The sublethal effects of pesticides on beneficial arthropods

Annual Review of Entomology

Volumn 52, Issue , 2007, Pages 81-106

  Desneux, Nicolas ^a   Decourtye, Axel ^b   Delpuech, Jean Marie ^c  

^a UNIVERSITY OF MINNESOTA   (United States)

^b VETAGRO SUP   (France)

^c UNIVERSITÉ LYON 1   (France)

Author keywords

Behavior; Ecotoxicology; Honey bee; Insecticide; Natural enemy

Indexed keywords

PESTICIDE;

ANIMAL; ANIMAL BEHAVIOR; ARTHROPOD; DRUG EFFECT; ECOSYSTEM; FERTILITY; INNATE IMMUNITY; INSECT CONTROL; LEARNING; LIFE CYCLE; LOCOMOTION; LONGEVITY; NERVOUS SYSTEM; ORIENTATION; POLLEN; REVIEW; SEX RATIO;

ANIMALS; ARTHROPODS; BEHAVIOR, ANIMAL; ECOSYSTEM; FERTILITY; IMMUNITY, NATURAL; INSECT CONTROL; LEARNING; LIFE CYCLE STAGES; LOCOMOTION; LONGEVITY; NERVOUS SYSTEM; ORIENTATION; PESTICIDES; POLLEN; SEX RATIO;

APINAE; APIS MELLIFERA; ARTHROPODA;

EID: 33846354297     PISSN: 00664170     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.ento.52.110405.091440     Document Type: Review

References (151)

