Skip to main content
SpringerLink
Log in

Mini-Review: Constraints on Effectiveness of Cyanogenic Glycosides in Herbivore Defense

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Cyanogenesis is the process by which hydrogen cyanide is released from endogenous cyanide containing compounds. Many cyanogenic plants release HCN in sufficient quantities to be toxic and, as a result, tend to be avoided by herbivores. However, there are many exceptions with some herbivores either immune to the cyanogenic status of the plant, or in some cases attracted to cyanogenic plants. This has led to a certain degree of scepticism regarding the role of cyanogenic glycosides as defense compounds. In this review, we examine evidence showing that differences in the effectiveness of cyanogenic glycosides in deterring herbivory can usually be reconciled when the morphology, physiology, and behavior of the animals, together with the concentration of cyanogenic glycosides in the host plant, are taken into account. Cyanogenic glycosides are not effective against all herbivores, and not all cyanogenic plants release enough cyanide to be considered toxic. Nevertheless, they do form part of the broad spectrum of toxic and distasteful compounds that herbivores must accommodate if they are to feed on cyanogenic plants.

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

Similar content being viewed by others

REFERENCES

  • Banea-Mayambu, J. P., Tylleskar, T., Gitebo, N., Gebre-Medhin, M., and Rosling, H.1997.Geographical and seasonal association between linamarin and cyanide exposure from cassava and the upper motor neurone disease Konzo in former Zaire. Trop. Med. Int. Health2:1143–1151.

    Google Scholar 

  • Banea-Mayambu, J. P., Tylleskar, T., Tylleskar, K., Gebre-Medhin, M., and Rosling, H. 2000. Dietary cyanide from insufficiently processed cassava and growth retardation in children in the Democratic Republic of Congo (formerly Zaire). Ann. Trop. Paediatr.20:34–40.

    Google Scholar 

  • Bernays, E. A., Chapman, R. F., Leather, E. M., McCaffery, A. R., and Modder, W. W. D.1977. The relationship of Zonocerus variegtus(L.) (Acridoidea: Pyrgomorphidae) with cassava (Manihot esculenta). Bull. Entomol. Res.67:391–404.

    Google Scholar 

  • Birk, R., Bravdo, B., and Shoseyov, O.1996. Detoxification of cassava by Asperigillus nigerB-1. Appl. Microbiol. Biotechnol.45:411–414.

    Google Scholar 

  • Boyd, F. T., Aamodt, O. S., Bohstedt, G. and Truog, F.1938. Sudan grass management for control of cyanide poisoning. J. Am. Soc. Agron.30:569–582.

    Google Scholar 

  • Bryant, J. P., Reichardt, P. B., and Clausen, T. P.1992. Chemically mediated interactions between woody plants and browsing mammals. J. Range Manage.45:18–24.

    Google Scholar 

  • Buhrmester, R. A., Ebinger, J. E., and Seigler, D. S.2000. Sambunigrin and cyanogenic variability in populations of Sambucus canadensisL. (Caprifoliaceae). Biochem. Syst. Ecol.28:689–695.

    Google Scholar 

  • Calatayud, P. A. and Le RÜ, B.1996. Study of the nutritional relationships between the cassava mealybug ant its host plant. Bull. Soc. Zool. Fr. Evol. Zool.121:391–398 (in French).

    Google Scholar 

  • Calatayud, P. A., Tertuliano, M., and Le RÜ, B.1994. Seasonal variation in secondary compounds in the phloem sap of cassava in relation to plant genotype and infestation by Phenacoccue manihoti(Homoptera: Pseudococcidae). Bull. Entomol. Res.84:453–459.

    Google Scholar 

  • Caradus, J. R. and Forde, M. B., 1996. Characterisation of white clover populations collected from the Caucuses and high altitude regions of eastern Turkey. Genet. Resour. Crop Evol.43:143–155.

    Google Scholar 

  • Caradus, J. R., Mackay, A. C., Charlton, J. F. L., and Chapman, D. F.1990. Genecology of white clover (Trifolium repensL.) from wet and dry hill country pastures. N. Z. J. Agric. Res.33:377–384.

    Google Scholar 

  • Cardoso, A. P., Ernesto, M., Cliff, J., Egan, S.V., and Bradbury, J.H.1998. Cyanogenic potential of cassava flour: Field trial in Mozambique of a simple kit. Int. J. Food Sci. Nutr.49:93–99.

