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No evidence for change in oviposition behaviour of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) after widespread adoption of transgenic insecticidal cotton

Published online by Cambridge University Press:  07 February 2012

M.P. Zalucki ,
J.P. Cunningham ,
S. Downes ,
P. Ward ,
C. Lange ,
M. Meissle ,
N.A. Schellhorn  and
J.M. Zalucki
M.P. Zalucki*
Affiliation:
School of Biological Sciences, The University of Queensland, St Lucia, Brisbane, 4072, Australia
J.P. Cunningham
Affiliation:
School of Biological Sciences, The University of Queensland, St Lucia, Brisbane, 4072, Australia
S. Downes
Affiliation:
CSIRO Ecosystem Sciences, Australian Cotton Research Institute, Narrabri, 2390, NSW
P. Ward
Affiliation:
School of Biological Sciences, The University of Queensland, St Lucia, Brisbane, 4072, Australia
C. Lange
Affiliation:
School of Biological Sciences, The University of Queensland, St Lucia, Brisbane, 4072, Australia
M. Meissle
Affiliation:
CSIRO Ecosystem Sciences, Brisbane, 4001, Australia
N.A. Schellhorn
Affiliation:
CSIRO Ecosystem Sciences, Brisbane, 4001, Australia
J.M. Zalucki
Affiliation:
School of Environment, Griffith University, Nathan, Brisbane, 4111, Australia
*
*Author for correspondence Fax: +61 7 33651655 E-mail: [email protected]
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Abstract

Cotton growing landscapes in Australia have been dominated by dual-toxin transgenic Bt varieties since 2004. The cotton crop has thus effectively become a sink for the main target pest, Helicoverpa armigera. Theory predicts that there should be strong selection on female moths to avoid laying on such plants. We assessed oviposition, collected from two cotton-growing regions, by female moths when given a choice of tobacco, cotton and cabbage. Earlier work in the 1980s and 1990s on populations from the same geographic locations indicated these hosts were on average ranked as high, mid and low preference plants, respectively, and that host rankings had a heritable component. In the present study, we found no change in the relative ranking of hosts by females, with most eggs being laid on tobacco, then cotton and least on cabbage. As in earlier work, some females laid most eggs on cotton and aspects of oviposition behaviour had a heritable component. Certainly, cotton is not avoided as a host, and the implications of these finding for managing resistance to Bt cotton are discussed.

Keywords

source-sinkhost preferenceBt cottonHelicoverpa armigeranatural selection
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 102 , Issue 4 , August 2012 , pp. 468 - 476
Copyright
Copyright © Cambridge University Press 2012

