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Temporal detection of Cry1Ab-endotoxins in coccinellid predators from fields of Bacillus thuringiensis corn

Published online by Cambridge University Press:  12 November 2007

J.D. Harwood ,
R.A. Samson  and
J.J. Obrycki
J.D. Harwood*
Affiliation:
Department of Entomology, University of Kentucky, S-225 Agricultural Science Center North, Lexington, KY 40546-0091, USA
R.A. Samson
Affiliation:
Department of Entomology, University of Kentucky, S-225 Agricultural Science Center North, Lexington, KY 40546-0091, USA
J.J. Obrycki
Affiliation:
Department of Entomology, University of Kentucky, S-225 Agricultural Science Center North, Lexington, KY 40546-0091, USA
*
*Author for correspondence Fax: (001) 859-323-1120 Email: [email protected]
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Abstract

The area planted to genetically engineered crops has increased dramatically in the last ten years. This has generated many studies examining non-target effects of bioengineered plants expressing Bacillus thuringiensis endotoxins. To date, most have focused on population-level effects in the field or laboratory evaluation of specific plant-herbivore or plant-herbivore-predator trophic pathways. Using a post-mortem enzyme-linked immunosorbent assay, we examined the uptake of Cry1Ab-endotoxins by predatory coccinellids and the importance of anthesis to this trophic pathway. Adult Coleomegilla maculata, Harmonia axyridis, Cycloneda munda and Coccinella septempunctata contained low, but detectable, quantities of Bt-endotoxin when screened by ELISA. This was most evident in C. maculata, with 12.8% of 775 individuals testing positive for Cry1Ab-endotoxins. Interestingly, the presence of endotoxins in gut samples was not confined to periods around anthesis, but coccinellid adults tested positive two weeks before and up to ten weeks after pollen was shed, suggesting tri-trophic linkages in their food chain facilitates the transfer of endotoxins into higher-order predators. This contrasts with adult Coleomegilla maculata entering overwintering sites where Bt-endotoxins were not detected in gut samples, indicating low levels of persistence of Cry1Ab-endotoxins within coccinellid predators. This study enhances our understanding of complex interactions between transgenic crops and non-target food webs, but further research is required to quantify the significance of specific trophic linkages in the field.

Keywords

Bacillus thuringiensisgut-content analysistransgenic cropsnon-target effectsfood webs
Type
Short Communication
Information
Bulletin of Entomological Research , Volume 97 , Issue 6 , December 2007 , pp. 643 - 648
Copyright
Copyright © Cambridge University Press 2007