    Google Scholar 

  • Chiwona-Karltun, L., Mkumbira, J., Saka, J., Bovin, M., Mahungun, M., and Rosling, H.1998.The importance of being bitter—aqualitative study on cassava cultivar preference in Malawi. Ecol.Food Nutr.37:219–245.

    Google Scholar 

  • Chiwona-Karltun, L., Tylleskar, T., Mkumbira, J., Gebre-Medhin, M., and Rosling, H.2000. Lowdietary cyanogen exposure from frequent consumption of potentially toxic cassava in Malawi. Int. J. Food Sci. Nutr.51:33–40.

    Google Scholar 

  • Cock, J.1982. Cassava: A basic energy source in the tropics. Science218:755–762.

    Google Scholar 

  • Compton, S. G. and Jones, D.A.1985. An investigation of the responses of herbivores to cyanogenesis in Lotus corniculatusL. Biol. J. Linn. Soc.26:21–38.

    Google Scholar 

  • Conn, E. E.1981. Cyanogenic glycosides, pp. 479–499, inE. E. Conn (ed.). The Biochemistry of Plants. A Comprehensive Treatise, Vol. 7, Secondary Plant Products. Academic Press, New York.

    Google Scholar 

  • Conn, E. E.1991. Metabolic studies on natural products: cyanogenic glycoside and cyanogenesis as possible models. Proc. Natl. Sci. Coun. ROC. Part B. Life Sci.15:220–225.

    Google Scholar 

  • Cooper-Driver, G. and Swain, T.1976. Cyanogenic polymorphism in bracken in relation to herbivore predation. Nature260:604.

    Google Scholar 

  • Cooper-Driver, G., Finch, S., and Swain, T.1977. Seasonal variation in secondary plant compounds in relation to the palatability of Pteridium aquilinum. Biochem. Syst. Ecol.5:177–183.

    Google Scholar 

  • Cork, S. J.1996. Optimal digestive strategies for arboreal herbivorous mammals in contrasting forest types: Why Koalas and Colobines are different. Aust. J. Ecol.21:10–20.

    Google Scholar 

  • Crush, J. R. and Caradus, J. R.1995. Cyanogenesis potential and iodine concentration in white clover (Trifolium repensL.) cultivars. N. Z. J. Agric. Res.38:309–316.

    Google Scholar 

  • Dirzo, R. and Harper, J. L.1982. Experimental studies on slug-plant interactions. III Differences in the acceptability of individual plants of Trifolium repensto slugs and snails. J. Ecol.70:101–117.

    Google Scholar 

  • Dritschilo W., Krummel, J., Nafus, D., and Pimentel, D.1979. Herbivorous insects colonising cyanogenic and acyanogenic Trifolium repens. Heredity42:49–56.

    Google Scholar 

  • Edwards, P. J.1989. Insect herbivory and plant defence theory, pp. 275–297, inP. J. Grubb and J. B. Whittaker (eds.). Towards a More Exact Ecology. Blackwell Scientific Publications, Oxford.

    Google Scholar 

  • Engler, H. S., Spencer, K. C., and Gilbert, L. E.2000. Insect metabolism: Preventing cyanide release from leaves. Nature406:144–145.

    Google Scholar 

  • Esashi, Y., Maruyama, A., Sasaki, S., Tani, A., and Yoshiyama, M.1996. Involvement of cyanogens in the promotion of germination of cocklebur seeds in response to various nitrogenous compounds, inhibitors of respiratory and ethylene. Plant Cell Physiol.37:545–549.

    Google Scholar 

  • Feeny, P.1976. Plant apparency and chemical defense. Recent Adv. Phytochem.10:1–40.

    Google Scholar 

  • Ferreira, C., Parra, R. P., and Terra, W. R.1997. The effect of dietary plant glycosides on larval β-glucosidases from Spodoptera frugiperdaand Diatraea saccaralis. Insect Biochem. Mol. Biol.27:55–59.

    Google Scholar 

  • Finnemore, H., Reichard, S. K., and Large, D. K.1935. Cyanogenetic glucosides in Australian plants. Part 3. Eucalyptus cladocalyx. J. Proc. R. Soc. N. S. W.69:209–214.

    Google Scholar 

  • Foulds, W.1982. Polymorphism for cyanogenesis in Lotus australisAndr. populations at Greenough Front Flats, Western Australia. Aust. J. Bot.30:211–217.

    Google Scholar 

  • Freeland, W. J. and Janzen, D. H.1974. Strategies in herbivory by mammals: The role of plant secondary compounds. Am. Nat.108:269–289.

