Assessing the risk to nontarget organisms from Bt corn resistant to corn rootworms (Coleoptera: Chrysomelidae): Tier-I testing with Orius insidiosus (Heteroptera: Anthocoridae)

Environmental Entomology

Volumn 37, Issue 3, 2008, Pages 838-844

  Duan, Jian J ^a,b   Telxeira, Debra ^c   Huesing, Joseph E ^a   Jiang, Changjian ^a  

^a MONSANTO COMPANY   (United States)

^b USDA ARS   (United States)

^c Smithers Viscient   (United States)

Author keywords

Biotechnology; Cry3Bb1; Nontarget organisms; Potassium arsenate; Protease inhibitor

Indexed keywords

CRY3BBL ENDOTOXIN, BACILLUS THURINGIENSIS; ENDOTOXIN;

ARSENATE; ASSESSMENT METHOD; BEETLE; BIOASSAY; BIOTECHNOLOGY; DIET; GENETICALLY MODIFIED ORGANISM; MAIZE; NONTARGET ORGANISM; POLLEN; POLLUTION EFFECT; POLLUTION EXPOSURE; POTASSIUM; TRANSGENIC PLANT;

ANIMAL; ARTICLE; BEETLE; DRUG EFFECT; GENETICS; HETEROPTERA; MAIZE; NYMPH; PARASITOLOGY; TOXICITY TESTING; TRANSGENIC PLANT;

ANIMALS; BEETLES; ENDOTOXINS; HETEROPTERA; NYMPH; PLANTS, GENETICALLY MODIFIED; TOXICITY TESTS; ZEA MAYS;

ANTHOCORIDAE; APOIDEA; CHRYSOMELIDAE; COLEOPTERA; DIABROTICA; HETEROPTERA; HEXAPODA; ORIUS INSIDIOSUS; ZEA MAYS;

EID: 46849104494     PISSN: 0046225X     EISSN: None     Source Type: Journal    
DOI: 10.1603/0046-225X(2008)37[838:ATRTNO]2.0.CO;2     Document Type: Article

References (37)

