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Larval Exposure to Oviposition Deterrents Alters Subsequent Oviposition Behavior in Generalist, Trichoplusia ni and Specialist, Plutella xylostella Moths

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Abstract

The present study was undertaken to determine the effects of larval feeding experience on subsequent oviposition behavior of the resulting moths. Larvae of the cabbage looper (Trichoplusia ni, Noctuidae) and the diamondback moth (Plutella xylostella, Plutellidae) were exposed to the phenylpropanoid allelochemical trans-anethole (at 100 ppm fw in artificial diet) or the limonoid allelochemical toosendanin (10 ppm sprayed on cabbage leaves). Both compounds had been shown to deter oviposition in naïve moths in previous choice tests. Moths developing from “experienced” larvae (both sexes) showed a decrease in oviposition deterrence response when given a choice between control and treated leaves, unlike naïve moths. This phenomenon, analogous to habituation to feeding deterrents in lepidopteran larva, occurred irrespective of duration of feeding on the deterrent compound. We also observed that F1larvae resulting from experienced moths (previously exposed to toosendanin as larvae) grew as well on toosendanin-treated foliage as on control foliage. In contrast, growth of F1larvae from naïve moths was significantly impaired by toosendanin. These results demonstrate that host-selection behavior in cabbage looper (a generalist) and diamondback moth (a specialist) may be shaped by feeding experience according to Hopkins' Host Selection Principle in addition to chemical legacy.

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References

  • Anderson, P., Hilker, M., and Lofqvist, J. 1995. Larval diet influence on oviposition behavior in Spodoptera littoralis. Entomol. Exp. Appl. 74:71–82.

    Google Scholar 

  • Barron, A. B. 2001. The life and death of Hopkin's host-selection principle. J. Insect Behav. 14:725–737.

    Google Scholar 

  • Berenbaum, M. R. and Zangerl, A. R. 1991. Acquisition of a native host plant by an introduced oligophagous herbivore. Oikos 62:153–159.

    Google Scholar 

  • Bernays, E. A. 1998. The value of being a resource specialist: Behavioral support for a neural hypothesis. Am. Nat. 151:451–464.

    Google Scholar 

  • Bernays, E. A. and Chapman, R. F. 1994. Effects of experience, pp. 206–229, in A. T. Miller and S. H. Emden (Eds.). Host Plant Selection by Phytophagous Insects. Chapman and Hall, New York.

    Google Scholar 

  • Bowers, M. D., Stamp, N. E., and Collinge, S. K. 1992. Early stage of host range expansion by a specialist herbivore, Euphydryas phaeton (Nymphalidae). Ecology 73:526–536.

    Google Scholar 

  • Camara, M. D. 1997. A recent host range expansion in Junonia coenia Hubner (Nymphalidae): Oviposition preference, survival, growth, and chemical defense. Evolution 51:873–884.

    Google Scholar 

  • Cassidy, M. D. 1978. Development of an induced food plant preference in the Indian stick insect, Carausius morosus. Entomol. Exp. Appl. 24:287–293.

    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. 1989. Recent advances in research on botanical insecticides in China, pp. 69–77, in J. T. Arnason, B. J. R. Philogene, and P. Morand (Eds.). Insecticides of Plant Origin. Am. Chem. Soc. Symp. Ser. 387, American Chemical Society, Washington, DC.

    Google Scholar 

  • Corbet, S. A. 1985. Insect chemosensory responses: A chemical legacy hypothesis. Ecol. Ent. 10:143–153.

    Google Scholar 

  • Courtney, S. P. 1983. Models of host plant location by butterflies: The effect of search images and searching efficiency. Oecologia 59:317–321.

    Google Scholar 

  • Craighead, F. C. 1921. Hopkin's host-selection principle as related to certain Cerambycid beetles. J. Agric. Res. 22:189–220.

    Google Scholar 

  • Cunningham, J. P., Jallow, F. M., Wright, J. D., and Zalucki, M. P. 1998. Learning in host selection in Helicoverpa armigera (Lepidoptera: Noctuidae). Anim. Behav. 55:22–27.

