Advertisement

American Journal of Potato Research

, Volume 85, Issue 6, pp 395–413 | Cite as

Colorado Potato Beetle Resistance to Insecticides

  • Andrei Alyokhin
  • Mitchell Baker
  • David Mota-Sanchez
  • Galen Dively
  • Edward Grafius
Review Article

Abstract

The Colorado potato beetle, Leptinotarsa decemlineata (Say), is widely regarded as the most important insect defoliator of potatoes. Its current range covers about 16 million km2 in North America, Europe, and Asia and continues to expand. This insect has a complicated and diverse life history, which is well-suited to agricultural environments, and makes it a complex and challenging pest to control. Dispersal, closely connected with diapause, feeding, and reproduction, allow the Colorado potato beetle to employ “bet-hedging” reproductive strategies, distributing its offspring in both space (within and between fields) and time (within and between years). The Colorado potato beetle played a large role in creating the modern pesticide industry, with hundreds of chemicals tested against it. High selection pressure, together with natural propensity to adapt to toxic substances, eventually resulted in a large number of insecticide-resistant Colorado potato beetle populations. Since the middle of the last century, the beetle has developed resistance to 52 different compounds belonging to all major insecticide classes. Resistance levels vary greatly among different populations and between beetle life stages, but in some cases can be very high (up to 2,000-fold). Known mechanisms of Colorado potato beetle resistance to insecticides include enhanced metabolism involving esterases, carboxylesterases and monooxygenases, and target site insensitivity, as well as reduced insecticide penetration and increased excretion. There is also some evidence of behavioral resistance. Resistance mechanisms are sometimes highly diverse even within a relatively narrow geographical area. Resistance is usually inherited as an incompletely dominant or incompletely recessive trait, with one or several genes involved in its determination. Because of pleiotropic effects of resistant alleles, insecticide-resistant beetles often have reduced relative fitness in the absence of insecticides. Rotating different classes of insecticides and reducing insecticidal pressure on pest populations by provision of temporal and spatial refuges from exposure to toxins have been proposed to delay evolution of resistance. However, insecticide resistance in this insect will likely remain a major challenge to the pest control practitioners. Still limited understanding of beetle biology, its flexible life history, and grower reluctance to adopt some of the resistance management techniques create impediments to successful resistance management. Overcoming these obstacles is not an easy task, but it will be crucial for sustainable potato production.

Keywords

Leptinotarsa decemlineata Life history Resistance mechanisms Resistance genetics Insecticide resistance management 

Resumen

El escarabajo de Colorado de la papa [(Leptinotarsa decemlineata (Say)] es considerado el insecto defoliador más importante de la papa. Su acción cubre una área de 16 millones de km2 en Norteamérica, Europa y Asia y continúa expandiéndose. Este insecto tiene un ciclo de vida complicado y diverso, el cual esta bien adecuado a entornos agrícolas y lo hace una plaga difícil de controlar. Su dispersión, íntimamente conectada con su quiescencia, hábitos de alimentación y reproducción permite al escarabajo de Colorado de la papa emplear estrategias de reproducción de “riesgo calculado”distribuyendo su descendencia en espacio (dentro del campo y entre campos) y tiempo (dentro y entre años). El escarabajo de Colorado de la papa jugó un rol muy amplio en la creación de la industria moderna de pesticidas, con cientos de químicos evaluados para su control. La alta presión de selección, junto a la propensión natural para adaptarse a las sustancias tóxicas, resultó en un gran número de poblaciones resistentes a los insecticidas. Desde mediados del siglo pasado, el escarabajo ha desarrollado resistencia a 52 diferentes compuestos pertenecientes a todas las clases importantes de insecticidas. Los niveles de resistencia varían mucho entre las diferentes poblaciones y estadíos en el ciclo de vida, pero en algunos casos pueden variar mucho más (hasta 2,000 veces). Los mecanismos conocidos de resistencia de este escarabajo a los insecticidas incluyen un elevado metabolismo de las esterasas, carboxilesterasas y monooxigenasas e insensibilidad al sitio objetivo, lo mismo que una penetración del insecticida reducida y excreción incrementada. También hay evidencia de resistencia por comportamiento. Los mecanismos de resistencia son a veces altamente variados, aun dentro de una reducida área geográfica. La resistencia es a menudo heredada como un carácter incompletamente dominante o incompletamente recesivo, con uno o varios genes involucrados en su determinación. Debido a los efectos pleiotrópicos de alelos resistentes, los escarabajos resistentes tienen una aptitud relativa reducida en ausencia de insecticidas. La rotación de diferentes clases de insecticidas y la reducción de la presión insecticida sobre las poblaciones de insectos por provisión de refugios temporales y espaciales contra la exposición de toxinas han sido propuestas para demorar la evolución de la resistencia. Sin embargo, la resistencia a insecticidas de este insecto permanecerá siendo un desafío para los practicantes de control de plagas. Todavía hay un limitado conocimiento sobre la biología del escarabajo, su ciclo de vida flexible y la renuencia del productor para adoptar algunas de las técnicas de manejo de la resistencia impiden el manejo exitoso de la resistencia. El vencer estos obstáculos no es tarea fácil, pero será importante para una producción sostenible de papa.

