Behavioural effects of pesticides in bees - Their potential for use in risk assessment

Ecotoxicology

Volumn 12, Issue 1-4, 2003, Pages 317-330

  Thompson, Helen M ^a  

^a CENTRAL SCIENCE LABORATORY   (United Kingdom)

Author keywords

Honey bees; Pesticides; Risk assessment; Sublethal

Indexed keywords

INSECTICIDE; PESTICIDE;

BEE; BEHAVIORAL RESPONSE; CHEMICAL POLLUTANT; PESTICIDE; RISK ASSESSMENT; SUBLETHAL EFFECT;

ANIMAL BEHAVIOR; BEHAVIOR DISORDER; CONDITIONED REFLEX; ENVIRONMENTAL EXPOSURE; FORAGING BEHAVIOR; HONEYBEE; NONHUMAN; OLFACTORY DISCRIMINATION; POPULATION MODEL; PREDICTION; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; SURVIVAL;

ANIMALS; BEES; BEHAVIOR, ANIMAL; ENVIRONMENTAL POLLUTANTS; INSECTICIDES; POPULATION DYNAMICS; RISK ASSESSMENT; SURVIVAL;

ANIMALIA; APIDAE; APINAE; APIS MELLIFERA; APOIDEA; HYMENOPTERA;

EID: 0037307389     PISSN: 09639292     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1022575315413     Document Type: Review

References (72)

