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Broad-scale suppression of cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae), associated with Bt cotton crops in Northern New South Wales, Australia

Published online by Cambridge University Press:  23 November 2016

G.H. Baker*
Affiliation:
CSIRO Agriculture & Food, GPO Box 1700, Canberra, ACT 2601, Australia
C.R. Tann
Affiliation:
CSIRO Agriculture & Food, Locked Bag 59, Narrabri, NSW 2390, Australia
*
*Author for correspondence Phone: +61 2 6246 4406 Fax: +61 2 6246 4094 E-mail: [email protected]

Abstract

The cotton bollworm, Helicoverpa armigera, is a major pest of many agricultural crops in several countries, including Australia. Transgenic cotton, expressing a single Bt toxin, was first used in the 1990s to control H. armigera and other lepidopteran pests. Landscape scale or greater pest suppression has been reported in some countries using this technology. However, a long-term, broad-scale pheromone trapping program for H. armigera in a mixed cropping region in eastern Australia caught more moths during the deployment of single Bt toxin cotton (Ingard®) (1996–2004) than in previous years. This response can be attributed, at least in part, to (1) a precautionary cap (30% of total cotton grown, by area) being applied to Ingard® to restrict the development of Bt resistance in the pest, and (2) during the Ingard® era, cotton production greatly increased (as did that of another host plant, sorghum) and H. armigera (in particular the 3rd and older generations) responded in concert with this increase in host plant availability. However, with the replacement of Ingard® with Bollgard II® cotton (containing two different Bt toxins) in 2005, and recovery of the cotton industry from prevailing drought, H. armigera failed to track increased host-plant supply and moth numbers decreased. Greater toxicity of the two gene product, introduction of no cap on Bt cotton proportion, and an increase in natural enemy abundance are suggested as the most likely mechanisms responsible for the suppression observed.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2016 

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References

Adamczyk, J.J. & Hubbard, D. (2006) Changes in populations of Heliothis virescens (F.) (Lepidoptera: Noctuidae) and Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) in the Mississippi Delta from 1986 to 2005 as indicated by adult male pheromone traps. Journal of Cotton Science 10, 155160.Google Scholar
Baker, G.H. & Tann, C.R. (2013) Mating of Helicoverpa armigera (Lepidoptera: Noctuidae) moths and their plant host origins as larvae within Australian cotton farming systems. Bulletin of Entomological Research 103, 171181.Google Scholar
Baker, G.H. & Tann, C.R. (In Press) Long-term changes in the numbers of Helicoverpa punctigera (Lepidoptera : Noctuidae) in a cotton production landscape in northern New South Wales, Australia. Bulletin of Entomological Research In Press.Google Scholar
Baker, G.H. & Tann, C.R. (2014) Refuge crop performance as part of the Bt resistance management strategy for Helicoverpa spp. (Lepidoptera : Noctuidae) in Australian cotton production systems. Austral Entomology 53, 240247.Google Scholar
Baker, G.H., Tann, C.R. & Fitt, G.P. (2008) Production of Helicoverpa spp. (Lepidoptera, Noctuidae) from different refuge crops to accompany transgenic cotton plantings in eastern Australia. Australian Journal of Agricultural Research 59, 723732.Google Scholar
Baker, G.H., Tann, C.R. & Fitt, G.P. (2011) A tale of two trapping methods: Helicoverpa spp. (Lepidoptera, Noctuidae) in pheromone and light traps in Australian cotton production systems. Bulletin of Entomological Research 101, 923.Google Scholar