1. Abramson CI, Squire J, Sheridan A, Mulder PG. 2004. The effect of insecticides considered harmless to honey bees (Apis mellifera): proboscis conditioning studies by using the insect growth regulators tebufenozide and diflubenzuron. Environ. Entomol. 33:378-88
2. Acheampong S, Stark JD. 2004. Effects of the agricultural adjuvant Sylgard 309 and the insecticide pymetrozine on demographic parameters of the aphid parasitoid, Diaeretiella rapae. Biol. Control 31:133-37
3. Ahmad M, Ossiewatsch HR, Basedow T. 2003. Effects of neem-treated aphids as food/hosts on their predators and parasitoids. J. Appl. Entomol. 127:458-64
4. Al-Deeb MA, Wilde GE, Zhu KY. 2001. Effects of insecticides used in corn, sorghum and alfalfa on the predator Onus insidiosus (Hemiptera: Anthocoridae). J. Econ. Entomol. 94:1353-60
5. Alix A, Cortesero AM, Nénon JP, Anger JP. 2001. Selectivity assessment of chlorfenvinphos reevaluated by including physiological and behavioral effects on an important beneficial insect. Environ. Toxicol. Chem. 20:2530-36
6. Amdam GV, Norberg K, Hagen A, Omholt SW. 2003. Social exploitation of vitellogenin. Proc. Natl. Acad. Sci. USA 100:1799-802
7. Armengaud C, Causse N, Ait-Oubah J, Ginolhac A, Gauthier M. 2000. Functional cytochrome oxidase histochemistry in the honeybee brain. Brain Res. 859:390-93
8. Armengaud C, Lambin M, Gauthier M. 2002. Effects of imidacloprid on the neural processes of memory in honey bees. See Ref. 48a, pp. 85-100
9. Armenia R, Martinez AM, Chapman JW, Magallanes R, Goulson D, et al. 2003. Impact of a nucleopolyhedrovirus bioinsecticide and selected synthetic insecticides on the abundance of insect natural enemies on maize in southern Mexico. J. Econ. Entomol. 96:649-61
10. Aupinel P, Fortini D, Dufour H, Taséi JN, Michaud B, et al. 2005. Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae. Bull. Insectol. 58:107-11
11. Banken JAO, Stark JD. 1998. Multiple routes of pesticide exposure and the risk of pesticides to biological controls: a study of neem and the sevenspotted lady beetle (Coleoptera: Coccinellidae). J. Econ. Entomol. 91:1-6
12. +-ATPase of emerging honeybees (Apis mellifera mellifera. L). Ecotoxicol. Environ. Safety 44:139-46
13. Bortolotti L, Sbrenna AM, Sbrenna G. 2005. Action of fenoxycarb on metamorphosis and cocoon spinning in Chrysoperla carnea (Neuroptera: Chrysopidae): identification of the JHA-sensitive period. Eur. J. Entomol. 102:27-32
14. 13a. Bos C, Masson C. 1983. Repellent effect of deltamethrin on honey bees. Agronomie 3:545-53
15. Brunner JF, Dunley JE, Doerr MD, Beers EH. 2001. Effects of pesticides on Colpoclypeus floras (Hymenoptera: Eulophidae) and Trichogramma platneri (Hymenoptera: Trichogrammatidae), parasitoids of leafrollers in Washington. J. Econ. Entomol. 94:1075-84
16. Candolfi MP, Bakker F, Cañez V, Miles M, Neumann C, et al. 1999. Sensitivity of non-target arthropods to plant protection products: Could Typhlodromus pyri and Aphidius spp. be used as indicator species? Chemosphere 39:1357-70
17. Candolfi MP, Barrett KL, Campbell P, Forster R, Grandy N, et al. 2001. Guidance document on regulatory testing and risk assessment procedures for plant protection products with non-target arthropods. In SETAC/ESCORT 2 Workshop Rep. 21-23, March 2000, Wageningen
18. Chandel RS, Gupta PR. 1992. Toxicity of diflubenzuron and penfluron to immature stages of Apis cerana indica F and Apis mellifera L. Apidologie 23:465-73
19. Charleston DS, Kfir R, Dicke M, Vet LEM. 2005. Impact of botanical pesticides derived from Melia azedarach and Azadirachta indica on the biology of two parasitoid species of the diamondback moth. Biol. Control 33:131-42
20. Claver MA, Ravichandran B, Khan MM, Ambrose DP. 2003. Impact of cypermethrin on the functional response, predatory and mating behaviour of a non-target potential biological control agent Acanthaspis pedestris (Stål) (Het., Reduviidae). J. Appl. Entomol. 127:18-22
