Skip to main content
SpringerLink
Log in

Decreased Response to Feeding Deterrents Following Prolonged Exposure in the Larvae of a Generalist Herbivore, Trichoplusia ni (Lepidoptera: Noctuidae)

  • Published:
Journal of Insect Behavior Aims and scope Submit manuscript

Abstract

We investigated the role of experience with several antifeedants on the feeding behavior of a generalist herbivore, Trichoplusia ni. Second-, third-, and fifth-instar larvae of T. ni were examined for their feeding responses to plant extracts (Melia volkensii, Origanum vulgare) and individual plant allelochemicals (cymarin, digitoxin, xanthotoxin, toosendanin, and thymol), after being exposed to them continually beginning as neonates. All tested instars of T. ni were capable of showing a decreased antifeedant response following prolonged exposure to most of the antifeedants tested compared with their naive conspecifics. Cardenolides (digitoxin and cymarin) were the exceptions. The response to oregano was affected as a result of previous exposure to different concentrations of oregano, unlike M. volkensii, leading us to conclude that T. ni sensitivity varies between stimuli and cannot be generalized. To demonstrate that decreased deterrence following prolonged exposure to M. volkensii was the result of learned habituation, three aversive stimuli were used. A high concentration of the particular antifeedant, xanthotoxin, acted as a noxious stimulus and dishabituated (reversed) the decrement in the antifeedant response to M. volkensii. Cold shock or CO2 was marginally effective in dishabituating the response. The fact that the decrease in antifeedant response can be dishabituated has implications for pest management.

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

  • Berdegue, M., White, K. K., and Trumble, J. T. (1997). Feeding deterrence of Spodoptera ex-igua (Lepidoptera: Noctuidae) larvae by low concentrations of linear furanocoumarins. Environ. Entomol. 26: 912–919.

    Google Scholar 

  • Berenbaum, M. R., Nitao, J. K., and Zangeri, A. R. (1991) Adaptive variation in the fura-nocoumarin composition of Pastinaca sativa (Apiaceae). J. Chem. Ecol. 17: 207–215.

    Google Scholar 

  • Bernays, E. A. (1983). Antifeedants in crop pest management. In Whitehead, D. L., and Bowers, W. S. (eds.), Natural Products for Innovative Pest Management, Pergamon Press, Oxford, pp. 259–271.

    Google Scholar 

  • Bernays, E. A., and Chapman, R. F. (1978). Plant chemistry and acridoid feeding behavior. In Harborne, J. B. (ed.), Coevolution of Plants and Animals, Academic Press, London, pp. 99–141.

    Google Scholar 

  • Bernays, E. A., and Chapman, R. F. (1994). Host Plant Selection by Phytophagous Insects, Chapman and Hall, New York, pp. 206–229.

    Google Scholar 

  • Bernays, E. A., and Chapman, R. F. (2000). Plant secondary compounds and grasshoppers: Beyond plant defenses. J. Chem. Ecol. 26: 1773–1794.

    Google Scholar 

  • Bernays, E. A., and Weiss, M. R. (1996). Induced food preferences in caterpillars: the need to identify mechanism. Entomol. Exp. Appl. 78: 1–8.

    Google Scholar 

  • Blaney, W. M., Schoonoven, L. M., and Simmonds, M. S. J. (1986). Sensitivity variations in insect chemoreceptors; A review. Experentia 42: 13–19.

    Google Scholar 

  • Bomford, M. K., and Isman, M. B. (1996). Desensitization of fifth instar Spodoptera litura to azadirachtin and neem. Entomol. Exp. Appl. 81: 307–313.

    Google Scholar 

  • Carew, T. J., and Sahley, C. L. (1986). Invertebrate learning and memory: From behavior to molecules. Annu. Rev. Neurosci. 9: 435–487.

    Google Scholar 

  • Chen, W., Isman, M. B., and Chiu, S. F. (1995). Antifeedant and growth inhibitory effects of the limonoid toosendanin and Melia toosendan extracts on the variegated cutworm, Peridroma saucia. J. Appl. Entomol. 119: 367–370.

    Google Scholar 

  • Chiu, S. F. (1984). The active principles and insecticidal properties of some Chinese plants with special reference to Meliaceae. In Schmutterer, H., and Ascher, K. R. S. (eds.), Natural Pesticides from the Neem Tree and Other Tropical Plants, Proc. 2nd Int. Neem Conf., Schrift der GTZ 161: 255–262.

  • Chiu, S. F. (1985). Experiments on the application of toosendanin, a natural product form Melia toosendan for the control of the cabbageworm (Pieris rapae L.). Acta Phytophylact. Sin. 12: 125–132.

    Google Scholar 

  • Chiu, S. F. (1989). Recent advances in research on botanical insecticides in China. In Aranson, B. J. R. Philogene and Morand, P. (eds.), Insecticides of Plant Origin, Am. Chem. Soc. Symp. Ser. 387, pp. 69–77.