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References

Baumgarte, S. & Tebbe, C.C. (2005) Field studies on the environmental fate of the Cry1Ab Bt-toxin produced by transgenic maize (MON810) and its effect on bacterial communities in the maize rhizosphere. Molecular Ecology 14, 2539–2551.Google Scholar
Benton, A.H. & Crump, A.J. (1979) Observations on aggregation and overwintering in the coccinellid beetle Coleomegilla maculata (De Geer). Journal of the New York Entomological Society 87, 154–159.Google Scholar
Carrière, Y., Ellers-Kick, 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 USA 100, 1519–1523.CrossRefGoogle ScholarPubMed
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 impact of transgenic cotton on biodiversity, pesticide use, and yield. Proceedings of the National Academy of Sciences USA 103, 7571–7576.CrossRefGoogle ScholarPubMed
Daly, T. & Buntin, G.D. (2005) Effect of Bacillus thuringiensis transgenic corn for lepidopteran control on nontarget arthropods. Environmental Entomology 34, 1292–1301.CrossRefGoogle Scholar
de la Poza, M., Pons, X., Farinós, G.P., López, C., Ortego, F., Eizaguirre, M., Castañera, P. & Albajes, R. (2005) Impact of farm-scale Bt maize on abundance of predatory arthropods in Spain. Crop Protection 24, 677–684.CrossRefGoogle Scholar
Dively, G.P. (2005) Impact of transgenic VIP3A×Cry1Ab lepidopteran-resistant field corn on the nontarget arthropod community. Environmental Entomology 34, 1267–1291.CrossRefGoogle Scholar
Dutton, A., Klein, H., Romeis, J. & Bigler, F. (2002) Uptake of Bt-toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea. Ecological Entomology 27, 441–447.Google Scholar
Ferry, N., Mulligan, E.A., Stewart, C.N., Tabashnik, B.E., Port, G.R. & Gatehouse, A.M.R. (2006) Prey-mediated effects of transgenic canola on a beneficial, non-target, carabid beetle. Transgenic Research 15, 501–514.Google Scholar
Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology 43, 701–726.CrossRefGoogle ScholarPubMed
Groot, A.T. & Dicke, M. (2002) Insect-resistant transgenic plants in a multi-trophic context. Plant Journal 31, 387–406.Google Scholar
Harwood, J.D., Wallin, W.G. & Obrycki, J.J. (2005) Uptake of Bt-endotoxins by non-target herbivores and higher order arthropod predators: molecular evidence from a transgenic corn agroecosystem. Molecular Ecology 14, 2815–2823.CrossRefGoogle Scholar
Harwood, J.D., Samson, R.A. & Obrycki, J.J. (2006) No evidence for the uptake of Bt Cry1Ab-endotoxins by the carabid predator Scarites subterraneus (Coleoptera: Carabidae) in laboratory and field experiments. Biocontrol Science & Technology 16, 377–388.Google Scholar
Head, G., Brown, C.R., Groth, M.E. & Duan, J.J. (2001) Cry1Ab protein levels in phytophagous insects feeding on transgenic corn: implications for secondary exposure risk assessment. Entomologia Experimentalis et Applicata 99, 37–45.CrossRefGoogle Scholar
Jasinski, J.R., Eisley, J.B., Young, C.E., Kovach, J. & Willson, H. (2003) Select nontarget arthropod abundance in transgenic and nontransgenic field crops in Ohio. Environmental Entomology 32, 407–413.Google Scholar
Lawrence, S. (2005) Agbio keeps on growing. Nature Biotechnology 23, 281.CrossRefGoogle ScholarPubMed
Lövei, G.L. & Arpaia, S. (2005) The impact of transgenic plants on natural enemies: a critical review of laboratory studies. Entomologia Experimentalis et Applicata 114, 1–14.CrossRefGoogle Scholar
Ludy, C. & Lang, A. (2006) Bt maize pollen exposure and impact on the garden spider, Araneus diadematus. Entomologia Experimentalis et Applicata 118, 145–156.CrossRefGoogle Scholar
Lundgren, J.G. & Wiedenmann, R.N. (2002) Coleopteran-specific Cry3Bb1 toxin from transgenic corn pollen does not affect the fitness of a nontarget species, Coleomegilla maculata DeGeer (Coleoptera: Coccinellidae). Environmental Entomology 31, 1213–1218.CrossRefGoogle Scholar
Lundgren, J.G. & Wiedenmann, R.N. (2005) Tritrophic interactions among Bt (CryMb1) corn, aphid prey, and the predator Coleomegilla maculata (Coleoptera: Coccinellidae). Environmental Entomology 34, 1621–1625.Google Scholar
Lundgren, J.G., Razzak, A.A. & Wiedenmann, R.N. (2004) Population responses and food consumption by predators Coleomegilla maculata and Harmonia axyridis (Coleoptera: Coccinellidae) during anthesis in an Illinois cornfield. Environmental Entomology 33, 958–963.Google Scholar
Lundgren, J.G., Huber, A. & Wiedenmann, R.N. (2005) Quantification of consumption of corn pollen by the predator Coleomegilla maculata (Coleoptera: Coccinellidae) during anthesis in an Illinois cornfield. Agricultural and Forest Entomology 7, 53–60.CrossRefGoogle Scholar
Martin, P.A.W. & Travers, R.S. (1989) Worldwide abundance and distribution of Bacillus thuringiensis isolates. Applied and Environmental Microbiology 55, 2437–2442.CrossRefGoogle ScholarPubMed
Men, X., Ge, F., Liu, X. & Yardim, F.N. (2003) Diversity of arthropod communities in transgenic Bt cotton and nontransgenic cotton agroecosystems. Environmental Entomology 32, 270–275.CrossRefGoogle Scholar
Naranjo, S.E. (2005) Long-term assessment of the effects of transgenic Bt cotton on the abundance of nontarget arthropod natural enemies. Environmental Entomology 34, 1193–1223.Google Scholar
Obrist, L.B., Dutton, A., Albajes, R. & Bigler, F. (2006) Exposure of arthropod predators to Cry1Ab toxin in Bt maize fields. Ecological Entomology 31, 143–154.Google Scholar
Obrycki, J.J., Ruberson, J.R. & Losey, J.E. (2004) Interactions between natural enemies and transgenic insecticidal crops. pp. 183–206in Ehler, L.E., Sforza, R. & Matielle, T. (Eds) Genetics, Evolution and Biological Control. Wallingford, CAB International.Google Scholar
Pilcher, C.D., Rice, M.E. & Obrycki, J.J. (2005) Impact of transgenic Bacillus thuringiensis corn and crop phenology on five nontarget arthropods. Environmental Entomology 34, 1302–1316.CrossRefGoogle Scholar
Raps, A., Kehr, J., Gugerli, P., Moar, W.J., Bigler, F. & Hilbeck, A. (2001) Immunological analysis of phloem sap of Bacillus thuringiensis corn and of the nontarget herbivore Rhopalosiphum padi (Homoptera: Aphididae) for the presence of Cry1Ab. Molecular Ecology 10, 525–533.Google Scholar
Reed, G.L., Jensen, A.S., Riebe, J., Head, G. & Duan, J.J. (2001) Transgenic Bt potato and conventional insecticides for Colorado potato beetle management: comparative efficacy and non-target impacts. Entomologia Experimentalis et Applicata 100, 89–100.CrossRefGoogle Scholar
Romeis, J., Meissle, M. & Bigler, F. (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nature Biotechnology 24, 63–71.CrossRefGoogle ScholarPubMed
Sheppard, S.K. & Harwood, J.D. (2005) Advances in molecular ecology: tracking trophic links through predator-prey food webs. Functional Ecology 19, 751–762.Google Scholar
Sisterson, M.S., Biggs, R.W., Olson, C., Carrière, Y., Dennehy, T.J. & Tabashnik, B.E. (2004) Arthropod abundance and diversity in Bt and non-Bt cotton fields. Environmental Entomology 33, 921–929.Google Scholar
Snow, A.A., Andow, D.A., Gepts, P., Hallerman, E.M., Power, A., Tiedje, J.M. & Wolfenbarger, L.L. (2005) Genetically engineered organisms and the environment: current status and recommendations. Ecological Applications 15, 377–404.Google Scholar
Wolfenbarger, L.L. & Phifer, P.R. (2000) Biotechnology and ecology – the ecological risks and benefits of genetically engineered plants. Science 290, 2088–2093.Google Scholar
Zwahlen, C. & Andow, D.A. (2005) Field evidence for the exposure of ground beetles to Cry1Ab from transgenic corn. Environmental Biosafety Research 4, 113–117.Google Scholar
Zwahlen, C., Hilbeck, A., Gugerli, P. & Nentwig, W. (2003) Degradation of the Cry1Ab protein within transgenic Bacillus thuringiensis corn tissue in the field. Molecular Ecology 12, 765–775.CrossRefGoogle ScholarPubMed