Evidence of Resistance to Cry34/35Ab1 Corn by Western Corn Rootworm (Coleoptera: Chrysomelidae): Root Injury in the Field and Larval Survival in Plant-Based Bioassays

Journal of Economic Entomology

Volumn 109, Issue 4, 2016, Pages 1872-1880

  Gassmann, Aaron J ^a   Shrestha, Ram B ^a   Jakka, Siva R K ^a,b   Dunbar, Mike W ^a   Clifton, Eric H ^a   Paolino, Aubrey R ^a   Ingber, David A ^a,c   French, B Wade ^d   Masloski, Kenneth E ^a   Dounda, John W ^a   St Clair, Coy R ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b Valent BioSciences Corporation   (United States)

^c UNIVERSITY OF DELAWARE   (United States)

^d NORTH CENTRAL AGRICULTURAL RESEARCH LABORATORY   (United States)

Author keywords

bioassay; Diabrotica virgifera virgifera; insect resistance management; integrated pest management; refuge strategy

Indexed keywords

EID: 84983739198     PISSN: 00220493     EISSN: 1938291X     Source Type: Journal    
DOI: 10.1093/jee/tow110     Document Type: Article

References (50)

1. Abbott, W. S. 1925. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 18: 265-267.
2. Abendroth, L. J., R. W. Elmore, M. J. Boyer, and S. K. Marlay. 2011. Corn growth and development. vol. PMR 1009, Iowa State University, Ames, Iowa.
3. Andow, D. A., S. G. Pueppke, A. W. Schaafsma, A. J. Gassmann, T. W. Sappington, L. J. Meinke, P. D. Mitchell, T. M. Hurley, R. L. Hellmich, and R. P. Porter. 2016. Early detection and mitigation of resistance to Bt maize by western corn rootworm (Coleoptera: Chrysomelidae) J. Econ. Entomol. 109: 1-12.
4. Carrière, Y., D. W. Crowder, and B. E. Tabashnik. 2010. Evolutionary ecology of insect adaptation to Bt crops. Evol. Appl. 3: 561-573.
5. Cullen, E. M., M. E. Gray, A. J. Gassmann, and B. E. Hibbard. 2013. Resistance to Bt corn by western corn rootworm (Coleoptera: Chrysomelidae) in the U.S. Corn Belt. J. Integr. Pest Manag. 4(3): IPM13012 (doi: dx.doi.org/10.1603/IPM13012)
6. Deitloff, J., M. W. Dunbar, D. A. Ingber, B. E. Hibbard, and A. J. Gassmann. 2015. Effects of refuges on the evolution of resistance to transgenic corn by the western corn rootworm, Diabrotica virgifera virgifera LeConte. Pest Manag. Sci. 72: 190-198. (DOI 10.1002/ps.3988).
7. Dun, Z., P. D. Mitchell, and M. Agosti. 2010. Estimating Diabrotica virgifera virgifera damage functions with field trial data: Applying an unbalanced nested error component model. J. Appl. Entomol. 134: 409-419.
8. (EPA) Environmental Protection Agency. 2005. Biopesticides Registration Action Document: Bacillus thuringiensis Cry34Ab1 and Cry35Ab1 Proteins and the Genetic Material Necessary for Their Production (PHP17662 T-DNA) in Event DAS-59122-7 Corn (OECD Unique Identifier: DAS-59122-7). (http://www3.epa.gov/pesticides/chem-search/ reg-actions/pip/cry3435ab1-brad.pdf) (accessed 4 January 2016).
9. (EPA) Environmental Protection Agency. 2006. Biopesticides registration action document: Modified Cry3A Protein and the Genetic Material Necessary for its Production (Via Elements of pZM26) in Event MIR604 Corn SYN-IR604-8 (http://www.epa.gov/oppbppd1/biopesticides/pips/ mcry3a-brad.pdf) (accessed 4 January 2016).
10. (EPA) Environmental Protection Agency. 2009. Pesticide Fact Sheet. (http:// www3.epa.gov/pesticides/chem-search/reg-actions/pip/smartstax-fact sheet.pdf) (accessed 4 January 2016).
11. (EPA) Environmental Protection Agency. 2010. Biopesticides registration action document: Bacillus thuringiensis Cry3Bb1 Protein and the Genetic Material Necessary for Its Production (Vector PV-ZMIR13L) in MON 863 Corn (OECD Unique Identifier: MON-ØØ863-5). (http://www3.epa.gov/ pesticides/chem-search/reg-actions/pip/cry3bb1-brad.pdf) (accessed 4 January 2016).
12. (EPA) Environmental Protection Agency. 2011a. Bt11 x 59122-7 x MIR 604 x 1507 (Cry1Ab x Cry34/35 x mCry3A x Cry1F). (http://www.epa.gov/ingre dients-used-pesticide-products/current-previously-registered-section-3-plant-incorporated) (accessed 4 January 2016).