References

  1. Ahammad-Sahib, K.I., R.M. Hollingworth, M.E. Whalon, P.M. Ioannidis, and E.J. Grafius. 1994. Polysubstrate monooxygenases and other xenobiotic-metabolizing enzymes in susceptible and resistant Colorado potato beetle. Pesticide Biochemistry and Physiology 49: 1–12.Google Scholar
  2. Alyokhin, A., G. Dively, M. Patterson, D. Rogers, M. Mahoney, and J. Wollam. 2006. Susceptibility of imidacloprid-resistant Colorado potato beetles to non-neonicotinoid insecticides in the laboratory and field trials. American Journal of Potato Research 83: 485–494.Google Scholar
  3. Alyokhin, A., G. Dively, M. Patterson, C. Castaldo, D. Rogers, M. Mahoney, and J. Wollam. 2007. Resistance and cross-resistance to imidacloprid and thiamethoxam in the Colorado potato beetle. Pest Management Science 63: 32–41.PubMedGoogle Scholar
  4. Alyokhin, A.V. 2007. Results of the 2007 Imidacloprid resistance survey in Maine populations of the Colorado potato beetle. Spudlines 45(3): 3–4.Google Scholar
  5. Alyokhin, A.V., and D.N. Ferro. 1999b. Electrophoretic confirmation of sperm mixing in mated Colorado potato beetles (Coleoptera: Chrysomelidae). Annals of the Entomological Society of America 92: 230–235.Google Scholar
  6. Alyokhin, A.V., and D.N. Ferro. 1999c. Relative fitness of Colorado potato beetle (Coleoptera: Chrysomelidae) resistant and susceptible to the Bacillus thuringiensis Cry3A toxin. Journal of Economic Entomology 92: 510–515.Google Scholar
  7. Alyokhin, A.V., and D.N. Ferro. 1999d. Modifications in flight and oviposition of Bt-resistant and Bt-susceptible Colorado potato beetles as a result of exposure to Bacillus thuringiensis subsp. tenebrionis Cry3A toxin. Entomologia Experimentalis et Applicata 90: 93–101.Google Scholar
  8. Alyokhin, A.V., and D.N. Ferro. 1999a. Reproduction and dispersal of summer-generation Colorado potato beetle (Coleoptera: Chrysomelidae). Environmental Entomology 28: 425–430.Google Scholar
  9. Anspaugh, D., D.G.G. Kennedy, and R.M. Roe. 1995. Purification and characterization of a resistance-associated esterase from the Colorado Potato Beetle, Leptinotarsa- Decemlineata (Say). Pesticide Biochemistry and Physiology 53: 84–96.Google Scholar
  10. Argentine, J.A., and J.M. Clark. 1990. Selection for abamectin resistance in Colorado potato beetle (Coleoptera, Chrysomelidae). Pesticide Science 28: 17–24.Google Scholar
  11. Argentine, J.A., J.M. Clark, and D.N. Ferro. 1989a. Genetics and synergism of resistance to azinphosmethyl and permethrin in the Colorado potato beetle (Coleoptera, Chrysomelidae). Journal of Economic Entomology 82: 698–705.Google Scholar
  12. Argentine, J.A., J.M. Clark, and D.N. Ferro. 1989b. Relative fitness of insecticide-resistant Colorado potato beetle strains (Coleoptera: Chrysomelidae). Environmental Entomology 18: 705–710.Google Scholar
  13. Argentine, J.A., K.Y. Zhu, S.H. Lee, and J.M. Clark. 1994. Biochemical-mechanisms of azinphosmethyl resistance in isogenic strains of Colorado potato beetle. Pesticide Biochemistry and Physiology 48: 63–78.Google Scholar
  14. Argentine, J.A., S.H. Lee, M.A. Sos, S.R. Barry, and J.M. Clark. 1995. Permethrin resistance in a near isogenic strain of Colorado potato beetle. Pesticide Biochemistry and Physiology 53: 97–115.Google Scholar
  15. Baker, M.B., and A.H. Porter. 2008. Use of sperm precedence to infer the overwintering cost of insecticide resistance in the Colorado potato beetles (Coleoptera: Chrysomelidae). Agricultural and Forest Entomology, in press.Google Scholar
  16. Baker, M.B., D.N. Ferro, and A.H. Porter. 2001. Management of a well established crop pest: Colorado potato beetle invasions on large and small scales. Biol Invasions 3: 295–306.Google Scholar
  17. Baker, M.B., A. Alyokhin, S.R. Dastur, A.H. Porter, and D.N. Ferro. 2005. Sperm precedence in the overwintered Colorado potato beetles (Coleoptera: Chrysomelidae) and its implications for insecticide resistance management. Annals of the Entomological Society of America 98: 989–995.Google Scholar
  18. Baker, M.B., A. Alyokhin, A.H. Porter, D.N. Ferro, S.R. Dastur, and N. Galal. 2007. Persistence and inheritance of costs of resistance to imidacloprid in Colorado potato beetle. Journal of Economic Entomology 100: 1871–1879.PubMedGoogle Scholar
  19. Baker, M.B., S.R. Dastur, T. Wong, and B.D. Jaffe. 2008. Mating competition between Colorado potato beetles (Coleoptera: Chrysomelidae) resistant or susceptible to imidacloprid does not show cost of resistance. Annals of the Entomological Society of America, in press.Google Scholar
  20. Benkovskaya, G.V., M.B. Udalov, A.G. Nikolenko, and T.L. Leontieva. 2006. Temporal and toxicological dynamics in the cover spot patterns of the Colorado potato beetle in South Ural. Resistant Pest Management 15: 13–15.Google Scholar
  21. Bethune, C.J.S. 1872. Report of the Entomological Society of Ontario for the year 1871. Toronto: Hunter, Ross.Google Scholar
  22. Biever, K.D., and R.L. Chauvin. 1990. Prolonged dormancy in a Pacific Northwest population of the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). Canadian Entomologist 122: 175–177.Google Scholar
  23. Bishop, B.A., and E.J. Grafius. 1991. An on-farm insecticide resistance test kit for Colorado potato beetle (Coleoptera: Chrysomelidae). American Potato Journal 68: 53–64.Google Scholar
  24. Bishop, B.A., and E.J. Grafius. 1996. Insecticide resistance in the Colorado potato beetle. In Chrysomelidae biology, vol. 1, eds. P. Jolivet, and T.H. HsiaoAmsterdam: SBP Academic Publishing.Google Scholar
