Early detection and mitigation of resistance to Bt maize by western corn rootworm (Coleoptera: Chrysomelidae)

Journal of Economic Entomology

Volumn 109, Issue 1, 2016, Pages 1-12

  Andow, David A ^a   Pueppke, Steven G ^b   Schaafsma, Arthur W ^c   Gassmann, Aaron J ^d   Sappington, Thomas W ^e   Meinke, Lance J ^f   Mitchell, Paul D ^g   Hurley, Terrance M ^a   Hellmich, Richard L ^e   Porter, R Pat ^h  

^a UNIVERSITY OF MINNESOTA   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c UNIVERSITY OF GUELPH   (Canada)

^d IOWA STATE UNIVERSITY   (United States)

^e AGRICULTURAL RESEARCH SERVICE   (United States)

^f UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^g UNIVERSITY OF WISCONSIN MADISON   (United States)

^h TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Bt resistance; Diabrotica virgifera virgifera; Insect resistance management; Integrated pest management; Western corn rootworm

Indexed keywords

BACTERIAL PROTEIN; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS; INSECTICIDE;

ANIMAL; BACILLUS THURINGIENSIS; BEETLE; BIOLOGICAL PEST CONTROL; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; INSECTICIDE RESISTANCE; MAIZE; TRANSGENIC PLANT;

ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; BEETLES; ENDOTOXINS; HEMOLYSIN PROTEINS; INSECTICIDE RESISTANCE; INSECTICIDES; PEST CONTROL, BIOLOGICAL; PLANTS, GENETICALLY MODIFIED; ZEA MAYS;

EID: 84983551900     PISSN: 00220493     EISSN: 1938291X     Source Type: Journal    
DOI: 10.1093/jee/tov238     Document Type: Article

References (124)