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References

Bagla, P. (2010) Hardy cotton-munching pests latest blow to GM crops. Science 327, 1439.CrossRefGoogle ScholarPubMed
Carriere, Y., Crowder, D.W. & Tabashnik, B.E. (2010) Evolutionary ecology of insect adaptation to Bt crops. Evolutionary Applications 3, 561–573.CrossRefGoogle ScholarPubMed
Castillochavez, C., Levin, S.A. & Gould, F. (1988) Physiological and behavioral adaptation to varying environments: a mathematical model. Evolution 42, 986–994.Google Scholar
Cunningham, J.P. (2012) Can mechanism help explain insect host choice? Journal of Evolutionary Biology 25, 244–251.CrossRefGoogle ScholarPubMed
Cunningham, J.P., West, S.A. & Zalucki, M.P. (2001) Host selection in phytophagous insects: a new explanation for learning in adults. Oikos 95, 537–543.Google Scholar
Endersby, N.M., Hoffmann, A.A., McKechnie, S.W. & Weeks, A.R. (2007) Is there genetic structure in populations of Helicoverpa armigera from Australia? Entomologia Experimentalis et Applicata 122, 253–263.CrossRefGoogle Scholar
Firempong, S. & Zalucki, M.P. (1990a) Host plant selection by Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae): role of certain plant attributes. Australian Journal of Zoology 37, 675–683.Google Scholar
Firempong, S. & Zalucki, M.P. (1990b) Host plant preferences of populations of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) from different geographic locations. Australian Journal of Zoology 37, 665–673.CrossRefGoogle Scholar
Gould, F. (1984) Role of behavior in the evolution of insect adaptation to insecticides and resistant host plants. Bulletin of the Entomological Society of America (USA) 30, 34–41.CrossRefGoogle Scholar
Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: 420 Integrating pest genetics and ecology. Annual Review of Entomology 43, 701–726.Google Scholar
Hendry, A.P., Kinnison, M.T., Heino, M., Day, T., Smith, T.B., Fitt, G.P., Bergstrom, C., Oakeshott, J., Jørgensen, P.S., Zalucki, M.P., Gilchrist, G., Southerton, S., Sih, A., Strauss, S., Denison, R.F. & Carroll, S.P. (2011) Evolutionary principles and their practical application. Evolutionary Applications 4, 159–183.CrossRefGoogle ScholarPubMed
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.Google 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.Google Scholar
Jallow, M.F.A., Cunningham, J.P. & Zalucki, M.P. (2004) Intra-specific variation for host plant use in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae): implications for management. Crop Protection 23, 955–964.Google Scholar
Janz, N. & Nylin, S. (2008) The oscillation hypothesis of host-plant range and speciation. pp. 203–215in Tilmon, K.J. (Ed.) Specialization, Speciation, and Radiation: The Evolutionary Biology of Herbivorous Insects. Berkley, CA, USA, University of California Press.Google Scholar
Jongsma, M.A., Gould, F., Legros, M., Yang, L.M., van Loon, J.J.A. & Dicke, M. (2010) Insect oviposition behavior affects the evolution of adaptation to Bt crops: consequences for refuge policies. Evolutionary Ecology 24, 1017–1030.CrossRefGoogle Scholar
Karigl, G. (1981) A recursive algorithm for the calculation of identity coefficients. Annals of Human Genetics 45, 299–305.Google Scholar
Kennedy, G.G., Gould, F., Deponti, O.M.B. & Stinner, R.E. (1987) Ecological, agricultural, genetic, and commercial considerations in the deployment of insect-resistant germplasm. Environmental Entomology 16, 327–338.Google Scholar
Khan, Z.R., Midega, C.A.O., Hutter, N.J., Wilkins, R.M. & Wadhams, L.J. (2006) Assessment of the potential of Napier grass (Pennisetum purpureum) varieties as trap plants for management of Chilo partellus. Entomologia Experimentalis et Applicata 119, 15–22.Google Scholar
Kumar, R.K. & Stanley, S. (2010) Comparative feeding behavior and ovipositional aspects of cotton bollworms Helicoverpa armigera on transgenic and non-transgenic cotton. Resistant Pest Management Newsletter 20, 26–28.Google Scholar
Liang, K.Y. & Zeger, S.L. (1986) Longitudinal data analysis using generalized linear models. Biometrika 73, 13–22.Google Scholar
