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Learning in Helicoverpa armigera (Lepidoptera: Noctuidae): a new look at the behaviour and control of a polyphagous pest

Published online by Cambridge University Press:  09 March 2007

J.P. Cunningham ,
M.P. Zalucki  and
S.A. West
J.P. Cunningham*
Affiliation:
Institute of Cell, Animal and Population Biology University of Edinburgh King's Buildings, West Mains Road, Scotland, EH9 3JT, UK
M.P. Zalucki
Affiliation:
Department of Entomology and Co-operative Research Centre for Tropical Pest Management, University of Queensland, Brisbane, Queensland 4072, Australia
S.A. West
Affiliation:
Institute of Cell, Animal and Population Biology University of Edinburgh King's Buildings, West Mains Road, Scotland, EH9 3JT, UK
*
* Fax: 0131 650 6564 E-mail: paul.cunningham@ed.ac.uk
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Abstract

Recent experimental evidence has shown that learning occurs in the host selection behaviour of Helicoverpa armigera (Hübner), one of the world‘s most important agricultural pests. This paper discusses how the occurrence of learning changes our understanding of the host selection behaviour of this polyphagous moth. Host preferences determined from previous laboratory studies may be vastly different from preferences exhibited by moths in the field, where the abundance of particular hosts may be more likely to determine host preference. In support of this prediction, a number of field studies have shown that the ‘attractiveness’ of different hosts for H. armigera oviposition may depend on the relative abundance of these host species. Insect learning may play a fundamental role in the design and application of present and future integrated pest management strategies such as the use of host volatiles, trap crops and resistant crop varieties for monitoring and controlling this important pest species.

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Type
Review Article
Information
Bulletin of Entomological Research , Volume 89 , Issue 3 , March 1999 , pp. 201 - 207
Copyright
Copyright © Cambridge University Press 1999

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References

Broadley, R.H. (1978) Distributions of Heliothis spp. (Lepidoptera: Noctuidae) eggs and 1st instar larvae on pre-flowering flue-cured tobacco plants in north Queensland. Queensland Journal of Agriculture and Animal Science 35, 73–76.Google Scholar
Butter, N.S. & Singh, S. (1996) Ovipositional response of Helicoverpa armigera to different cotton genotypes. Phytoparasitica 24, 97–102.CrossRefGoogle Scholar
Courtney, S.P., Chen, G.K. & Gardner, A. (1989) A general model for individual host selection. Oikos 55, 55–65.CrossRefGoogle Scholar
Cunningham, J.P., Jallow, M.F.A., Wright, D.J. & Zalucki, M.P. (1998a) Learning in host selection in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Animal Behaviour 55, 227–234.CrossRefGoogle ScholarPubMed
Cunningham, J.P., West, S.A. & Wright, D.J. (1998b) Learning in nectar foraging behaviour in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Ecological Entomology 23, 363–369.CrossRefGoogle Scholar
Fan, R., Anderson, P. & Hansson, B.S. (1997) Behavioural analysis of olfactory conditioning in the moth Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae). Journal of Experimental Biology, 200, 2969–2976.CrossRefGoogle ScholarPubMed
Firempong, S. & Zalucki, M.P. (1990a) Host plant preferences of populations of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) from different geographic locations. Australian Journal of Zoology 37, 665–673CrossRefGoogle Scholar
Firempong, S. & Zalucki, M.P. (1990b) Host plant selection by Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae): role of certain plant attributes. Australian Journal of Zoology, 37, 675–883.CrossRefGoogle Scholar