  25. Blom, P.E., S. Fleischer, and Z. Smilowitz. 2002. Spatial and temporal dynamics of Colorado potato beetle (Coleoptera: Chrysomelidae) in fields with perimeter and spatially targeted insecticides. Environmental Entomology 31: 149–159.Google Scholar
  26. Boiteau, G. 1988a. Sperm utilization and post-copulatory female-guarding in the Colorado potato beetle, Leptinotarsa decemlineata. Entomologia Experimentalis et Applicata 47: 183–187.Google Scholar
  27. Boiteau, G. 1988b. Control of the Colorado potato beetle, Leptinotarsa decemlineata (Say): learning from the Soviet experience. Bulletin of the Entomological Society of America 20: 9–14.Google Scholar
  28. Boiteau, G., R.H. Parry, and C.R. Harris. 1987. Insecticide resistance in New Brunswick populations of the Colorado potato beetle (Coleoptera: Chrysomelidae). Canadian Entomologist 119: 459–463.Google Scholar
  29. Boiteau, G., Y. Pelletier, G.C. Misener, and G. Bernard. 1994. Development and evaluation of a plastic trench barrier for protection of potato from walking adult Colorado potato beetles (Coleoptera: Chrysomelidae). Journal of Economic Entomology 87: 1325–1331.Google Scholar
  30. Boiteau, G., A. Alyokhin, and D.N. Ferro. 2003. The Colorado potato beetle in movement. Canadian Entomologist 135: 1–22.Google Scholar
  31. Bourguet, D., A. Genissel, and M. Raymond. 2000. Insecticide resistance and dominance levels. Journal of Economic Entomology 93: 1588–1595.PubMedGoogle Scholar
  32. Bourguet, D., M. Desquilbet, and S. Lemarie. 2005. Regulating insect resistance management: the case of non-Bt corn refuges in the US. Journal of Environmental Management 76: 210–220.PubMedGoogle Scholar
  33. Brown, A.W.A. 1951. Chemical control of insects feeding on plants. Insect control by chemicals. 574–667. New York: John Wiley.Google Scholar
  34. Brust, G.E. 1994. Natural enemies in straw-mulch reduce Colorado potato beetle populations and damage in potato. Biological Control 4: 163–169.Google Scholar
  35. Bulmer, M.G., and J.J. Bull. 1982. Models of polygenic sex determination and sex ratio evolution. Evolution 36: 13–26.Google Scholar
  36. Caprio, M.A. 1998. Evaluating resistance management strategies for multiple toxins in the presence of external refuges. Journal of Economic Entomology 91: 1021–1031.Google Scholar
  37. Caprio, M., and E. Grafius. 1990. Effects of light, temperature and feeding status on flight initiation in postdiapause Colorado potato beetle. Environmental Entomology 19: 281–285.Google Scholar
  38. Carriere, Y., C. Ellers-Kirk, R. Biggs, B. Degain, D. Holley, C. Yafuso, P. Evans, T.J. Dennehy, and B.E. Tabashnik. 2005. Effects of cotton cultivar on fitness costs associated with of pink bollworm (Lepidoptera: Gelechiidae) to bt cotton. Journal of Economic Entomology 98: 947–954.PubMedGoogle Scholar
  39. Carrière, Y., and B.E. Tabashnik. 2001. Reversing insect adaptation to transgenic insecticidal plants. Proceedings of the Royal Society of London Series B 268: 1475–1480.PubMedGoogle Scholar
  40. Casagrande, R.A. 1987. The Colorado potato beetle: 125 years of mismanagement. Bulletin of the Entomological Society of America 33: 142–150.Google Scholar
  41. Clark, J.M. 1997. Insecticides as tools in probing vital receptors and enzymes in excitable membranes. Pesticide Biochemistry and Physiology 57: 235–254.Google Scholar
  42. Clark, J.M., S.H. Lee, H.J. Kim, K.S. Yoon, and A.G. Zhang. 2001. DNA-based genotyping techniques for the detection of point mutations associated with insecticide resistance in Colorado potato beetle Leptinotarsa decemlineata. Pest Management Science 57: 968–974.PubMedGoogle Scholar
  43. Crow, J.F. 1957. Genetics of insect resistance. Annual Review of Entomology 2: 227–246.Google Scholar
  44. De Kort, C.A.D. 1990. Thirty-five years of diapause research with the Colorado potato beetle. Entomologia Experimentalis et Applicata 56: 1–13.Google Scholar
  45. Denholm, I., and M.W. Rowland. 1992. Tactics for managing pesticide resistance in arthropods: theory and practice. Annual Review of Entomology 37: 91–112.PubMedGoogle Scholar
  46. De Wilde, J. 1948. Developpement embryonnaire et postembryonnaire dy doryphore (Leptinotarsa decemlineata Say) en function de la temperature. In Proceedings 8th International Congress of Entomology, Stockholm, Sweden, 310–321.Google Scholar
  47. De Wilde, J. 1962. The relation between diapause research and control of the Colorado potato beetle Leptinotarsa decemlineata Say. Annals of Applied Biology 50: 605–608.Google Scholar
  48. DiFonzo, C.D., D.W. Ragsdale, E.B. Radcliffe, N.C. Gunmestad, and G.A. Secor. 1996. Crop borders reduce potato virus Y incidence in seed potato. Annals of Applied Biology 129: 289–302.Google Scholar
  49. Dingle, H. 1985. Migration. In Insect physiology, biochemistry, and pharmacology, eds. G.A. Kerkut, and L.I. Gilbert, 9: 375–415. Oxford: Pergamon Press.Google Scholar
  50. Dively, G.P., P.A. Follett, J.J. Linduska, and G.K. Roderick. 1998. Use of imidacloprid-treated row mixtures for Colorado potato beetle (Coleoptera: Chrysomelidae) management. Journal of Economic Entomology 91: 376–387.Google Scholar
  51. Ferro, D.N. 1993. Potential for resistance to Bacillus thuringiensis: Colorado potato beetle (Coleoptera: Chrysomelidae)—a model system. American Entomologist 39: 38–44.Google Scholar
  52. Ferro, D.N. 1994. Biological control of the Colorado potato beetle. In Advances in potato pest biology and management, eds. G.W. Zehnder, R.K. Jansson, M.L. Powelson, and K.V. Raman, 357–375. St. Paul: APS Press.Google Scholar