1. Atkins, E.L. and Kellum, D. (1986). Comparative morphogenic and toxicity studies on the effect of pesticides on honeybee brood. J. Apicult. Res. 25, 242-55.
2. Atkins, E.L., Macdonald, R.L. and Greywood-Hale, E.A. (1975a). Repellent additives to reduce pesticide hazards to honey bees: field tests. Environ. Entomol. 4, 207-10.
3. Atkins, E.L., Macdonald, R.L., McGovern, T.P., Beroza, M. and Greywood-Hale, E.A. (1975b). Repellent additives to reduce pesticide hazards to honey bees: laboratory testing. J. Apicult. Res. 14, 85-97.
4. Barker, R.J. and Taber, S. (1977). Effects of diflubenzuron fed to caged honey bees. Environ. Entomol. 6, 167-8.
5. Belzunces, L.P., Vandame, R. and Xingfa Gu. (2001). Joint effects of pyrethrinoid insecticides and azole fungicides on honeybee thermoregulation. In L.P. Belzunces, C. Pelissier and G.B. Lewis (eds) Hazards of Pesticides to Bees, pp. 297-8. France: INRA.
6. Bendahou, N., Fleche, C. and Bounias, M. (1999). Biological and biochemical effects of chronic exposure to very low levels of dietary cypermethrin (Cymbush) on honeybee colonies (Hymenoptera: Apidae). Ecotoxicol. Environ. Saf. 44, 147-53.
7. Breed, M.D., Stiller, T.M., Blum, M.S. and Page, E.R. Jr (1992). Honeybee nestmate recognition: effects of queen fecal pheromones. J. Chem. Ecol. 18, 1633-40.
8. Bromenshenk, J.J., Cronn, R.C. and Nugent, J.J. (1996). Monitoring fluoride with honey bees in the upper Snake River Plain of Idaho. J. Environ. Qual. 25, 868-77.
9. Bromenshenk, J.J., Doskocil, J., Olbu, G.J., DeGrandi-Hoffman, G. and Roth, S.A. (1991a). PC BEEPOP, an ecotoxicological simulation-model for honey-bee populations. Environ. Toxicol. Chem. 10, 547-58.
10. Bromenshenk, J.J., Gudatis, J.L., Carlson, S.R., Thomas, J.M. and Simmons, M.A. (1991b). Population-dynamics of honey-bee nucleus colonies exposed to industrial pollutants. Apidologie 22, 359-69.
11. Chandel, R.S. and Gupta, P.R. (1992). Toxicity of diflubenzuron and penfluron to immature stages of Apis cerana indica and Apis mellifera L. Apidologie 23, 465-73.
12. Cox, R.L. and Wilson, W.T. (1984). Effects of permethrin on the behavior of individually tagged honey bees, Apis mellifera L. (Hymenoptera: Apidae). Environ. Entomol. 13, 375-8.
13. Davis, A.R., Solomon, K.R. and Shuel, R.W. (1988). Laboratory studies of honeybee larval growth and development as affected by systemic insecticides at adult sub-lethal levels. J. Apicult. Res. 27, 146-61.
14. De Wael, L., De Greef, M. and Van Laere, O. (1995). Toxicity of pyriproxifen and fenoxycarb to bumble bee brood using a new method for testing insect growth regulators. J. Apicult. Res. 34, 3-8.
15. Decourtye, A., Le Metayer, M., Pottiau, H., Tissuer, M., Odoux, J.F. and Pham-Delegue, M.H. (1999). Impairment of olfactory learning performances in the honeybee after long term ingestion of imidacloprid. In L.P. Belzunces, C. Pelissier and G.B. Lewis, (eds) Hazards of Pesticides to Bees, pp. 113-17. France: INRA.
16. Delabie, J., Bos, C., Fonta, C. and Masson, C. (1985). Toxic and repellent effects of cypermethrin on the honeybee: laboratory, glasshouse and field experiments. Pesti. Sci. 16, 409-15.
17. Deng, G. and Waddington, K.D. (1997). Methoprene does not affect food preferences and foraging performance in honey bee workers. J. Insect. Behav. 10, 229-35.
18. Downs, S.G., Ratnieks, F.L.W., Jefferies, S.L. and Rigby, H.E. (2000). The role of floral oils in the nestmate recognition system of honey bees (Apis mellifera L.). Apidologie 31, 357-65.
19. Ebadi, R., Gary, N.E. and Lorenzen, K. (1980). Effects of carbon dioxide and low temperature narcosis on honey bees, Apis mellifera. Environ. Entomol. 9, 144-7.
20. EPA (Draft 1996). Honey bee acute contact toxicity. Ecological Effects Test Guidelines OPPTS 850.3020, USEPA.
21. EPPO (1992). Guideline on test methods for evaluating the side-effects of plant protection products on honeybees. Bull. OEPP/EPPO Bull. 22, 203-16.
22. EPPO (1993). Decision making scheme for the environmental risk assessment of plant protection products. Chapter 10 Honeybees. Bull. OEPP/EPPO Bull. 23, 151-65.
23. Goulson, D. and Stout, J.C. (2001). Homing ability of the bumble bee Bombus terrestris (Hymenoptera: Apidae). Apidologie 32, 105-11.
