Pesticide-Induced Stress in Arthropod Pests for Optimized Integrated Pest Management Programs

Annual Review of Entomology

Volumn 61, Issue , 2016, Pages 43-62

  Guedes, R N C ^a   Smagghe, G ^b   Stark, J D ^c   Desneux, N ^d  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^b GHENT UNIVERSITY   (Belgium)

^c WASHINGTON STATE UNIVERSITY   (United States)

^d Institut Sophia Agrobiotech   (France)

Author keywords

Behavioral avoidance; Dominance shift; Ecological backlashes; Pest outbreaks; Pest resurgence; Pesticide induced hormesis

Indexed keywords

PESTICIDE;

ANIMAL; ARTHROPOD; ECOTOXICOLOGY; PEST CONTROL;

ANIMALS; ARTHROPODS; ECOTOXICOLOGY; PEST CONTROL; PESTICIDES;

EID: 84953445022     PISSN: 00664170     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-ento-010715-023646     Document Type: Review

References (142)

1. Aktar MW, Sengupta D, Chowdhury A. 2009. Impact of pesticide use in agriculture: their benefits and hazards. Interdiscip. Toxicol. 2:1-12
2. Alto BW, Lampman RL, Kesavaraju B, Muturi EJ. 2013. Pesticide-mediated release from competition among competing Aedes aegypti and Aedes albopictus (Diptera: Culicidae). J. Med. Entomol. 50:1240-49
3. Antunes EC, Della Lucia TMC, Guedes RNC, Serrão JE. 2005. Abamectin-driven alterations on queen ovaries of the leaf-cutting ant Acromyrmex subterraneus subterraneus. Sociobiology 44:178-88
4. Antunes EC, Guedes RNC,Della Lucia TMC,Serrão JE. 2000. Sub-lethal effects of abamectin suppressing colonies of the leaf-cutting ant Acromyrmex subterraneus subterraneus. Pest Manag. Sci. 56:1059-64
5. Araújo RA, Badji CA, Correa AS, Ladeira JA, Guedes RNC. 2004. Deltamethrin impact in soil surface Coleoptera associated with maize crop in no tillage and conventional plantation systems. Neotrop. Entomol. 33:379-85
6. Araújo RA, Guedes RNC, Oliveira MGA, Ferreira GH. 2008. Enhanced activity of carbohydrate-and lipid-metabolizing enzymes in insecticide-resistant populations of the maize weevil, Sitophilus zeamais. Bull. Entomol. Res. 98:417-24
7. AyyanathMM,Cutler GC, Scott-Dupree CD, Sibley PK. 2013. Transgenerational shifts in reproduction hormesis in green peach aphid exposed to low concentrations of imidacloprid. PLOS ONE 8(9):e74532
8. Badji CA, Guedes RNC, Correa AS, Ferreira GH, Nascimento IC. 2006. Deltamethrin-induced impact on ant assemblages in tropical maize fields under conventional and no-tillage cultivation. Sociobiology 48:701-15
9. Badji CA, Guedes RNC, Silva AA, Araújo RA. 2004. Impact of deltamethrin on arthropods in maize under conventional and no-tillage cultivation. Crop Prot. 23:1031-39
10. Badji CA, Guedes RNC, Silva AA, Correa AS, Queiroz MELR, Michereff-Filho M. 2007. Non-target impact of deltamethrin on soil arthropods of maize fields under conventional and no-tillage cultivation. J. Appl. Entomol. 131:50-58
11. Bahlai CA, Xue Y, McCreary CM, Schaafsma AW, Hallett RH. 2010. Choosing organic pesticides over synthetic pesticides may not effectively mitigate environmental risks in soybeans. PLOS ONE 5(6):e11250
12. Banks JE, Ackleh AS, Stark JD. 2010. The use of surrogate species in risk assessments: using life history data to safeguard against false negatives. Risk Anal. 30:175-82
13. Banks JE, Stark JD, Vargas RI, Ackleh AS. 2014. Deconstructing the surrogate species concept: a life history approach to the protection of ecosystem services. Ecol. Appl. 24:770-78