21. Colin ME, Bonmatin JM, Moineau I, Gaimon C, Brun S, Vermandere JP. 2004. A method to quantify and analyze the foraging activity of honey bees: relevance to the sublethal effects induced by systemic insecticides. Arch. Environ. Contam. Toxicol. 47:387-95
22. Cônsoli FL, Parra JRP, Hassan SA. 1998. Side effects of insecticides used in tomato fields on the egg parasitoid Trichogramma pretiosum Riley (Hym., Trichogrammatidae), a natural enemy of Tuta absoluta (Meyrick)(Lep., Gelechiidae). J. Appl. Entomol. 122:43-47
23. Corrales N, Campos M. 2004. Population, longevity, mortality and fecundity of Chrysoperla carnea (Neuroptera, Chrysopidae) from olive orchards with different agricultural management systems. Chemosphere 57:1613-19
24. Cox RL, Wilson WT. 1987. The behavior of insecticide-exposed honey bees. Am. Bee J. 127:118-19
25. Croft BA. 1990. Arthropod Biological Control Agents and Pesticides. New York: Wiley. 723 pp.
26. Dechaume-Moncharmont FX. 2003. Butinage collectif chez l'abeille Apis mellifera L.: etude théorique et expérimentale. PhD thesis. Univ. Pierre-et-Marie-Curie, Paris. 309 pp.
27. Dechaume-Moncharmont FX, Decourtye A, Hennequet-Hantier C, Pons O, Pham-Delègue MH. 2003. Statistical analysis of honeybee survival after chronic exposure to insecticides. Environ. Toxicol. Chem. 22:3088-94
28. Decourtye A, Armengaud C, Renou M, Devillers J, Cluzeau S, et al. 2004. Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pestic. Biochem. Phys. 78:83-92
29. Decourtye A, Devillers J, Cluzeau S, Charreton M, Pham-Delègue MH. 2004. Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol. Environ. Safety 57:410-19
30. Decourtye A, Devillers J, Genecque E, Le Menach K, Budzinski H, et al. 2005. Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis mellifera. Arch. Environ. Contam. Toxicol. 48:242-50
31. Decourtye A, Lacassie E, Pham-Delègue MH. 2003. Learning performances of honeybees (Apis mellifera L.) are differentially affected by imidacloprid according to the season. Pest Manag. Sci. 59:269-78
32. Decourtye A, Pham-Delègue MH. 2002. The proboscis extension response: assessing the sublethal effects of pesticides on the honey bee. See Ref. 48a, pp. 67-84
33. Decourtye A, Tisseur M, Taséi JN, Pham-Delègue MH. 2005. Toxicité et risques liés à l'emploi de pesticides chez les pollinisateurs: cas de l'abeille domestique. In Enjeux Phytosanitaires pour L'agriculture et L'environnement au XXI Siècle, ed. C Regnault-Roger, pp. 283-99. Paris: Lavoisier. 1013 pp.
34. Delabie J, Bos C, Fonta C, Masson C. 1985. Toxic and repellent effects of cypermethrin on the honeybee: laboratory, glasshouse and field experiments. Pestic. Sci. 16:409-15
35. Delpuech JM, Bardon C, Boulétreau M. 2005. Increase of the behavioral response to kairomones by the parasitoid wasp Leptopilina heterotoma surviving insecticides. Arch. Environ. Contam. Toxicol. 49:186-91
36. Delpuech JM, Frey F, Carton Y. 1996. Action of insecticides on the cellular immune reaction of Drosophila melanogaster against the parasitoid Leptopilina boulardi. Environ. Toxicol. Chem. 15:2267-71
37. Delpuech JM, Froment B, Fouillet P, Pompanon F, Janillon S, Boulétreau M. 1998. Inhibition of sex pheromone communications of Trichogramma brassicae (Hymenoptera) by the insecticide chlorpyrifos. Environ. Toxicol. Chem. 17:1107-13
38. Delpuech JM, Gareau E, Terrier O, Fouillet P. 1998. Sublethal effects of the insecticide chlorpyrifos on the sex pheromonal communication of Trichogramma brassicae. Chemosphere 36:1775-85
39. Delpuech JM, Legallet B, Fouillet P. 2001. Partial compensation of the sublethal effect of delthamethrin on the sex pheromonal communication of Trichogramma brassicae. Chemosphere 42:985-91
40. Delpuech JM, Legallet B, Terrier O, Fouillet P. 1999. Modifications of the sex pheromonal communication of Trichogramma brassicae by a sublethal dose of deltamethrin. Chemosphere 38:729-39