Firempong, S. & Zalucki, M.P. (1991) Host plant selection by Helicoverpa armigera (Lepidoptera: Noctuidae): the role of some herbivore attributes. Australian Journal of Zoology, 39, 343–350.Google Scholar
Fitt, G.P. (1989) The ecology of Heliothis in relation to agroecosystems. Annual Review of Entomology, 34, 17–52.CrossRefGoogle Scholar
Fitt, G.P. & Boyan, G.S. (1991) Methods for studying behaviour. pp. 122–151in Zalucki, M.P. (Ed.) Heliothis: research methods and prospects. London, Springer-Verlag.CrossRefGoogle Scholar
Goulson, D. & Cory, J.S. (1993) Flower constancy and learning in foraging preferences of the green-veined white butterfly Pieris napi. Ecological Entomology 18, 315–320.CrossRefGoogle Scholar
Goulson, D., Ollerton, J. & Sluman, C. (1997) Foraging strategies in the small skipper butterfly, Thymelicus flavus; when to switch? Animal Behaviour 53, 1009–1016.CrossRefGoogle Scholar
Gu, H. & Walter, G.H. (1998) Is the common sowthistle (Sonchus oleraceus) a primary host plant of the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae)? Oviposition and larval performance. Zeitscrift für Angewandte Entomologie 123, 99–105.Google Scholar
Hartlieb, E. (1995) Odor learning in the moth Helicoverpa armigera in classical conditioning experiments in Elsner, N. & Menzel, R. (Eds) Learning and Memory. Proceedings of the 23rd Gottingen Neurobiology Conference 1995, Vol. 1, Abstract 38. Stuttgart, Thieme Verlag.Google Scholar
Hartlieb, E. (1996) Olfactory conditioning in the moth Heliothis virescens. Naturwissenschaften 83, 87–88.Google Scholar
Hartlieb, E. & Rembold, H. (1996) Behavioral response of female Helicoverpa (Heliothis) armigera HB. (Lepidoptera: Noctuidae) moths to synthetic pigeonpea (Cajanus cajan L.) kairomone. Journal of Chemical Ecology 22, 821–837.CrossRefGoogle Scholar
Hokkanen, H.M.T. (1991) Trap cropping in pest management. Annual Review of Entomology 36, 119–138.CrossRefGoogle Scholar
Jallow, M.F.A. & Zalucki, M.P. (1995) A technique for measuring intraspecific variation in oviposition preference in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Journal of the Australian Entomological Society, 34, 281–288.CrossRefGoogle Scholar
Jallow, M.F.A. & Zalucki, M.P. (1996) Within- and between-population variation in host-plant preference and specificity in Australian Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Australian Journal of Zoology 44, 503–519.CrossRefGoogle Scholar
Jallow, M.F.A. & Zalucki, M.P. (1998) Effects of egg load on the host-selection behaviour of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Australian Journal of Zoology 46, 291–299.Google Scholar
Janz, N., Nylin, S. & Wedell, N. (1994) Host plant utilization in the comma butterfly: sources of variation and evolutionary implications. Oecologia 99, 132–140.CrossRefGoogle ScholarPubMed
Karowe, D.N. (1989) Facultative monophagy as a consequence of prior feeding experience: behavioural and physiological specialization in Colias philodice larvae. Oecologia 78, 106–111.CrossRefGoogle ScholarPubMed
Kelber, A. (1996) Colour learning in the hawkmoth Macroglossum stellatarum. Journal of Experimental Biology 199, 1127–1131.Google Scholar
Kelber, A. & Pfaff, M. (1997) Spontaneous and learned preferences for visual flower features in a diurnal hawkmoth. Israel Journal of Plant Sciences 45, 235–245.CrossRefGoogle Scholar
Landolt, P.J. & Molina, O. (1996) Host-finding by cabbage looper moths (Lepidoptera: Noctuidae): learning of host odour upon contact with host foliage. Journal of Insect Behaviour 9, 899–908.CrossRefGoogle Scholar
Lewis, A.C. (1986) Memory constraints and flower choice in Pieris rapae. Science 232, 863–865.CrossRefGoogle ScholarPubMed
Lewis, A.C. (1989) Flower visit constancy in Pieris rapae, the cabbage butterfly. Journal of Animal Ecology 58, 1–13.Google Scholar