    Google Scholar 

  • Cunningham, J. P., Zalucki, M. P., and West, S. A. 1999. Learning in Helicoverpa armigera (Lepidoptera: Noctuidae): A new look at the behavior and control of a polyphagous pest. Bull. Entomol. Res. 89:201–207.

    Google Scholar 

  • 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 

  • Feeny, P. P., Rosenberry, L., and Carter, M. 1983. Chemical aspects of oviposition behavior in butterflies, pp. 27–76, in S. Ahmad (Ed.). Host-Seeking Behavior and Mechanisms. Academic Press, London.

    Google Scholar 

  • Futuyama, D. J., Keese, M. C., and Scheffer, S. J. 1993. Genetic constraints and the phylogeny of insect–plant associations—Responses of Ophraella communa (Coleoptera, Chrysomelidae) to host plants of its congeners. Evolution 47:888–905.

    Google Scholar 

  • Hershberger, W. A. and Smith, M. P. 1967. Conditioning in Drosophila melanogaster. Anim. Behav. 15:259–270.

    Google Scholar 

  • Hoffman, A. A. 1985. Early adult experience in Drosophila: Comparing apples and oranges. Am. Nat. 126:41–51.

    Google Scholar 

  • Hopkins, A. D. 1917. A discussion of H.G. Hewitt's paper on “Insect behavior.” J. Econ. Entomol. 10:92–93.

    Google Scholar 

  • Hovanitz, W. and Chang, V. C. S. 1963. Ovipositional preference tests with Pieris. J. Res. Lepid 2:185–200.

    Google Scholar 

  • Huang, X. P. and Renwick, J. A. A. 1993. Differential selection of host plants by two Pieris species: The role of oviposition stimulants and deterrents. Entomol. Exp. Appl. 68:59–69.

    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. Agric. Food Chem. 49:715–720.

    Google Scholar 

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

    Google Scholar 

  • Isman, M. B. and Rodriguez, E. 1983. Larval growth inhibitors from species of Parhenium (Asteraceae). Phytochemistry 22:2709–2713.

    Google Scholar 

  • Jaenike, J. 1982. Environmental modification of oviposition behavior in Drosophilla. Am. Nat. 119:784–802.

    Google Scholar 

  • Jaenike, J. 1983. Induction of host preference in Drosophila mealnogaster. Oecologia 58:320–325.

    Google Scholar 

  • Jaenike, J. 1990. Host specialization in phytophagous insects. Annu. Rev. Ecol. Syst. 21: 243–273.

    Google Scholar 

  • Jermy, T., Hanson, F. E., and Dethier, V. G. 1968. Induction of specific food preference on lepidopterous larvae. Entomol. Exp. Appl. 11:211–230.

    Google Scholar 

  • Kuznetzov, V. I. 1952. The question of adaptation in lepidopterous species to new feeding conditions. Tr. Zool. Inst. Akad. Nauk. SSRR 24:271–322.

    Google Scholar 

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

    Google Scholar 

  • Papaj, D. R. 1986. Shifts in foraging behavior by a Battus philenor population field evidence for switching by individual butterflies. Behav. Ecol. Sociobiol. 19:31–39.

    Google Scholar 

  • Parmesan, C., Singer, M. C., and Harris, I. 1995. Absence of adaptive learning from the oviposition foraging behavior of a checkerpost butterfly. Anim. Behav. 50:161–175.

    Google Scholar 

  • Prokopy, R. J., Averill, A. L., Cooley, S. S., and Roitberg, C. A. 1982. Associative learning in egg-laying site selection by apple maggot flies. Science 218:76–77.

    Google Scholar 

  • Rausher, M. D. 1978. Search image for leaf shape in a butterfly. Science 200:1071–1073.

    Google Scholar 

  • Rausher, M. D. 1980. Host abundance, juvenile survival, and oviposition preference in Battus philenor. Evolution 34:342–355.