41. Delpuech JM, Meyet J. 2003. Reduction in the sex ratio of the progeny of a parasitoid wasp (Trichogramma brassicae) surviving the insecticide chlorpyrifos. Arch. Environ. Contam. Toxicol. 45:203-8
42. Delpuech JM, Tekinel-Ozalp P. 1991. Epigenetic influences of insecticide on host-parasitoid relations. Redia 74:417-24
43. DeRuijter A, VanderSteen J. 1987. A field study on the effect on honeybee brood of insegar (fenoxycarb) applied on blooming apple orchards. Apidologie 18:356-57
44. Desneux N, Denoyelle R, Kaiser L. 2006. A multi-step bioassay to assess the effect of the deltamethrin on the parasitic wasp Aphidius ervi. Chemosphere 65:1697-706
45. Desneux N, Fauvergue X, Dechaume-Moncharmont FX, Kerhoas L, Ballanger Y, Kaiser L. 2005. Diaeretiella rapae limits Myzus persicae populations following applications of deltamethrin in oilseed rape. J. Econ. Entomol. 98:9-17
46. Desneux N, Pham-Delègue MH, Kaiser L. 2004. Effects of sublethal and lethal doses of lambda-cyhalothrin on oviposition experience and host searching behaviour of a parasitic wasp, Aphidius ervi. Pest Manag. Sci. 60:381-89
47. Desneux N, Rafalimanana H, Kaiser L. 2004. Dose-response relationship in lethal and behavioural effects of different insecticides on the parasitic wasp Aphidius ervi. Chemosphere 54:619-27
48. Desneux N, Ramirez-Romero R, Kaiser L. 2006. Multi-step bioassay to predict recolonization potential of emerging parasitoids after a pesticide treatment. Environ. Toxicol. Chem. 25:2675-82
49. Desneux N, Wajnberg E, Fauvergue X, Privet S, Kaiser L. 2004. Sublethal effects of a neurotoxic insecticide on the oviposition behaviour and the patch-time allocation in two aphid parasitoids, Diaeretiella rapae and Aphidius matricariae. Entomol. Exp. Appl. 112:227-35
50. 48a. Devillers J, Pham-Delègue MH, eds. 2002. Honey Bees: Estimating the Environmental Impact of Chemicals. London/New York: Taylor & Francis. 336 pp.
51. Dhadialla TS, Carlson GR, Le DP. 1998. New insecticides with ecdysteroidal and juvenile hormone activity. Annu. Rev. Entomol. 43:545-69
52. Dinter A, Poehling HM. 1995. Side effects of insecticides on two erigonid spider species. Entomol. Exp. Appl. 74:151-63
53. El Hassani AK, Dacher M, GauthierM, Armengaud C. 2005. Effects of sublethal doses of fipronil on the behavior of the honeybee (Apis mellifera). Pharmacol. Biochem. Behav. 82:30-39
54. 51a. Fahrbach SE. 2006. Structure of the mushroom bodies of the insect brain. Annu. Rev. Entomol. 51:209-32
55. 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
56. Galvan TL, Koch RL, Hutchison WD. 2005. Effects of spinosad and indoxacarb on survival, development and reproduction of the multicolored Asian lady beetle (Coleoptera: Coccinellidae). Biol. Control 34:108-14
57. George PJE, Ambrose DP. 1999. Insecticidal impact on the post-embryonic development of Rhynocoris kumarii Ambrose and Livingstone (Het., Reduviidae). J. Appl. Entomol. 123:509-12
58. George PJE, Ambrose DP. 1999. Post-embryonic developmental changes in non-target Rhynocoris fuscipes (Fabricius) (Insecta: Heteroptera: Reduviidae) by insecticides in cotton agroecosystem. J. Adv. Zool. 20:12-16
59. George PJE, Ambrose DP. 2004. Impact of insecticides on the haemogram of Rhynocoris kumarii Ambrose and Livingstone (Hem., Reduviidae). J. Appl. Entomol. 128:600-4
60. George PJE, Ambrose DP. 2004. Toxic effects of insecticides in the histomorphology of alimentary canal, testis and ovary in a reduviid Rhynocoris kumarii Ambrose and Livingstone (Hemiptera: Reduviidae). J. Adv. Zool. 25:46-50
61. Guez D, Suchail S, Gauthier M, Maleszka R, Belzunces LP. 2001. Contrasting effects of imidacloprid on habituation in 7- and 8-day-old honeybees (Apis mellifera). Neurobiol. Learn. Mem. 76:183-91