  53. Ferro, D.N., J.A. Logan, R.H. Voss, and J.S. Elkinton. 1985. Colorado potato beetle (Coleoptera: Chrysomelidae) temperature-dependent growth and feeding rates. Environmental Entomology 14: 343–348.Google Scholar
  54. Ferro, D.N., A.F. Tuttle, and D.C. Weber. 1991. Ovipositional and flight behavior of overwintered Colorado potato beetle (Coleoptera: Chrysomelidae). Environmental Entomology 20: 1309–1314.Google Scholar
  55. Ferro, D.N., A.V. Alyokhin, and D.B. Tobin. 1999. Reproductive status and flight activity of the overwintered Colorado potato beetle. Entomologia Experimentalis et Applicata 91: 443–448.Google Scholar
  56. Feyereisen, R. 2005. Insect cytochrome P450. In Comprehensive molecular insect science, eds. L. Gilbert, K. Latrou, and S. Gill, 2–77. Amsterdam: Elsevier.Google Scholar
  57. Follett, P.A., G.G. Kennedy, and F. Gould. 1993. A simulation model that explores Colorado potato beetle (Coleoptera: Chrysomelidae) adaptation to insecticides. Environmental Entomology 22: 283–296.Google Scholar
  58. Follett, P.A., F. Gould, and G.G. Kennedy. 1995. High-realism model of Colorado potato beetle (Coleoptera: Chrysomelidae) adaptation to permethrin. Environmental Entomology 24: 167–178.Google Scholar
  59. Forgash, A.J. 1985. Insecticide resistance in the Colorado potato beetle. In Proceedings of the Symposium on the Colorado Potato Beetle, 17th International Congress of Entomology, eds. D.N. Ferro, and R.H. Voss, 33–53. Amherst: Massachusetts Experiment Station, University of Massachusetts.Google Scholar
  60. French, N.M. III, P. Follett, B.A. Nault, and G.G. Kennedy. 1993. Colonization of potato fields in eastern North Carolina by Colorado potato beetle. Entomologia Experimentalis et Applicata 68: 247–256.Google Scholar
  61. Gauthier, N.L., R.N. Hofmaster, and M. Semel. 1981. History of Colorado potato beetle controlIn Advances in potato pest management, eds. J.H. Lashomb, and R. Casagrande, 13–33. Stroudsburg: Hutchinson Ross Publishing Co.Google Scholar
  62. Gouamene-Lamine, C.N., K.S. Yoon, and J.M. Clark. 2003. Differential susceptibility to abamectin and two bioactive avermectin analogs in abamectin-resistant and -susceptible strains of Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera : Chrysomelidae). Pesticide Biochemistry and Physiology 76: 15–23.Google Scholar
  63. Grafius, E. 1995. Is local selection followed by dispersal a mechanism for rapid development of multiple insecticide resistance in the Colorado potato beetle? American Entomologist 41: 104–109.Google Scholar
  64. Grafius, E. 1997. Economic impact of insecticide resistance in the Colorado potato beetle (Coleoptera: Chrysomelidae) on the Michigan potato industry. Journal of Economic Entomology 90: 1144–1151.Google Scholar
  65. Grafius, E.J., and D.S. Douches. 2008. The present and future role of insect-resistant genetically modified potato cultivars in potato IPM. In Integration of insect-resistant G.M. crops within IPM programs, eds. J. Romeis, A.M. Shelton, and G.G. KennedyNew York: Springer(in press).Google Scholar
  66. Harcourt, D.G. 1971. Population dynamics of Leptinotarsa decemlineata (Say) in eastern Ontario. III. Major population processes. Canadian Entomologist 103: 1049–1061.Google Scholar
  67. Harris, C.R., and H.J. Svec. 1981. Colorado potato beetle resistance to carbofuran and several other insecticides in Quebec Leptinotarsa decemlineata. Journal of Economic Entomology 74: 421–424.Google Scholar
  68. Harris, C.R., and S.A. Turnbull. 1986. Contact toxicity of some pyrethroids insecticides, alone and in combination with piperonyl butoxide, to insecticide-susceptible and pyrethroid-resistant strains of the Colorado potato beetle (Coleoptera: Chrysomelidae). Canadian Entomologist 118: 1173–1176.Google Scholar
  69. Hawthorne, D.J. 2001. AFLP-based genetic linkage map of the Colorado potato beetle Leptinotarsa decemlineata: Sex chromosomes and a pyrethroid-resistance candidate gene. Genetics 158: 695–700.PubMedGoogle Scholar
  70. Hawthorne, D.J. 2003. Quantitative trait locus mapping of pyrethroid resistance in Colorado potato beetle, Leptinotarsa decemlineata (say) (Coleoptera: Chrysomelidae). Journal of Economic Entomology 96: 1021–1030.PubMedGoogle Scholar
  71. Heim, D.C., G.G. Kennedy, and J.W. Van Duyn. 1990. Survey of insecticide resistance among North Carolina Colorado potato beetle (Coleoptera: Chrysomelidae) populations. Journal of Economic Entomology 83: 1229–1235.Google Scholar
  72. Heim, D.C., G.G. Kennedy, F.L. Gould, and J.W. Van Duyn. 1992. Inheritance of fenvalerate and carbofuran resistance in Colorado beetles—Leptinotarsa decemlineata (Say)—from North Carolina. Pesticide Science 34: 303–311.Google Scholar
  73. Hitchner, L.S. 1952. The insecticide industry. In insects, the yearbook of agriculture 1952. 450–457. Washington, DC: House Doc. 413.Google Scholar
  74. Hofmaster, R.N., R.L. Waterfield, and J.C. Boyd. 1967. Insecticides applied to the soil for control of eight species of insects on Irish potatos in Virginia. Journal of Economic Entomology 60: 1311–1318.Google Scholar
  75. Hough-Goldstein, J.A., and J.M. Whalen. 1996. Relationship between crop rotation distance from previous potatoes and colonization and population density of Colorado potato beetle. Journal of Agricultural Entomology 13: 293–300.Google Scholar