Lewis, A.C. (1993) Learning and the evolution of resources: pollinators and flower morphology. pp. 219–242in Papaj, D.R. & Lewis, A.C.(Eds) Insect learning: ecological and evolutionary perspectives. New York, Chapman & Hall.CrossRefGoogle Scholar
Luther, G.C., Valenzuela, H.R. & Defrank, J. (1996) Impact of cruciferous trap crops on lepidopteran pests of cabbage in Hawaii. Environmental Entomology 25, 39–47.Google Scholar
McCaffery, A.R., Walker, A.J. & Topper, C.P. (1991) Insecticide resistance in the bollworm, Helicoverpa armigera from Indonesia. Pesticide Science 32, 85–90.Google Scholar
Mitchell, E.R., Tingle, F.C. & Heath, R.R. (1991) Flight activity of Heliothis virescens (F.) females (Lepidoptera: Noctuidae) with reference to host plant volatiles. Journal of Chemical Ecology 17, 259–266.CrossRefGoogle ScholarPubMed
Nyambo, B.T. (1988) Significance of host-plant phenology in the dynamics and pest incidence of the cotton bollworm, Heliothis armigera Hübner (Lepidoptera: Noctuidae), in Western Tanzania. Crop Protection 7, 161–167.Google Scholar
Papaj, D.R. (1986a) Conditioning of leaf-shape discrimination by chemical cues in the butterfly, Battus philenor. Animal Behaviour 34, 1281–1288.CrossRefGoogle Scholar
Papaj, D.R. (1986b) Shifts in foraging behaviour by a Battus philenor population: field evidence for switching by individual butterflies. Behavioural Ecology and Sociobiology 19, 31–39.CrossRefGoogle Scholar
Papaj, D.R. (1986c) Interpopulation differences in host preference and the evolution of learning in the butterfly Battus philenor. Evolution 40, 518–530.Google Scholar
Papaj, D.R. & Lewis, A.C. (1993) Insect learning: ecological and evolutionary perspectives. 398 pp. New York, Chapman & Hall.CrossRefGoogle Scholar
Papaj, D.R. & Prokopy, R.J. (1989) Ecological and evolutionary aspects of learning in phytophagous insects. Annual Review of Entomology 34, 315–350.CrossRefGoogle Scholar
Papaj, D.R. & Rausher, M.D. (1987) Genetic differences and phenotype plasticity as causes of variation in oviposition preference in Battus philenor. Oecologia 74, 24–30.CrossRefGoogle ScholarPubMed
Parmesan, C., Singer, M.C. & Harris, I. (1995) Absence of adaptive learning from the oviposition foraging behaviour of a checkerspot butterfly. Animal Behaviour 50, 161–175.CrossRefGoogle Scholar
Parsons, F.S. (1940) Investigations on the cotton bollworm, Heliothis armigera (Hb.). Part III. Relations between oviposition and the flowering curves of food plants. Bulletin of Entomological Research 31, 147–177.CrossRefGoogle Scholar
Prokopy, R.J. & Lewis, W.J. (1993) Application of learning to pest management. pp. 308–342in Papaj, D.R. & Lewis, A.C.(Eds) Insect learning: ecological and evolutionary perspectives. New York, Chapman & Hall.Google Scholar
Pyke, B., Rice, M.J., Sabine, B. & Zalucki, M.P. (1987) The push-pull strategy - behavioural control of Heliothis. Australian Cotton Grower 8, 7–9.Google Scholar
Rausher, M.D. (1983) Ecology of host-selection behaviour in phytophagous insects. pp. 223–257in Denno, R.R. & McClure, M.S. (Eds) Variable plants and herbivores in natural and managed systems. New York, Academic Press.CrossRefGoogle Scholar
Reed, W. & Pawar, C.S. (1982) Heliothis: a global problem. pp. 9–14in Reed, W. & Kumble, V. (Eds) Proceedings of the International Workshop on Heliothis Management. Pantanchera, India, ICRISAT.Google Scholar
Rembold, H., Köhne, A.C. & Schroth, A. (1991) Behavioural response of Heliothis armigera Hb. (Lep., Noctuidae) moths on a synthetic chickpea (Cicer arietinum L.) kairomone. Journal of Applied Entomology 112, 252–262.CrossRefGoogle Scholar
Renwick, J.A.A. & Chew, F.S. (1994) Oviposition behaviour in lepidoptera. Annual Review of Entomology 39, 377–400.CrossRefGoogle Scholar
