The global status of insect resistance to neonicotinoid insecticides

Pesticide Biochemistry and Physiology

Volumn 121, Issue , 2015, Pages 78-87

  Bass, Chris ^a   Denholm, Ian ^b   Williamson, Martin S ^a   Nauen, Ralf ^c  

^a ROTHAMSTED RESEARCH   (United Kingdom)

^b UNIVERSITY OF HERTFORDSHIRE   (United Kingdom)

^c BAYER CROPSCIENCE AG   (Germany)

Author keywords

Imidacloprid; Neonicotinoids; Nicotinic acetylcholine receptor; Resistance management; Resistance mechanisms; Sucking pests

Indexed keywords

ALEYRODIDAE; APHIDIDAE; ARCHAEORRHYNCHA; COLEOPTERA; DIPTERA; HEXAPODA;

INSECTICIDE; NICOTINIC AGENT;

ANIMAL; INSECTICIDE RESISTANCE;

ANIMALS; INSECTICIDE RESISTANCE; INSECTICIDES; NICOTINIC AGONISTS;

EID: 84930374199     PISSN: 00483575     EISSN: 10959939     Source Type: Journal    
DOI: 10.1016/j.pestbp.2015.04.004     Document Type: Review

References (107)

1. Jeschke P., Nauen R., Schindler M., Elbert A. Overview of the status and global strategy for neonicotinoids. J. Agric. Food Chem 2011, 59:2897-2908.
2. Nauen R., Jeschke P., Copping L. In focus: neonicotinoid insecticides. Pest Manag. Sci 2008, 64:1081.
3. Elbert A., Haas M., Springer B., Thielert W., Nauen R. Applied aspects of neonicotinoid uses in crop protection. Pest Manag. Sci 2008, 64:1099-1105.
4. Nauen R., Denholm I. Resistance of insect pests to neonicotinoid insecticides: current status and future prospects. Arch. Insect Biochem. Physiol 2005, 58:200-215.
5. Cahill M., Gorman K., Day S., Denholm I., Elbert A., Nauen R. Baseline determination and detection of resistance to imidacloprid in Bemisia tabaci (Homoptera: Aleyrodidae). Bull. Entomol. Res 1996, 86:343-349.
6. Michigan State University Arthropod pesticide resistance database accessed 06.05.15. http://www.pesticideresistance.com.
7. Oliveira M.R.V., Henneberry T.J., Anderson P. History, current status, and collaborative research projects for Bemisia tabaci. Crop Prot 2001, 20:709-723.
8. De Barro P.J., Liu S.S., Boykin L.M., Dinsdale A.B. Bemisia tabaci: a statement of species status. Annu. Rev. Entomol 2011, 56:1-19.
9. Dinsdale A., Cook L., Riginos C., Buckley Y.M., De Barro P.J. Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Ann. Entomol. Soc. Am 2010, 103:196-208.
10. Boykin L.M. Bemisia tabaci nomenclature: lessons learned. Pest Manag. Sci 2014, 70:1454-1459.
11. Ma D., Gorman K., Devine G., Luo W., Denholm I. The biotype and insecticide resistance status of whitelies, Bemisia tabaci (Hemiptera: Aleyrodidae), invading cropping systems in Xinjiang Uygur Autonomous Region, northwestern China. Crop Prot 2007, 26:612-617.
12. Pan H., Chu D., Ge D., Wang S., Wu Q., Xie W., et al. Further spread of and domination by Bemisia tabaci (Hemiptera: Aleyrodidae) biotype Q on field crops in China. J. Econ. Entomol 2011, 104:978-985.
13. Erdogan C., Moores G.D., Gurkan M.O., Gorman K.J., Denholm I. Insecticide resistance and biotype status of populations of the tobacco whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) from Turkey. Crop Prot 2008, 27:600-605.
14. Feng Y.T., Wu Q.J., Wang S.L., Chang X.L., Xie W., Xu B.Y., et al. Cross-resistance study and biochemical mechanisms of thiamethoxam resistance in B-biotype Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Manag. Sci 2010, 66:313-318.
15. Fernandez E., Gravalos C., Haro P.J., Cifuentes D., Bielza P. Insecticide resistance status of Bemisia tabaci Q-biotype in south-eastern Spain. Pest Manag. Sci 2009, 65:885-891.