Brévault, T., Nibouche, S., Achaleke, J., & Carrière, Y. (2012) Assessing the role of non-cotton refuges in delaying Helicoverpa armigera resistance to Bt cotton in West Africa. Evolutionary Applications 5, 5365.Google Scholar
Carrière, Y., Ellers-Kirk, C., Sisterson, M., Antilla, L., Whitlow, M., Dennehy, T.J. & Tabashnik, B.E. (2003) Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton. Proceedings of the National Academy of Sciences of the United States of America 100, 15191523.Google Scholar
Cattaneo, M.G., Yafuso, C., Schmidt, C., Huang, C-Y., Rahman, M., Olson, C., Ellers-Kirk, C., Orr, B.J., Marsh, S.E., Antilla, L., Dutilleul, P. & Carrière, Y. (2006) Farm-scale evaluation of the impacts of transgenic cotton on biodiversity, pesticide use, and yield. Proceedings of the National Academy of Sciences of the United States of America 103, 75717576.Google Scholar
Dowling, D. (Ed.) (2015) Cotton Yearbook 2015. The Australian Cottongrower. Toowoomba, Australia, Greenmount Press.Google Scholar
Downes, S. & Mahon, R. (2012 a) Evolution, ecology and management of resistance in Helicoverpa spp. to Bt cotton in Australia. Journal of Invertebrate Pathology 110, 281286.Google Scholar
Downes, S. & Mahon, R. (2012 b) Successes and challenges of managing resistance in Helicoverpa armigera to Bt cotton in Australia. GM Crops and Food: Biotechnology in Agriculture and the Food Chain 3, 228234.CrossRefGoogle ScholarPubMed
Downes, S.J., Mahon, R.J. & Olsen, K. (2007) Adaptive resistance management in Australia for Bt-cotton: current status and future challenges. Journal of Invertebrate Pathology 95, 208213.Google Scholar
Downes, S.J., Parker, T.L. & Mahon, R.J. (2009) Frequency of alleles conferring resistance to the Bacillus thuringiensis toxins Cry1Ac and Cry2Ab in Australian populations of Helicoverpa punctigera (Lepidoptera : Noctuidae) from 2002 to 2006. Journal of Economic Entomology 102, 733742.Google Scholar
Downes, S., Mahon, R., Rossiter, L., Kauter, G., Leven, T., Fitt, G. & Baker, G. (2010 a) Adaptive management of pest resistance by Helicoverpa species (Noctuidae) in Australia to the Cry 2Ab Bt toxin in Bollgard II® cotton. Evolutionary Applications 3, 574584.CrossRefGoogle Scholar
Downes, S.J., Parker, T.L. & Mahon, R.J. (2010 b) Incipient resistance of Helicoverpa punctigera to the Cry2Ab Bt toxin in Bollgard® cotton. PLoS ONE 5, e12567.Google Scholar
Downes, S., Wilson, L., Knight, K., Kauter, G. & Leven, T. (2015) Preamble to the Resistance Management Plan (RMP) for Bollgard II 2015–16. pp. 6576 in Maas, S., Ceeney, S. & Redfern, R. (Eds) Cotton Pest Management Guide 2015–16. Toowoomba, Australia, CRDC & Greenmount Press.Google Scholar
Firempong, S. & Zalucki, M.P. (1990) Host plant selection by Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae): role of certain plant attributes. Australian Journal of Zoology 37, 675683.CrossRefGoogle Scholar
Fitt, G.P. (1989) The ecology of Heliothis species in relation to agroecosystems. Annual Review of Entomology 34, 1752.CrossRefGoogle Scholar
Fitt, G.P. (2000) An Australian approach to IPM in cotton: integrating new technologies to minimise insecticide dependence. Crop Protection 19, 793800.Google Scholar
Fitt, G.P. (2004) Implementation and impact of transgenic Bt cottons in Australia. pp. 371381 in Swanepoel, A. (Ed.) Cotton Production for the New Millenium. Proceedings of the 3 rd World Cotton Research Conference . Pretoria, South Africa, Agricultural Research Council – Institute for Industrial Crops.Google Scholar