  76. Hough-Goldstein, J.A., G.E. Heimpel, H.E. Bechmann, and C.E. Mason. 1993. Arthropod natural enemies of the Colorado potato beetle. Crop Protection 12: 324–334.Google Scholar
  77. Hoy, C.W., and G. Head. 1995. Correlation between behavioral and physiological responses to transgenic potatoes containing Bacillus thuringiensis delta-endotoxin in Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Journal of Agricultural Entomology 88: 480–486.Google Scholar
  78. Hoy, C.W., J.A. Wyman, T.T. Vaughn, D.A. East, and P. Kaufman. 1996. Food, ground cover, and Colorado potato beetle (Coleoptera: Chrysomelidae) dispersal in late summer. Journal of Agricultural Entomology 89: 963–969.Google Scholar
  79. Hueth, D., and U. Regev. 1974. Optimal agricultural pest management with increasing pest resistance. American Journal of Agricultural Economics 56: 543–553.Google Scholar
  80. Insecticide Resistance Action Committee (IRAC). 2008. IRAC mode of action classification, version 5.1. http://www.irac-online.org/documents/IRAC%20MoA%20Classification%20v5_3.pdf. Accessed 15 April 2008.
  81. Ioannidis, P.M., E. Grafius, and M.E. Whalon. 1991. Patterns of insecticide resistance to azinphosmethyl, carbofuran, and permethrin in the Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology 84: 1417–1423.Google Scholar
  82. Ioannidis, P.M., E.J. Grafius, J.M. Wierenga, M.E. Whalon, and R.M. Hollingworth. 1992. Selection, inheritance and characterization of carbofuran resistance in the Colorado potato beetle (Coleoptera, Chrysomelidae). Pesticide Science 35: 215–222.Google Scholar
  83. Isely, D. 1935. Variations in the seasonal history of the Colorado potato beetle. Journal of the Kansas Entomological Society 8: 142–145.Google Scholar
  84. Jacques, R.L. 1988. The potato beetles. Leiden: E. J. Brill.Google Scholar
  85. Jermy, T., and G. Saringer. 1955. A burgonyabogar (Leptinotarsa decemlineata Say). Budapest: Mezögazd Kiadó.Google Scholar
  86. Johnson, C.G. 1969. Migration and dispersal of insects by flight. London: Methuen and Co.Google Scholar
  87. Jolivet, P. 1991. The Colorado beetle menaces Asia (Leptinotarsa decemlineata Say 1824) (Col. Chrysomelidae). L’Entomologiste 47: 29–48.Google Scholar
  88. Kearsey, M.J., and H.S. Pooni. 1996. The genetical analysis of quantitative traits. London: Chapman and Hall.Google Scholar
  89. Kim, H.J., and J.M. Clark. 2002. Evaluation of resistant point mutations in recombinant acetylcholinesterase of Colorado potato beetle. Abstracts of Papers of the American Chemical Society 224: U103–U103.Google Scholar
  90. Kim, H.J., D.J. Hawthorne, T. Peters, G.P. Dively, and J.M. Clark. 2005. Application of DNA-based genotyping techniques for the detection of kdr-like pyrethroid resistance in field populations of Colorado beetle. Pesticide Biochemistry and Physiology 81: 85–96.Google Scholar
  91. Kim, H.J., J.B. Dunn, K.S. Yoon, and J.M. Clark. 2006. Target site insensitivity and mutational analysis of acetylcholinesterase from a carbofuran-resistant population of Colorado potato beetle, Leptinotarsa decemlineata (Say). Pesticide Biochemistry and Physiology 84: 165–179.Google Scholar
  92. Kim, H.J., K.S. Yoon, and J.M. Clark. 2007. Functional analysis of mutations in expressed acetylcholinesterase that result in azinphosmethyl and carbofuran resistance in Colorado potato beetle. Pesticide Biochemistry and Physiology 88: 181–190.Google Scholar
  93. Krishnan, N., D. Kodrik, F. Turanli, and F. Sehnal. 2007. Stage-specific distribution of oxidative radicals and antioxidant enzymes in the midgut of Leptinotarsa decemlineata. Journal of Insect Physiology 53: 67–74.PubMedGoogle Scholar
  94. Lactin, D.J., and N.J. Holliday. 1994. Behavioral responses of Colorado potato beetle larvae to combinations of temperature and insolation, under field conditions. Entomologia Experimentalis et Applicata 72: 255–263.Google Scholar
  95. Lashomb, J.H., and Y.-S. Ng. 1984. Colonization by the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Cerambycidae) in rotated and non-rotated potato fields. Environmental Entomology 13: 1352–1356.Google Scholar
  96. Lee, S., and J.M. Clark. 1996. Tissue distribution and biochemical characterization of carboxylesterases associated with permethrin resistance in a near isogenic strain of Colorado potato beetle. Pesticide Biochemistry and Physiology 56: 208–219.Google Scholar
  97. Lee, S.H., and J.M. Clark. 1998. Purification and characterization of multiple-charged forms of permethrin carboxylesterase(s) from the hemolymph of resistant Colorado potato beetle. Pesticide Biochemistry and Physiology 60: 31–47.Google Scholar
  98. Lee, S.H., J.B. Dunn, J.M. Clark, and D.M. Soderlund. 1999. Molecular analysis of kdr-like resistance in a permethrin-resistant strain of Colorado potato beetle. Pesticide Biochemistry and Physiology 63: 63–75.Google Scholar
  99. Levine, E., H. Oloumi-Sadeghi, and J.R. Fisher. 1992. Discovery of multiyear diapause in Illinois and South Dakota Northern corn rootworm (Coleoptera: Cerambycidae) eggs and incidence of the prolonged diapause trait in Illinois. Journal of Economic Entomology 85: 262–267.Google Scholar
  100. Liu, Y.B., B.E. Tabashnik, T.J. Dennehy, A.L. Patin, and A.C. Bartlett. 1999. Development time and resistance to Bt crops. Nature 400: 519.PubMedGoogle Scholar
  101. Liu, Z.W., M.S. Williamson, S.J. Lansdell, Z.J. Han, I. Denholm, and N.S. Millar. 2006. A nicotinic acetylcholine receptor mutation (Y151S) causes reduced agonist potency to a range of neonicotinoid insecticides. Journal of Neurochemistry 99: 1273–1281.PubMedGoogle Scholar
