Bt-maize effects on biological parameters of the non-target aphid Sitobion avenae (Homoptera: Aphididae) and Cry1Ab toxin detection

Pesticide Biochemistry and Physiology

Volumn 91, Issue 2, 2008, Pages 110-115

  Ramirez Romero, Ricardo ^a   Desneux, Nicolas ^a   Chaufaux, Josette ^a   Kaiser, Laure ^a  

^a CEMAGREF   (France)

Author keywords

Bt maize; Cry1Ab; ELISA; Non target insect; Risk assessment; Sitobion avenae

Indexed keywords

APHIDIDAE; HEMIPTERA; HEXAPODA; SITOBION AVENAE; ZEA MAYS;

EID: 43049162807     PISSN: 00483575     EISSN: 10959939     Source Type: Journal    
DOI: 10.1016/j.pestbp.2008.01.010     Document Type: Article

References (54)

1. G. Brookes, P. Barfoot, GM crops: the first ten years-global socio-economic and environmental impacts, ISAAA Brief No. 36, ISAAA, Ithaca, NY, 2006, p. 96.
2. Koziel M.G., Beland G.L., Bowman C., Carozzi N.B., Crenshaw R., Crossland L., Dawson J., Desai N., Hill M., Kadwell S., Launis K., Lewis K., Maddox D., McPherson K., Meghji M.R., Merlin E., Rhodes R., Warren G.W., Wright M., and Evola S.V. Field performance of Elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis. Biotechnology 11 (1993) 194-200
3. Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum J., Feitelson J., Zeigler D.R., and Dean D.H. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62 (1998) 775-806
4. Chaufaux J., Seguin M., Swanson J.J., Bourguet D., and Siegfried B.D. Chronic exposure of the european corn borer (Lepidoptera: Crambidae) to Cry1Ab Bacillus thuringiensis toxin. J. Econ. Entomol. 94 6 (2001) 1564-1570
5. Knowles B.H., and Dow J.A.T. The crystal δ-endotoxins of Bacillus thuringiensis: models for their mechanism of action on the insect gut. Bioessays 15 7 (1993) 469-476
6. Broderick N.A., Raffa K.F., and Handelsman J. Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc. Natl. Acad. Sci. USA 103 41 (2006) 15196-15199
7. Kaiser L., Pham-Delègue M.-H., and Ramirez-Romero R. Bt-corn and insect helpers. Biofutur 207 (2001) 30-33
8. O'Callaghan M., Glare T.R., Burguess E.P.J., and Malone L.A. Effects of plants genetically modified for insect resistance on nontarget organisms. Annu. Rev. Entomol. 50 (2005) 271-292
9. Losey J.F., Rayor L.S., and Carter M.E. Transgenic pollen harms monarch larvae. Nature 399 (1999) 214
10. Jesse L.C.H., and Obrycki J.J. Field deposition of Bt transgenic corn pollen: lethal effects on the monarch butterfly. Oecologia 125 (2000) 241-248
11. Pleasants J.M., Hellmich R.L., Dively G.P., Sears M.K., Stanley-Horn D.E., Mattila H.R., Foster J.E., Clark P., and Jones G.D. Corn pollen deposition on milkweeds in and near cornfields. Proc. Natl. Acad. Sci. USA 98 21 (2001) 11919-11924
12. Sears M.K., Hellmich R.L., Stanley-Horn D.E., Oberhauser K.S., Pleasants J.M., Mattila H.R., Siegfried B.D., and Dively G.P. Impact of Bt corn pollen on monarch butterfly populations: a risk assessment. Proc. Natl. Acad. Sci. USA 98 21 (2001) 11937-11942
13. Hellmich R.L., Siegfried B.D., Sears M.K., Stanley-Horn D.E., Daniels M.J., Mattila H.R., Spencer T., Bidne K.G., and Lewis L.C. Monarch larvae sensitivity to Bacillus thuringiensis-purified proteins and pollen. Proc. Natl. Acad. Sci. USA 98 21 (2001) 11925-11930
14. Stanley-Horn D.E., Dively G.P., Hellmich R.L., Mattila H.R., Sears M.K., Rose R., Jesse L.C.H., Losey J.E., Obrycki J.J., and Lewis L. Assessing the impact of Cry1Ab-expressing corn pollen on monarch butterfly larvae in field studies. Proc. Natl. Acad. Sci. USA 98 21 (2001) 11931-11936