1. Abbott, W. S. 1925. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 18: 265-267.
2. Alves, A. P., T. A. Spencer, B. E. Tabashnik, and B. D. Siegfried. 2006. Inheritance of resistance to Cry1Ab Bacillus thuringiensis toxin in Ostrinia nubilalis (Lepidoptera: Crambidae). J. Econ. Entomol. 99: 494-501.
3. Alstad, D. N., and D. A. Andow. 1995. Managing the evolution of insect resistance to transgenic plants. Science 268: 1894-1896.
4. Andow, D. A. 2001. Resisting resistance to Bt corn, pp. 99-124. In D. K. Letourneau and B. E. Burrows (eds.), Genetically engineered organisms: assessing environmental and human health effects. CRC Press, Boca Raton, FL.
5. Andow, D. A., and A. R. Ives. 2002. Monitoring and adaptive resistance management. Ecol. Appl. 12: 1378-1390.
6. Binning, R. R., S. A. Lefko, A. Y. Millsap, S. D. Thompson, and T. M. Nowatzki. 2010. Estimating western corn rootworm (Coleoptera: Chrysomelidae) larval susceptibility to event DAS-59122-7 maize. J. Appl. Entomol. 134: 551-561.
7. Branson, T. F., G. R. Sutter, and J. R. Fisher. 1980. Plant response to stress induced by artificial infestations of western corn rootworm. Environ. Entomol. 9: 253-257.
8. Brent, K. J. 1986. Detection and monitoring of resistant forms: an overview, pp. 298-312. In NRC, pesticide resistance: Strategies and tactics for management. National Academies Press, Washington, DC.
9. Brévault, T., S. Heuberger, M. Zhang, C. Ellers-Kirk, X. Ni, L. Masson, X. Li, B. E. Tabashnik, and Y. Carrière. 2013. Potential shortfall of pyramided transgenic cotton for insect resistance management. Proc. Natl. Acad. Sci. USA 110: 5806-5811.
10. Caprio, M. A., D. V. Sumerford, and S. R. Simms. 2000. Evaluating transgenic plants for suitability in pest and resistance management programs, pp. 805-828. In L. Lacey and H. Kaya, (eds.), Field manual of techniques in invertebrate pathology. Kluwer, Boston, MA.
11. Carrière, Y., T. J. Dennehy, B. Pedersen, S. Haller, C. Ellers-Kirk, L. Antilla, Y.-B. Liu, E. Willott, and B. E. Tabashnik. 2001a. Large-scale management of insect resistance to transgenic cotton in Arizona: Can transgenic insecticidal crops be sustained? J. Econ. Entomol. 94: 315-325.
12. Carrière, Y., C. Ellers-Kirk, M. Sisterson, L. Antilla, M. Whitlow, T. J. Dennehy, and B. E. Tabashnik. 2001b. Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton. Proc. Natl. Acad. Sci. USA. 100: 1519-1523.
13. Carrière, Y., M. S. Sisterson, and B. E. Tabashnik. 2004. Resistance management for sustainable use of Bacillus thuringiensis crops in integrated pest management, pp. 65-95. In A. R. Horowitz and I. Ishaaya. (eds.), Insect pest management: Field and protected crops. Springer-Verlag, Berlin Heidelberg, Germany.
14. Carrière, Y., D. W. Crowder, and B. E. Tabashnik. 2010. Evolutionary ecology of insect adaptation to Bt crops. Evol. Appl. 3: 561-573.
15. Carrière, Y., N. Crickmore, and B. E. Tabashnik. 2015. Optimizing pyramided transgenic Bt crops for sustainable pest management. Nat. Biotechnol. 33: 161-168.
16. Chiang, H. C. 1973. Bionomics of the northern and western corn rootworms. Annu. Rev. Entomol. 18: 47-72.
17. Crow, J. F. 1960. Genetics of insecticide resistance: General considerations. Misc. Pub. Entomol. Soc. Am. 2: 69-74.
18. 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: D1-D6.
19. Darnell, S. J., L. J. Meinke, and L. J. Young. 2000. Influence of corn phenology on adult western corn rootworm (Coleoptera: Chrysomelidae) distribution. Environ. Entomol. 29: 587-595.
20. 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. DOI 10.1002/ps.3988 (online early).