1. Al-Deeb, M. A., and G. E. Wilde. 2003. Effect of Bt corn expressing the Cry3Bb1 toxin for corn rootworm control on above ground nontarget arthropods. Environ. Entomol. 32: 1164-1170.
2. Al-Deeb, M. A., G. E. Wilde, J. M. Blair, and T. C. Todd. 2004. Effect of Bt corn rootworm on non-target soil microarthropods and nematodes. Environ. Entomol. 32:859-865.
3. Askari, A., and V. M. Stern. 1972. Biology and feeding habits of Orius tristicolor (Hemiptera: Anthocoridae), Ann. Entomol. Soc. Am. 65: 96-100.
4. Bhatti, M. A., J. J. Duan, G. Head, C. Jiang, J. M. McKee, T. E. Nickson, C. L. Pilcher, and C. D. Pilcher. 2005a. Field evaluation of the impact of transgenic Bt corn resistant to corn rootworm (Coleoptera: Chrysomelidae) on ground-dwelling invertebrates. Environ. Entomol. 34: 1325-1335.
5. Bhatti, M. A., J. J. Duan, G. Head, C. Jiang, J. M. McKee, T. E. Nickson, C. L. Pilcher, and C. D. Pilcher. 2005b. Field evaluation of the impact of transgenic Bt corn resistant to corn rootworm (Coleoptera: Chrysomelidae): effect on foliage-dwelling arthropods. Environ. Entomol. 34:1336-1345.
6. Brandt, S., T. Coudron, J. Habibi, G. Brown, O. Ilagan, R. Wagner, M. Wright, E. Backus, and J. Huesing. 2004. Interaction of two Bacillus thuringiensis delta-endotoxins with the digestive system of Lygus hesperus. Curr. Microbiol. 48: 1-9.
7. Cohen, A. C. 1995. Extra-oral digestion in predaceous terrestrial arthropoda. Annu. Rev. Entomol. 40: 85-103.
8. Corey, D., S. Kambhampati, and G.Wilde. 1998. Electronic analysis of Orius insidiosus (Hemiptera: Anthocoridae) feeding habits in field corn. J. Kansas Entomol. Soc. 71: 11-17.
9. Desneux,N.,R.J. O'Neil, and H.J.S. Yoo. 2006. Suppression of population growth of the soybean aphid, Aphis glycines Matsumura, by predators: the identification of a key predator, and the effects of prey dispersion, predator density and temperature. Environ. Entomol. 35: 1342-1349.
10. Donovan, W. P., M. J. Rupar, A. C. Slaney, T. Malvar, M. C. Gawron-Burke, and T. B. Johnson. 1992. Characterization of two genes encoding Bacillus thuringiensis insecticidal crystal proteins toxic to Coleoptera species. Appl. Environ. Microbiol. 58: 3921-3927.
11. Duan, J. J., M. S. Paradise, J. G. Lundgren, J. T. Bookout, C. Jiang, and R. N. Wiedenmann. 2006. Assessing non-target impacts of Bt corn resistant to corn rootworms: tier-1 testing with larvae of Poecilus chalcites (Coleoptera: Carabidae). Environ. Entomol. 35: 135-142.
12. Duan, J.J., J. Huesing, and D.Teixeira. 2007. Development of tier-1 toxicity assays for Orius insidiosus (Heteroptera: Anthocoridae) for assessing the risk of plant-incorporated protectants to nontarget heteropterans. Environ Entomol. 36: 982-988.
13. Dudin, Y. A., B-P. Tonnu, L. D. Abee, and R. P. Lirette. 2001. Bt Cry3Bb1.11098 and NPTII protein levels in samples of tissue collected from corn event MON 863 grown in 1999 field trials. MSL-17181. Monsanto Company, St. Louis, MO.
14. Gonzalez-Zamora, J. E., S. Camunez, and C. Avilla. 2007. Effects of Bacillus thuringiensis Cry toxins on develomental and reproductive characteristics of the predator Orius albidipennis (Hemiptera: Anthocoridae) under laboratory conditions. Environ. Entomol. 36: 1246-1253.
15. Habibi, J., T. Coudron, E. Backus, S. Brandt, R. Wagner, M. Wright, and J. Huesing. 2008. Morphology and histology of the alimentary canal of Lygus hesperus (Heteroptera: Cimicomoropha: Miridae). Ann. Entomol. Soc. Am. 101: 159-171.
16. Harwood, J. D., W. G. Wallin, J. J. Obrycki, and O'Neil. 2005. Uptake of Bt endotoxins by nontarget herbivores and higher order arthropod predators: molecular evidence from a transgenic corn agroecosystem. Mol. Ecol. 14: 2815-2823.
17. Harwood, J. D., N. Desneux, H.Y.S. Yoo, D. L. Rowley, M. H. Greenstone, J. J. Obrycki, and R. J. O'Neil. 2007. Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach. Mol. Ecol. 16: 4390-4400.
18. Herman, R. A., P. N. Scherer, D. L. Young, C. A. Mihaliak, T. Meade, A. T. Woodsworth, B. A. Stockhoff, and K. E. Narva. 2002. Binary insecticidal crystal protein from Bacillus thuringiensis, strain PS149B1: effects of individual protein components and mixtures in laboratory bioassays. J. Econ. Entomol. 95: 635-639.