    Google Scholar 

  • Frehner, M. and Conn, E. E.1987. The linamarin β-glucosidase in Costa Rica wild bean (Phaseolus lunatusL.) is apoplastic. Plant Physiol.84:1296–1300.

    Google Scholar 

  • Glander, K. E., Wright, P. C., Seigler, D. S., Randrianasol, V., and Randrianasol, B.1989. Consumption of cyanogenic bamboo by a newly discovered species of bamboo lemur. Am. J Primatol.19:119–124.

    Google Scholar 

  • Gleadow, R.M. and Woodrow, I. E., 2000a. Temporal and spatial variation in cyanogenic glycosides in Eucalyptus cladocalyx. Tree Physiol.20:591–598.

    Google Scholar 

  • Gleadow, R. M. and Woodrow, I. E.2000b. Polymorphism in cyanogenic glycoside content and cyanogenic β-glucosidase activity in natural populations of Eucalyptus cladocalyx. Aust. J. Plant Physiol.27:693–699.

    Google Scholar 

  • Gleadow, R. M., Foley, W., and Woodrow, I. E.1998. EnhancedCO2 alters the relationship between photosynthesis and defence in cyanogenic Eucalyptus cladocalyxF. Muell. Plant, Cell Environ.21:12–22.

    Google Scholar 

  • Goodger, J. Q., Capon, R.J., and Woodrow, I. E.2002. Cyanogenic polymorphism in Eucalyptus polyanthemosSchauer subsp. vestita L. Johnson and K. Hill (Myrtaceae). Biochem. Syst. Ecol.30:In press.

  • Harborne, J. B.1982. Introduction to Ecological Biochemistry. Academic Press, New York.

    Google Scholar 

  • Haskins, F. A., Gorz, H. J., and Johnson, B. E.1987. Seasonal variation in leaf hydrocyanic acid potential of low-and high-dhurrin sorghums. Crop Sci.27:903–906.

    Google Scholar 

  • Hopkins, A.1995. Factors influencing cattle bracken-poisoning in Great Britain, pp. 120–123, inR. Thornton Smith and J. A. Taylor (eds.). Bracken: An Environmental Issue. Bracken 94 Conference, Aberystwyth, Wales, July 1994. International Bracken Group Special Publication No. 2 August 1995.

  • Hruska, A. J.1988. Cyanogenic glucosides as defense compounds. A review of the evidence. J. Chem. Ecol.14:2213–2217.

    Google Scholar 

  • Hughes, M. A.1991. The cyanogenic polymorphism in Trifolium repensL. (white clover). Heredity66:105–115.

    Google Scholar 

  • Hughes, M. A.1992. A molecular and biochemical analysis of the structure of the cyanogenic β-glucosidase (Linamerase) from cassava (Manihot esculentaCranz). Arch. Biochem. Biophys.295:273–279.

    Google Scholar 

  • Jones, D. A.1962. Selective eating of the acyanogenic form of the plant Lotus corniculatusL. by various animals. Nature193:1109–1110.

    Google Scholar 

  • Jones, D. A.1972. Cyanogenic glycosides and their function, pp. 105–123, inJ. B. Harborne (ed.). Phytochemical Ecology. Proceedings of the Phytochemical Society No. 8. Academic Press, London.

    Google Scholar 

  • Jones, D.A.1988. Cyanogenesis in animal-plant interactions, pp. 151–165, inD. Evered and S. Harnett (eds.). Cyanide Compounds in Biology. John Wiley & Sons, Chichester, United Kingdom.

    Google Scholar 

  • Jones, D. A.1998. Why are so many food plants cyanogenic? Phytochemistry47:155–162.

    Google Scholar 

  • Kakes, P.1989. An analysis of the costs and benefits of the cyanogenic system in Trifolium repensL. Theor. Appl. Genet.77:111–118.

    Google Scholar 

  • Keymer, R. J. and Ellis, W. M.1978. Experimental studies on Lotus corniculatisL. from Anglesey polymorphic for cyanogenesis. Heredity40:189–206.

    Google Scholar 

  • King, N. L. R. and Bradbury, J. H.1995. Bitterness of cassava: Identification of a new apiosyl glucoside and other compounds that affect its bitter taste. J. Sci. Food Agric.68:223–230.

    Google Scholar 

  • Lechtenberg, M. and Nahrstedt, A.1999. Cyanogenic glycosides, pp. 147–191, inR. Ikan (ed.). Naturally Occurring Glycosides. John Wiley & Sons, Chichester, United Kingdom.