16. Horowitz A.R., Ishaaya I. Dynamics of biotypes B and Q of the whitefly Bemisia tabaci and its impact on insecticide resistance. Pest Manag. Sci 2014, 70:1568-1572.
17. Nauen R., Stumpf N., Elbert A. Toxicological and mechanistic studies on neonicotinoid cross resistance in Q-type Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Manag. Sci 2002, 58:868-875.
18. Roditakis E., Grispou M., Morou E., Kristoffersen J.B., Roditakis N., Nauen R., et al. Current status of insecticide resistance in Q biotype Bemisia tabaci populations from Crete. Pest Manag. Sci 2009, 65:313-322.
19. Wang Z.Y., Yan H.F., Yang Y.H., Wu Y.D. Biotype and insecticide resistance status of the whitefly Bemisia tabaci from China. Pest Manag. Sci 2010, 66:1360-1366.
20. Rauch N., Nauen R. Identification of biochemical markers linked to neonicotinoid cross resistance in Bemisia tabaci (Hemiptera: Aleyrodidae). Arch. Insect Biochem. Physiol 2003, 54:165-176.
21. Karunker I., Benting J., Lueke B., Ponge T., Nauen R., Roditakis E., et al. Over-expression of cytochrome P450 CYP6CM1 is associated with high resistance to imidacloprid in the B and Q biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae). Insect Biochem. Mol. Biol 2008, 38:634-644.
22. Karunker I., Morou E., Nikou D., Nauen R., Sertchook R., Stevenson B.J., et al. Structural model and functional characterization of the Bemisia tabaci CYP6CM1vQ, a cytochrome P450 associated with high levels of imidacloprid resistance. Insect Biochem. Mol. Biol 2009, 39:697-706.
23. Roditakis E., Morou E., Tsagkarakou A., Riga M., Nauen R., Paine M., et al. Assessment of the Bemisia tabaci CYP6CM1vQ transcript and protein levels in laboratory and field-derived imidacloprid-resistant insects and cross-metabolism potential of the recombinant enzyme. Insect Sci 2011, 18:23-29.
24. Nauen R., Bielza P., Denholm I., Gorman K. Age-specific expression of resistance to a neonicotinoid insecticide in the whitefly Bemisia tabaci. Pest Manag. Sci 2008, 64:1106-1110.
25. Jones C.M., Daniels M., Andrews M., Slater R., Lind R.J., Gorman K., et al. Age-specific expression of a P450 monooxygenase (CYP6CM1) correlates with neonicotinoid resistance in Bemisia tabaci. Pestic. Biochem. Physiol 2011, 101:53-58.
26. Nauen R., Vontas J., Kaussmann M., Wolfel K. Pymetrozine is hydroxylated by CYP6CM1, a cytochrome P450 conferring neonicotinoid resistance in Bemisia tabaci. Pest Manag. Sci 2013, 69:457-461.
27. Gorman K., Slater R., Blande J.D., Clarke A., Wren J., McCaffery A., et al. Cross-resistance relationships between neonicotinoids and pymetrozine in Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Manag. Sci 2010, 66:1186-1190.
28. Daborn P.J., Lumb C., Harrop T.W.R., Blasetti A., Pasricha S., Morin S., et al. Using Drosophila melanogaster to validate metabolism-based insecticide resistance from insect pests. Insect Biochem. Mol. Biol 2012, 42:918-924.
29. Xie W., Yang X., Wang S.L., Wu Q.J., Yang N.N., Li R.M., et al. Gene expression profiling in the thiamethoxam resistant and susceptible B-biotype sweetpotato whitefly, Bemisia tabaci. J. Insect Sci 2012, 12:46.
30. Yang N., Xie W., Jones C.M., Bass C., Jiao X., Yang X., et al. Transcriptome profiling of the whitefly Bemisia tabaci reveals stage-specific gene expression signatures for thiamethoxam resistance. Insect Mol. Biol 2013, 22:485-496.