Roome, R.E. (1975) Activity of adult Heliothis armigera (Hb.) (Lepidoptera, Noctuidae) with reference to the flowering of sorghum and maize in Botswana. Bulletin of Entomological Research 65, 523–530.Google Scholar
Shanower, T.G. & Romeis, J. (1999) Insect pests of pigeonpea and their management. Annual Review of Entomology 44, 77–96.CrossRefGoogle ScholarPubMed
Singh, J. & Sidhu, A.S. (1990) Present status of Heliothis on cotton and strategies for its management in Punjab, Harayana and Rajisthan. Proceedings of the First National Workshop on Heliothis Management: Current Status and Future Strategies. Kanpur, India.Google Scholar
Stanton, M.L. (1984) Short-term learning and the searching accuracy of egg laying butterflies. Animal Behaviour 32, 33–40.CrossRefGoogle Scholar
Stephens, D.W. (1993) Learning and behavioural ecology: incomplete information and environmental predictability. pp. 195–218in Papaj, D.R. & Lewis, A.C.(Eds) Insect learning: ecological and evolutionary perspectives. New York, Chapman & Hall.Google Scholar
Swihart, C.A. & Swihart, S.L. (1970) Colour selection and learned feeding preferences in the butterfly, Heliconius charitonius Linn. Animal Behaviour 18, 60–64.CrossRefGoogle Scholar
Thompson, J.N. (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomologia Experimentalis et Applicata 47, 3–14.Google Scholar
Thompson, J.N. (1993) Preference hierarchies and the origin of geographic specialization in host use in swallowtail butterflies. Evolution 47, 1585–1594.Google Scholar
Tingle, F.C. & Mitchell, E.R. (1992) Attraction of Heliothis virescens (F.) Lepidoptera: Noctuidae) to volatiles from extracts of cotton flowers. Journal of Chemical Ecology 18, 907–914.CrossRefGoogle ScholarPubMed
Tingle, F.C., Mitchell, E.R. & Heath, R.R. (1990) Preferences of mated Heliothis virescens and H. subflexa females for host and non host volatiles in a flight tunnel. Journal of Chemical Ecology 16, 2889–2898.Google Scholar
Topper, C.P. (1987) Nocturnal behaviour of adults of Heliothis armigera (Hübner) (Lepidoptera: Noctuidae) in the Sudan Gezira and pest control implications. Bulletin of Entomological Research 77, 541–554.Google Scholar
Traynier, R.M.M. (1984) Associative learning in the oviposition behaviour of the cabbage butterfly, Pieris rapae. Physiological Entomology 9, 465–472.CrossRefGoogle Scholar
Traynier, R.M.M. (1986) Visual learning in the oviposition behaviour of the cabbage butterfly, Pieris rapae. Entomologia Experimentalis et Applicata 40, 25–33.CrossRefGoogle Scholar
Udayagiri, S. & Mason, C.E. (1995) Host plant constituents as oviposition stimulants for a generalist herbivore: European corn borer. Entomologia Experimentalis et Applicata 76, 59–65.Google Scholar
Wardhaugh, K.G., Room, P.M. & Greenup, L.R. (1980) The incidence of Heliothis armigera (Hübner) and H. punctigera Wallengren (Lepidoptera: Noctuidae) on cotton and other host-plants in the Namoi Valley of New South Wales. Bulletin of Entomological Research 70, 113–131.CrossRefGoogle Scholar
Waser, N.M. (1986) Flower constancy, definition, cause and measurement. American Naturalist 127, 583–603.CrossRefGoogle Scholar
Well, H. & Wells, P.H. (1986) Optimal diet, minimal uncertainty and individual constancy in the foraging honeybees, Apis mellifera. Journal of Animal Ecology 55, 881–891.CrossRefGoogle Scholar
Zalucki, M.P., Daglish, G., Firempong, S. & Twine, P.H. (1986) The biology and ecology of Heliothis armigera (Hübner) and H. punctigera Wallengren (Lepidoptera: Noctuidae) in Australia: what do we know? Australian Journal of Zoology 34, 779–814.Google Scholar
Zalucki, M.P., Murray, D.A.H., Gregg, P.C., Fitt, G.P., Twine, P.H. & Jones, C. (1994) Ecology of Helicoverpa armigera (Hübner) and H. punctigera (Wallengren) in the inland of Australia: larval sampling and host plant relationships during winter and spring. Australian Journal of Zoology 42, 329–346.CrossRefGoogle Scholar