (2019) The responses of wild jacamars (Galbula ruficauda, Galbulidae) to aposematic, aposematic and cryptic, and cryptic butterflies in central Brazil. Ecol Entomol 44:441–450

    Article  Google Scholar 

  • Pinheiro CEG, Cintra R (2017) Butterfly predators in the neotropics: which birds are involved? J Lep Soc 71:109–114

    Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Rammert U (1982) The reaction of birds to the larval defensive system of Zygaena trifolii (Esper, 1783) (Lepidoptera: Zygaenidae). In: Dutreix C, Naumann C, Tremewan W (eds) Recent advances in burnet moth research (Lepidoptera: Zygaenidae). Koeltz Scientific Books, Koenigstein, pp 38–42

    Google Scholar 

  • Roper TJ, Marples NM (1997) Odour and colour as cues for taste-avoidance learning in domestic chicks. Anim Behav 53:1241–1250

    Article  CAS  PubMed  Google Scholar 

  • Wiklund C, Järvi T (1982) Survival of distasteful insects after being attacked by naïve birds: a reappraisal of the theory of aposematic coloration evolving through individual selection. Evolution 36:998–1002

    Article  PubMed  Google Scholar 

  • Zagrobelny M, Bak S, Møller BL (2008) Cyanogenesis in animals and plants. Phytochem 69:1457–1468

    Article  CAS  Google Scholar 

  • Zagrobelny M, Castro ECP, Møller BL, Bak S (2018) Cyanogenesis in arthropods: from chemical warfare to nuptial gifts. Insects 9:51

    Article  PubMed Central  Google Scholar 

Download references

Acknowledgements

I would like to dedicate this study to Professor José Roberto Trigo (1956–2017), head of the Chemical Ecology Lab at the University of Campinas. Dr Trigo provided space and technical and logistic support for this study, to which I am grateful. Sadly, Dr Trigo passed away before seeing the final draft of this work. I would also like to thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP Proc 00/02115–0) for a postdoctoral fellowship and for providing laboratory grants to JRT. I thank M.A. Foglio (Centro de Pesquisas Químicas e Biológicas Aplicadas, University of Campinas) for providing linamarin samples and the Instituto de Agronomia de Campinas for cassava material. Special thanks are due to J. Paiva for assistance with chemical analysis, P. R. Guimarães for helping with the palatability experiments, Érika Castro for drawings of chemical structures, and Marcus V. Vieira for helping in implementing the GLMM analysis. I am especially grateful to Mika Zagrobelny and Érika Castro for critically reading the first draft of this paper and to the anonymous reviewers for suggestions that have greatly improved the manuscript.

Author information

Authors and Affiliations

  1. Department of Ecology, Federal University of Rio Grande Do Norte, Natal, Rio Grande do Norte, 59078-900, Brazil

    Márcio Zikán Cardoso

Authors
  1. Márcio Zikán Cardoso
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Márcio Zikán Cardoso.

Additional information

Communicated by Günther Raspotnig.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cardoso, M.Z. The effect of cyanogenic glucosides and their breakdown products on predation by domestic chicks. Chemoecology 30, 131–138 (2020). https://doi.org/10.1007/s00049-020-00304-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00049-020-00304-6

Keywords

Search

Navigation