31. Yang X., Xie W., Wang S.L., Wu Q.J., Pan H.P., Li R.M., et al. Two cytochrome P450 genes are involved in imidacloprid resistance in field populations of the whitefly, Bemisia tabaci, in China. Pestic. Biochem. Physiol 2013, 107:343-350.
32. Devine G.J., Harling Z.K., Scarr A.W., Devonshire A.L. Lethal and sublethal effects of imidacloprid on nicotine- tolerant Myzus nicotianae and Myzus persicae. Pestic. Sci 1996, 48:57-62.
33. Nauen R., Strobel J., Tietjen K., Otsu Y., Erdelen C., Elbert A. Aphicidal activity of imidacloprid against a tobacco feeding strain of Myzus persicae (Homoptera: Aphididae) from Japan closely related to Myzus nicotianae and highly resistant to carbamates and organophosphates. Bull. Entomol. Res 1996, 86:165-171.
34. Bass C., Zimmer C.T., Riveron J.M., Wilding C.S., Wondji C.S., Kaussmann M., et al. Gene amplification and microsatellite polymorphism underlie a recent insect host shift. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:19460-19465.
35. Puinean A.M., Foster S.P., Oliphant L., Denholm I., Field L.M., Millar N.S., et al. Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. PLoS Genet 2010, 6:e1000999.
36. Philippou D., Field L.M., Moores G.D. Metabolic enzyme(s) confer imidacloprid resistance in a clone of Myzus persicae (Sulzer) (Hemiptera: Aphididae) from Greece. Pest Manag. Sci 2009, 66:390-395.
37. Bass C., Puinean A.M., Andrews M.C., Culter P., Daniels M., Elias J., et al. Mutation of a nicotinic acetylcholine receptor β subunit is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. BMC Neurosci 2011, 12:51.
38. Grutter T., Changeux J.P. Nicotinic receptors in wonderland. Trends Biochem. Sci 2001, 26:459-463.
39. Shimomura M., Yokota M., Ihara M., Akamatsu M., Sattelle D.B., Matsuda K. Role in the selectivity of neonicotinoids of insect-specific basic residues in loop D of the nicotinic acetylcholine receptor agonist binding site. Mol. Pharmacol 2006, 70:1255-1263.
40. Panini M., Dradi D., Marani G., Butturini A., Mazzoni E. Detecting the presence of target-site resistance to neonicotinoids and pyrethroids in Italian populations of Myzus persicae. Pest Manag. Sci 2013, 70:931-938.
41. Slater R., Paul V.L., Andrews M., Garbay M., Camblin P. Identifying the presence of neonicotinoid resistant peach-potato aphid (Myzus persicae) in the peach growing regions of southern France and northern Spain. Pest Manag. Sci 2011, 68:634-638.
42. Gore J., Cook D., Catchot A., Leonard B.R., Stewart S.D., Lorenz G., et al. Cotton aphid (Heteroptera: Aphididae) susceptibility to commercial and experimental insecticides in the Southern United States. J. Econ. Entomol 2013, 106:1430-1439.
43. Herron G.A., Wilson L.J. Neonicotinoid resistance in Aphis gossypii Glover (Aphididae: Hemiptera) from Australian cotton. Aust. J. Entomol 2011, 50:93-98.
44. Koo H.N., An J.J., Park S.E., Kim J.I., Kim G.H. Regional susceptibilities to 12 insecticides of melon and cotton aphid, Aphis gossypii (Hemiptera: Aphididae) and a point mutation associated with imidacloprid resistance. Crop Prot 2014, 55:91-97.
45. Shi X.G., Zhu Y.K., Xia X.M., Qiao K., Wang H.Y., Wang K.Y. The mutation in nicotinic acetylcholine receptor beta 1 subunit may confer resistance to imidacloprid in Aphis gossypii (Glover). J. Food Agric. Environ 2012, 10:1227-1230.
46. Foster S.P., Denholm I., Thompson R. Variation in response to neonicotinoid insecticides in peach potato aphids, Myzus persicae (Hemiptera: Aphididae). Pest Manag. Sci 2003, 59:166-173.
