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How do herbivorous insects cope with noxious secondary plant compounds in their diet?

  • Conference paper
Proceedings of the 11th International Symposium on Insect-Plant Relationships

Part of the book series: Series Entomologica ((SENT,volume 57))

Abstract

Herbivorous insects use a variety of physiological mechanisms to cope with noxious (i.e., unpalatable and/or toxic) compounds in their food plants. Here, I review what is known about this coping process, focusing on one species of caterpillar, the tobacco hornworm (Manduca sexta). Herbivorous insects possess both preingestive (i.e., chemosensory) and postingestive response mechanisms for detecting plant secondary compounds. Stimulation of either class of detection mechanism inhibits feeding rapidly by reducing biting rate and/or bite size. This aversive response is highly adaptive during encounters with secondary plant compounds that are toxic. The insect’s dilemma is that many harmless or mildly toxic compounds also activate the aversive response. To overcome this dilemma, herbivorous insects employ at least three mechanisms for selectively deactivating their aversive response to relatively harmless secondary plant compounds: (1) the presence of carbohydrates can mask the unpalatable taste of some secondary plant compounds; (2) prolonged dietary exposure to some unpalatable secondary plant compounds can initiate long-term adaptation mechanisms in the peripheral and central gustatory system; and (3) dietary exposure to toxic compounds can induce production of P450 detoxication enzymes. Thus, herbivorous insects utilize an integrated suite of physiological mechanisms to detect potentially toxic compounds in foods, and then selectively adapt to those that do not pose a serious threat to their growth and survivorship.

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References

  • Baldwin, I. T., 1998. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proceedings of the National Academy of Sciences U.S.A. 95: 8113–8118.

    Article  CAS  Google Scholar 

  • Bernays, E. A. 1990. Plant secondary compounds deterrent but not toxic to the grass specialist acridid Locusta migratoria: implications for the evolution of graminivory. Entomologia Experimentalis et Applicata 54: 53–56.

    Article  CAS  Google Scholar 

  • Bernays, E. A., 1991. Relationship between deterrence and toxicity of plant secondary metabolites for the grasshopper Schistocerca americana. Journal of Chemical Ecology 17: 2519–2526.

    Article  CAS  Google Scholar 

  • Bernays, E. A., 1997. Feeding by lepidopteran larvae is dangerous. Ecological Entomology 22: 121–123.

    Article  Google Scholar 

  • Bernays, E. A., 1998. Evolution of feeding behavior in insect herbivores. Bioscience 48: 35–44.

    Article  Google Scholar 

  • Bernays, E. A. & R. F. Chapman, 1987. The evolution of deterrent responses in plant-feeding insects. In: R. F. Chapman, E. A. Bernays & J. G. Stoffolano, Jr. (eds), Perspectives in Chemoreception and Behavior, Springer-Verlag, New York, pp. 159–173.

    Chapter  Google Scholar 

  • Bernays, E. A. & R. F. Chapman, 1994. Host-Plant Selection by Phytophagous Insects. Chapman and Hall, New York.

    Google Scholar 

  • Bernays, E. A. & M. Cornelius, 1992. Relationship between deterrence and toxicity of plant secondary compounds for the alfalfa weevil Hypera brunneipennis. Entomologia Experimentalis et Applicata 64: 289–292.

    Article  CAS  Google Scholar 

  • Bernays, E. A. & H. A. Woods, 2000. Foraging in nature by larvae of Manduca sexta - influenced by an endogenous oscillation. Journal of Insect Physiology 46: 825–836.

    Article  PubMed  CAS  Google Scholar 

  • Blaney, W. M. & M. S. J. Simmonds, 1987. Experience: a modifier of neural and behavioural sensitivity. In: V. Labeyrie, G. Fab-res and D. Lachaise (eds), Insects-Plants, Dr. W. Junk Publishers, Dordrecht, The Netherlands, pp. 237–241.

    Google Scholar 

  • Blaney, W. M. & M. S. J. Simmonds, 1990. A behavioural and electrophysiological study of the role of tarsal chemoreceptors in feeding by adults of Spodoptera, Heliothis virescens and Helicoverpa armigera. Journal of Insect Physiology 36: 743–756.

    Article  CAS  Google Scholar 

  • Blom, F., 1978. Sensory activity and food intake: a study of input-output relationships in two phytophagous insects. Netherlands Journal of Zoology 28: 277–340.

    Article  Google Scholar 

  • Boer, G. de, 1993. Plasticity in food preference and diet-induced differential weighting of chemosensory information in larval Manduca sexta. Journal of Insect Physiology 39: 17–24.