21. Devos, Y., L. N. Meihls, J. Kiss, and B. E. Hibbard. 2013. Resistance evolution to the first generation of genetically modified Diabrotica-active Bt-maize events by western corn rootworm: management and monitoring considerations. Trans. Res. 22: 269-299.
22. Dun, Z., P. D. Mitchell, and M. Agosti. 2010. Estimating Diabrotica virgifera virgifera damage functions with field data: Applying an unbalanced nested error component model. J. Appl. Entomol. 134: 409-419.
23. Farias, J., D. A. Andow, R. Horikoshi, R. Sorgatto, A. Santos, and C. Omoto. 2014. Field-evolved resistance to Cry1F maize by Spodoptera frugiperda (Lepidoptera: Noctuidae) in Brazil. Crop Prot. 64: 150-158.
24. Frank, D. L., R. Kurtz, N. A. Tinsley, A. J. Gassmann, L. J. Meinke, D. Moellenbeck, M. E. Gray, L. W. Bledsoe, C. H. Krupke, R. E. Estes, et al. 2015. Effect of seed blends and soil-insecticide on western and northern corn rootworm emergence from mCry3A+eCry3.1Ab Bt Maize. J. Econ. Entomol. 108: 1260-1270.
25. Fuglie, K., P. Heisey, J. King, C. E. Pray, and D. Schimmelpfennig. 2012. The contribution of private industry to agricultural innovation. Science 338: 1031-1032.
26. Gassmann, A. J. 2012. Field-evolved resistance to Bt maize by western corn rootworm: Predictions from the laboratory and effects in the field. J. Invert. Pathol. 110: 287-293.
27. Gassmann, A. J., Y. Carrière, and B. E. Tabashnik. 2009. Fitness costs of insect resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 54: 147-163.
28. 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.
29. 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.
30. 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. Nat. Acad. Sci. USA. 111: 5141-5146.
31. Gillette, C. P. 1912. Diabrotica virgifera Lec. A corn rootworm. J. Econ. Entomol. 5: 364-66.
32. Godfrey, L. D., L. J. Meinke, and R. J. Wright. 1993. Vegetative and reproductive biomass accumulation in field corn: Response to root injury by western corn rootworm (Coleoptera: Chrysomelidae). J. Econ. Entomol. 86: 1557-1573.
33. Gould, F. 1998. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 43: 701-726.
34. Gould, F., M. B. Cohen, J. S. Bentur, G. G. Kennedy, and J. van Duyn. 2006. Impact of small fitness costs on pest adaptation to crop varieties with multiple toxins: a heuristic model. J. Econ. Entomol. 99: 2091-2099.
35. Gray, M. E., A. S. Felsot, K. L. Steffey, and E. Levine. 1992. Planting time application of soil insecticides and western corn rootworm (Coleoptera: Chrysomelidae) emergence: implications for long-term management programs. J. Econ. Entomol. 85: 544-553.
36. 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.
37. 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.
38. Head, G., M. Carroll, T. Clark, T. Galvan, R. M. Huckaba, P. Price, L. Samuel, and N. P. Storer. 2014. Efficacy of SmartStaxVR insect-protected corn hybrids against corn rootworm: the value of pyramiding the Cry3Bb1 and Cry34/35Ab1 proteins. Crop Prot. 57: 38-47.
39. Hibbard, B. E., L. N. Meihls, M. R. Ellersieck, and D. W. Onstad. 2010. Density-dependent and density-independent mortality of the western corn rootworm: Impact on dose calculations of rootworm-resistant Bt corn. J. Econ. Entomol. 103: 77-84.
40. Hibbard, B. E., D. L. Frank, R. Kurtz, E. Boudreau, M. R. Ellersieck, and F. Odhiambo. 2011. Mortality impact of Bt transgenic maize roots expressing eCry3.1Ab, mCry3A, and eCry3.1Ab plus mCry3A on western corn rootworm larvae in the field. J. Econ. Entomol. 104: 1584-1591.
41. Hill, R. E., and Z. B. Mayo. 1974. Trap-corn to control rootworms. J. Econ. Entomol. 67: 748-750.