47. Sogawa K., Cheng C.H. Economic thresholds, nature of damage, and losses caused by the brown planthopper. Brown Planthopper: Threat to Rice Production in Asia 1979, 125-142. The International Rice Research Institute, Los Banos, Laguna, Philippines.
48. Gorman K., Liu Z., Denholm I., Bruggen K.-U., Nauen R. Neonicotinoid resistance in rice brown planthopper, Nilaparvata lugens. Pest Manag. Sci 2008, 64:1122-1125.
49. Matsumura M., Sanada-Morimura S., Otuka A., Ohtsu R., Sakumoto S., Takeuchi H., et al. Insecticide susceptibilities in populations of two rice planthoppers, Nilaparvata lugens and Sogatella furcifera, immigrating into Japan in the period 2005-2012. Pest Manag. Sci 2014, 70:615-622.
50. Wang Y., Wu S., Zhu Y.C., Chen J., Liu F., Zhao X., et al. Dynamics of imidacloprid resistance and cross-resistance in the brown planthopper, Nilaparvata lugens. Entomol. Exp. Appl 2009, 131:20-29.
51. Wang Y.H., Chen J., Zhu Y.C., Ma C.Y., Huang Y., Shen J.L. Susceptibility to neonicotinoids and risk of resistance development in the brown planthopper, Nilaparvata lugens (Stal) (Homoptera: Delphacidae). Pest Manag. Sci 2008, 64:1278-1284.
52. Zhang X.L., Liu X.Y., Zhu F.X., Li J.H., You H., Lu P. Field evolution of insecticide resistance in the brown planthopper (Nilaparvata lugens Stal) in China. Crop Prot 2014, 58:61-66.
53. Liu Z.W., Williamson M.S., Lansdell S.J., Denholm I., Han Z.J., Millar N.S. A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper). Proc. Natl. Acad. Sci. U.S.A. 2005, 102:8420-8425.
54. Wen Y., Liu Z., Bao H., Han Z. Imidacloprid resistance and its mechanisms in field populations of brown planthopper, Nilaparvata lugens Stål in China. Pestic. Biochem. Physiol 2009, 94:36-42.
55. Zewen L., Zhaojun H., Yinchang W., Lingchun Z., Hongwei Z., Chengjun L. Selection for imidacloprid resistance in Nilaparvata lugens: cross-resistance patterns and possible mechanisms. Pest Manag. Sci 2003, 59:1355-1359.
56. Puinean A.M., Denholm I., Millar N.S., Nauen R., Williamson M.S. Characterisation of imidacloprid resistance mechanisms in the brown planthopper, Nilaparvata lugens Stål (Hemiptera: Delphacidae). Pestic. Biochem. Physiol 2010, 97:129-132.
57. Bass C., Carvalho R.A., Oliphant L., Puinean A.M., Field L.M., Nauen R., et al. Overexpression of a cytochrome P450 monooxygenase, CYP6ER1, is associated with resistance to imidacloprid in the brown planthopper, Nilaparvata lugens. Insect Mol. Biol 2011, 20:763-773.
58. Ding Z., Wen Y., Yang B., Zhang Y., Liu S., Liu Z., et al. Biochemical mechanisms of imidacloprid resistance in Nilaparvata lugens: over-expression of cytochrome P450 CYP6AY1. Insect Biochem. Mol. Biol 2013, 43:1021-1027.
59. Pang R., Li Y., Dong Y., Liang Z., Zhang Y., Zhang W. Identification of promoter polymorphisms in the cytochrome P450 CYP6AY1 linked with insecticide resistance in the brown planthopper, Nilaparvata lugens. Insect Mol. Biol 2014, 23:768-778.
60. Pospischil R., Junkersdorf J., Horn K. Control of house flies, Musca domestica (Diptera: Muscidae), with Imidacloprid WG 10 in pig farms (Germany). Proceedings of the Fifth International Conference on Urban Pests 2005, 309-317. Perniagaan Ph'ng at P&Y Design Network, Malaysia. L.Y. Chow, W.H. Robinson (Eds.).
61. Wen Z.M., Scott J.G. Cross-resistance to imidacloprid in strains of German cockroach (Blattella germanica) and house fly (Musca domestica). Pestic. Sci 1997, 49:367-371.