    Google Scholar 

  • Lieberei, R., Selmar, D., and Biehl, B.1985. Metabolisation of cyanogenic glucosides in Hevea brasiliensis. Plant Syst. Evol.150:49–63.

    Google Scholar 

  • Magalhaes, C. P., Xavier, J., and Campos, A. P.2000. Biochemical basis of the toxicity of manipueira (liquid extract of cassava roots) to nematodes and insects. Phytochem. Anal.11:57–60.

    Google Scholar 

  • Manning, K.1988. Detoxification of cyanide by plants and hormone action, pp. 92–110, inD. Evered and S. Harnett (eds.). Cyanide Compounds in Biology. John Wiley & Sons, Chichester, United Kingdom.

    Google Scholar 

  • Martin, J. H., Couch, J. F., and Briese, R. R.1938. Hydrocyanic acid content of different parts of the sorghum plant. J. Am. Soc. Agron.30:725–734.

    Google Scholar 

  • McBee, G. G. and Miller, F. R.1980. Hydrocyanic acid potential in several sorghum breeding lines as affected by nitrogen fertilization and variable harvests. Crop Sci.20:232–234.

    Google Scholar 

  • McMahon, J. M., White, W. L. B., and Sayre, R. T.1995. Cyanogenesis in cassava (Manihot esculentaCrantz). J. Exp. Bot.46:731–741.

    Google Scholar 

  • MØller, B. L. and Poulton, J. E.1993. Cyanogenic glucosides, pp. 183–207, inP. J. Lea (ed.). Methods in Plant Biochemistry, Volume 9. Academic Press, London.

    Google Scholar 

  • MØller, B. L. and Seigler, D. S.1999. Biosynthesis of cyanogenic glycosides, cyanolipids, and related compounds, pp. 563–609, inB. K. Singh (ed.). Plant Amino Acids: Biochemistry and Biotechnology. Marcel Dekker, New York.

    Google Scholar 

  • Mowat, D. J. and Clawson, S.1996. Oviposition and hatching of the clover weevil Sitona lepidusGyll (Coleoptera, Curculionidae). Grass Forage Sci.51:418–423.

    Google Scholar 

  • Nahrstedt, A.1985. Cyanogenesis and the role of cyanogenic compounds in insects Plant Syst. Evol.150:35–47.

    Google Scholar 

  • Nahrstedt, A.1988. Cyanogenic compounds as protecting agents for organisms, pp. 131–150, inD. Evered and S. Harnett (eds.). Cyanide Compounds in Biology. John Wiley & Sons, Chichester, United Kingdom.

    Google Scholar 

  • Nass, H. G.1972. Cyanogenesis: Its inheritance in Sorghum bicolor, Sorghum sudanese, Lotus, and Trifolium repens—a review. Crop Sci.12:503–506.

    Google Scholar 

  • Osbourne, A. E.1996. Preformed antimicrobial compounds and plant defense against fungal attack. Plant Cell8:1821–1831.

    Google Scholar 

  • Patel, C. J. and Wright, M. J.1958. The effect of certain nutrients upon the hydrocyanic acid content of sudan grass grown in nutrient solution. Agron. J.50:645–647.

    Google Scholar 

  • Patton, C. A., Ranney, T. G., Burton, J. D., and Wallenbach, J. F.1997. Natural pest resistance of Prunustaxa to feeding by adult Japanese beetles—role of endogenous allelochemicals in host plant resistance. J. Am. Soc. Hortic. Sci.122:668–672.

    Google Scholar 

  • Poulton, J. E.1988. Localization and catabolism of cyanogenic glycosides, pp. 67–91, inD. Evered and S. Harnett (eds.). Cyanide Compounds in Biology. John Wiley & Sons, Chichester, United Kingdom.

    Google Scholar 

  • Pratt, A.1937. The Call of the Koala. Robertson & Mullens, Melbourne.

    Google Scholar 

  • Provenza, F. D., Pfister, J. A., and Cheney, C. D.1992. Mechanisms of learning in diet selection with reference to phytotoxicosis in herbivores J. Range Manage.45:36–45.

    Google Scholar 

  • Robinson, M. E.1930. Cyanogenesis in plants. Biol. Rev.5:126–142.

    Google Scholar 

  • Saucy, F., Studer, J., aerni, V., and Schneiter, B.1999. Preference for acyanogenic white clover (Trifolium repens) in the vole Arvicola terrestris: I. Experiments with two varieties. J. Chem. Ecol.25:1441–1454.