62. Gupta PR, Chandel RS. 1995. Effects of diflubenzuron and penfluron on workers of Apis cerana indica F. and Apis mellifera L. Apidologie 26:3-10
63. Hamilton GC, Lashomb JH. 1997. Effect of insecticides on two predators of the Colorado potato beetle (Coleoptera: Chrysomelidae). Fla. Entomol. 80:10-23
64. Haseeb M, Amano H. 2002. Effects of contact, oral and persistent toxicity of selected pesticides on Cotesia plutellae (Hym., Braconidae), a potential parasitoid of Plutella xylostella (Lep., Plutellidae). J. Appl. Entomol. 126:8-13
65. Haynes KF. 1988. Sublethal effects of neurotoxic insecticides on insect behavior. Annu. Rev. Entomol. 33:149-68
66. Hutchinson TP. 2000. Graphing the survivorship of bees. Insectes Soc. 47:292-96
67. Idris AB, Grafius E. 1993. Pesticides affect immature stages of Diadegma insulare (Hymenoptera, Ichneumonidae) and its host, the diamondback moth (Lepidoptera, Plutellidae). J. Econ. Entomol. 86:1203-12
68. Jaycox ER, Skowrone W, Guynn G. 1974. Behavioral changes in worker honey bees (Apis mellifera) induced by injections of a juvenile hormone mimic. Ann. Entomol. Soc. Am. 67:529-35
69. Jervis MA, Copland MJW. 1996. The life cycle. In Insect Natural Enemies: Practical Approaches to Their Study and Evaluation, ed. MA Jervis, N Kidd, pp. 63-102. London: Chapman & Hall
70. Jewess PJ, Lee PW, Nicholls PH, Plimmer JR. 1999. Benzoylureas. In Metabolic Pathways of Agrochemicals. Part 2: Insecticides and Fungicides, ed. TR Roberts, DH Hutson, pp. 795-816. Cambridge, UK: R. Soc. Chem.
71. Johansen CA, Mayer DF. 1990. Pollinator Protection. A Bee and Pesticide Handbook. New Haven, CT: Wicwas. 212 pp.
72. Jones WT. 1982. Sex-ratio and host size in a parasitoid wasp. Behav. Ecol. Sociobiol. 10:207-10
73. Kevan PG. 1991. Pollination: keystone process in sustainable global productivity. Acta Hortic. 288:103-10
74. Kevan PG. 1999. Pollinators as bioindicators of the state of the environment: species, activity and diversity. Agric. Ecosyst. Environ. 74:373-93
75. Kjaer C, Jepson PC. 1995. The toxic effects of direct pesticide exposure for a nontarget weed-dwelling chrysomelid beetle (Gastrophysa polygoni) in cereals. Environ. Toxicol. Chem. 14:993-99
76. Komeza N, Fouillet P, Boulétreau M, Delpuech JM. 2001. Modification, by the insecticide chlorpyrifos, of the behavioral response to kairomones of a Drosophila parasitoid, Leptopilina boulardi. Arch. Environ. Contam. Toxicol. 41:436-42
77. Kreissl S, Bicker G. 1989. Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee. J. Comp. Neurol. 286:71-84
78. Krespi L, Rabasse JM, Dedryver CA, Nenon JP. 1991. Effect of three insecticides on the life cycle of Aphidius uzbekistanicus Luz. (Hym., Aphidiidae). J. Appl. Entomol. 111:113-19
79. Kühner C, Klingauf F, Hassan SA. 1985. Development of laboratory and semi-field methods to test the side effect of pesticides on Diaeretiella rapae (Hym. Aphidiidae). Med. Fac. Landbouww. Rijksuniv. Gent 50:531-38
80. Kunkel BA, Held DW, Potter DA. 2001. Lethal and sublethal effects of bendiocarb, halofenozide, and imidacloprid on Harpalus pennsylvanicus (Coleoptera: Carabidae) following different modes of exposure in turfgrass. J. Econ. Entomol. 94:60-67
81. Lambin M, Armengaud C, Raymond S, Gauthier M. 2001. Imidacloprid induced facilitation of the proboscis extension reflex habituation in the honeybee. Arch. Insect Biochem. Physiol. 48:129-34
82. Lefort S, Tisseur M, Decourtye A. 2005. De la traçabilité même chez les butineuses! Bull. Tech. Apicole 32:153-64
83. Little EE. 1990. Behavioral toxicology: stimulating challenges for a growing discipline. Environ. Toxicol. Chem. 9:1-2
84. Liu TX, Chen TY. 2001. Effects of the insect growth regulator fenoxycarb on immature Chrysoperla rufilabris (Neuroptera: Chrysopidae). Fla. Entomol. 84:628-33