13. (EPA) Environmental Protection Agency. 2011b. Biopesticides Registration Action Document: MON 89034 x TC1507 x MON 88017 x DAS-59122-7 (SmartStaxVR ) B.t. Corn Seed Blend. (http://www3.epa.gov/pesticides/chem- search/reg-actions/pip/smartstax-seedblend.pdf) (accessed 4 January 2016).
14. (EPA) Environmental Protection Agency. 2012. Optimum AcreMax Xtreme (Cry1F x Cry34/35 x Cry1Ab x mCry3A)-seed blend. (http://www.epa. gov/ingredients-used-pesticide-products/current-previously-registered-sec tion-3-plant-incorporated) (accessed 4 January 2016).
15. (EPA) Environmental Protection Agency. 2013. White Paper on Corn Rootworm Resistance Monitoring for Bt Plant-Incorporated Protectants. (http://www.regulations.gov/#!documentDetail;D=EPA-HQ-OPP-2013-0490-0008) (accessed 15 April 2016).
16. (EPA) Environmental Protection Agency. 2016a. Framework to delay corn rootworm resistance (https://www.epa.gov/regulation-biotechnologyunder-tsca-and-fifra/framework-delay-corn-rootworm-resistance) (accessed 6 April 2016).
17. (EPA) Environmental Protection Agency. 2016b. Current and Previously Registered Section 3 Plant-Incorporated Protectant (PIP) Registrations. (http://www.epa.gov/ingredients-used-pesticide-products/current-previ ously-registered-section-3-plant-incorporated) (accessed 4 January 2016).
18. Gassmann, A. J. 2012. Field-evolved resistance to Bt maize by western corn rootworm: predictions from the laboratory and effects in the field. J. Invertebr. Pathol. 110: 287-293.
19. Gassmann, A. J., J. L. Petzold-Maxwell, R. S. Keweshan, and M. W. Dunbar. 2011. Field-evolved resistance to Bt maize by western corn rootworm. PLoS ONE 6: e22629. (doi:22610.21371/journal.pone.0022629).
20. Gassmann, A. J., J. L. Petzold-Maxwell, R. S. Keweshan, and M. W. Dunbar. 2012. Western corn rootworm and Bt maize: Challenges of pest resistance in the field.GM Crops Food 3: 235-244.
21. Gassmann, A. J., J. L. Petzold-Maxwell, E. H. Clifton, M. W. Dunbar, A. M. Hoffmann, D. A. Ingber, and R. S. Keweshan. 2014. Field-evolved resistance by western corn rootworm to multiple Bacillus thuringiensis toxins in transgenic maize. Proc. Natl. Acad. Sci. USA. 111: 5141-5146.
22. Gould, F. 1998. Sustainability of transgenic insecticidal cultivars: Integrating pest genetics and ecology. Annu. Rev. Entomol. 43: 701-726.
23. Gray, M. E., K. L. Steffey, R. E. Estes, and J. B. Schroeder. 2007. Responses of transgenic maize hybrids to variant western corn rootworm larval injury. J. Appl. Entomol. 131: 386-390.
24. Gray, M. E., T. W. Sappington, N. J. Miller, J. Moeser, and M. O. Bohn. 2009. Adaptation and invasiveness of western corn rootworm: intensifying research on a worsening pest. Annu. Rev. Entomol. 54: 303-321.
25. Hammack, L., M. M. Ellsbury, R. L. Roehrdanz, and J. L. J. Pikul. 2003. Larval sampling and instar determination in field populations of northern and western corn rootworm (Coleoptera: Chrysomelidae). J. Econ. Entomol. 96: 1153-1159.
26. Hughson, S. A., and J. L. Spencer. 2015. Emergence and abundance of western corn rootworm (Coleoptera: Chrysomelidae) in Bt cornfields with structured and seed blend refuges. J. Econ. Entomol. 108: 114-125.
27. Jaffe, G. 2009. Complacency on the Farm: Significant Noncompliance with EPA's Refuge Requirements Threatens the Future Effectiveness of Genetically Engineered Pest-protected Corn. Center for Science in the Public Interest, Washington, DC.
28. James, C. 2013. Global Status of Commercialized Biotech/GM Crops: 2013. ISAAA Brief No. 46. ISAAA, Ithaca, New York.
29. Keweshan, R. S., G. P. Head, and A. J. Gassmann. 2015. Effects of pyramided Bt corn and blended refuges on western corn rootworm and northern corn rootworm (Coleoptera: Chrysomelidae). J. Econ. Entomol. 108: 720-729.
30. Lefko, S. A., T. M. Nowatzki, S. D. Thompson, R. R. Binning,M. A. Pascual, M. L. Peters, E. J. Simbro, and B. H. Stanley. 2008. Characterizing laboratory colonies of western corn rootworm (Coleoptera: Chrysomelidae) selected for survival on maize containing event DAS-59122-7. J. Appl. Entomol. 132: 189-204.
31. Levine, E., and H. Oloumi-Sadeghi. 1991. Management of diabroticite rootworms in corn. Annu. Rev. Entomol. 36: 229-255.