42. Hitchon, A. J., J. L. Smith, B. W. French, and A. W. Schaafsma. 2015. Impact of the Bt corn proteins Cry34/35Ab1 and Cry3Bb1, alone or pyramided, on western corn rootworm (Coleoptera: Chrysomelidae) beetle emergence in the field. J. Econ. Entomol. 108: 1986-1993.
43. Hoffmann, A. M., B. W. French, S. T. Jaronski, and A. J. Gassmann. 2014. Effects of entomopathogens on mortality of western corn rootworm and fitness costs of resistance to Cry3Bb1 maize. J. Econ. Entomol. 107: 352-360.
44. Hoffmann, A. M., B. W. French, R. L. Hellmich, N. Lauter, and A. J. Gassmann. 2015. Fitness costs of resistance to Cry3Bb1 maize by western corn rootworm. J. Appl. Entomol. 139: 403-415.
45. Huang, F., D. A. Andow, and L. L. Buschman. 2011. Success of the high dose/ refuge resistance management strategy after fifteen years of Bt crop use in North America. Entomol. Exp. Appl. 140: 1-16.
46. Hurley, T. M., and P. D. Mitchell. 2013. Insect resistance management: Adoption and compliance, pp. 227-253. In D. W. Onstad, (ed.), Insect resistance management: Biology, economics, and prediction, 2nd ed. Academic Press, San Diego, CA.
47. Ivezić , M., E. Raspudić , M. Brmež, I. Majić , I. Brkić , J. J. Tollefson, M. Bohn, B. E. Hibbard, and D. Šimić . 2009. A review of resistance breeding options targeting western corn rootworm (Diabrotica virgifera virgifera LeConte). Agric. For. Entomol. 11: 307-311.
48. Kang, J., and C. H. Krupke. 2009. Likelihood of multiple mating in the male western corn rootworm, Diabrotica virgifera virgifera LeConte. Environ. Entomol. 102: 2096-2100.
49. 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.
50. Krupke, C., P. Marquardt, W. Johnson, S. Weller, and S. P. Conley. 2009. Volunteer corn presents new challenges for insect resistance management. Agron. J. 101: 797-799.
51. 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.
52. Levine, E., and H. Oloumi-Sadeghi. 1996. Western corn rootworm (Coleoptera: Chrysomelidae) larval injury to corn grown for seed production following soybeans grown for seed production. J. Econ. Entomol. 89: 1010-1016.
53. Marquardt, P. T., and C. H. Krupke. 2009. Dispersal behavior of western corn rootworms in Bt and refuge cornfield environments. Environ. Entomol. 38: 176-182.
54. Marra, M. C., N. E. Piggott, and B. K. Goodwin. 2012. The impact of corn rootworm protected biotechnology traits in the United States. AgBioForum 15: 217-230.
55. McDougall, P. 2011. The cost and time involved in the discovery, development and authorisation of a new plant biotechnology derived trait. Consultancy Study for Crop Life International, (http://www.croplife.org/PhillipsMcDougallStudy)
56. Meihls, L. N., M. L. Higdon, B. D. Siegfried, N. J. Miller, T. W. Sappington, M. R. Ellersieck, T. A. Spencer, and B. E. Hibbard. 2008. Increased survival of western corn rootworm on transgenic corn within three generations of on-plant greenhouse selection. Proc. Natl. Acad. Sci. USA 105: 19177-19182.
57. Meihls, L. N., M. L. Higdon, M. Ellersieck, and B. E. Hibbard. 2011. Selection for resistance to mCry3A-expressing transgenic corn in western corn rootworm. J. Econ. Entomol. 104: 1045-1054.
58. Meihls, L. N., M. L. Higdon, M. Ellersieck, B. E. Tabashnik, and B. E. Hibbard. 2012. Greenhouse-selected resistance to Cry3Bb1-producing corn in three western corn rootworm populations. PLoS ONE 7: e51055.
59. Meinke, L. J., B. D. Siegfried, R. J. Wright, L. D. Chandler. 1998. Adult susceptibility of Nebraska western corn rootworm (Coleoptera: Chrysomelidae) populations to selected insecticides. J. Econ. Entomol. 91: 594-600.
60. 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.