14. Barbieri RF, Lester PJ, Miller AS, Ryan KG. 2013. A neurotoxic pesticide changes the outcome of aggressive interactions between native and invasive ants. Proc. R. Soc. B 280:20132157
15. Barbosa WF, Smagghe G, Guedes RNC. 2015. Pesticides and reduced-risk insecticides, native bees and pantropical stingless bees: pitfalls and perspectives. Pest Manag. Sci. 71:1059-53
16. Bayley M. 2002. Basic behaviour: the use of animal locomotion in behavioural ecotoxicology. In Behavioural Ecotoxicology, ed. G Dell'Omo, pp. 211-30. Chichester, UK:Wiley
17. Beale MH, Birkett MA, Bruce TJA, Chamberlain K, Field LM, et al. 2006. Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior. PNAS 103:10509-13
18. Biondi A, Desneux N, Siscaro G, Zappalà L. 2012. Using organic-certified rather synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere 87:803-12
19. Biondi A, Zappalà L, Stark JD, Desneux N. 2013. Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLOS ONE 8(9):e76548
20. Braga LS, Correa AS, Pereira EJG, Guedes RNC. 2011. Face or flee? Fenitrothion resistance and behavioral response in populations of the maize weevil, Sitophilus zeamais. J. Stored Prod. Res. 47:161-67
21. Broderick NA, Raffa KF, Handelsman J. 2006. Midgut bacteria required for Bacillus thuringiensis insecticidal activity. PNAS 103:15196-99
22. Calabrese EJ. 2008. Hormesis: why it is important to toxicology and toxicologists. Environ. Chem. 27:1451-74
23. Calabrese EJ, Blain R. 2005. The occurrence of hormetic dose responses in the toxicological literature, the hormesis database: an overview. Toxicol. Appl. Pharmacol. 202:289-301
24. Cameron R, Lang EB, Annan IB, Portillo HE, Alvarez JM. 2013. Use of fluorescence, a novel technique to determine reduction in Bemisia tabaci (Hemiptera: Aleyrodidae) nymph feeDing when exposed to Benevia and other insecticides. J. Econ. Entomol. 106:597-603
25. Casida JE, Durkin KA. 2013. Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu. Rev. Entomol. 58:99-117
26. Chen Z, Qu YY, Xiao D, Song LF, Gao X-W, et al. 2015. Lethal and social-mediated effects of ten insecticides on the subterranean termite Reticulitermes speratus. J. Pest Sci. doi: 10. 1007/s10340-015-0656-0
27. Chong CS, Hoffman AA, Thomson LJ. 2007. Commercial agrochemical applications in vineyards do not influence ant communities. Environ. Entomol. 36:1374-83
28. Civolani S, Cassanelli S, Chicca M, Rison JL, Bassi A, et al. 2014. An EPG study of the probing behavior of adult Bemisia tabaci biotype Q (Hemiptera: Aleyrodidae) following exposure to cyantraniliprole. J. Econ. Entomol. 107:910-19
29. Coats JR. 1994. Risks from natural versus synthetic insecticides. Annu. Rev. Entomol. 39:489-515
30. Connell JH. 1978. Diversity in tropical rain forests and coral reefs. Science 199:1302-10
31. Cooper J, Dobson H. 2007. The benefits of pesticides to mankind and the environment. Crop Prot. 26:1337-48
32. Cordeiro EMG, Correa AS, Guedes RNC. 2014. Insecticide-mediated shift in ecological dominance between two competing species of grain beetles. PLOS ONE 9(6):e100990
33. Cordeiro EMG, Correa AS, Venzon M, Guedes RNC. 2010. Insecticide survival and behavioral avoidance in the lacewings Chrysoperla externa and Ceraeochrysa cubana. Chemosphere 81:1352-57
34. Cordeiro EMG, de Moura ILT, Fadini MAM, Guedes RNC. 2013. Beyond selectivity: Are behavioral avoidance and hormesis likely causes of pyrethroid-induced outbreaks of the red mite Oligonychus ilicis? Chemosphere 93:1111-16