32. Li, H., M. Olson, G. Lin, T. Hey, S. Y. Tan, and K. E. Narva. 2013. Bacillus thuringiensis Cry34Ab1/35Ab1 interactions with western corn rootworm midgut membrane binding sites. PLoS ONE 8: e53079. (doi:10.1371/ journal.pone.0053079).
33. Meinke, L. J., B. D. Siegfried, R. J. Wright, and L. D. Chandler. 1998. Adult susceptibility of Nebraska western corn rootworm (Coleoptera: Chrysomelidae) populations to selected insecticides. J. Econ. Entomol. 91: 594-600.
34. Meinke, L. J., T. W. Sappington, D. W. Onstad, T. Guillemaud, N. J. Miller, J. Komáromi, N. Levay, L. Furlan, J. Kiss, and F. Toth. 2009. Western corn rootworm (Diabrotica virgifera virgifera LeConte) population dynamics. Agric. For. Entomol. 11: 29-46.
35. Nowatzki, T. M., S. A. Lefko, R. R. Binning, S. D. Thompson, T. A. Spencer, and B. D. Siegfried. 2008. Validation of a novel resistance monitoring technique for corn rootworm (Coleoptera: Chrysomelidae) and event DAS-59122-7 maize. J. Appl. Entomol. 132: 177-188.
36. Oleson, J. D., Y.-L. Park, T. M. Nowatzki, and J. J. Tollefson. 2005. Node-injury scale to evaluate root injury by corn rootworms (Coleoptera: Chrysomelidae). J. Econ. Entomol. 98: 1-8.
37. Petzold-Maxwell, J. L., S. T. Jaronski, E. H. Clifton, M. W. Dunbar, M. A. Jackson, and A. J. Gassmann. 2013a. Interactions among Bt maize, entomopathogens and rootworm species (Coleoptera: Chrysomelidae) in the field: Effects on survival, yield and root injury. J. Econ. Entomol. 106: 622-632.
38. Petzold-Maxwell, J. L., L. J. Meinke, M. E. Gray, R. E. Estes, and A. J. Gassmann. 2013b. Effect of Bt maize and soil insecticides on yield, injury, and rootworm survival: Implications for resistance management. J. Econ. Entomol. 106: 1941-1951.
39. Roush, R. T. 1998. Two-toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Philos. Trans. R. Soc. Lond. B. Biol. Sci. 353: 1777-1786.
40. SAS. 2013. SAS Enterprise Guide 6.1. SAS Institute Inc, Cary.
41. Schrader, P. M., R. E. Estes, N. A. Tinsley, A. J. Gassmann, and M. E. Gray. 2016. Evaluation of adult emergence and larval root injury for Cry3Bb1-resistant populations of the western corn rootworm. J. Appl. Entomol. (in press).
42. Shrestha, R. B., S.R.K. Jakka, B. W. French, and A. J. Gassmann. 2016. Fieldbased assessment of resistance to Bt corn by western corn rootworm (Coleoptera: Chrysomelidae). J. Econ. Entomol. (in press) (DOI: http://dx. doi.org/10.1093/jee/tow087).
43. Spencer, J. L., E. Levine, S. A. Isard, and T. R. Mabry. 2005. Movement, dispersal and behaviour of western corn rootworm adults in rotated maize and soybean fields, pp. 121-144. In S. Vidal, U. Kuhlmann and C. R. Edwards (eds.), Western Corn Rootworm: Ecology and Management. CABI Publishing, Cambridge, United Kingdom.
44. Spencer, J. L., B. E. Hibbard, J. Moeser, and D. W. Onstad. 2009. Behaviour and ecology of the western corn rootworm (Diabrotica virgifera virgifera LeConte). Agric. For. Entomol. 11: 9-27.
45. Spencer, J. L., S. A. Hughson, and E. Levine. 2014. Insect resistance to crop rotation, pp. 233-278. In D. W. Onstad (ed.), Insect Resistance Management: Biology, Economics and Predictions. Academic Press, London.
46. Storer, N. P., J. N. Babcock, and J. M. Edwards. 2006. Field measures of western corn rootworm (Coleoptera: Chrysomelidae) mortality caused by Cry34/Cry35Ab1 proteins expressed in maize event 59122 and implications for trait durability. J. Econ. Entomol. 99: 1381-1387.
47. Tabashnik, B. E., and F. Gould. 2012. Delaying corn rootworm resistance to Bt corn. J. Econ. Entomol. 105: 767-776.
48. Tabashnik, B. E., A. J. Gassmann, D. W. Crowder, and Y. Carrière. 2008. Insect resistance to Bt crops: Evidence versus theory. Nat. Biotechnol. 26: 199-202.
49. Tinsley, N. A., R. E. Estes, and M. E. Gray. 2013. Validation of a nested error component model to estimate damage caused by corn rootworm larvae. J. Appl. Entomol. 137: 161-169.
50. Wangila, D. S., A. J. Gassmann, J. L. Petzold-Maxwell, B. W. French, and L. J. Meinke. 2015. Susceptibility of Nebraska western corn rootworm populations (Coleoptera: Chrysomelidae) populations to Bt corn events. J. Econ. Entomol. 108: 742-751.