61. Miller, N. J., T. Guillemaud, R. Giordano, B. D. Siegfried, M. E. Gray, L. J. Meinke, and T. W. Sappington. 2009. Genes, gene flow and adaptation of Diabrotica virgifera virgifera. Agric. For. Entomol. 11: 47-60.
62. Moar, W., R. Roush, A. Shelton, J. Ferré, S. MacIntosh, B. R. Leonard, and C. Abel. 2008. Field-evolved resistance to Bt toxins.Nat. Biotech. 26: 1072-1074.
63. Murphy, A. F., M. D. Ginzel, and C. H. Krupke. 2010. Evaluating western corn rootworm (Coleoptera: Chrysomelidae) emergence and root damage in a seed mix refuge. J. Econ. Entomol. 103: 147-157.
64. National Research Council. 2010. The impact of genetically engineered crops on farm sustainability in the United States. National Academies Press, Washington, DC.
65. 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.
66. 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.
67. Onstad, D. W. 2008. Major issues in insect resistance management, pp. 1-16. In D. W. Onstad, (ed.), Insect resistance management: Biology, economics and prediction. Academic Press, New York, NY.
68. Onstad, D. W., and L. J. Meinke. 2010. Modeling evolution of Diabrotica virgifera virgifera (Coleoptera:Chrysomelidae) to transgenic corn with two insecticidal traits. J. Econ. Entomol. 103: 849-860.
69. Onstad, D. W., M. G. Joselyn, S. A. Isard, E. Levine, J. L. Spencer, L. W. Bledsoe, C. R. Edwards, C. D. DiFonzo, and H. Willson. 1999. Modeling the spread of western corn rootworm (Coleoptera: Chrysomelidae) populations adapting to soybean-corn rotation. Environ. Entomol. 28: 188-194.
70. Onstad, D. W., D. W. Crowder, P. D. Mitchell, C. A. Guse, J. L. Spencer, E. Levine, and M. E. Gray. 2003. Economics versus alleles: balancing integrated pest management and insect resistance management for rotation-resistant western corn rootworm (Coleoptera: Chrysomelidae). J. Econ. Entomol. 96: 1872-1885.
71. Onstad, D. W., P. D. Mitchell, T. M. Hurley, J. G. Lundgren, R. P. Porter, C. H. Krupke, J. L. Spencer, C. D. DiFonzo, T. S. Baute, R. L. Hellmich, et al. 2011. Seeds of change: corn seed mixtures for resistance management and IPM. J. Econ. Entomol. 104: 343-352.
72. Osteen, C. D., and J. Fernandez-Cornejo. 2013. Economic and policy issues of U.S. agricultural pesticide use trends. Pest Manag. Sci. 69: 1001-1025.
73. Oswald, K., B. W. French, C. Nielson, and M. Bagley. 2012. Assessment of fitness costs in Cry3Bb1 resistant and susceptible western corn rootworm (Coleoptera: Chrysomelidae) laboratory colonies. J. Appl. Entomol. 136: 730-740.
74. Pedigo, L. P., S. H. Hutchins, and L. G. Higley. 1986. Economic injury levels in theory and practice. Annu. Rev. Entomol. 31: 341-368.
75. Petzold-Maxwell, J. L., X. Cibils-Stewart, B. W. French, and A. J. Gassmann. 2012. Adaptation by western corn rootworm (Coleoptera: Chrysomelidae) to Bt maize: inheritance, fitness costs and feeding preference. J. Econ. Entomol. 105: 1407-1418.
76. Petzold-Maxwell, J. L., L. J. Meinke, M. E. Gray, R. E. Estes, and A. J. Gassmann. 2013a. Effect of Bt maize and soil insecticides on yield, injury, and rootworm survival: implications for resistance management. J. Econ. Entomol. 106: 1941-1951.
77. Petzold-Maxwell, J. L., S. T. Jaronski, E. H. Clifton, M. W. Dunbar, M. A. Jackson, and A. J. Gassmann. 2013b. 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.
78. Porter, P., E. Cullen, T. Sappington, A. Schaafsma, S. Pueppke, D. Andow, J. Bradshaw, L. Buschman, Y. J. Cardoza, C. DiFonzo, et al. 2012. Comment submitted by Patrick Porter, North Central Coordinating Committee NCCC46 and Other Corn Entomologists. EPA Docket: EPA-HQ-OPP- 2011-0922 (http://www.regulations.gov/#!documentDetail;D=EPA-HQOPP- 2011-0922-0013)