35. Correa AS, ToméHVV, Braga LS, Martins JC, de Oliveira LO, Guedes RNC. 2014. Are mitochondrial lineages, mitochondrial lysis and respiration rate associated with phosphine susceptibility in the maize weevil Sitophilus zeamais? Ann. Appl. Biol. 165:137-46
36. Croft BA. 1990. Arthropod Biological Control Agents and Pesticides. New York:Wiley
37. Cutler GC. 2013. Insects, insecticides and hormesis: evidence and considerations for study. Dose Response 11:154-77
38. Czaja K, Góralxzyk K, Strucinski P, Hernik A, KorczW, et al. 2015. Biopesticides-towards increased consumer safety in the European Union. Pest Manag. Sci. 15:3-6
39. Decourtye A, Henry M, Desneux N. 2013. Environment: overhaul pesticide testing on bees. Nature 497:188
40. Della Lucia TMC, Gandra LC, Guedes RNC. 2014. Managing leaf-cutting ants: peculiarities, trends and challenges. Pest Manag. Sci. 70:14-23
41. Desneux N, Decourtye A, Delpuech J-M. 2007. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52:81-106
42. Desneux N, Fauvergue X, Decahume-Moncharmont F-X, Kerhoas L, Ballanger Y, Kaiser L. 2005. Diaeretiella rapae limits Myzus persicae populations after applications of deltamethrin in oilseed rape. J. Econ. Entomol. 98:9-17
43. Devine GJ, FurlongMJ. 2007. Insecticide use: contexts and ecological consequences. Agric. Hum. Values 24:281-306
44. Douglas AE. 2015. Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60:17-34
45. Exophily in anophelines and malaria control. 1958. WHO Chron. 12 81-82
46. Fang S-M. 2012. Insect glutathione S-transferase: a review of comparative genomic studies and response to xenobiotics. Bull. Insectol. 65:265-71
47. Food Agric. Organ. (FAO). 2013. FAO Statistics Yearbook 2013. Rome: FAO
48. Forbes VE, Calow P. 1999. Is the per capita rate of increase a good measure of population-level effects in ecotoxicology? Environ. Toxicol. Chem. 18:1544-56
49. Forbes VE, Calow P. 2002. Population growth rate as a basis for ecological risk assessment of toxic chemicals. Philos. Trans. R. Soc. B 357:1299-306
50. Gao Y, Reitz SR,Wei Q, Yu W, Zhang Z, Lei Z. 2014. Local crop planting systems enhance insecticidemediated displacement of two invasive leafminer fly. PLOS ONE 9(3):e92625
51. Ghimire N, Woodward RT. 2013. Under-and over-use of pesticides: an international analysis. Ecol. Econ. 89:73-81
52. Gilbert LI, Gill SS. 2010. Insect Control: Biological and Synthetic Agents. London: Academic
53. Gould F. 1984. Role of behavior in the evolution of insect adaptation to insecticides and resistant host plants. Bull. Entomol. Soc. Am. 30:34-40
54. Guedes NMP, Guedes RNC, Ferreira GH, Silva LB. 2009. Flight take-off and walking behavior of insecticide-susceptible and-resistant strains of Sitophilus zeamais exposed to deltamethrin. Bull. Entomol. Res. 99:393-400
55. Guedes NMP, Guedes RNC, Silva LB, Cordeiro EMG. 2009. Deltamethrin-induced feeDing plasticity in pyrethroid-susceptible and-resistant strains of the maize weevil, Sitophilus zeamais. J. Appl. Entomol. 133:524-32
56. GuedesNMP,Tolledo J, Correa AS,Guedes RNC. 2010. Insecticide-induced hormesis in an insecticideresistant strain of the maize weevil, Sitophilus zeamais. J. Appl. Entomol. 134:142-48
57. Guedes RNC, Campbell JF, Arthur FH, Opit GP, Zhu KY,Throne JE. 2008. Acute lethal and behavioral sublethal responses of two stored-product psocids to surface insecticides. Pest Manag. Sci. 64:1314-22