15. Prasifka P.L., Hellmich R.L., Prasifka J.R., and Lewis L.C. Effects of Cry1Ab-expressing corn anthers on the movement of monarch butterfly larvae. Environ. Entomol. 36 1 (2007) 228-233
16. Dicke F.F., and Guthrie W.D. The most important corn insects. In: Sprague G.F., and Dudley J.W. (Eds). Corn and Corn Improvement (1988), ASA-CSSA-SSSA, Madison 767-867
17. Desneux N., Decouryte A., and Delpuech J.M. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol 52 (2007) 81-106
18. Ode P.J. Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu. Rev. Entomol. 51 (2006) 163-185
19. Head G., Brown C.R., Groth M.E., and Duan J.J. Cry1Ab protein levels in phytophagous insects feeding on transgenic corn: implications for secondary exposure risk assessment. Entomol. Exp. Appl. 99 (2001) 37-45
20. Raps A., Kehr J., Gugerli P., Moar W.J., Bigler F., and Hilbeck A. Immunological analysis of phloem sap of Bacillus thuringiensis corn and of the nontarget herbivore Rhopalosiphum padi (Homoptera: Aphididae) for the presence of Cry1Ab. Mol. Ecol. 10 (2001) 525-533
21. Dutton A., Klein H., Romeis J., and Bigler F. Uptake of Bt-toxin by hervibores feeding on transgenic maize and consequences for the predator Chrysoperla carnea. Ecol. Entomol. 27 (2002) 441-447
22. Saxena D., and Stotzky G. Bt corn has a higher lignin content than non-Bt corn. Am. J. Bot. 88 9 (2001) 1704-1706
23. Poerschmann J., Gathmann A., Augustin J., Langer U., and Górecki T. Molecular composition of leaves and stems of genetically modified Bt and near-isogenic non-Bt maize-characterization of lignin patterns. J. Environ. Qual. 34 (2005) 1508-1518
24. Halpin C., Knight M.E., Foxon G.A., Campbell M.M., Boudet A.M., Boon J.J., Chabbert B., Tollier M.T., and Schuch W. Manipulation of lignin quality by down-regulation of cinnamyl alcohol-dehydrogenase. Plant J. 6 3 (1994) 339-350
25. Lozzia G.C., Furlanis C., Manachini B., and Rigamonti I.E. Effects of Bt corn on Rhopalosiphum padi (Rhynchota: Aphididae) and on its predator Chrysoperla carnea Stephen (Neuroptera: Chrysopidae). Boll. Zool. Agr. Bachic. Ser. II 30 2 (1998) 153-164
26. Lumbierres B., Albajes R., and Pons X. Transgenic Bt maize and Rhopalosiphum padi (Hom., Aphididae) performance. Ecol. Entomol. 29 (2004) 309-317
27. Asin L., and Pons X. Effects of soil insecticide treatments on maize aphids and aphid predators in Catalonia. Crop Prot. 18 (1999) 389-395
28. Haack L., Simon J.-C., Gauthier J.P., Plantegenest M., and Dedryver C.-A. Evidence for predominant clones in a cyclically parthenogenetic organism provided by combined demographic and genetic analyses. Mol. Ecol. 9 (2000) 2055-2066
29. Vickerman G.P., and Wratten S.D. The biology and pest status of cereal aphids (Hemiptera: Aphididae) in Europe: a review. B. Entomol. Res. 69 (1979) 1-32
30. Llewellyn K.S., Loxdale H.D., Harrington R., Brookes C.P., Clark S.J., and Sunnucks P. Migration and genetic structure of the grain aphid (Sitobion avenae) in Britain relates to climate and clonal fluctuation as revealed using microsatellites. Mol. Ecol. 12 (2003) 21-34
31. Weber G. On the ecological genetics of Sitobion avenae (F.) (Hemiptera, Aphididae). Z. Angew. Entomol. 100 (1985) 100-110
32. Hardy J. Entomology IX. The aphides of corn and grasses 1. Aphis avenae, Linnaeus. North Br. Agriculturist J. Horticulture (1850) 596
33. Watt A.D. Wild grasses and the grain aphid (Sitobion avenae). In: Thresh J.M. (Ed). Pests, Pathogens & Vegetation (1981), Pitman, London