79. Prasifka, P. L., D. M. Rule, N. P. Storer, S. P. Nolting, and W. H. Hendrix III. 2013. Evaluation of corn hybrids expressing Cry34Ab1/Cry35Ab1 and Cry3Bb1 against the western corn rootworm (Coleoptera: Chrysomelidae). J. Econ. Entomol. 106: 823-829.
80. Pruess, K. P., J. F. Witkowski, and E. S. Raun. 1974. Population suppression of western corn rootworm by adult control with ULV malathion. J. Econ. Entomol. 67: 651-655.
81. Prystupa, B., C. R. Ellis, and P.E.A. Teal. 1988. Attraction of adult Diabrotica (Coleoptera: Chrysomelidae) to corn silks and analysis of the host-finding response. J. Chem. Ecol. 14: 635-651.
82. Quiring, D. T., and P. R. Timmons. 1990. Influence of reproductive ecology on feasibility of mass trapping Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae). J. Appl. Ecol. 27: 965-982.
83. Reidell, W. E. 1990. Rootworm and mechanical damage effects on root morphology and water relations in maize. Crop Sci. 30: 628-631.
84. Rice, M. E. 2004. Transgenic rootworm corn: assessing potential agronomic, economic, and environmental benefits. Plant Health Prog. doi:10.1094/ PHP-2004-0301-01-RV. (http://www.plantmanagementnetwork.org/sub/ php/review/2004/rootworm/)
85. Roush, R. T. 1998. Two-toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Phil. Trans. R. Soc. Lond. B Biol. Sci. 353: 1777-1786.
86. Sappington, T. W. 2014. Emerging issues in Integrated Pest Management implementation and adoption in the North Central USA, pp. 65-97. In R. Peshin and D. Pimental (eds.), Integrated Pest Management - experiences with implementation, global overview, vol. 4. Springer Science+Business Media, Dordrecht, Netherlands.
87. Sappington, T. W., B. D. Siegfried, and T. Guillemaud. 2006. Coordinated Diabrotica genetics research: Accelerating progress on an urgent insect pest problem. Am. Entomol. 52: 90-97.
88. Sawicki, R. 1987. Definition, detection and documentation of insecticide resistance, pp. 105-117, In M. G. Ford, D. W. Holloman, B.P.S. Khambay, and R. M. Sawicki (eds.), Combating resistance to xenobiotics: Biological and chemical approaches. Ellis Horwood Ltd., Chichester, United Kingdom.
89. Schaafsma, A. W., P. Baufeld, and C. R. Ellis. 1999. Influence of cropping practices on corn rootworm in Canada as a basis for assessment of the potential impacts of Diabrotica virgifera in Germany. EPPO Bull. 29: 145-154.
90. Shi, G., J. P. Chavas, and J. Lauer. 2013. Commercialized transgenic traits, maize productivity and yield risk. Nat. Biotech. 31: 111-114.
91. Siegfried, B. D., T. T. Vaughn, and T. Spencer. 2005. Baseline susceptibility of western corn rootworm (Coleoptera: Chrysomelidae) to Cry3Bb1 Bacillus thuringiensis toxin. J. Econ. Entomol. 98: 1320-1324.
92. Siegfried, B. D., M. Rangasamy, H. Wang, T. Spencer, C. V. Haridas, B. Tenhumberg, D. V. Sumerford, and N. P. Storer. 2014. Estimating the frequency of Cry1F resistance in field populations of the European corn borer (Lepidoptera: Crambidae). Pest Manag. Sci. 70: 725-733.
93. Spencer, J. L. and E. Levine. 2008. Resistance to crop rotation, pp. 153-183. In D. W. Onstad (ed.), Insect resistance management: Biology, economics and prediction. Academic Press, New York, NY.
94. 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.
95. Spencer, J., D. Onstad, C. Krupke, S. Hughson, Z. Pan, B. Stanley, and L. Flexner. 2012. Isolated females and limited males: Evolution of insect resistance in structured landscapes. Entomol. Exp. Appl. 146: 38-49.
96. Spike, B. P., and J. J. Tollefson. 1991. Yield response of corn subjected to western corn rootworm (Coleoptera: Chrysomelidae) infestation and lodging. J. Econ. Entomol. 84: 1585-1590.