85. Liu TX, Stansly PA. 2004. Lethal and sublethal effects of two insect growth regulators on adult Delphastus catalinae (Coleoptera: Coccinellidae), a predator of whiteflies (Homoptera: Aleyrodidae). Biol. Control 30:298-305
86. Longley M, Jepson PC. 1996. Effects of honeydew and insecticide residues on the distribution of foraging aphid parasitoids under glasshouse and field conditions. Entomol. Exp. Appl. 81:189-98
87. Longley M, Jepson PC. 1996. The influence of insecticide residues on primary parasitoid and hyperparasitoid foraging behaviour in the laboratory. Entomol. Exp. Appl. 81:259-69
88. Malone LA, Tregidga EL, Todd JH, Burgess EPJ, Philip BA, et al. 2002. Effects of ingestion of a biotin-binding protein on adult and larval honey bees. Apidologie 33:447-58
89. Mamood A, Waller G. 1990. Recovery of learning responses by honeybees following a sublethal exposure to permethrin. Physiol. Entomol. 15:55-60
90. Mayer DF, Lunden JD. 1999. Field and laboratory tests of the effects of fipronil on adult female bees of Apis mellifera, Megachile rotundata and Nomia melanderi. J. Apic. Res. 38:191-97
91. Medina P, Budia F, Del Estal P, Vinuela E. 2004. Influence of azadirachtin, a botanical insecticide, on Chrysoperla carnea (Stephens) reproduction: toxicity and ultrastructural approach. J. Econ. Entomol. 97:43-50
92. Menzel R. 1999. Memory dynamics in the honeybee. J. Comp. Physiol. A 185:323-40
93. Menzel R, Greggers U, Hammer M. 1993. Functional organization of appetitive learning and memory in a generalist pollinator, the honey bee. In Insect Learning: Ecological and Evolutionary Perspectives, ed. DR Papaj, AC Lewis, pp. 79-125. New York: Chapman & Hall. 416 pp.
94. Menzel R, Müller U. 1996. Learning and memory in honeybees: from behavior to neural substrates. Annu. Rev. Neurosci. 19:379-404
95. Naumann K, Currie RW, Isman MB. 1994. Evaluation of the repellent effects of a neem insecticide on foraging honeybees and other pollinators. Can. Entomol. 126:225-30
96. OEPP/EPPO. 1992. Guideline on test methods for evaluating the side effects of plant protection products on honeybees. Bull. OEPP/EPPO 22:203-15
97. OEPP/EPPO. 2003. Environmental risk assessment scheme for plant protection products. Bull. OEPP/EPPO 33:141-45
98. Oomen PA, DeRuijter A, VanderSteen J. 1992. Method for honeybee brood feeding tests with insect growth-regulating insecticides. Bull. OEPP/EPPO 22:613-16
99. O'Toole C. 1996. Bee systematics in Europe: the continuing crisis and some possible cures. In The Conservation of Bees, ed. A Matheson, SL Buchmann, C O'Toole, P Westrich, IH Williams, pp. 227-32. London: Academic. 254 pp.
100. Papaefthimiou C, Theophilidis G. 2001. The cardiotoxic action of the pyrethroid insecticide deltamethrin, the azole fungicide prochloraz, and their synergy on the semi-isolated heart of the bee Apis mellifera macedonica. Pestic. Biochem. Phys. 69:77-91
101. Pilling ED, Bromleychallenor KAC, Walker CH, Jepson PC. 1995. Mechanism of synergism between the pyrethroid insecticide lambda-cyhalothrin and the imidazole fungicide prochloraz, in the honeybee (Apis mellifera L.). Pestic. Biochem. Physiol. 51:1-11
102. Pinto LZ, Bitondi MMG, Simoes ZLP. 2000. Inhibition of vitellogenin synthesis in Apis mellifera workers by a juvenile hormone analogue, pyriproxyfen. J. Insect. Physiol. 46:153-60
103. Polonsky J, Bhatnagar SC, Griffitsh DC, Pickett JA, Woodcock CM. 1989. Activity of quassinoids as antifeedants against aphids. J. Chem. Ecol. 15:993-98
104. Qi BY, Gordon G, Gimme W. 2001. Effects of neem-fed prey on the predacious insects Harmonia conformis (Boisduval) (Coleoptera: Coccinellidae) and Mallada signatus (Schneider) (Neuroptera: Chrysopidae). Biol. Control 22:185-90
105. Rafalimanana H, Kaiser L, Delpuech JM. 2002. Stimulating effects of the insecticide chlorpyrifos on host searching and infestation efficacy of a parasitoid wasp. Pest Manag. Sci. 58:321-28