  • Dethier, V. G. (1982). Mechanisms of host-plant recognition. Entomol. Exp. Appl. 31: 49–56.

    Google Scholar 

  • Dimock, M. B., Renwick, J. A. A., Radke, C. D., and Sachdev-Gupta, K. (1991). Chemical constituents of an unacceptable crucifer, Erysimum cheiranthoides, deter feeding by Pieris rapae. J. Chem. Ecol. 17: 525–533.

    Google Scholar 

  • Gill, J. S. (1972). Studies on Insect Feeding Deterrents with Special Reference to Fruit Extracts of the Neem Tree, Azadirachta indica A. Juss. Ph.D. thesis, University of London, London.

    Google Scholar 

  • Huang, X. P., and Renwick, J. A. A. (1994). Cardenolides as oviposition deterrents to two Pieris species: Structure-activity relationships. J. Chem. Ecol. 20: 1039–1051.

    Google Scholar 

  • Huang, X. P., and Renwick, J. A. A. (1995). Cross habituation to feeding deterrents and acceptance of a marginal host plant by Pieris rapae larvae. Entomol. Exp. Appl. 76: 295–302.

    Google Scholar 

  • Hummelbrunner, L. A., and Isman, M. B. (2001). Acute, sublethal, antifeedant, and synergistic effects of monoterpenoid essential oil compounds on the tobacco cutworm, Spodoptera litura. J. Agr. Food Chem. 49(2): 715–720.

    Google Scholar 

  • Isman, M. B. (2002). Insect antifeedants. Pestic. Outlook 13: 129–176.

    Google Scholar 

  • Isman, M. B., Koul, O., Luczynski, A., and Kaminski, A. (1990). Insecticidal and antifeedant bioactivities of neem oils and their relationship to azadirachtin content. J. Agr. Food Chem. 38: 1406–1411.

    Google Scholar 

  • Isman, M. B., Wan, A. J., and Passreiter, C. (2001). Insecticidal activities of essential oils to the tobacco cutworm, Spodoptera litura. Fitoterapia 72: 65–68.

    Google Scholar 

  • Jermy, T. (1966). Feeding inhibitors and food preference in chewing phytophagous insects. Entomol. Exp. Appl. 9: 1–12.

    Google Scholar 

  • Jermy, T. (1987). The role of experience in the host selection of phytophagous insects. In Chapman, R. F., Bernays, E. A., and Stoffolano, J. G. (eds.), Perspectives in Chemoreception and Behavior, Springer-Verlag, New York, pp. 143–157.

    Google Scholar 

  • Jermy, T., Bernays, E. A., and Szentesi, A. (1982). The effect of repeated exposure to feeding deterrents on their acceptability to phytophagous insects. In Visser, J. H., and Minks, A. K. (eds.), Proceedings, 5th International Symposium Insect-Plant Relationships, Waginengen, PU DOC, Waningen, pp. 25–32.

    Google Scholar 

  • Karpouhtsis, I., Pardali, E., Feggou, E., Kokkini, S., Scouras, Z. G., and Mavragan-Tsipidou, P. (1998). Insecticidal and genotoxic activities of oregano essential oils. J. Agr. Food Chem. 46: 1111–1115.

    Google Scholar 

  • Ma, W. C. (1972). Dynamics of feeding responses in Pieris brassicae Linn. as a function of chemosensory input: A behavioral, ultrastructural, and physiological study. Meded. Land-bouwhogesch. Wageningen 72: 1–162.

    Google Scholar 

  • Miller, J. R., and Strickler, K. L. (1984). Finding and accepting host plants. In Bell, W., and Carde, R. (eds.), Chemical Ecology of Insects, Chapman and Hall, London, pp. 127–155.

    Google Scholar 

  • Mitchell, B. K., and Sutcliffe, J. F. (1984). Sensory inhibition as a mechanism of feeding deterrence: Effects of three alkaloids on leaf beetle feeding. Physiol. Entomol. 9: 57–64.

    Google Scholar 

  • Mwangi, R. W. (1982). Locust antifeedant activity in fruits of Melia volkensii. Entomol. Exp. Appl. 32: 277–280.

    Google Scholar 

  • Mwangi, R. W., and Rembold, H. (1987). Growth regulating activity of Melia volkensii extracts against the larvae of Aedes aegypti. In Schmutterer, H., and Ascher, K. R. S. (eds.), Proc. 3rd Int. Neem Conf., Schrift der GTZ, Vol. 206, pp. 669–681.

  • Mwangi, R. W., and Rembold, H. (1988). Growth inhibiting and larvicidal effects of Melia volkensii extracts on Aedes aegypti larvae. Entomol. Exp. Appl. 46: 103–108.

    Google Scholar 

  • Raffa, K. F., and Frazier, J. L. (1988). Ageneral model for quantifying behavioral desensitization to antifeedants. Entomol. Exp. Appl. 46: 93–100.