62. Kaufman P.E., Gerry A.C., Rutz D.A., Scott J.G. Monitoring susceptibility of house flies (Musca domestica L.) in the United States to imidacloprid. J. Agric. Urban Entomol 2006, 23:195-200.
63. Scott J.G., Leichter C.A., Rinkevihc F.D., Harris S.A., Su C., Aberegg L.C., et al. Insecticide resistance in house flies from the United States: resistance levels and frequency of pyrethroid resistance alleles. Pestic. Biochem. Physiol 2013, 107:377-384.
64. Kaufman P.E., Nunez S.C., Mann R.S., Geden C.J., Scharf M.E. Nicotinoid and pyrethroid insecticide resistance in houseflies (Diptera: Muscidae) collected from Florida dairies. Pest Manag. Sci 2010, 66:290-294.
65. Kristensen M., Jespersen J.B. Susceptibility to thiamethoxam of Musca domestica from Danish livestock farms. Pest Manag. Sci 2008, 64:126-132.
66. Markussen M.D.K., Kristensen M. Cytochrome P450 monooxygenase-mediated neonicotinoid resistance in the house fly Musca domestica L. Pestic. Biochem. Physiol 2010, 98:50-58.
67. Khan H., Abbas N., Shad S.A., Afzal M.B.S. Genetics and realized heritability of resistance to imidacloprid in a poultry population of house fly, Musca domestica L. (Diptera: Muscidae) from Pakistan. Pestic. Biochem. Physiol 2014, 114:38-43.
68. Li J., Wang Q.M., Zhang L., Gao X.W. Characterization of imidacloprid resistance in the housefly Musca domestica (Diptera: Muscidae). Pestic. Biochem. Physiol 2012, 102:109-114.
69. Kavi L.A.K., Kaufman P.E., Scott J.G. Genetics and mechanisms of imidacloprid resistance in houseflies. Pestic. Biochem. Physiol 2014, 109:64-69.
70. Hojland D.H., Jensen K.M.V., Kristensen A. A comparative study of P450 gene expression in field and laboratory Musca domestica L. strains. Pest Manag. Sci 2014, 70:1237-1242.
71. Markussen D.K.M., Kristensen M. Low expression of nicotinic acetylcholine receptor subunit Mdα2 in neonicotinoid-resistant strains of Musca domestica L. Pest Manag. Sci 2010, 66:1257-1262.
72. Scott J.G., Warren W.C., Beukeboom L.W., Bopp D., Clark A.G., Giers S.D., et al. Genome of the housefly, Musca domestica L., a global vector of diseases with adaptations to a septic environment. Genome Biol 2014, 15:466.
73. Olson E.R., Dively G.P., Nelson J.O. Baseline susceptibility to imidacloprid and cross resistance patterns in Colorado potato beetle (Coleoptera: Chrysomelidae) populations. J. Econ. Entomol 2000, 93:447-458.
74. Zhao J.Z., Bishop B.A., Grafius E.J. Inheritance and synergism of resistance to imidacloprid in the Colorado potato beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol 2000, 93:1508-1514.
75. Mota-Sanchez D., Hollingworth R.M., Grafius E.J., Moyer D.D. Resistance and cross-resistance to neonicotinoid insecticides and spinosad in the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). Pest Manag. Sci 2006, 62:30-37.
76. Hollingworth R.M., Mota-Sanchez D., Whalon M.E., Graphius E. Comparative pharmokinetics of imidacloprid in susceptible and resistant Colorado potato beetles. Proc 10th IUPAC Int. Cong. Chemistry of Crop Protection, Basel 2002, 1:312.
77. Tan J.G., Salgado V.L., Hollingworth R.M. Neural actions of imidacloprid and their involvement in resistance in the Colorado potato beetle, Leptinotarsa decemlineata (Say). Pest Manag. Sci 2008, 64:37-47.
78. Gorman K., Hewitt F., Denholm I., Devine G.J. New developments in insecticide resistance in the glasshouse whitefly (Trialeurodes vaporariorum) and the two-spotted spider mite (Tetranychus urticae) in the UK. Pest Manag. Sci 2002, 58:123-130.