24. Guez, D., Suchail, S., Gauthier, M., Maleszka, R. and Belzunces, L.P. (2001). Contrasting effects of imidacloprid on habituation in 7- and 8-day-old honeybees (Apis mellifera). Neurobiol. Learn. Mem. 76, 183-91.
25. Gupta, P.R. and Chandel, R.S. (1995). Effects of diflubenzuron and penfluron on workers of Apis cerana indica F and Apis mellifera L. Apidologie 26, 3-10.
26. Haynes, K.F. (1988). Sublethal effects of neurotoxic insecticides on insect behavior. Annual Rev. Entomol. 33, 149-68.
27. Jay, S.C. (1964). Starvation studies of larval honey bees. Can. J. Zool. 42, 455-62.
28. Jaycox, E.R., Skowronek, W. and Guynn, G. (1974). Behavioral changes in worker honey bees (Apis mellifera) induced by injections of juvenile hormone mimic. Ann. Entomolog. Soc. America 67, 529-34.
29. Kevan, P.G. (1999). Pollinators as bioindicators of the state of the environment: species activity and diversity. Agricult. Ecosyst. Environ. 74, 373-93.
30. Koch, W. and Weiber, P. (1997). Exposure of honey bees during pesticide application under field conditions. Apidologie 28, 439-47.
31. Kirchner, W.H. (1998). The effect of sublethal doses of imidachloprid on the foraging behaviour and orientation ability of honeybees. Unpublished Stdy Report, Konstanz, 13pp.
32. Le Blanc, J. (1985). Field experiments and the effects of a new pyrethroid insecticide WL-85871 on bees foraging artificial aphid honeydew on winter wheat. Pestic. Sci. 16, 206.
33. MacKenzie, K.E. and Winston, M.L. (1989). Effects of sublethal exposure to diazinon on longevity and temporal division of labor in the honey bee (Hymenoptera: Apidae). J. Econom. Entomol. 82, 75-82.
34. Mamood, A.N. and Waller, G.D. (1990). Recovery of learning responses by honeybees following sublethal exposure to permethrin. Physiol. Entomol. 15, 55-60.
35. Mayer, D.F., Kovacs, G. and Lunden, J.D. (1998). Field and laboratory tests on the effects of cyhalothrin on adults of Apis mellifera, Megachile rotundata and Nomia melanderi. J. Apicult. Res. 37, 33-7.
36. Mayer, D.F. and Lunden, J.D. (1999). Field and laboratory tests of the effects of fipronil on adult female bees of Apis mellifera, Megachile rotundata and Nomia melanderi. J. Apicult. Res. 38, 191-7.
37. Menzel, R. (1993). Associative learning in honey bees. Apidologie 24, 157-68.
38. Menzel, R., Geiger, K., Joerges, J., Muller, U. and Chittka, L. (1998). Bees travel homeward routes by integrating separately acquired vector memories. Anim. Behav. 55, 139-52.
39. Moriarty, F. (1969). The sublethal effects of synthetic insecticides on insects. Biologic. Rev. 44, 321-57.
40. Nation, J.L., Robinson, F.A., Yu, S.J. and Bolten, A.B. (1986). Influence upon honeybees of chronic exposure to very low levels of selected insecticides in their diet. J. Apicult. Res. 25, 170-7.
41. Naumann, K., Currie, R.W. and Isman, M.B. (1994). Evaluation of the repellent effects of a neem insecticide on foraging honey bees and other pollinators. Can. Entomolog. 126, 225-30.
42. Nigg, H.N., Russ, R.V., Mahon, W.D., Stamper, J.H. and Knapp, J.L. (1991). Contamination of sucrose solution with aldicarb sulfoxide inhibits foraging by honeybees (Hymenoptera: Apidae). J. Econom. Entomol. 84, 810-3.
43. NRCC. (1981). Pseticide-Pollinator Interactions, NRCC/CNRC Ottawa, Publication No. 18471, 190pp.
44. OECD (1998a). Guidelines for the testing of chemicals Number 213 Honeybees, Acute Oral Toxicity Test, OECD. Environmental Health and Safety Division, Paris.
45. OECD (1998b). Guidelines for the testing of chemicals Number 214 Honeybees, Acute Contact Toxicity Test, OECD. Environmental Health and Safety Division, Paris.
46. Oomen, P.A., De Ruijter, A. and van der Steen, J. (1992). Method for honeybee brood feeding tests with insect growth-regulating insecticides. Bull. OEPP/EPPO Bull. 22, 613-16.
47. Pajot, S. (2001). Dossier Gaucho. Abielles et Fleurs 616, 160-5.
48. Pham-Delegue, M.H., Girard, C., Le Metayer, M, Picard-Nizou, A.-L., Hennequet, C., Pons, O. and Jouanin, L. (2000). Long-term effects of soybean protease inhibitors on digestive enzymes, survival and learning abilities of honeybees. Entomolog. Experiment. Appli. 95, 21-9.