Fitt, G.P. (2008) Have Bt crops led to changes in insecticide use patterns and impacted IPM? pp. 309328 in Romeis, J., Shelton, T.M. & Kennedy, G. (Eds) Integration of insect-resistant GM crops within IPM programs. Progress in Biological Control Series. Heidelberg, Germany, Springer-Verlag.Google Scholar
Fitt, G.P. & Cotter, S.C. (2004) The Helicoverpa problem in Australia : biology and management. pp. 4561 in Sharma, H.C. (Ed.) Heliothis/Helicoverpa Management. Emerging Trends and Strategies for Future Research . New Delhi, India, Oxford & IBH Publishing.Google Scholar
Fitt, G.P. & Daly, J.C. (1990) Abundance of overwintering pupae and the spring generation of Helicoverpa spp. (Lepidoptera: Noctuidae) in northern New South Wales, Australia: implications for pest management. Journal of Economic Entomology 83, 18271836.Google Scholar
Fitt, G.P., Gregg, P., Zalucki, M. & Twine, P. (1990) The ecology of Heliothis spp. in inland Australia : what relevance to the cotton industry? pp. 313325 in Proceedings of the 5th Australian Cotton Conference. Surfers Paradise, Queensland, Australia.Google Scholar
Forrester, N.W., Cahill, M., Bird, L.J. & Layland, J.K. (1993) Management of pyrethroid and endosulfan resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) in Australia. Bulletin of Entomological Research 83, 563578.Google Scholar
Gao, Y.-L., Feng, H.-Q. & Wu, K.-M. (2010) Regulation of the seasonal population patterns of Helicoverpa armigera moths by Bt cotton planting. Transgenic Research 19, 557562.Google Scholar
Greenplate, J.T., Mullins, J.W., Penn, S.R., Dahm, A., Reich, B.J., Osborn, J.A., Rahn, P.R., Ruschke, L.& Shappley, Z.W. (2003) Partial characterization of cotton plants expressing two toxin proteins from Bacillus thuringiensis: relative toxin contribution, toxin interaction, and resistance management. Applied Entomology 127, 340347.Google Scholar
Hutchison, W.D., Burkness, E.C., Mitchell, P.D., Moon, R.D., Leslie, T.W., Fleisher, S.J., Abrahamson, M., Hamilton, K.L., Steffey, K.L., Gray, M.E., Hellmich, R.L., Kaster, L.V., Hunt, T.E., Wright, R.J., Pecinovsky, K., Rabaey, T.L., Flood, B.R. & Raun, E.S. (2010) Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers. Science 330, 222225.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, 503519.Google Scholar
Maas, S. (Ed.) (2014) Australian Cotton Production Manual 2014. Toowoomba, Australia, Greenmount Press.Google Scholar
Maelzer, D.A. & Zalucki, M.P. (1999) Analysis of long-term light-trap data for Helicoverpa spp. (Lepidoptera: Noctuidae) in Australia: the effect of climate and crop plants. Bulletin of Entomological Research 89, 455463.Google Scholar
Maelzer, D.A., Zalucki, M.P. & Laughlin, R. (1996) Analysis and interpretation of long term light trap data for Helicoverpa punctigera (Lepidoptera: Noctuidae) in Australia: population changes and forecasting pest pressure. Bulletin of Entomological Research 86, 547557.Google Scholar
Mahon, R., Olsen, K., Garsia, K. & Young, S. (2007) Resistance to Bacillus thuringiensis toxin Cry2Ab in a strain of Helicoverpa armigera (Lepidoptera: Noctuidae) in Australia. Journal of Economic Entomology 100, 894902.Google Scholar
Mahon, R.J., Downes, S.J. & James, B. (2012) Vip3A resistance alleles exist at high levels in Australian targets before release of cotton expressing this toxin. PLoS ONE 7, e39192.Google Scholar
Olsen, K.M., Daly, J.C., Holt, H.E. & Finnegan, E.J. (2005) Season-long variation in expression of Cr1Ac gene and efficacy of Bacillus thuringiensis toxin in transgenic cotton against Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Economic Entomology 98, 10071017.Google Scholar