79. Bi J.L., Toscano N.C. Current status of the greenhouse whitefly, Trialeurodes vaporariorum, susceptibility to neonicotinoid and conventional insecticides on strawberries in southern California. Pest Manag. Sci 2007, 63:747-752.
80. Gorman K., Devine G., Bennison J., Coussons P., Punchard N., Denholm I. Report of resistance to the neonicotinoid insecticide imidacloprid in Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). Pest Manag. Sci 2007, 63:555-558.
81. Karatolos N., Denholm I., Williamson M., Nauen R., Gorman K. Incidence and characterisation of resistance to neonicotinoid insecticides and pymetrozine in the greenhouse whitefly, Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae). Pest Manag. Sci 2010, 66:1304-1307.
82. Pappas M.L., Migkou F., Broufas G.D. Incidence of resistance to neonicotinoid insecticides in greenhouse populations of the whitefly, Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) from Greece. Appl. Entomol. Zool 2013, 48:373-378.
83. Ovcarenko I., Lindstrom L., Saikkonen K., Vanninen I. Variation in mortality among populations is higher for pymetrozine than for imidacloprid and spiromesifen in Trialeurodes vaporariorum in greenhouses in Finland. Pest Manag. Sci 2014, 70:1524-1530.
84. Karatolos N., Pauchet Y., Wilkinson P., Chauhan R., Denholm I., Gorman K., et al. Pyrosequencing the transcriptome of the greenhouse whitefly, Trialeurodes vaporariorum reveals multiple transcripts encoding insecticide targets and detoxifying enzymes. BMC Genomics 2011, 12:56.
85. Matsumura M., Takeuchi M., Satoh M., Sanada-Morimura S., Otuka A., Watanabe T., et al. Species-specific insecticide resistance to imidacloprid and fipronil in the rice planthoppers Nilaparvata lugens and Sogatella furcifera in East and South-east Asia. Pest Manag. Sci 2008, 64:1115-1121.
86. Su J.Y., Wang Z.W., Zhang K., Tian X.R., Yin Y.Q., Zhao X.Q., et al. Status of insecticide resistance of the whitebacked planthopper, Sogatella furcifera (Hemiptera: Delphacidae). Fla Entomol 2013, 96:948-956.
87. Zhang K., Zhang W., Zhang S., Wu S.F., Ban L.F., Su J.Y., et al. Susceptibility of Sogatella furcifera and Laodelphax striatellus (Hemiptera: Delphacidae) to Six Insecticides in China. J. Econ. Entomol 2014, 107:1916-1922.
88. Gao B.L., Wu J., Huang S.J., Mu L.F., Han Z.J. Insecticide resistance in field populations of Laodelphax striatellus Fallen (Homoptera: Delphacidae) in China and its possible mechanisms. Int. J. Pest Manage 2008, 54:13-19.
89. Tiwari S., Mann R.S., Rogers M.E., Stelinski L.L. Insecticide resistance in field populations of Asian citrus psyllid in Florida. Pest Manag. Sci 2011, 67:1258-1268.
90. Tiwari S., Killiny N., Stelinski L.L. Dynamic insecticide susceptibility changes in Florida populations of Diaphorina citri (Hemiptera: Psyllidae). J. Econ. Entomol 2013, 106:393-399.
91. Vazquez-Garcia M., Velazquez-Monreal J., Medina-Urrutia V.M., Cruz-Vargas C.D., Sandoval-Salazar M., Virgen-Calleros G., et al. Insecticide resistance in adult Diaphorina citri Kuwayama from lime orchards in Central West Mexico. Southwest. Entomol 2013, 38:579-596.
92. Reyes M., Franck P., Charmillot P.J., Ioriatti C., Olivares J., Pasqualin E., et al. Diversity of insecticide resistance mechanisms and spectrum in European populations of the Codling moth, Cydia pomonella. Pest Manag. Sci 2007, 63:890-902.