49. Rieth, J.P. and Levin, M.D. (1988). The repellent effect of two pyrethroid insecticides on the honey bee. Physiol. Entomol. 13, 213-18.
50. Rieth, J.P. and Levin, M.D. (1989). Repellency of two phenyl-acetate-ester pyrethroids to the honeybee. J. Apicult. Res. 28, 175-9.
51. Robinson, G.E. (1985). Effects of a juvenile hormone analogue on honey bee foraging behaviour and alarm pheromone production. J. Insect Physiol. 31, 277-82.
52. Schmuck, R. (1999). No causal relationship between Gaucho seed dressing in sunflowers and the French bee syndrome. Pflanzenschutz-Nachrichten Bayer 52(99), 257-99.
53. Schmuck, R., Schoning, R., Stork, A. and Schramel, O. (2001). Risk posed to honeybees (Apis mellifera L., Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Manag. Sci. 57, 225-38.
54. Schricker, B. and Stephen, W.P. (1970). The effect of sublethal doses of parathion on honeybee behaviour. I. Oral adminstration and the communication dance. J. Apicult. Res. 9, 141-53.
55. Shires, S.W., Le Blanc, J., Murray, A., Forbes, S. and Debray, P. (1984). A field trial to assess the effects of a new pyrethroid insecticide, WL85871, on foraging honeybees in oilseed rape. J. Apicult. Res. 23, 217-26.
56. Smirle, M.J. (1993). The influence of colony population and brood rearing intensity on the activity of detoxifying enzymes in worker honey bees. Physiol. Entomol. 18, 420-4.
57. Solomon, M.G. and Hooker, K.J.M. (1989). Chemical repellents for reducing pesticide hazard to honeybees in apple orchards. J. Apicult. Res. 28, 223-7.
58. Stephen, W.P. and Schricker, B. (1970). The effect of sublethal doses of parathion II Site of parathion activity, and signal integration. J. Apicult. Res. 9, 155-64.
59. Stone, J.C., Abramson, C.I. and Price, J.M. (1997). Task dependent effects of Dicofol (Kelthane) on learning in the honey bee (Apis mellifera). Bull. Environ. Contam. Toxicol. 58, 177-83.
60. Stoner, A. and Wilson, W.T. (1982). Diflubenzuron (Dimilin): effect of long-term feeding of low doses in sugar cake or sucrose syrup on honey bees in standard-size field colonies. Amer. Bee J. 122, 579-82.
61. Stoner, A., Wilson, W.T. and Harvey, J. (1983). Dimethoate (Cygon): effect of long-term feeding of low doses on honey bees in standard size field colonies. The Southwestern Entomolog. 8, 174-7.
62. Stoner, A., Wilson, W.T. and Harvey, J. (1985). Acephate (Orthene): effects on honey bee queen, brood and worker survival. Amer. Bee J. 125, 448-50.
63. Stoner, A., Wilson, W.T. and Rhodes, H.A. (1982). Carbofuran: effect of long-term feeding of low doses in sucrose syrup on honey bees in standard-size field colonies. Environ. Entomol. 11, 53-9.
64. Suchail, S., Guez, D. and Belzunces, L.P. (2000). Characteristics of Imidacloprid toxicity in two Apis mellifera subspecies. Environ. Toxicol. Chem. 19, 1901-5.
65. Tasei, J.N. (2001). Effects of insect growth regulators on honey bees and non-apis bees. A review. Apidologie 32, 527-45.
66. Tasei, J.N., Carre, S., Moscatelli, B. and Grondeau, C. (1988). Recherche de la D L 50 de la deltamethrine (Decis) chez Megachile Rotundata F. abeille pollinisatrice de la luzerne (Medicago sativa L.) et des effets de doses infralethales sur les adultes et les larves. Apidologie 19, 291-306.
67. Tasei, J.N., Lerin, J. and Ripault, G. (2000). Sub-lethal effects of imidacloprid on bumblebees, Bombus terrestris (Hymenoptera: Apidae) during a laboratory feeding test. Pest Manag. Sci. 56, 784-8.
68. Tasei, J.N., Ripault, G. and Rivault, E. (2001). Effects of Gaucho seed coating on bumblebees visiting sunflower. In L.P. Belzunces, C. Pelissier and G.B. Lewis (eds) Hazards of Pesticides to Bees, pp. 207-12. France: INRA.
69. Taylor, K.S., Waller, G.D. and Crowder, L.A. (1987). Impairment of a classical conditioned response of the honey bee (Apis mellifera L.) by sublethal doses of synthetic pyrethroid insecticides. Apidologie 18, 243-52.
70. Vandame, R., Meled, M., Colin, M.E. and Belzunces, L.P. (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.
71. Waller, G.D., Barker, R.J. and Martin, J.H. (1979). Effects of dimethoate on honeybee foraging. Chemosphere 7, 461-3.
72. Winston, M.L. and Punnett, E.N. (1982). Factors affecting temporal division of labour in honeybees. Can. J. Zool. 60, 2947-52.