106. Reingold SC, Camhi JM. 1978. Abdominal grooming in cockroach: development of an adult behavior. J. Insect Physiol. 24:101-10
107. Reynolds DR, Riley JR. 2002. Remote-sensing, telemetric and computer-based technologies for investigating insect movement: a survey of existing and potential techniques. Comput. Electron. Agric. 35:271-307
108. Richards KW. 1993. Non-Apis bees as crop pollinators. Rev. Suisse Zool. 100:807-22
109. Rieth JP, Levin MD. 1988. The repellent effect of two pyrethroid insecticides on the honeybee. Physiol. Entomol. 13:213-18
110. Rosenheim JA, Hoy MA. 1988. Sublethal effects of pesticides on the parasitoid Aphytis melinus (Hymenoptera: Aphelinidae). J. Econ. Entomol. 81:476-83
111. Rumpf S, Frampton C, Dietrich DR. 1998. Effects of conventional insecticides and insect growth regulators on fecundity and other life-table parameters of Micromus tasmaniae (Neuroptera: Hemerobiidae). J. Econ. Entomol. 91:34-40
112. Rumpf S, Hetzel F, Frampton C. 1997. Lacewings (Neuroptera: Hemerobiidae and Chrysopidae) and integrated pest management: enzyme activity as biomarker of sublethal insecticide exposure. J. Econ. Entomol. 90:102-8
113. Saber M, Hejazi MJ, Kamali K, Moharramipour S. 2005. Lethal and sublethal effects of fenitrothion and deltamethrin residues on the egg parasitoid Trissolcus grandis (Hymenoptera: Scelionidae). J. Econ. Entomol. 98:35-40
114. Salerno G, Colazza S, Conti E. 2002. Sub-lethal effects of deltamethrin on walking behaviour and response to host kairomone of the egg parasitoid Trissolcus basalts. Pest Manag. Sci. 58:663-68
115. 111a. Schmid-Hempel P. 2005. Evolutionary ecology of insect immune defenses. Annu. Rev. Entomol. 50:529-51
116. Schmuck R. 1999. No causal relationship between Gaucho seed dressing in sunflowers and the French bee symptome. Pflanzenschutz Nachrichten Bayer 52:257-99
117. Schmuck R. 2004. Effects of a chronic dietary exposure of the honeybee Apis mettifera (Hymenoptera: Apidae) to imidacloprid. Arch. Environ. Contam. Toxicol. 47:471-78
118. Schneider MI, Smagghe G, Gobbi A, Vinuela E. 2003. Toxicity and pharmacokinetics of insect growth regulators and other novel insecticides on pupae of Hyposoter didymator (Hymenoptera: Ichneumonidae), a parasitoid of early larval instars of lepidopteran pests. J. Econ. Entomol. 96:1054-65
119. Schneider MI, Smagghe G, Pineda S, Vinuela E. 2004. Action of insect growth regulator insecticides and spinosad on life history parameters and absorption in third-instar larvae of the endoparasitoid Hyposoter didymator. Biol. Control 31:189-98
120. Singh SR, Walters KFA, Port GR, Northing P. 2004. Consumption rate and predatory activity of adult and fourth instar larvae of the seven spot ladybird, Coccinella septempunctata (L.), following contact with dimethoate residue and contaminated prey in laboratory arenas. Biol. Control 30:127-33
121. Smallman BN, Mansingh A. 1969. Cholinergic system in insect development. Annu. Rev. Entomol. 14:387-408
122. Stapel JO, Cortesero AM, Lewis WJ. 2000. Disruptive sublethal effects of insecticides on biological control: altered foraging ability and life span of a parasitoid after feeding on extrafloral nectar of cotton treated with systemic insecticides. Biol. Control 17:243-49
123. Stark JD, Banken JAO. 1999. Importance of population structure at the time of toxicant exposure. Ecotoxicol. Environ. Safety 42:282-87
124. Stark JD, Banks JE. 2003. Population-level effects of pesticides and other toxicants on arthropods. Annu. Rev. Entomol. 48:505-19
125. Stark JD, Vargas R, Miller N. 2004. Toxicity of spinosad in protein bait to three economically important tephritid fruit fly species (Diptera: Tephritidae) and their parasitoids (Hymenoptera: Braconidae). J. Econ. Entomol. 97:911-15
126. Stone J, Abramson C, Price J. 1997. Task-dependent effects of dicofol (Kelthane) on learning in the honey bee (Apis mellifera). B. Environ. Contam. Toxicol. 58:177-83