93. Voudouris C.C., Sauphanor B., Franck P., Reyes M., Mamuris Z., Tsitsipis J.A., et al. Insecticide resistance status of the codling moth Cydia pomonella (Lepidoptera: Tortricidae) from Greece. Pestic. Biochem. Physiol 2011, 100:229-238.
94. Knight A.L. Cross-resistance between azinphos-methyl and acetamiprid in populations of codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae), from Washington State. Pest Manag. Sci 2010, 66:865-874.
95. Cichon L.B., Soleno J., Anguiano O.L., Garrido S.A.S., Montagna C.M. Evaluation of cytochrome P-450 activity in field populations of Cydia pomonella (Lepidoptera: Tortricidae) resistant to azinphosmethyl, acetamiprid, and thiacloprid. J. Econ. Entomol 2013, 106:939-944.
96. Grigg-McGuffin K., Scott I.M., Bellerose S., Chouinard G., Cormier D., Scott-Dupree C. Susceptibility in field populations of codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae), in Ontario and Quebec apple orchards to a selection of insecticides. Pest Manag. Sci 2015, 71:234-242.
97. Reyes M., Franck P., Olivares J., Margaritopoulos J., Knight A., Sauphanor B. Worldwide variability of insecticide resistance mechanisms in the codling moth, Cydia pomonella L. (Lepidoptera: Tortricidae). Bull. Entomol. Res 2009, 99:359-369.
98. Zhao G.Y., Liu W., Brown J.M., Knowles C.O. Insecticide resistance in-field and laboratory strains of western flower thrips (Thysanoptera, Thripidae). J. Econ. Entomol 1995, 88:1164-1170.
99. Minakuchi C., Inano Y., Shi X.Y., Song D.L., Zhang Y.J., Miura K., et al. Neonicotinoid resistance and cDNA sequences of nicotinic acetylcholine receptor subunits of the western flower thrips Frankliniella occidentalis (Thysanoptera: Thripidae). Appl. Entomol. Zool 2013, 48:507-513.
100. Gao C.F., Ma S.Z., Shan C.H., Wu S.F. Thiamethoxam resistance selected in the western flower thrips Frankliniella occidentalis (Thysanoptera: Thripidae): cross-resistance patterns, possible biochemical mechanisms and fitness costs analysis. Pestic. Biochem. Physiol 2014, 114:90-96.
101. Denholm I., Rowland M.W. Tactics for managing pesticide resistance in arthropods: theory and practice. Annu. Rev. Entomol 1992, 37:91-112.
102. Elbert A., Bailo-Schleiermacher I., Bruggen K.-U., Nauen R., Rogers D., Steffens R., et al. Guidelines on resistance management for neonicotinoids. Pflanzenschutz-Nachr. Bayer 2005, 58:1-32.
103. Cahill M., Denholm I. Managing resistance to the chloronicotinyl insecticides - rhetoric or reality?. Neonicotinoid Insecticides and the Nicotinic Acetylcholine Receptor 1999, 253-270. Springer Verlag, Tokyo. I. Yamamoto, J. Casida (Eds.).
104. Bass C., Puinean A.M., Zimmer C.T., Denholm I., Field L.M., Foster S.P., et al. The evolution of insecticide resistance in the peach potato aphid, Myzus persicae. Insect Biochem. Mol. Biol 2014, 51:41-51.
105. Zhu Y., Loso M.R., Watson G.B., Sparks T.C., Rogers R.B., Huang J.X., et al. Discovery and characterisation of sulfoxaflor, a novel insecticide targeting sap-feeding pests. J. Agric. Food Chem 2011, 59:2950-2957.
106. Nauen R., Jeschke P., Velten R., Beck M.E., Ebbinghaus-Kintscher U., Thielert W., et al. Flupyradifurone: a brief profile of a new butenolide insecticide. Pest Manag. Sci 2014, 71:850-862.
107. Longhurst C., Babcock J.M., Denholm I., Gorman K., Thomas J.D., Sparks T.C. Cross-resistance relationships of the sulfoximine insecticide sulfoxaflor with neonicotinoids and other insecticides in the whiteflies Bemisia tabaci and Trialeurodes vaporariorum. Pest Manag. Sci 2013, 69:809-813.