Lu, B.-Q. (2011) Thresholds and mechanisms of survival for Bt-susceptible Helicoverpa spp. Living on Bollgard II® cotton. PhD thesis, University of New England, Maine, USA.Google Scholar
Lynch, M. & Walsh, B. (1998) Genetics and Analysis of Quantitative Traits. Sunderland, MA, USA, Sinauer and Associates, Inc.Google Scholar
Mahon, R.J., Olsen, K.M., Downes, S. & Addison, S. (2007) Frequency of Alleles Conferring Resistance to the Bt Toxins Cry1Ac and Cry2Ab in Australian Populations of Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Economic Entomology 100, 1844–1853.Google Scholar
Matten, S.R., Head, G.P. & Quemada, H.D. (2008) How governmental regulation can help or hinder the integration of Bt crops within IPM programs. pp. 27–39in Romeis, J., Shelton, A.M. & Kennedy, G.G. (Eds) Integration of Insect Resistant Genetically Modified Crops within IPM Programs. New York, USA, Springer.CrossRefGoogle Scholar
Mayhew, P.J. (1997) Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79, 417–428.Google Scholar
Mayhew, P.J. (2001) Herbivore host choice and optimal bad motherhood. Trends in Ecology & Evolution 16, 165–167.Google Scholar
Midega, C.A.O., Khan, Z.R., Pickett, J.A. & Nylin, S. (2011) Host plant selection behaviour of Chilo partellus and its implication for effectiveness of a trap crop. Entomologia Experimentalis et Applicata 138, 40–47.CrossRefGoogle Scholar
Nylin, S. & Janz, N. (1993) Oviposition preference and larval performance in Polygonia c-album (Lepidoptera: Nymphalidae) – the choice between bad and worse. Ecological Entomology 18, 394–398.Google Scholar
Nylin, S. & Janz, N. (1996) Host plant preference in the comma butterfly (Polygonia c-album): Do parents and offspring agree? Ecoscience 3, 285–289.Google Scholar
Peck, S.L., Gould, F. & Ellner, S.P. (1999) Spread of resistance in spatially extended regions of transgenic cotton: Implications for management of Heliothis virescens (Lepidoptera: Noctuidae). Journal of Economic Entomology 92, 1–16.Google Scholar
Prentice, R.L. (1988) Correlated binary regression with covariates specific to each binary observation. Biometrics 44, 1033–1048.CrossRefGoogle ScholarPubMed
Prentice, R.L. & Zhao, L.-P. (1991) Estimating equations for parameters in means and covariances of multivariate discrete and continuous responses. Biometrics 47, 825–839.Google Scholar
Renwick, J.A.A. & Chew, F.S. (1994) Oviposition behaviour in Lepidoptera. Annual Review of Entomology 39, 377–400.Google Scholar
Rochester, W.A., Zalucki, M.P., Ward, A., Miles, M. & Murray, D.A.H. (2002) Testing insect movement theory: empirical analysis of pest data routinely collected from agricultural crops. Computers and Electronics in Agriculture 35, 139–149.Google Scholar
Schneider, J.C. & Roush, R.T. (1986) Genetic differences in oviposition preference between two populations of Heliothis virescens. pp. 163–171in Huettel, M.D. (Ed.) Evolutionary Genetics of Invertebrate Behaviour. New York, USA, Plenum Press.Google Scholar
Shelton, A.M., Hatch, S.L., Zhao, J.-Z., Chen, M., Earle, E.D. & Cao, J. (2008) Suppression of diamondback moth using Bt-transgenic plants as a trap crop. Crop Protection 27, 403–409.Google Scholar
Singer, M.C. (1984) Butterfly-host plant relationships. pp. 81–88in Vane-Wright, R.I. & Ackery, P. (Eds) The Biology of Butterflies. London, UK, Academic Press.Google Scholar
Sisterson, M.S., Carriere, Y., Dennehy, T.J. & Tabashnik, B.E. (2005) Evolution of resistance to transgenic crops: Interactions between insect movement and field distribution. Journal of Economic Entomology 98, 1751–1762.Google Scholar
Storer, N.P., Peck, S.L., Gould, F., Van Duyn, J.W. & Kennedy, G.G. (2003) Spatial processes in the evolution of resistance in Helicoverpa zea (Lepidoptera: Noctuidae) to Bt transgenic corn and cotton in a mixed agroecosystem: a biology-rich stochastic simulation model. Journal of Economic Entomology 96, 156–172.CrossRefGoogle Scholar
Tabashnik, B.E. (1994) Delaying insect adaptation to transgenic plants: seed mixtures and refugia reconsidered. Proceedings of the Royal Society of London, Series B: Biological Sciences 255, 7–12.Google Scholar