    Article  Google Scholar 

  • Brattsten, L. B., C. F. Wilkinson and T. Eisner, 1977. Herbivore-plant interactions: Mixed-function oxidases and secondary plant substances. Science 196: 1349–1352.

    Google Scholar 

  • Chapman, R. F., A. A.coli-Christensen and P. R. White, 1991. Sensory coding for feeding deterrence in the grasshopper Schistocerca americana. Journal of Experimental Biology 158: 24 1259.

    Google Scholar 

  • Cottee, P. K., E. A. Bernays and A. J. Mordue, 1988. Comparisons of deterrency and toxicity of selected secondary plant compounds to an oligophagous and a polyphagous acridid. Entomologia Experimentalis et Applicata 46: 241–247.

    Article  CAS  Google Scholar 

  • Dahanukar, A., K. Foster, W. M. van der Goes van Naters and J. R. Carlson, 2001. A Gr receptor is required for response to the sugar

    Google Scholar 

  • trehalose in taste neurons of Drosophila. Nature Neuroscience 4: 1182–1186.

    Google Scholar 

  • Dethier, V. G., 1980. Evolution of receptor sensitivity to secondary plant substances with special reference to deterrents. American Naturalist 115: 45–66.

    Article  Google Scholar 

  • Dethier, V. G., 1993. The role of taste in food intake: a comparative view. In: S. A. Simon and S. D. Roper (eds), Mechanisms of Taste Transduction, CRC Press, Boca Raton, pp. 3–25.

    Google Scholar 

  • Dethier, V. G. and E. Bowdan, 1989. The effect of alkaloids on the sugar receptors of the blowfly. Physiological Entomology 14: 127–136.

    Article  CAS  Google Scholar 

  • Detzel, A. and M. Wink, 1993. Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicals. Chemoecology 4: 8–18.

    Article  CAS  Google Scholar 

  • Frazier, J. L., 1986. The perception of plant allelochemicals that inhibit feeding. In: L. B. Brattsten and S. Ahmad (eds), Molecular Aspects of Insect-Plant Interactions, Plenum Press, New York, pp. 1–42.

    Chapter  Google Scholar 

  • Glendinning, J. I., 1996. Is chemosensory input essential for the rapid rejection of toxic foods? The Journal of Experimental Biology 199: 1523–1534.

    PubMed  CAS  Google Scholar 

  • Glendinning, J. I. and N. A. Gonzalez, 1995. Gustatory habituation to deterrent compounds in a grasshopper: concentration and compound specificity. Animal Behaviour 50: 915–927.

    Article  Google Scholar 

  • Glendinning, J. I. and T. T. Hills, 1997. Electrophysiological evidence for two transduction pathways within a bitter-sensitive taste receptor. Journal of Neurophysiology 78: 734–745.

    PubMed  CAS  Google Scholar 

  • Glendinning, J. I. and F. Slansky, Jr., 1995. Consumption of a toxic food by caterpillars increases with dietary exposure: evidence for a role of detoxification enzymes. Journal of Comparative Physiology A 176: 337–345.

    Article  CAS  Google Scholar 

  • Glendinning, J. I., S. Valcic and B. N. Timmermann, 1998. Maxillary palps can mediate taste rejection of plant allelochemicals by caterpillars. Journal of Comparative Physiology A 183: 35–44.

    Article  CAS  Google Scholar 

  • Glendinning, J. I., M. Tarre and K. Asaoka, 1999. Contribution of different bitter-sensitive taste cells to feeding inhibition in a caterpillar (Manduca sexta). Behavioral Neuroscience 113: 840–854.

    Article  PubMed  CAS  Google Scholar 

  • Glendinning, J. I., N. Nelson and E. A. Bernays, 2000a. How do inositol and glucose modulate feeding in Manduca sexta caterpillars? The Journal of Experimental Biology 203: 1299–1315.

    PubMed  CAS  Google Scholar 

  • Glendinning, J. I., N. Chaudhari and S. C. Kinnamon, 2000b. Taste transduction and molecular biology. In: T. Finger, W. L. Silver

    Google Scholar 

  • and D. Restrepo (eds), The Neurobiology of Taste and Smell, 2nd ed., Wiley-Liss, New York, pp. 315–351.

    Google Scholar 

  • Glendinning, J. I., H. Brown, M. Capoor, A. Davis, A. Gbedemah

    Google Scholar 

  • and E. Long, 2001a. A peripheral mechanism for behavioral adaptation to specific `bitter’ taste stimuli in an insect. The Journal of Neuroscience 21: 3688–3696.