    Google Scholar 

  • Resetarits, W. J. 1996. Oviposition site choice and life history evolution. Am. Zool. 36:205–215.

    Google Scholar 

  • Rietdorf, K. and Steidle, J. L. M. 2002. Was Hopkins right? Influence for larval and early adult experience on the olfactory response in the granary weevil Sitophilus granarius (Coleoptera, Curculionidae). Physiol. Entomol. 27:223–227.

    Google Scholar 

  • Singer, M. C. 1986. The definition and measurement of oviposition preference in plant feeding insects, pp. 65–94, in J. R. Miller and T. R. Miller (Eds.). Insect–Plant Interactions. Springer, New York.

    Google Scholar 

  • Singer, M. C., Thomas, C. D., Billington, H. L., and Parmesan, C. 1989. Variation among conspecific insect populations in the mechanistic basis of diet breadth. Anim. Behav. 37:751–759.

    Google Scholar 

  • Singer, M. C., Thomas, C. D., Billington, H. L., and Parmesan, C. 1994. Correlates of speed of evolution of host preference in a set of twelve populations of the butterfly Euphydryas editha. Ecoscience 1:107–114.

    Google Scholar 

  • Smith, M. A. and Cornell, H. V. 1979. Hopkins host-selection in Nasonia vitripenni and its implications for sympatric speciation. Anim. Behav. 27:365–370.

    Google Scholar 

  • Solarz, L. S. and Newman, M. R. 2001. Variation in hostplant preference and performance by the milfoil weevil, Euhrychiopsis lecontei Dietz. exposed to native and exotic watermilfoils. Oecologia 126:66–75.

    Google Scholar 

  • Statistix 7. 2000. Analytical Software, Statistix 7 for Windows 95, 98, NT, 2000. Analytical Software, Tallahassea, Florida.

    Google Scholar 

  • Szentesi, A. and Jermy, T. 1989. The role of experience in host plant choice by phytophagous insects, pp. 39–74, in E. A. Bernays (Ed.). Insect–Plant Ineractions, Vol. 11. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Tabashnik, B. E. and Slansky, F., Jr. 1985. Nutritional ecology of forb foliage-chewing insects, pp. 369–391, in F. Slansky, Jr. and J. G. Rodriguez (Eds.). Nutritional Ecology of Insects, Mites, and Spiders. Wiley, New York.

    Google Scholar 

  • Thompson, J. N. 1986. Constraints on arms races in coevolution. Trends Ecol. Evol. 1:105–107.

    Google Scholar 

  • Thompson, J. N. 1988. Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol. Exp. Appl. 47:3–14.

    Google Scholar 

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

    Google Scholar 

  • Thorpe, W. H. 1939. Further studies on pre-imaginal olfactory conditioning in insects. Proc. R. Soc. London Ser. B 127:424–433.

    Google Scholar 

  • Thorpe, W. H. and Jones, F. G. W. 1937. Olafactory conditioning and its relation to the problem of host selection. Proc. R. Soc. London Ser. B 124:56–81.

    Google Scholar 

  • Traynier, R. M. M. 1984. Associative learning in the ovipositional behavior of the cabbage butterfly, Pieris rapae. Physiol. Entomol. 9:465–472.

    Google Scholar 

  • Wiklund, C. 1975. The evolutionary relationship between adult oviposition preferences and larval host plant range in Papilio machaon L. Oecologia 18:185–197.

    Google Scholar 

  • Zar, J. H. 1984. Biostatistical Analysis, pp. 168–190, Prentice-Hall Inc., Englewood Cliffs, New Jersey.

    Google Scholar 

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

    Google Scholar 

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Correspondence to Murray B. Isman.

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Akhtar, Y., Isman, M.B. Larval Exposure to Oviposition Deterrents Alters Subsequent Oviposition Behavior in Generalist, Trichoplusia ni and Specialist, Plutella xylostella Moths. J Chem Ecol 29, 1853–1870 (2003). https://doi.org/10.1023/A:1024802328458

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