  102. Logan, P.A., R.A. Casagrande, H.H. Faubert, and F.A. Drummond. 1985. Temperature-dependent development and feeding of immature Colorado potato beetles, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae). Environmental Entomology 14: 275–283.Google Scholar
  103. MacQuarrie, C.J.K., and G. Boiteau. 2003. Effect of diet and feeding history on flight of Colorado potato beetle, Leptinotarsa decemlineata. Entomologia Experimentalis et Applicata 107: 207–213.Google Scholar
  104. May, M.L. 1981. Role of body temperature and thermoregulation in the biology of the Colorado potato beetle. In Advances in potato pest management, eds. J.H. Lashomb, and R. Casagrande, 86–104. Stroudsburg: Hutchinson Ross Publishing Co.Google Scholar
  105. McCauley, D.E., and L.M. Reilly. 1984. Sperm storage and sperm precedence in the milkweed beetle, Tetraopes tetraophthalmus (Forster) (Coleoptera: Cerambycidae). Annals of the Entomological Society of America 77: 526–530.Google Scholar
  106. McGaughey, W., and M.E. Whalon. 1992. Managing insect resistance to Bacillus thuringiensis toxins. Science 258: 1451–1455.PubMedGoogle Scholar
  107. McKenzie, J.A. 2000. The character or the variation: The genetic analysis of the insecticide-resistance phenotype. Bulletin of Entomological Research 90: 3–7.PubMedGoogle Scholar
  108. Milner, M., K.J.S. Kung, J.A. Wyman, J. Feldman, and E. Nordheim. 1992. Enhancing overwintering mortality of Colorado potato beetle (Coleoptera: Chrysomelidae) by manipulating the temperature of its diapause habitat. Journal of Economic Entomology 85: 1701–1708.Google Scholar
  109. Minder, I.F., and D.V. Petrova. 1966. Ecological and physiological characteristics of the summer rest of the Colorado beetle. In Ecology and physiology of diapause in the Colorado beetle, ed. K.V. Arnoldi, 257–279. Moscow: Nauka.Google Scholar
  110. Misener, G.C., G. Boiteau, and L.P. McMillan. 1993. A plastic-lining trenching device for the control of Colorado potato beetle: Beetle Excluder. American Potato Journal 70: 903–908.Google Scholar
  111. Miyo, T., C.B.O. Keil, J.A. Hough-Goldstein, and Y. Oguma. 1999. Inheritance of resistance to esfenvalerate in Colorado potato beetles (Coleoptera : Chrysomelidae). Journal of Economic Entomology 92: 1031–1038.Google Scholar
  112. Mohammadi Sharif, M., M.J. Hejazi, A. Mohammadi, and M.R. Rashidi. 2007. Resistance status of the Colorado potato beetle, Leptinotarsa decemlineata, to endosulfan in East Azarbaijan and Ardabil provinces of Iran. 7pp. J Insect Sci 7:31, available online: insectscience.org/7.31.Google Scholar
  113. Mota-Sanchez, D. 2003. Resistance and metabolism of imidacloprid in Colorado Potato Beetle, Leptinotarsa decemlineta Say (Coleoptera: Chrysomelidae), Entomol. 122. East Lansing: Michigan State University.Google Scholar
  114. Mota-Sanchez, D., R.M. Hollingworth, E.J. Grafius, and D.D. Moyer. 2006. Resistance and cross-resistance to neonicotinoid insecticides and spinosad in the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera : Chrysomelidae). Pest Management Science 62: 30–37.PubMedGoogle Scholar
  115. Mowry, T.M., and L.E. Sandvol. 1995. Survey of Colorado potato beetle insecticide resistance in Idaho. American Potato Journal 72: 551–558.Google Scholar
  116. National Potato Council. 2008. Neonicotinoid insecticides: A grower approach to resistance management of Colorado potato beetle and green peach aphid in potato. http://www.nationalpotatocouncil.org/NPC/pressroom_newsflashes.cfm. Accessed 7 April 2008.
  117. Nauen, R., and I. Denholm. 2005. Resistance of insect pests to neonicotinoid insecticides: Current status and future prospects. Archives of Insect Biochemistry and Physiology 58: 200–215.PubMedGoogle Scholar
  118. Ng, Y.-S., and J.H. Lashomb. 1983. Orientation by the Colorado potato beetle (Leptinotarsa decemlineata Say). Animal Behaviour 31: 617–618.Google Scholar
  119. Noronha, C., G.M. Duke, J.M. Chinn, and M.S. Goettel. 2001. Differential susceptibility to insecticides by Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) populations from western Canada. Phytoprotection 82: 113–121.Google Scholar
  120. Olson, E.R., G.P. Dively, and J.O. Nelson. 2000. Baseline susceptibility to imidacloprid and cross resistance patterns in Colorado potato beetle (Coleoptera: Chrysomelidae) populations. Journal of Economic Entomology 93: 447–458.PubMedGoogle Scholar
  121. Pourmirza, A.A. 2005. Local variation in susceptibility of Colorado potato beetle (Coleoptera: Chrysomelidae) to insecticide. Journal of Economic Entomology 98: 2176–2180.PubMedGoogle Scholar
  122. Quinton, R.J. 1955. DDT-resistant Colorado potato beetles? Proceedings of the North Central Branch of the Entomological Society of America 9: 94–95.Google Scholar
  123. Rahardja, U., and M.E. Whalon. 1995. Inheritance of resistance to Bacillus thuringiensis subsp. tenebrionis CryIIIA delta-endotoxin in Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology 88: 21–26.PubMedGoogle Scholar
  124. Rankin, M.E., M.L. McAnnely, and J.E. Bodenhamer. 1986. The oogenesis-flight syndrome revisited. In Insect flight, dispersal, and migration, ed. W. Danthanarayana, 27–48. New York: Springer-Verlag.Google Scholar
  125. Roderick, G.K., L.G. De Mendoza, G.P. Dively, and P.A. Follett. 2003. Sperm precedence in Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae): Temporal variation assessed by neutral markers. Annals of the Entomological Society of America 96: 631–636.Google Scholar