19. Knop-Wright, M., S. Brandt, T. Coudron, R. Wagner, J. Habibi, E. Backus, and J. Huesing. 2006. Characterization of digestive proteolytic activity in Lygus hesperus Knight (Hemiptera: Miridae). J. Insect Physiol. 52: 717-728.
20. Lattin, J. D. 1999. Bionomics of the Anthocoridae. Annu. Rev. Entomol. 44: 207-231.
21. Lundgren, G. J., J. K. Fergen, and W. E. Riedell. 2008. The influence of plant anatomy on oviposition and reproductive success of the omnivorous bug, Orius insidiosus. Anim. Behav. 75: 1495-1502.
22. Mendelsohn, M., J. Rough. Z. Vaituzis, and K. Matthews. 2003. Are Bt crops safe? Nature (Lond.) Biotechnol. 21: 1003-1009.
23. O'Callaghan, M., T. R. Glare, E.P.J. Burgess, and L. A. Malone. 2005. Effects of plants genetically modified for insect resistance on nontarget organisms. Annu. Rev. Entomol. 50: 271-292.
24. Pilcher, C. D., J. J. Obrycki, M. E. Rice, and L. C. Lewis. 1997. Preimaginal development, survival and field abundance of insect predators on transgenic Bacillus thuringiensis corn. Environ. Entomol. 26: 446-454.
25. Ponsard, S., A. P. Gutierrez, and N.J. Mills. 2002. Effects of Bt-toxin (Cry1Ac) in transgenic cotton on the adult longevity of four heteropteran predators. Environ. Entomol. 31: 1197-1205.
26. Romeis, J., M. Meissle, and F. Bigler. 2006. Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nature (Lond.) Biotechnol. 24: 63-71.
27. Bomeis, J., D. Bartsch, F. Bigler, M. P. Candolfi, M.C.C. Gielkens, S. E. Hartley, R. L. Hellmich, J. E. Huesing, P. C. Jepson, R. Layton, H. Quemada, A. Raybould, R. I. Rose, J. Schiemann, M. K. Sears, A. M. Shelton, L. Sweet, Z. Vaituzis, and J. D. Wolt. 2008. Assessment of risk of insect-resistant transgenic crops on nontarget arthropods. Nature Biotechnology 26: 203-208.
28. Butledge, C. E., and R. J. O'Neil. 2005. Orius insidiosus (Say) as a predator of the soybean aphid, Aphis glycines Matsumura. Biol. Control 33: 56-64.
29. SAS Institute. 2002-2003. SAS on-line documentation, version 9.1 SAS Institute, Cary, NC.
30. Torres, J. B., and J. R. Ruberson. 2007. Interactions of Bacillus thuringiensis Cry1Ac toxin in genetically engineered cotton with predatory heteropterans. Transgenic Res. (doi: 10.1007/s11248-007-9109-8).
31. U.S. Environmental Protection Agency [EPA]. 1998. Guidelines for ecological risk assessment. U.S. Environmental Protection Agency, Risk Assessment Forum, Washington, DC.
32. U.S. Environmental Protection Agency [EPA]. 2003. Biopesticides registration action document: Event MON 863 Bacillus thuringiensis Cry3Bb1 corn. U.S. Environmental Protection Agency, Office of Pesticide Programs and Biopesticides and Pollution Prevention Division, Washington, DC.
33. U.S. Environmental Protection Agency [EPA]. 2005. Biopesticides registration action document: Bacillus thuringiensis Cry34Ab1 and Cry35Ab1 proteins and the genetic material necessary for their production (plasmid insert PHP 17662) in event DAS-59122-7 corn. U.S. Environmental Protection Agency, Office of Pesticide Programs and Biopesticides and Pollution Prevention Division, Washington, DC.
34. U.S. Environmental Protection Agency [EPA]. 2007. White paper on tier-based testing for the effects of protein-aceous insecticidal plant-incorporated protectants on non-target arthropods for regulatory risk assessments. U.S. Environmental Protection Agency, Office of Pesticide Programs and Biopesticides and Pollution Prevention Division, Washington, DC.
35. Vaughn, T., T. Cavato, G. Brar, T. Coombe, T. DeGooyer, S. Ford, M. Groth, A. Howe, S. Johnson, K. Kolacz, C. Pilcher, J. Purcell, C. Romano, L. English, and J. Pershing. 2005. A method of controlling corn rootworm feeding using Bacillus thuringiensis protein expressed in transgenic maize. Crop Sci. 45: 931-938.
36. Ward, D. P., T. A. DeGooyer, T. T. Vaughn, G. P. Head, M. J. McKee, J. D. Astwood, and J. C. Pershing. 2004. Genetically enhanced maize as a potential management option for corn rootworm: YieldGard® rootworm maize case-study, pp. 239-262. In S. Vidal (ed.), Western corn root-worm: ecology and management. CABI Publishing, Oxon, United Kingdom.
37. Zwahlen, C., W. Nentwig, F. Bigler, and A. Hilbeck. 2000. Tritrophic interactions of transgenic Bacillus thuringiensis corn, Anaphothrips obscurus (Thysanoptera: Thripidae), and the predator Orius majusculus (Heteroptera: Anthocoridae). Environ. Entomol. 29: 846-850.