    Google Scholar 

  • Glendinning, J. I., S. Domdom and E. Long, 2001b. Selective adaptation to noxious foods by an insect. Journal of Experimental Biology 204: 3355–3367.

    PubMed  CAS  Google Scholar 

  • Hansberry, R. and W. W. Middlekauff, 1940. Toxicity of nicotine administered internally to several species of insect. Journal of Economic Entomology 33: 511–517.

    CAS  Google Scholar 

  • Harborne, J. B. and H. Baxter, 1993. Phytochemical Dictionary: A Handbook of Bioactive Compounds from Plants. Taylor and Francis, Washington, D.C.

    Google Scholar 

  • Harley, K. L. S. and A. J. Thorsteinson, 1967. The influence of plant chemicals on the feeding behavior, development, and survival of the two-striped grasshopper, Melanoplus bivittatus (Say), Acrididae: Orthoptera. Canadian Journal of Zoology 45: 305–319.

    Google Scholar 

  • Ishimoto, H., A. Matsumoto and T. Tanimura, 2000. Molecular identification of a taste receptor gene for trehalose in Drosophila. Science 289: 116–119.

    Article  PubMed  CAS  Google Scholar 

  • Jenny, T., E. A. Bernays and A. Szentesi, 1982. The effect of repeated exposure to feeding deterrents on their acceptability to phytophagous insects. In: H. Visser and A. Minks (eds), Proceedings of the 5th international Symposium on Insect-Plant Relationships, PUDOC, Wageningen, pp. 25–32.

    Google Scholar 

  • Loon, J. J. A. van and L. M. Schoonhoven, 1999. Specialist deterrent chemoreceptors enable Pieris caterpillars to discriminate between chemically different deterrents. Entomologia Experimentalis et Applicata 91: 29–35.

    Article  Google Scholar 

  • Ma, W.-C., 1972. Dynamics of feeding responses in Pieris brassicae Linn as a function of chemosensory input: a behavioural and electrophysiological study. Mededelingen Landbouwhogeschool Wageningen 72–11: 1–162.

    Google Scholar 

  • Morris, C. E., 1983. Uptake and metabolism of nicotine by the CNS of a nicotine-resistant insect, the tobacco hornworm (Manduca sexto). Journal of Insect Physiology 29: 807–817.

    Article  CAS  Google Scholar 

  • Morris, C. E., 1984. Eletrophysiological effects of cholinergic agents on the CNS of a nicotine-resistant insect, the tobacco hornworm (Manduca sexta). The Journal of Experimental Biology 229: 361–374.

    CAS  Google Scholar 

  • Mullin, C. A., S. Chyb, H. Eichenseer, B. Hollister and J. L. Frazier, 1994. Neuroreceptor mechanisms in insect gustation: a pharmacological approach. Journal of Insect Physiology 40: 913–931.

    Article  CAS  Google Scholar 

  • Murakami, M. and H. Kijima, 2000. Transduction ion channels directly gated by sugars on the insect taste cell. Journal of General Physiology 15: 455–466.

    Article  Google Scholar 

  • Negherbon, W. 0., 1959. Handbook of Toxicology. Vol. III: Insecticides, A Compendium, W.B. Saunders Co., Philadelphia.

    Google Scholar 

  • Nelson, N. and E. A. Bernays, 1998. Inositol in two host plants of Manduca sexto. Entomologia Experimentalis et Applicata 88: 189–191.

    Article  CAS  Google Scholar 

  • Peterson, S. C., F. E. Hanson and J. D. Warthen Jr., 1993. Deterrence coding by a larval Manduca chemosensory neurone mediating rejection of a non-host plant, Canna generalis L. Physiological Entomology 18: 285–295.

    Article  Google Scholar 

  • Schoonhoven, L. M., 1969. Sensitivity changes in some insect chemoreceptors and their effect on food selection behavior. Proceedings Koninklijke Nederlandse Akademie van Wetenschappen ( Amsterdam ), Series C 72: 491–498.

    Google Scholar 

  • Schoonhoven, L. M., 1972. Plant recognition by lepidopterous larvae. In: H. F. van Emden (eds), Insect/Plant Relationships, Blackwell Scientific Publications, Oxford, pp. 87–99.

    Google Scholar 

  • Schoonhoven, L. M., 1978. Long-term sensitivity changes in some insect taste receptors. Drug Research (Abstract) 28: 2367.

    Google Scholar 

  • Schoonhoven, L. M. and F. Blom, 1988. Chemoreception and feeding behavior in a caterpillar: towards a model of brain functioning in insects. Entomologia Experimentalis et Applicata 49: 123–129.