34. Watt A.D., and G Dixon A.F. The role of cereal growth stages and crowding in the induction of alatae in Sitobion avenae and its consequences for population growth. Ecol. Entomol. 6 (1981) 441-447
35. Case T.J., Holt R.D., Mcpeek M.A., and Keit T.H. The community context of species' borders: ecological and evolutionary perspectives. Oikos 108 (2005) 28-46
36. Harmon J.P., White J.A., and Andow D.A. Oviposition behavior of Ostrinia nubilalis (Lepidoptera: Crambidae) in response to potential intra- and interspecific interactions. Environ. Entomol. 32 (2003) 334-339
37. Birch L.C. The intrinsic rate of natural increase of an insect population. J. Anim. Ecol. 17 (1948) 15-26
38. DeLoach C.J. Rate of increase of populations of cabbage, green peach and turnip aphids at constant temperatures. Ann. Entomol. Soc. Am. 67 (1974) 332-339
39. SPSS, Systat 10 statistics I & II, Chicago, USA, 2000
40. Sokal R.R., and Rohlf F.J. Biometry. third ed. (1995), Freeman and Company, New York
41. Zar J.H. Biostatical Analysis. fourth ed. (1998), Pearson Education, New Jersey p. 663
42. Pons X., Lumbierres B., López C., and Albajes R. Abundance of non-target pests in transgenic Bt-maize: a farm scale study. Eur. J. Entomol. 102 (2005) 73-79
43. Assin L., and Pons X. Effect of high temperature on the growth and reproduction of corn aphids (Homoptera: Aphididae) and implications for their population dynamics on the northeastern Iberian peninsula. Environ. Entomol. 30 6 (2001) 1127-1134
44. Beck D.L., Dunn G.M., Routley D.G., and Bowman J.S. Biochemical basis of resistance in corn to the corn leaf aphid. Crop Sci. 23 (1983) 995-998
45. Bokonon-Ganta A.H., Bernal J.S., Pietrantonio P.V., and Setamou M. Survivorship and development of fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), on conventional and transgenic maize cultivars expressing Bacillus thuringiensis Cry9C and Cry1A(b) endotoxins. Int. J. Pest Manag. 49 (2003) 169-175
46. Vojtech E., Meissle M., and Poppy G.M. Effects of Bt maize on the herbivore Spodoptera littoralis (Lepidoptera: Noctuidae) and the parasitoid Cotesia marginiventris (Hymenoptera: Braconidae). Transgenic Res. 14 (2005) 133-144
47. Nguyen H.T., and Jehle J.A. Quantitative analysis of the seasonal and tissue-specific expression of Cry1Ab in transgenic maize Mon810. J. Plant Dis. Prot. 114 2 (2007) 82-87
48. Lynch R.E., Wiseman B.R., Plaisted D., and Warnick D. Evaluation of transgenic sweet corn hybrids expressing CryIA(b) toxin for resistance to corn earworm and fall armyworm (Lepidoptera: Noctuidae). J. Econ. Entomol. 92 1 (1999) 246-252
49. Powell G., Tosh C.R., and Hardie J. Host plant selection by aphids: behavioral, evolutionary, and applied perspectives. Annu. Rev. Entomol. 51 (2006) 309-330
50. Stout M.J., Thaler J.S., and Thomma B.P.H.J. Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu. Rev. Entomol. 51 (2006) 663-689
51. URL 1. Available from: .
52. Romeis J., Meissle M., and Bigler F. Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat. Biotechnol. 24 1 (2006) 63-71
53. Johnson M.T., and Gould F. Interaction of genetically engineered host plant resistance and natural enemies of Heliothis virescens (Lepidoptera: Noctuidae) in tobacco. Environ. Entomol. 21 (1992) 586-597
54. Ridick E.W., Dively G., and Barbosa P. Effect of a seed-mix deployment of Cry3A-transgenic and nontransgenic potato on the abundance of Lebia grandis (Coleoptera: Carabidae) and Coleomegilla maculata (Coleoptera: Coccinellidae). Ann. Entomol. Soc. Am. 91 (1998) 647-653