58. Guedes RNC, Cutler GC. 2014. Insecticide-induced hormesis and arthropod pest management. Pest Manag. Sci. 70:690-97
59. Guedes RNC,Magalhães LC, Cosme LV. 2009. Stimulatory sublethal response of a generalist predator to permethrin: hormesis, hormoligosis, or homeostatic regulation? J. Econ. Entomol. 102:170-76
60. Guedes RNC,Oliveira EE, Guedes NMP, Ribeiro B, Serrão JE. 2006. Cost andmitigation of insecticide resistance in the maize weevil, Sitophilus zeamais. Physiol. Entomol. 31:30-38
61. GuoL,Desneux N, Sonoda S, Liang P,Han P, GaoX-W. 2013. Sublethal and transgenerational effects of chlorantraniliprole on biological traits of the diamondback moth, Plutella xylostella L. Crop Prot. 48:29-34
62. Haddi K, Mendonça LP, dos Santos MF, Guedes RNC, Oliveira EE. 2015. Metabolic and behavioral mechanisms of indoxacarb resistance in Sitophilus zeamais (Coleoptera: Curculionidae). J. Econ. Entomol. 108:362-69
63. Hallett RH, Bahlai CA, Xue Y, Schaafsma AW. 2014. Incorporating natural enemy units into a dynamic action threshold for the soybean aphid, Aphis glycines (Homoptera: Aphididae). Pest Manag. Sci. 70:879-88
64. Hanson N, Stark JD. 2011. A comparison of simple and complex populationmodels to reduce uncertainty in ecological risk assessments of chemicals: example with three species of Daphnia. Ecotoxicology 20:1268-76
65. Hanson N, Stark JD. 2012. Comparison of population level and individual level endpoints to evaluate ecological risk of chemicals. Environ. Sci. Technol. 46:5590-98
66. Hardin MR, Benrey B, CollM, LampWO, Roderick GK, Barbosa P. 1995. Arthropod pest resurgence: an overview of potential mechanisms. Crop Prot. 14:3-18
67. Haskell PT, McEwen P. 1998. Ecotoxicology: Pesticides and Beneficial Organisms. Dordrecht,Neth. : Kluwer
68. Haynes KF. 1988. Sublethal effects of neurotoxic insecticides on insect behavior. Annu. Rev. Entomol. 33:149-68
69. He Y, Zhao J, Zheng Y,WengQ, Biondi A, et al. 2013. Assessment of potential sublethal effects of various insecticides on key biological traits of the tobacco whitefly, Bemisia tabaci. Int. J. Biol. Sci. 9:246-55
70. Hellou J. 2011. Behavioural ecotoxicology, an early warning signal to assess environmental quality. Environ. Sci. Pollut. Res. 18:1-11
71. Hellou J, Cheeseman K, Desnoyers E, Johnston D, Jouvenelle ML, et al. 2008. A non-lethal chemically based approach to investigate the quality of harbor sediments. Sci. Total Environ. 389:178-87
72. Isman MB, Grieneisen ML. 2014. Botanical insecticide research: many publications, limited useful data. Trends Plant Sci. 19:140-45
73. Jager T, Barsi A, Ducrot V. 2013. Hormesis on life-history traits: Is there such a thing as a free lunch? Ecotoxicology 22:263-70
74. JagerT,Crommentuijn T, Van GestelCAM,KooijmanSALM. 2004. Simultaneous modeling ofmultiple endpoints in life-cycle toxicity tests. Environ. Sci. Technol. 38:2894-900
75. Jatav KS, Dhar J. 2014. Hybrid approach for pest control with impulsive releasing of natural enemies and chemical pesticides: a plant-pest-natural enemy model. Nonlinear Anal. Hybrid Syst. 12:79-92
76. Kesavaraju B, Afify A, Gaugler R. 2013. Strain specific differences in intraspecific competition in Aedes albopictus (Diptera: Culicidae). J. Med. Entomol. 49:988-92
77. Kikuchi Y,Hayatsu M, Hosokawa T, Nagayama A, Tago K, FukatsuT. 2012. Symbiont-mediated insecticide resistance. PNAS 109:8618-22
78. Köhler H-R, Triebskorn R. 2013. Wildlife ecotoxicology of pesticides: Can we track effects to the population level and beyond? Science 341:759-65