  126. Rose, R.L., and W.A. Brindley. 1985. An evaluation of the role of oxidative enzymes in Colorado potato beetle resistance to carbamate insecticides. Pesticide Biochemistry and Physiology 23: 74–84.Google Scholar
  127. Silcox, C.A., G.M. Ghidiu, and A.J. Forgash. 1985. Laboratory and field evaluation of piperonyl butoxide as a pyrethroid synergist against the Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology 78: 1399–1405.Google Scholar
  128. Soderlund, D.M., C.W. Hessney, and M.G. Jiang. 1983. Metabolism of fenvalerate by resistant Colorado potato beetles adults. Abstracts of Papers of the American Chemical Society 186: 28–PEST.Google Scholar
  129. Solbreck, C. 1978. Migration, diapause, and direct development as alternative life histories in a seed bug, Neacoryphus bicruci. In Evolution of insect migration and diapause, ed. H. Dingle, 195–217. New York: Springer.Google Scholar
  130. Stankovic, S., A. Zabel, M. Kostic, B. Manojlovic, and S. Rajkovic. 2004. Colorado potato beetle [Leptinotarsa decemlineata (Say)] resistance to organophosphates and carbamates in Serbia. Journal of Pest Science 77: 11–15.Google Scholar
  131. Stegwee, D., E.C. Kimmel, J.A. de Boer, and S. Henstra. 1963. Hormonal control of reversible degeneration of flight muscle in the Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera). Journal of Cell Biology 19: 519–527.PubMedGoogle Scholar
  132. Stewart, J.G., G.G. Kennedy, and A.V. Sturz. 1997. Incidence of insecticide resistance in populations of Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae), on Prince Edward Island. Canadian Entomologist 129: 21–26.Google Scholar
  133. Stone, B.F. 1968. A formula for determining degree of dominance in cases of monofactorial inheritance of resistance to chemicals. Bulletin of the World Health Organization 38: 325–326.PubMedGoogle Scholar
  134. Stoner, K.A. 1993. Effects of straw and leaf mulches and sprinkle irrigation on the abundance of Colorado potato beetle (Coleoptera: Chrysomelidae) on potato in Connecticut. Journal of Entomological Science 28: 393–403.Google Scholar
  135. Szentesi, A. 1985. Behavioral aspects of female guarding and inter-male conflict in the Colorado potato beetle. In Proceedings of the Symposium on the Colorado Potato Beetle, 17th International Congress of Entomology, eds. D.N. Ferro, and R.H. Voss, 127–137. Amherst: Massachusetts Experiment Station, University of Massachusetts.Google Scholar
  136. Tabashnik, B.E. 1994. Evolution of resistance to Bacillus thuringiensis. Annual Review of Entomology 39: 47–79.Google Scholar
  137. Tan, J.G., D. Mota-Sanchez, V.L. Salgado, and R.M. Hollingworth. 2005. Decreased nicotinic sensitivity to imidacloprid as a resistance mechanism in the Colorado potato beetle, Leptinotarsa decemlineata (SAY). Abstracts of Papers of the American Chemical Society 229: U68–U68.Google Scholar
  138. Tan, J.G., V. Salgado, and R.M. Hollingworth. 2008. Neural actions of imidacloprid and their involvement in resistance in the Colorado potato beetle, Leptinotarsa decemlineata (Say). Pest Management Science 64: 37–47.PubMedGoogle Scholar
  139. Tauber, M.J., and C.A. Tauber. 2002. Prolonged dormancy in Leptinotarsa decemlineata (Coleoptera: Chrysomelidae): a ten-year field study with implications for crop rotation. Environmental Entomology 31: 499–504.Google Scholar
  140. Trisyono, A., and M.E. Whalon. 1997. Fitness costs of resistance to Bacillus thuringiensis in Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology 90: 267–271.Google Scholar
  141. Trouvelot, B. 1936. Remarques sur l’ecologie du doryphore en 1935 dans le massif central et le centre de la France. Revue de Zoologie Agricole et Appliqueée 25: 33–37.Google Scholar
  142. Ushatinskaya, R.S. 1962. Colorado potato beetle diapause and development of its multi-year infestations. Zashchita Rastenii 6: 53–54.Google Scholar
  143. Ushatinskaya, R.S. 1966. Prolonged diapause in the Colorado beetle and conditions of its development. In Ecology and physiology of diapause in the Colorado beetle, ed. K.V. Arnoldi, 120–143. Moscow: Nauka.Google Scholar
  144. Vlasova, V.A. 1978. A prediction of the distribution of Colorado beetle in the Asiatic territory of the USSR. Zashchita Rastenii 6: 44–45.Google Scholar
  145. Voss, R.H., and D.N. Ferro. 1990. Phenology of flight and walking by Colorado potato beetle (Coleoptera: Chrysomelidae) adults in western Massachusetts. Environmental Entomology 19: 117–122.Google Scholar
  146. Walgenbach, J.F., and J.A. Wyman. 1984. Colorado potato beetle (Coleoptera: Chrysomelidae) development in relation to temperature in Wisconsin. Annals of the Entomological Society of America 77: 604–609.Google Scholar
  147. Weber, D. 2003. Colorado beetle: Pest on the move. Pesticide Outlook 14: 256–259.Google Scholar
  148. Weber, D.C., and D.N. Ferro. 1993. Distribution of overwintering Colorado potato beetle in and near Massachusetts potato fields. Entomologia Experimentalis et Applicata 66: 191–196.Google Scholar
  149. Weber, D.C., and D.N. Ferro. 1994. Colorado potato beetle: diverse life history poses challenge to management. In Advances in potato pest biology and management, eds. G.W. Zehnder, R.K. Jansson, M.L. Powelson, and K.V. Raman, 54–70. St. Paul: APS Press.Google Scholar
  150. Weber, D.C., and D.N. Ferro. 1996. Flight and fecundity of Colorado potato beetles fed on different diets. Annals of the Entomological Society of America 89: 297–306.Google Scholar