97. Storer, N. P., J. M. Babcock, and J. M. Edwards. 2006. Field measures of western corn rootworm (Coleoptera: Chrysomelidae) mortality caused by Cry34/35Ab1 proteins expressed in maize event 59122 and implications for trait durability. J. Econ. Entomol. 99: 1381-1387.
98. Storer, N. P., J. M. Babcock, M. Schlenz, T. Meade, G. D. Thompson, J. W. Bing, and R. M. Huckaba. 2010. Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J. Econ. Entomol. 103: 1031-1038.
99. Sumerford, D. V., G. P. Head, A. Shelton, J. Greenplate, and W. Moar. 2013. Field-evolved resistance: assessing the problem and ways to move forward. J. Econ. Entomol. 106: 1525-1534.
100. Sutter, G. R., J. R. Fisher, N. C. Elliott, and T. F. Branson. 1990. Effect of insecticide treatments on root lodging and yields of maize in controlled infestations of western corn rootworms (Coleoptera: Chrysomelidae). J. Econ. Entomol. 83: 2414-2420.
101. Tabashnik, B. E., and B. A. Croft. 1982. Managing pesticide resistance in crop-arthropod complexes: Interactions between biological and operational factors. Environ. Entomol. 11: 1137-1144.
102. Tabashnik, B. E., and F. Gould. 2012. Delaying corn rootworm resistance to Bt corn. J. Econ. Entomol. 105: 767-776.
103. Tabashnik, B. E., J.B.J. van Rensburg, and Y. Carrière. 2009. Field-evolved insect resistance to Bt crops: Definition, theory, and data. J. Econ. Entomol. 102: 2011-2025.
104. Tabashnik, B. E., M. S. Sisterson, P. C. Ellsworth, T. J. Dennehy, L. Antilla, L. Liesner, M. Whitlow, R. T. Staten, J. A. Fabrick, G. C. Unnithan, et al. 2010. Suppressing resistance to Bt cotton with sterile insect releases. Nat. Biotech. 28: 1304-1307.
105. Tabashnik, B. E., T. Brévault, and Y. Carrière. 2013. Insect resistance to Bt crops: lessons from the first billion acres. Nat. Biotech. 31: 510-521.
106. Tabashnik, B. E., D. Mota-Sanchez, M. E. Whalon, R. M. Hollingworth, and Y. Carrière. 2014. Defining terms for proactive management of resistance to Bt crops and pesticides. J. Econ. Entomol. 107: 496-507.
107. Tinsley, N. A., R. E. Estes, and M. E. Gray. 2012. Validation of a nested error component model to estimate damage caused by corn rootworm larvae. J. Appl. Entomol. 137: 161-169.
108. Tinsley, N. A., R. E. Estes, P. M. Schrader, and M. E. Gray. 2015. Evaluating multiple approaches for managing western corn rootworm larvae with seed blends. J. Appl. Entomol. 139: 76-86.
109. Tomlin, C.D.S. 1997. The pesticide manual. British Crop Protection Council, Farnham, United Kingdom.
110. Urías-López, M. A., and L. J. Meinke. 2001. Influence of western corn rootworm (Coleoptera: Chrysomelidae) larval injury on yield of different types of maize. J. Econ. Entomol. 94: 106-111.
111. (USDA-NASS) US Department of Agriculture-National Agricultural Statistics Service. 2015. Quick Stats 2.0. Washington DC (http://www.nass.usda.gov/ Quick-Stats/) (accessed 17 March 2015).
112. USEPA), US Environmental Protection Agency. 1998 The environmental protection agency's white paper on Bacillus thuringiensis plant-pesticide resistance management. Prevention, Pesticides and Toxic Substances (7511W), EPA 739-S-98-001 May 1998 (http://nepis.epa.gov/EPA/html/DLwait.htm?url=/Exe/ZyPDF.cgi/20000TQB.PDF?Dockey=20000TQB.PDF ) (accessed 12 June 2015).
113. (USEPA) US Environmental Protection Agency. 2001. Biopesticides registration action document: Bacillus thuringiensis plant-incorporated protectants (10/16/01) (http://www.epa.gov/oppbppd1/biopesticides/pips/bt-brad.htm) (accessed 1 April 2015).