79. Kralj-Fi?ser S, Schuett W. 2014. Studying personality variation in invertebrates: Why bother? Anim. Behav. 91:41-52
80. Krämer W, Schirmer U, Jeschke P,Witschel M. 2012. Modern Crop Protection Compounds, Vol. 3: Insecticides. Weinheim, Ger. : Wiley-VCH
81. Kramarz PE, Banks JE, Stark JD. 2007. Density-dependent response of the pea aphid (Hemiptera: Aphididae) to imidacloprid. J. Entomol. Sci. 42:200-6
82. Landis WG, Matthews RA, Matthews GB. 1997. Design and analysis of multispecies toxicity tests for pesticide registration. Ecol. Appl. 7:1111-16
83. Larsen AE. 2013. Agricultural landscape simplification does not consistently drive insecticide use. PNAS 110:15330-35
84. Liang P, Tian Y-A, Biondi A, Desneux N, Gao X-W. 2012. Short-term and transgenerational effects of the neonicotinoid nitenpyram on susceptibility to insecticides in two whitefly species. Ecotoxicology 21:1889-98
85. Lima DB, Melo JWS, Guedes RNC, Siqueira HAA, Pallini A, Gondim MG Jr. 2013. Survival and behavioural response to acaricides of the coconut mite predator Neoseiulus baraki. Exp. Appl. Acarol. 60:381-93
86. Liu B, Wang Y, Kang B. 2014. Dynamics on a pest management SI model with control strategies of different frequencies. Nonlinear Anal. Hybrid Syst. 12:66-78
87. Liu N. 2015. Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annu. Rev. Entomol. 60:537-59
88. Lockwood JA, Sparks TC, Story RN. 1984. Evolution of insect resistance to insecticides: a reevaluation of the roles of physiology and behavior. Bull. Entomol. Soc. Am. 30:41-51
89. Lopes KVG, Silva LB, Reis AP,Oliveira MGA, Guedes RNC. 2010. Modified?-amylase activity among insecticide-resistant and-susceptible strains of the maize weevil, Sitophilus zeamais. J. Insect Physiol. 56:1050-57
90. Lu YH, Wu KM, Jiang YY, Guo YY, Desneux N. 2012. Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487:362-65
91. Luckey TD. 1968. Insecticide hormoligosis. J. Econ. Entomol. 61:7-12
92. Lundgren JG, Hesler LS, Clay SA, Fausti SF. 2013. Insect communities in soybeans of eastern South Dakota: the effects of vegetation management and pesticides on soybean aphids, bean leaf beetles, and their natural enemies. Crop Prot. 43:104-18
93. Maltby L. 1999. Studying stress: the importance of organism-level responses. Ecol. Appl. 9:431-40
94. Metcalf RL. 1980. Changing role of insecticides in crop protection. Annu. Rev. Entomol. 25:219-56
95. Misra JR, Horner M,LamG,ThummelCS. 2011. Transcriptional regulation of xenobiotic detoxification in Drosophila. Genes Dev. 25:1796-806
96. Monzo C, Qureshi JA, Stansly PA. 2014. Insecticide sprays, natural enemy assemblages and predation on Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae). Bull. Entomol. Res. 104:576-85
97. Morales JA, Cardoso DG, Della Lucia TMC, Guedes RNC. 2013. Weevil×insecticide: Does 'personality' matter? PLOS ONE 8(6):e67283
98. Muturi EJ, Costanzo K, Kesavaraju B, Alto BW. 2011. Can pesticides and larval competition alter susceptibility of Aedes mosquitoes (Diptera: Culicidae) to arbovirus infection? J. Med. Entomol. 48:429-36
99. Nash MA, Hoffmann AA, Thomson LJ. 2010. Identifying signature of chemical applications on indigenous and invasive nontarget arthropod communities in vineyards. Ecol. Appl. 20:1693-703
100. Navntoft S, Esbjerg P, Riedel W. 2006. Effects of reduced pesticide dosages on carabids (Coleoptera: Carabidae) in winter wheat. Agric. For. Entomol. 8:57-62