    Google Scholar 

  • Renwick, J. A. A., Radke, C. D., and Sachdev-Gupta, K. (1989). Chemical constituents of Erysimum cheiranthoides: Deterring oviposition by the cabbage butterfly, Pieris rapae. J. Chem. Ecol. 15: 2161–2169.

    Google Scholar 

  • Sachdev-Gupta, K., Radke, C. D., and Renwick, J. A. A. (1993a). Antifeedant activity of cucurbitacins from Iberis amara against larvae of Pieris rapae. Phytochemistry 33: 1385–1388.

    Google Scholar 

  • Sachdev-Gupta, K., Radke, C. D., Renwick, J. A. A., and Dimmock, M. B. (1993b). Cardenolides from Erysimum cheiranthoides: Feeding deterrents to Pieris rapae larvae. J. Chem. Ecol. 19: 1355–1369.

    Google Scholar 

  • Schoonhoven, L. M. (1977). On the individuality of insect feeding behavior. Proc. Kon. Ned. Akad. Wtsch. C 72: 491–498.

    Google Scholar 

  • Schoonhoven, L. M. (1982). Biological aspects of antifeedants. Entomol. Exp. Appl. 31: 57–69.

    Google Scholar 

  • Schoonhoven, L. M. (1987). What makes a caterpillar eat? The sensory code underlying feedin behavior. In Chapman, R. F., Bernays, E. A., and Stoffolano, J. G. (eds.), Perspectives in Chemoreception and Behavior, Springer-Verlag, New York, pp. 69–97.

    Google Scholar 

  • Simmonds, M. S. J., and Blaney, W. M. (1984). Some neurophysiological effects of azadirachtin on lepidopterous larvae and their feeding responses. In Schmutterrer, H., and Ascher, K. R. S. (eds.), Natural Pesticides from the Neem Tree (Azadirachta indica A. Juss) and Other Tropical Plants, Proc. 2nd Int. Neem Conf. Schrift der GTZ 161: 163–180.

  • Sivropoulou, A., Papanikolaou, E., Nikolaou, C., Kokkini, S., Lanaras, T., and Arsenakis, M. (1996). Antimicrobial and cytotoxic activities of Origanum essential oils. J. Agr. Food Chem. 44: 1202–1205.

    Google Scholar 

  • Statistix 7 (2000). Analytical Software, Statistix 7 for Windows 95, 98, NT, 2000, Analytical Software, Tallahassee, FL.

    Google Scholar 

  • Szentesi, A., and Bernays, E. A. (1984). Astudy of behavioral habituation to a feeding deterrent in nymphs of Schistocerca gregaria. Physiol. Entomol. 9: 329–340.

    Google Scholar 

  • Szentesi, A., and Jermy, T. (1989). The role of experience in host plant choice by phytophagous insects. In Bernays, E. A. (ed.), Insect-Plant Interactions, Vol. 2, CRC Press, Boca Raton, FL pp. 39–74.

    Google Scholar 

  • Thompson, D. P. (1989). Fungitoxic activity of essential oil components on food storage fungi. Mycologia 81: 151–153.

    Google Scholar 

  • Thompson, R. F., and Spencer, W. F. (1966). Habituation: A model phenomenon for the study of neuronal substrates of behavior. Psychol. Rev. 73: 16–43.

    Google Scholar 

  • Usher, B. F., Bernays, E. F., and Barbehenn, R. V. (1988). Antifeedant tests with larvae of Pseudaletia unipuncta: Variability of behavioral response. Entomol. Exp. Appl. 48: 203–212

    Google Scholar 

  • Yajima, T., and Munakata, K. (1979). Phloroglucinol type furanocoumarins, a group of potent naturally-occurring insect antifeedants. Agr. Biol. Chem. 43: 1701–1706.

    Google Scholar 

  • Zar, J. H. (1984). Biostatistical Analysis, Prentice–Hall, Englewood Cliffs, NJ, pp. 168–190.

    Google Scholar 

  • Zhang, X., and Chiu, S.-F. (1983). The antifeeding and repellent effects of meliaceous plants to some insect pests. J. South China Agr. Univ. 4: 1–7.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Agricultural Sciences, University of British Columbia, Vancouver, BC, Canada, V6T 1Z4

    Yasmin Akhtar & Murray B. Isman

  2. Department of Psychology, University of British Columbia, Vancouver, BC, Canada, V6T 1Z4

    Catharine H. Rankin

Authors
  1. Yasmin Akhtar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Catharine H. Rankin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Murray B. Isman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Murray B. Isman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Akhtar, Y., Rankin, C.H. & Isman, M.B. Decreased Response to Feeding Deterrents Following Prolonged Exposure in the Larvae of a Generalist Herbivore, Trichoplusia ni (Lepidoptera: Noctuidae). Journal of Insect Behavior 16, 811–831 (2003). https://doi.org/10.1023/B:JOIR.0000018322.45068.a9

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:JOIR.0000018322.45068.a9

Search

Navigation