    Article  Google Scholar 

  • Schoonhoven, L. M. & J. J. A. van Loon, 2002. An inventory of taste in caterpillars: each species is its own key. Acta Zoologica Academiae Scientiarum Hungaricae 48 (Suppl. 1): 215–263.

    Google Scholar 

  • Shields, V. D. C. & B. K. Mitchell, 1995a. Sinigrin as a feeding deterrent in two crucifer-feeding, polyphagous lepidopterous species and the effects of feeding stimulant mixtures on deterrency. Philosophical Transactions of the Royal Society of London B 347: 439–446.

    Article  CAS  Google Scholar 

  • Shields, V. D. C. & B. K. Mitchell, 1995b. The effect of phagostimulant mixtures on deterrent receptor(s) in two crucifer-feeding lepidopterous species. Philosophical Transactions of the Royal Society of London B 347: 459–464.

    Article  CAS  Google Scholar 

  • Simmonds, M. S. J. & W. M. Blaney, 1983. Some neurophysiological effects of azadirachtin on lepidopterous larvae and their feeding response. In: H. Schmutterer and K. R. S. Ascher (eds), Proceedings of the Second International Neem Conference, Deutsche Gesellschaft für Technische Zusammernarbeit (GTZ) GmbH, Eschborn: 163–180.

    Google Scholar 

  • Slansky, J. F., 1993. Nutritional ecology: the fundamental quest for nutrients. In: N. E. Stamp & T. M. Casey (eds), Caterpillars: Ecological and Evolutionary Constraints on Foraging, Chapman and Hall, New York, pp. 29–91.

    Google Scholar 

  • Snyder, M. S. & J. I. Glendinning, 1996. Causal connection between detoxification enzyme activity and consumption of a toxic plant compound. Journal of Comparative Physiology A 179: 255–261.

    Google Scholar 

  • Snyder, M. J., E.-L. Hsu & R. Feyereisen, 1993. Induction of cytochrome P-450 activities by nicotine in the tobacco hornworm, Manduca sexto. Journal of Chemical Ecology 19: 2903–2916.

    Article  CAS  Google Scholar 

  • Snyder, M. J., J. K. Walding & R. Feyereisen, 1994. Metabolic fate of the allelochemical nicotine in the tobacco hornworm Manduca sexto. Insect Biochemistry and Molecular Biology 24: 837–846.

    Article  CAS  Google Scholar 

  • Szentesi, A. & E. A. Bemays, 1984. A study of behavioural habituation to a feeding deterrent in nymphs of Schistocerca gregaria. Physiological Entomology 9: 329–340.

    Google Scholar 

  • Usher, B. F., E. A. Bernays & R. V. Barbehenn, 1988. Antifeedant tests with larvae of Pseudaletia unipuncta: variability of behavioral response. Entomologia Experimentalis et Applicata 48: 203–212.

    Article  Google Scholar 

  • Yu, S. J. & E. L. Hsu, 1993. Induction of detoxification enzymes in phytophagous insects: Roles of insecticide synergists, larval age and species. Archives of Insect Biochemistry and Physiology 24: 21–32.

    Google Scholar 

  • Zangerl, A. R. & M. R. Berenbaum, 1993. Plant chemistry, insect adaptations to plant chemistry, and host plant utilization patterns. Ecology 74: 47–54.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biological Science, Barnard College, Columbia University, 3009 Broadway, New York, NY, 10027, USA

    John I. Glendinning

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  1. John I. Glendinning
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Editors and Affiliations

  1. Chemistry Department, Royal Veterinary and Agricultural University, Thorvaldsensvej 40, DK-1871, Frederiksberg C, Denmark

    Jens Kvist Nielsen

  2. Danish Environmental Research Institute, Vejlsøvej 25, DK-8600, Silkeborg, Denmark

    Christian Kjær

  3. Department of Entomology, Wageningen University, Binnenhaven 7, P.O. Box 8031, NL-6700 EH, Wageningen, The Netherlands

    Louis M. Schoonhoven

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© 2002 Springer Science+Business Media Dordrecht

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Glendinning, J.I. (2002). How do herbivorous insects cope with noxious secondary plant compounds in their diet?. In: Nielsen, J.K., Kjær, C., Schoonhoven, L.M. (eds) Proceedings of the 11th International Symposium on Insect-Plant Relationships. Series Entomologica, vol 57. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-2776-1_2

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  • DOI: https://doi.org/10.1007/978-94-017-2776-1_2

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-90-481-6129-4

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