101. NayakMK, Collins PJ, Pavic H, Kopittke RA. 2003. Inhibition of egg development by phosphine in the cosmopolitan pest of stored products Liposcelis bostrychophila (Psocoptera: Liposcelididae). Pest Manag. Sci. 59:1191-96
102. Ndiath MO, Mazenot C, Sokhna C, Trape J-F. 2014. How the malaria vector Anopheles gambiae adapts to the use of insecticide-treated nets by African populations. PLOS ONE 9(6):e97700
103. Newman MC, Clements WH. 2008. Ecotoxicology: A Comprehensive Treatment. Boca Raton, FL: CRC Press
104. Oerke EC. 2006. Crop losses to pests. J. Agric. Sci. 144:31-43
105. Oliveira CM, Auad AM, Mendes SM, Frizzas MR. 2014. Crop losses and the economic impact of insect pests on Brazilian agriculture. Crop Prot. 56:50-54
106. Pékar S. 1999. Effect of IPM practices and conventional spraying on spider population dynamics in an apple orchard. Agric. Ecosyst. Environ. 73:155-66
107. Pickett AD. 1949. A critique on insect chemical control methods. Can. Entomol. 81:67-76
108. Pimentel MAG, Faroni LRA, Correa AS, Guedes RNC. 2012. Phosphine-induced walking response of the lesser grain borer (Rhyzopertha dominica). Pest Manag. Sci. 68:1368-73
109. Pontasch KW, Cairns J Jr. 1991. Multispecies toxicity tests using indigenous organisms: predicting the effect of complex effluents in streams. Arch. Environ. Contam. Toxicol. 20:103-12
110. Qin W, Tang S, Cheke RA. 2014. The effects of resource limitation on a predator-prey model with control measures as nonlinear pulses. Math. Prob. Eng. 2014:450935
111. Qu YY, Xiao D, Li JY, Chen Z, Biondi A, et al. 2015. Sublethal and hormesis effects of imidacloprid on the soybean aphid Aphis glycines. Ecotoxicology 24:479-87
112. Reitz SR, Trumble JT. 2002. Competitive displacement among insects and arachnids. Annu. Rev. Entomol. 47:435-65
113. RipperWE. 1956. Effect of pesticides on balance of arthropod populations. Annu. Rev. Entomol. 1:403-38
114. Roitberg BD, Gillespie DR. 2014. Natural enemies on the landscape-integrating life-history theory and landscapes. Biol. Control 75:39-47
115. Rondeau G, Sánchez-Bayo F, Tennekes HA, Decourtye A, Ram?rez-Romero R, Desneux N. 2014. Delayed and time-cumulative toxicity of imidacloprid in bees, ants and termites. Sci. Rep. 4:5566
116. Roubos CR, Rodriguez-Saona C, Isaacs R. 2014. Mitigating the effects of insecticides on arthropod biological control at field and landscape scales. Biol. Control 75:28-38
117. Schreinemachers P, Tipraqsa P. 2012. Agriculture pesticides and land use intensification in high, middle and low income countries. Food Policy 37:616-26
118. Shea K, Roxburgh SH, Rauschert ES. 2004. Moving from pattern to process: coexistence mechanisms under intermediate disturbance regimes. Ecol. Lett. 7:491-508
119. Simon S, Bouvier J-C, Debras J-F, Sauphanor B. 2010. Biodiversity and pest management in orchard systems. A review. Agron. Sustain. Dev. 30:139-52
120. Sjöberg P,RämertB,Thierfelder T, Hillbur. 2015. Ban of a broad-spectrum insecticide in apple orchards: effects on tortricid populations,management strategies, and fruit damage. J. Pest Sci. doi: 10. 1007/s10340-015-0648-0
121. Stark JD. 1992. Comparison of the impact of a neem seed-kernel extract formulation, Margosan-O and chlorpyrifos on non-target invertebrates inhabiting turf grass. Pestic. Sci. 36:293-99
122. Stark JD, Banks JE. 2003. Population-level effects of pesticides and other toxicants on arthropods. Annu. Rev. Entomol. 48:505-19