  151. Wegorek, W. 1957a. Badania nad biologia i ekologia stonki ziemniaczanej (Leptinotarsa decemlineata Say). Roczn Nauk Roln 74A2: 135–185.Google Scholar
  152. Wegorek, W. 1957b. Badania nad zimovaniem stonki ziemniaczanej (Leptinotarsa decemlineata Say). Roczn Nauk Roln 74A2: 316–338.Google Scholar
  153. Weisz, R., Z. Smilowitz, and B. Christ. 1994. Distance, rotation, and border crops affect Colorado potato beetle (Coleoptera: Chrysomelidae) colonization and population density and early blight (Alternaria solani) severity in rotated potato fields. Journal of Economic Entomology 87: 723–729.Google Scholar
  154. Weisz, R., Z. Smilowitz, and S. Fleischer. 1996. Evaluating risk of Colorado potato beetle (Coleoptera: Chrysomelidae) infestation as a function of migratory distance. Journal of Economic Entomology 89: 435–441.Google Scholar
  155. Whalon, M.E., and D.N. Ferro. 1998. Bt-potato resistance management. In Now or never: Serious new plans to save a natural pest control, eds. M. Mellon, and J. Rissler, 107–136. Cambridge: UCS.Google Scholar
  156. Whalon, M.E., D.L. Miller, R.M. Hollingsworth, E.J. Grafius, and J.R. Miller. 1993. Selection of a Colorado potato beetle (Coleoptera: Chrysomelidae) strain resistant to Bacillus thuringiensis. Journal of Economic Entomology 86: 226–233.Google Scholar
  157. Whalon, M.E., D. Mota-Sanchez, and R.M. Hollingworth. 2008. The MSU arthropod pesticide resistance database. http://www.pesticideresistance.org. Accessed 7 April 2008.
  158. Wierenga, J.M., and R.M. Hollingworth. 1992. Inhibition of insect acetylcholinesterase by the potato glycoalkaloid -chaconine. Natur Tox 1: 96–99.Google Scholar
  159. Wierenga, J.M., and R.M. Hollingworth. 1993. Inhibition of altered acetylcholinesterases from insecticide-resistant Colorado potato beetles (Coleoptera: Chrysomelidae). Journal of Economic Entomology 86: 673–679.Google Scholar
  160. Wierenga, J.M., and R.M. Hollingworth. 1994. The role of metabolic enzymes in insecticide-resistant Colorado potato beetles. Pesticide Science 40: 259–264.Google Scholar
  161. Wierenga, J.M., D.L. Norris, and M.E. Whalon. 1996. Stage-specific mortality of Colorado potato beetle (Coleoptera: Chrysomelidae) feeding on transgenic potatoes. Journal of Economic Entomology 89: 1047–1052.Google Scholar
  162. Wiktelius, S. 1981. Wind dispersal of insects. Grana 20: 205–207.CrossRefGoogle Scholar
  163. Worner, S.P. 1988. Ecoclimactic assessment of potential establishment of exotic pests. Journal of Economic Entomology 81: 973–983.Google Scholar
  164. Wright, R.J. 1984. Evaluation of crop rotation for control of Colorado potato beetle (Coleoptera: Chrysomelidae) in commercial potato fields on Long Island. Journal of Economic Entomology 77: 1254–1259.Google Scholar
  165. Yang, B. 1994. Muscle development, energy source utilization, and metabolism hormone activity in Colorado potato beetle, Leptinotarsa decemlineata (Say) flight. M.S. Thesis, University of Massachusetts.Google Scholar
  166. Yoon, K.S., J.O. Nelson, and J.M. Clark. 2002. Selective induction of abamectin metabolism by dexamethasone, 3-methylcholanthrene, and phenobarbital in Colorado potato beetle, Leptinotarsa decemlineata (Say). Pesticide Biochemistry and Physiology 73: 74–86.Google Scholar
  167. Zehnder, G.W. 1986. Timing of insecticides for control of Colorado potato beetle (Coleoptera: Chrysomelidae) in eastern Virginia based on differential susceptibility of life stages. Journal of Economic Entomology 79: 851–856.Google Scholar
  168. Zehnder, G.W., and W.D. Gelernter. 1989. Activity of the M-ONE formulation of a new strain of Bacillus thuringiensis against the Colorado potato beetle (Coleoptera: Chrysomelidae): Relationship between susceptibility and insect life stage. Journal of Economic Entomology 82: 756–61.Google Scholar
  169. Zehnder, G.W., and J. Hough Goldstein. 1990. Colorado potato beetle (Coleoptera: Chrysomelidae) population development and effects on yield of potatoes with and without straw mulch. Journal of Economic Entomology 83: 1982–1987.Google Scholar
  170. Zhao, J.Z., B.A. Bishop, and E.J. Grafius. 2000. Inheritance and synergism of resistance to imidacloprid in the potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology 93: 1508–1514.PubMedCrossRefGoogle Scholar
  171. Zhu, K.Y., and J.M. Clark. 1995. Cloning and sequencing of a cDNA encoding acetylcholinesterase in Colorado potato beetle, Leptinotarsa decemlineata (Say). Insect Biochemistry and Molecular Biology 25: 1129–1138.PubMedGoogle Scholar
  172. Zhu, K.Y., and J.M. Clark. 1997. Validation of a point mutation of acetylcholinesterase in Colorado potato beetle by polymerase chain reaction coupled to enzyme assay. Pesticide Biochemistry and Physiology 57: 28–35.Google Scholar
  173. Zhu, K.Y., S.H. Lee, and J.M. Clark. 1996. A point mutation of acetylcholinesterase associated with azinphosmethyl resistance and reduced fitness in Colorado potato beetle. Pesticide Biochemistry and Physiology 55: 100–108.PubMedGoogle Scholar

Copyright information

© Potato Association of America 2008

Authors and Affiliations

  • Andrei Alyokhin
    • 1
  • Mitchell Baker
    • 2
  • David Mota-Sanchez
    • 3
  • Galen Dively
    • 4
  • Edward Grafius
    • 3
  1. 1.School of Biology and EcologyUniversity of MaineOronoUSA
  2. 2.Biology DepartmentQueens College of CUNYFlushingUSA
  3. 3.Department of EntomologyMichigan State UniversityEast LancingUSA
  4. 4.Department of EntomologyUniversity of MarylandCollege ParkUSA

Personalised recommendations