Tabashnik, B.E. & Carrière, Y. (2010) Field-evolved resistance to Bt Cotton: bollworm in the U.S. and pink bollworm in India. Southwestern Entomologist 35, 417–424.Google Scholar
Tabashnik, B.E., Dennehy, T.J. & Carriere, Y. (2005) Delayed resistance to transgenic cotton in pink bollworm. Proceedings of the National Academy of Sciences of the United States of America 102, 15389–15393.Google Scholar
Tabashnik, B.E., Van Rensburg, J.B.J. & Carriere, Y. (2009) Field-evolved insect resistance to Bt crops: definitions, theory and data. Journal of Economic Entomology 102, 2011–2025.CrossRefGoogle ScholarPubMed
Teakle, R.E. (1991) Laboratory culture of Heliothis spp. and identification of diseases. pp. 11–21in Zalucki, M.P. (Ed.) Heliothis Research Methods and Prospects, New York, USA, Springer-Verlag.Google 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.CrossRefGoogle Scholar
Thrall, P.H., Oakshott, J.G., Fitt, G.P., Southerton, S., Burdon, J.J., Sheppard, A., Russell, R.J., Zalucki, M.P., Heino, M. & Denison, R.F. (2011) Evolution in agriculture: the application of evolutionary approaches to the management of biotic interactions in agro-ecosystems. Evolutionary Applications 4, 200–215.CrossRefGoogle Scholar
Torres, J.B. & Ruberson, J.R. (2006) Spatial and temporal dynamics of oviposition behavior of bollworm and three of its predators in Bt and non-Bt cotton fields. Entomologia Experimentals et Applicata 120, 11–22.Google Scholar
Van Rensburg, J.B.J. (2007) First report of field resistance by stem borer, Busseola fusca (Fuller) to Bt-transgenic maize. South African Journal Plant Soil 24, 147–151.Google Scholar
Walter, G.H. & Benfield, M.D. (1994) Temporal host-plant use in 3 polyphagous Heliothinae, with special reference to Helicoverpa punctigera (Wallengren) (Noctuidae, Lepidoptera). Australian Journal of Ecology 19, 458–465.CrossRefGoogle Scholar
Wang, C.-Z., Dong, J.-F., Tang, D.-L., Zhang, J.-H., Li, W. & Qin, J. (2004) Host selection of Helicoverpa armigera and H. assulta and its inheritance. Progress in Natural Science 14, 880–884.CrossRefGoogle Scholar
Wardhaugh, K.G., Room, P.M. & Greenup, L.R. (1980) The incidence of Heliothis armigera (Hübner) and Heliothis 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.Google Scholar
Weeks, A.R., Endersby, N.M., Lange, C.L., Lowe, A., Zalucki, M.P. & Hoffmann, A.A. (2010) Genetic variation among Helicoverpa armigera populations as assessed by microsatellites: a cautionary tale about accurate allele scoring. Bulletin of entomological Research 100, 445–450.Google Scholar
West, S.A. & Cunningham, J.P. (2002) A General model for host plant selection in phytophagous insects. Journal of theoretical Biology 214, 499–513.Google Scholar
Wu, K.-M., Lu, Y.-H., Feng, H.-Q., Jiang, Y.-Y. & Zhao, J.-Z. (2008) Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. Science 321, 1676–1678.Google Scholar
Yang, Y.-Z., Johnson, M.-L. & Zalucki, M.P. (2008) Possible effect of genetically modified cotton on foraging habits of early instar Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) larvae. Australian Journal of Entomology 47, 137–141.Google Scholar
Zalucki, M.P., Daglish, G., Firempong, S. & Twine, P. (1986) The biology and ecology of Heliothis armigera (Hübner) and Heliothis punctigera Wallengren (Lepidoptera: Noctuidae) in Australia: What do we know? Australian Journal of Zoology 34, 779–814.CrossRefGoogle 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 areas of eastern Australia: larval sampling and host plant relationships during winter/spring. Australian Journal of Zoology 42, 329–346.CrossRefGoogle Scholar
Zalucki, M.P., Clarke, A.R. & Malcolm, S.B. (2002) Ecology and behaviour of first instar larval Lepidoptera. Annual Review of Entomology 47, 361–393.Google Scholar
Zalucki, M.P., Adamson, D. & Furlong, M.J. (2009) The future of IPM: whither or wither? Australian Journal of Entomology 48, 85–96.Google Scholar
Zhang, H., Yin, W., Zhao, J., Jin, L., Yang, Y., Wu, S., Tabashnik, B.E. & Wu, Y. (2011) Early warning of cotton Bollworm resistance associated with intensive planting of Bt cotton in China. PLoS ONE 6(8), e22874 (doi:10.1371/journal.pone.0022874).Google Scholar