123. Stark JD, Banks JE, Vargas R. 2004. How risky is risk assessment: the role that life history strategies play in susceptibility of species to stress. PNAS 101:732-36
124. Stark JD, Tanigoshi L, Bounfour M, Antonelli A. 1997. Reproductive potential: its influence on the susceptibility of a species to pesticides. Ecotoxicol. Environ. Saf. 37:273-79
125. Stark JD, Vargas R, Banks JE. 2007. Incorporating ecologically relevant measures of pesticide effect for estimating the compatibility of pesticides and biocontrol agents. J. Econ. Entomol. 100:1027-32
126. Su Q, Oliver KM, Xie W, Wu Q, Wang S, Zhang Y. 2015. The whitefly-associated facultative symbiont Hamiltonella defensa suppresses induced plant defenses in tomato. Funct. Ecol. 29:1007-18
127. Su Q, Zhou X, Zhang Y. 2013. Symbiont-mediated functions in insect hosts. Commun. Integr. Biol. 6(3):e23804
128. Sun D-B, Liu Y-Q, Qin L, Xu J, Li F-F, Liu SS. 2013. Competitive displacement between two invasive whiteflies: insecticide application and host plant effects. Bull. Entomol. Res. 103:344-53
129. Tiwari S, Gondhalekar AD, Mann RS, Scharf ME, Stelinski LL. 2011. Characterization of five CYP4 genes from Asian citrus psyllid and their expression levels in Candidatus Liberibacter asiaticus-infected and uninfected psyllids. Insect Mol. Biol. 20:733-44
130. Tomé HVV, Cordeiro EMG, Rosado JF, Guedes RNC. 2012. Egg exposure to pyriproxyfen in the tomato leaf miner Tuta absoluta: ovicidal activity or behavioural-modulated hatching mortality? Ann. Appl. Biol. 160:35-42
131. Tomé HVV, Martins JC, Correa AS, Galdino TVS, Picanço MC, Guedes RNC. 2013. Azadirachtin avoidance by larvae and adult females of the tomato leafminer Tuta absoluta. Crop Prot. 46:63-69
132. Tomé HVV, Pascini TV, Dangelo RAC, Guedes RNC, Martins GF. 2014. Survival and swimming behavior of insecticide-exposed larvae and pupae of the yellow fever mosquito Aedes aegypti. Parasites Vectors 7:195
133. Torres JB, Ruberson JR. 2005. Canopy-and ground-dwelling predatory arthropods in commercial Bt and non-Bt cotton fields: patterns and mechanisms. Environ. Entomol. 34:1242-56
134. US Environ. Prot. Agency (EPA). 2014. Pesticides: Regulating Pesticides. Washington, DC: US EPA
135. US Environ. Prot. Agency (EPA). 2015. Biopesticides. Washington, DC: US EPA. http://www. epa. gov/pesticides/biopesticides/
136. Vilca Mallqui KS, Vieira JL, GuedesRNC,Gontijo LM. 2014. Azadirachtin-induced hormesis mediating shift in fecundity-longevity trade-off in the Mexican bean weevil (Chrysomelidae: Bruchinae). J. Econ. Entomol. 107:860-66
137. Villaverde JJ, Sevilla-Morán B, Sand?n-España P, López-Goti C, Alonso-Prados JL. 2014. Biopesticides in the framework of the European Pesticide Regulation (EC) No. 1107/2009. Pest Manag. Sci. 70:2-5
138. Vomesh JR, Kraus JM. 2009. Pesticide alters habitat selection and aquatic community composition. Oecologia 160:379-85
139. Welch KD, Harwood JD. 2014. Temporal dynamics of natural enemy-pest interactions in a changing environment. Biol. Control 75:18-27
140. Whalon ME, Mota-Sanchez D, Hollingworth RM. 2008. Global Pesticide Resistance in Arthropods. Wallingford, UK: CABI
141. Yan M, Li Y, Xiang Z. 2014. Time delayed stage-structured predator-prey model with birth pulse and pest control tactics. Abstr. Appl. Anal. 2014:1-15
142. Yu H, Li Y, Li X, Wu K. 2014. Arthropod abundance and diversity in transgenic Bt soybean. Environ. Entomol. 43:1124-34