127. Streit S, Bock F, Pirk CWW, Tautz J. 2003. Automatic life-long monitoring of individual insect behaviour now possible. Zoology 106:169-71
128. Suchail S, Guez D, Belzunces LP. 2001. Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environ. Toxicol. Chem. 20:2482-86
129. Takeda K. 1961. Classical conditioned response in the honey bee. J. Insect Physiol. 6:168-79
130. Taséi JN, Lerin J, Ripault G. 2000. Sub-lethal effects of imidacloprid on bumblebees, Bombus teirestris (Hymenoptera: Apidae), during a laboratory feeding test. Pert Manag. Sci. 56:784-88
131. Taséi JN, Sabik H, Pirastru L, Langiu E, Blanche JM, et al. 1994. Effects of sublethal doses of deltamethrin (Decis ce) on Bombus terrestris. J. Apic. Res. 33:12 9-3 5
132. Thompson HM. 2003. Behavioural effects of pesticides in bees: their potential for use in risk assessment. Ecotoxicology 12:317-30
133. Tran DH, Takagi M, Takasu K. 2004. Effects of selective insecticides on host searching and oviposition behavior of Neochrysocharis formosa (Westwood) (Hymenoptera: Eulophidae), a larval parasitoid of the American serpentine leafminer. Appl. Entomol. Zool. 39:435-41
134. Umoru PA, Powell W, Clark SJ. 1996. Effect of pirimicarb on the foraging behaviour of Diaeretiella rapae (Hymenoptera: Braconidae) on host-free and infested oilseed rape plants. Bull. Entomol. Res. 86:193-201
135. Van Driesche RG, Bellows TS. 1996. Biological Control. New York: Chapman & Hall. 539 pp.
136. Van Erp S, Booth L, Gooneratne R, O'Halloran K. 2002. Sublethal responses of wolf spiders (Lycosidae) to organophosphorus insecticides. Environ. Toxicol. 17:449-56
137. Vandame R, Belzunces LP. 1998. Joint actions of deltamethrin and azole fungicides on honey bee thermoregulation. Neurosci. Lett. 251:57-60
138. Vandame R, Meled M, Colin ME, Belzunces LP. 1995. Alteration of the homing-flight in the honey bee Apis mellifera L. exposed to sublethal dose of deltamethrin. Environ. Toxicol. Chem. 14:855-60
139. Vet LEM, Dicke M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37:141-72
140. Viggiani G. 1984. Bionomics of the Aphelinidae. Annu. Rev. Entomol. 29:257-76
141. Villa S, Vighi M, Finizio A, Serini GB. 2000. Risk assessment for honeybees from pesticide-exposed pollen. Ecotoxicology 9:287-97
142. Visscher PK, Dukas R. 1997. Survivorship of foraging honey bees. Insectes Soc. 44:1-5
143. Von Frisch K. 1967. The Dance Language and Orientation of Bees. Cambridge, MA: Harvard Univ. Press. 566 pp.
144. Wackers FL, Lewis WJ. 1999. A comparison of color-, shape- and pattern-learning by the hymenopteran parasitoid Microplitis croceipes. J. Comp. Physiol. A 184:387-93
145. Walthall WK, Stark JD. 1997. Comparison of two population-level ecotoxicological endpoints: the intrinsic (rm) and instantaneous (ri) rates of increase. Environ. Toxicol. Chem. 16:1068-73
146. Weick J, Thorn RS. 2002. Effects of acute sublethal exposure to coumaphos or diazinon on acquisition and discrimination of odor stimuli in the honey bee (Hymenoptera: Apidae)_ J. Econ. Entomol. 95:227-36
147. Wiles JA, Jepson PC. 1993. The dietary effects of deltamethrin upon Nebria brevicollis (F.) (Coleoptera: Carabidae). Pestic. Sci. 38:329-34
148. Wiles JA, Jepson PC. 1994. Sub-lethal effects of deltamethrin residues on the within-crop behaviour and distribution of Coccinella septempunctata. Entomol. Exp. Appl. 72:33-45
149. Wong-Riley MTT. 1989. Cytochrome oxidase: an endogenous metabolic marker of neuronal activity. Trends Neurosci. 12:94-101
150. Zanuncio TV, Serrao JE, Zanuncio JC, Guedes RNC. 2003. Permethrin-induced hormesis on the predator Supputius cincticeps (Stål, 1860) (Heteroptera: Pentatomidae). Crop Prot. 22:941-47
151. Zhang SW, Lehrer M, Srinivasan MV. 1999. Honeybee memory: navigation by associative grouping and recall of visual stimuli. Neurobiol. Learn. Mem. 72:180-201