    Google Scholar 

  • Saunders, J. A., Conn, E. E., Chin Ho Lin, and Stocking, C. R.1977. Subcellular localization of the cyanogenic glycoside of Sorghumby autoradiography. Plant Physiol.59:647–652.

    Google Scholar 

  • Schappert, P. J. and Shore, J. S.1999a. Cyanogenesis in Turnera ulmifoliaL. (Turneraceae). I. Phenotypic distribution and genetic variation for cyanogenesis on Jamaica. Heredity74:392–404.

    Google Scholar 

  • Schappert, P. J. and Shore, J. S.1999b. Effects of cyanogenesis polymorphism in Turnera ulmifoliaon Euptoieta hegesiaand potential Anolispredators. J. Chem. Ecol.25:1455–1479.

    Google Scholar 

  • Schappert, P. J. and Shore, J. S.1999c. Cyanogenesis, herbivory and plant defense in Turnera ulmifoliaon Jamaica. Ecoscience6:511–520.

    Google Scholar 

  • Schappert, P. J. and Shore, J. S.2000. Cyanogenesis in Turnera ulmifoliaL. (Turneraceae). I. Developmental expression, heritability and cost of cyanogenesis. Evol. Ecol. Res.2:337–352.

    Google Scholar 

  • Schreiner, I., Nafus, D., and Pimentel, D.1984. Effects of cyanogenesis in bracken fern (Pteridium aquilinum) on associated insects. Ecol. Entomol.9:69–70.

    Google Scholar 

  • Schwarz, B., Wray, V., and Proksch, P.1996. A cyanogenic glycoside from Canthium schimperianum. Phytochemistry42:633–636.

    Google Scholar 

  • Scriber, J. M.1978. Cyanogenic glycosides in Lotus corniculatus. Their effect upon growth, energy budget, and nitrogen utilization of the southern armyworm, Spodoptera eridania. Oecologia34:143–155.

    Google Scholar 

  • Seigler, D. S.1998. Cyanogenic glycosides and cyanolipids, pp. 273–296, inD. S. Seigler (ed.). Plant Secondary Metabolism. Kluwer Academic Press, Boston.

    Google Scholar 

  • Selmar, D.1993. Transport of cyanogenic glucosides: Linustatin uptake by Heveacotyledons. Planta191:191–199.

    Google Scholar 

  • Selmar, D., Lieberei, R., and Biehl, B.1988. Mobilization and utilization of cyanogenic glycosides. The linustatin pathway. Plant Physiol.86:711–716.

    Google Scholar 

  • Swain, E., Li, C. P., and Poulton, J. E.1992. Tissue and subcellular localization of enzymes catabolizing (R)-amygdalin in mature Prunus serotinaseeds. Plant Physiol.100:291–300.

    Google Scholar 

  • Tattersal, D. B., Bak, S., Jones, P. R., Olsen, C. E., Nielsen, J. K., Hansen, M. L., HØj, P. B., and MØller, B. L.2001. Resistance to an herbivore through engineered glucoside synthesis. Science293:1826–1828.

    Google Scholar 

  • Thomsen, K. and Brimer, L.1997. Cyanogenic constituents in woody plants in natural lowland rain forest in Costa Rica. Bot. J. Linn. Soc.124:273–294.

    Google Scholar 

  • Viette, M., Tettamanti, C., and Saucy, F.2000. Preference for acyanogenic white clover (Trifolium repens) in the vole Arvicola terrestris. II. Generlization and further investigations. J. Chem. Ecol.26:101–122.

    Google Scholar 

  • Webber, J. J., Roycroft, C. R., and Callinan, J. D.1985. Cyanide poisoning of goats from sugar gums (Eucalyptus cladocalyx). Aust. Vet. J.62:28.

    Google Scholar 

  • Woodrow, I. E.1994. Optimal acclimation of the C3 photosynthetic system under enhanced CO2. Photosynth. Res.39:410–412.

    Google Scholar 

  • Zentek, J.1997. Case report – bloat and diarrhoea in calves. [German] Deutsch. Tier. Wochenschr.104:153–155.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Botany, The University of Melbourne, Victoria, Australia, 3010

    Roslyn M. Gleadow & Ian E. Woodrow

Authors
  1. Roslyn M. Gleadow
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ian E. Woodrow
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Roslyn M. Gleadow.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gleadow, R.M., Woodrow, I.E. Mini-Review: Constraints on Effectiveness of Cyanogenic Glycosides in Herbivore Defense. J Chem Ecol 28, 1301–1313 (2002). https://doi.org/10.1023/A:1016298100201

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1016298100201

Search

Navigation