114. (USEPA), US Environmental Protection Agency. 2002. A set of scientific issues being considered by the Environmental Protection Agency regarding: Corn rootworm plant-incorporated protectant non-target insect and insect resistance management issues. FIFRA Science Advisory Panel Meeting Minutes No. 2002-05. (http://www.epa.gov/scipoly/sap/meetings/2002/august/ august2002final.pdf) (accessed 1 April 2015).
115. (USEPA) US Environmental Protection Agency. 2007. Biopesticides registration action document. Modified Cry3A protein and the genetic material necessary for its production (via elements of pZM26) in eventMIR604 corn SYN-IR604-8, March 2007. (http://www.epa.gov/pesticides/chem-search/reg-actions/registration/ decision-PC-006509-1-Mar-07.pdf) (accessed 1 April 2015).
116. US Environmental Protection Agency. 2010a. 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) PC Code: 006484 Bacillus thuringiensis Cry3Bb1 protein and the genetic material necessary for its production (Vector PV-ZMIR39) in MON 88017 corn (OECD Unique Identifier: MON-88Ø17-3) PC Code: 006498, September 2010. (http://www.epa.gov/oppbppd1/biopesticides/pips/cry3bb1-brad.pdf) (accessed 1 April 2015).
117. (USEPA), US Environmental Protection Agency. 2010b. 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) PC Code: 006490, September 2010 ( http://www.epa.gov/ opp00001/biopesticides/pips/cry3435ab1-brad.pdf) (accessed 1 April 2015)
118. US Environmental Protection Agency. 2010b. 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) PC Code: 006490, September 2010 (http://www.epa.gov/ opp00001/biopesticides/pips/cry3435ab1-brad.pdf) (accessed 1 April 2015) (USEPA) US Environmental Protection Agency. 2012. BPPD IRM Team review of Monsanto's 2010 corn rootworm monitoring data, unexpected damage reports for Cry3Bb1 expressing Bt Corn and academic reports of Cry3Bb1 field failures as well as corn rootworm resistance (EPA Reg. Nos. 524-551, 524-552, 524-528, 524-545, and 68467-7); MRIDs 486050-01 and 486050-02. Memorandum dated Oct 11, 2012 (http:// www.regulations.gov/#!documentDetail;D=EPA-HQ-OPP-2011-0922-0037) (accessed 1 April 2015).
119. (USEPA), US Environmental Protection Agency. 2014. A set of scientific issues being considered by the Environmental Protection Agency regarding scientific uncertainties associated with corn rootworm resistance monitoring for Bt corn plant incorporated protectants (PIPs). FIFRA Science Advisory Panel Meeting Minutes No. 2014-01. December 4-5, 2013. (http://www.regulations.gov/#!documentDetail;D=EPA-HQ-OPP-2013-0490-0044) (accessed 1 April 2015).
120. van Rensburg, J.B.J. 2007. First report of field resistance by stem borer, Busseola fusca (Fuller) to Bt-transgenic maize. S. Afr. J. Plant Soil 24: 147-51.
121. Vaughn, T., T. Cavato, G. Brar, T. Coombe, T. DeGooyer, S. Ford, M. Groth, A. Howe, S. Johnson, K. Kolacz, et al. 2005. A method of controlling corn rootworm feeding using a Bacillus thuringiensis protein expressed in transgenic maize. Crop Sci. 45: 931-938.
122. Wangila, D. S., A. J. Gassmann, J. L. Petzold-Maxwell, B.W. French, and L. J. Meinke. 2015. Susceptibility of Nebraska western corn rootworm (Coleoptera: Chrysomelidae) populations to Bt corn events. J. Econ. Entomol. 108: 742-751.
123. Whalon, M., D. Mota-Sanchez, and R. M. Hollingworth. 2008. Analysis of global pesticide resistance in arthropods, pp. 5-31. In M. Whalon, D. Mota-Sanchez, and R. M. Hollingworth, (eds.), Global pesticide resistance in arthropods. CABI International, Wallingford, United Kingdom.
124. WHO. 1957. Expert Committee on Malaria, seventh report.WHO Tech. Rep. Ser. No. 125. World Health Organization, Geneva, Switzerland.