Reed, W. & Pawar, C.S. (1982) Heliothis : a global problem. pp. 914 in Reed, W. & Kumble, V. (Eds) Proceedings of International Workshop on Heliothis Management Problem . Patancheru, India, ICRISAT.Google Scholar
Roush, R.T., Fitt, G.P., Forrester, N.W. & Daly, J.C. (1998) Resistance management for insecticidal transgenic crops : theory and practice. pp. 247257 in Zalucki, M.P., Drew, R.A.I. & White, G.G. (Eds) Pest Management – Future Challenges. Proceedings of the 6th Australasian Applied Entomology Conference , Vol. 1. Brisbane, Australia, University of Queensland Press.Google Scholar
Shelton, A.M., Zhao, J.Z. & Roush, R.T. (2002) Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annual Review of Entomology 47, 845881.Google Scholar
Tabashnik, B.E. (2008) Delaying insect resistance to transgenic crops. Proceedings of the National Academy of Sciences of the United States of America 105, 1902919030.Google Scholar
Tabashnik, B.E., Gassmann, A.J., Crowder, D.W. & Carrière, Y. (2008) Insect resistance to Bt crops: evidence versus theory. Nature Biotechnology 26, 199202.Google Scholar
Tabashnik, B.E., Van Rensburg, J.B.J. & Carrière, Y. (2009) Field-evolved insect resistance to Bt crops: definition, theory, and data. Journal of Economic Entomology 102, 20112025.Google Scholar
Tabashnik, B.E., Brévault, T. & Carrière, Y. (2013) Insect resistance to Bt crops: lessons from the first billion hectares. Nature Biotechnology 31, 510521.Google Scholar
Tay, W.T., Soria, M.F., Walsh, T., Thomazoni, D., Silvie, P., Behere, G.T., Anderson, C. & Downes, S. (2013) A brave new world for an Old World pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLoS ONE 8, e80134.Google Scholar
Wan, P., Huang, Y., Tabashnik, B.E., Huang, M. & Wu, K. (2012) The halo effect: suppression of pink bollworm on non-Bt cotton by Bt cotton in China. PLoS ONE 7, e42004.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, 113131.Google Scholar
Wilson, A.G.L. (1983) Abundance and mortality of overwintering Heliothis spp. Journal of the Australian Entomological Society 22, 191199.Google Scholar
Wilson, A.G.L., Lewis, T. & Cunningham, R.B. (1979) Overwintering and spring emergence of Heliothis armigera (Hübner) (Lepidoptera; Noctuidae) in the Namoi Valley, New South Wales. Bulletin of Entomological Research 69, 97109.Google Scholar
Wilson, L., Downes, S., Khan, M., Whitehouse, M., Baker, G., Grundy, P. & Maas, S. (2013) IPM in the transgenic era: a review of the challenges from emerging pests in Australian cotton systems. Crop & Pasture Science 64, 737749.Google Scholar
Wu, K-M. & Guo, Y. (2005) The evolution of cotton pest management practices in China. Annual Review of Entomology 50, 3152.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, 16761678.Google Scholar
Zalucki, M.P. (2015) From natural history to continental scale perspectives: an overview of contributions by Australian entomologists to applied ecology – a play in three acts. Austral Entomology 54, 235245.Google Scholar
Zalucki, M.P. & Furlong, M.J. (2005) Forecasting Helicoverpa populations in Australia: a comparison of regression based models and a bioclimatic based modelling approach. Insect Science 12, 4556.Google 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, 779814.Google Scholar
Zalucki, M.P., Cunningham, J.P., Downes, S., Ward, P., Lange, C., Meissle, M., Schellhorn, N.A. & Zalucki, J.M. (2012) No evidence for change in oviposition behaviour of Heliothis armigera (Hübner) (Lepidoptera: Noctuidae) after widespread adoption of transgenic insecticidal cotton. Bulletin of Entomological Research 102, 468476.Google Scholar
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