Ecotoxicity of neonicotinoid insecticides to bees

Advances in Experimental Medicine and Biology

Volumn 683, Issue , 2010, Pages 85-95

  Decourtye, Axel ^a   Devillers, James ^b  

^a ACTA   (France)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ACETAMIPRID; ALKENE; CLOTHIANIDIN; DINOTEFURAN; IMIDACLOPRID; INSECTICIDE; NEONICOTINOID; NITENPYRAM; THIACLOPRID; THIAMETHOXAM; UNCLASSIFIED DRUG;

ACUTE TOXICITY; ANIMAL BEHAVIOR; BEHAVIORAL SCIENCE; CHRONIC TOXICITY; ECOTOXICITY; FORAGING BEHAVIOR; HONEYBEE; IMMOBILIZATION; LARVA; LD 50; LEARNING; NEUROTOXICITY; NONHUMAN; ORIENTATION; PRIORITY JOURNAL; REVIEW; SURVIVAL RATE; TOXICITY TESTING; ANIMAL; BEE; CHEMISTRY; DRUG EFFECT; ECOTOXICOLOGY; SURVIVAL;

APOIDEA;

ANIMALS; BEES; BEHAVIOR, ANIMAL; ECOTOXICOLOGY; INSECTICIDES; SURVIVAL ANALYSIS;

EID: 79958023734     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4419-6445-8_8     Document Type: Review

References (73)

1. Klein AM, Vaissière B, Cane JH et al. Importance of crop pollinators in changing landscapes for world crops. Proc R Soc Lond B Biol Sci 2007; 274:303-313. (Pubitemid 47055453)
2. Williams IH. The dependence of crop production within the European Union on pollination by honey bees. Agric Zool Rev 1994; 6:229-257.
3. Goulson D, Lye GC, Darvill B. Decline and conservation of bumble bees. Annu Rev Entomol 2008; 53:11.1-11.18.
4. Biesmeijer JC, Roberts SPM, Reemer M et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 2006; 313:351-354. (Pubitemid 44480959)
5. Committee on the Status of Pollinators in North America. Status of Pollinators in North America 2006.
6. Allen-Wardell G, Bernhardt P, Bitner R et al. The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conserv Biol 1998; 12:8-17. (Pubitemid 28153802)
7. Cluzeau S. Risk assessment of plant protection products on honey bees. In: Devillers J, Pham-Delègue MH, eds. Honey Bees: Estimating the Environmental Impact of Chemicals. London: Taylor and Francis 2002:42-55.
8. European and Mediterranean Plant Protection Organism. Guideline on test methods for evaluating the side-effects of plant protection products on honey bees. EPPO Bull 1992; 22:203-215.
9. Maus C, Curé G, Schmuck R. Safety of imidacloprid seed dressings to honey bees: A comprehensive overview and compilation of the current state of knowledge. Bull Insect 2003; 56(1):51-57.
10. Maxima L, van der Sluijs JP. Uncertainty: Cause or effect of stakeholders' debates?: Analysis of a case study: The risk for honeybees of the insecticide Gaucho®. Sci Total Environ 2007; 376(1-3):1-17.
11. Stark JD, Jepson PC, Mayer DF. Limitation to use of topical toxicity data for prediction of pesticide side effect in the field. J Econ Entomol 1995; 88:1081-1088.
12. Suchail S, Guez D, Belzunces LP. Characteristics of imidacloprid toxicity in two Apis mellifera subspecies. Environ Toxicol Chem 2000; 19:1901-1905. (Pubitemid 30399751)
13. Atkins EL, Kellum D, Atkins KW. Reducing pesticide hazards to honey bees: Mortality prediction techniques and integrated management strategies. Division of Agricultural Sciences University of California USA 1981; 3-22.
14. Mayer DF, Johansen CA. How to reduce bee poisoning from pesticides, Pacific Northwest Extension Publication, PNW 1999; 518:14.
15. Devillers J, Decourtye A, Budzinski H et al. Comparative toxicity and hazards of pesticides to Apis and non-Apis bees. A chemometrical study, SAR QSAR Environ Res 2003; 14:389-403. (Pubitemid 37458084)
16. Suchail S, Debrauwer L, Belzunces LP. Metabolism of imidacloprid in Apis mellifera. Pest Manag Sci 2003; 60:291-296. (Pubitemid 38268800)
17. Nauen R, Ebbinghaus-Kintscher U, Elbert A et al. Acetylcholine receptors as sites for developing neonicotinoid insecticides. In: Ishaaya I ed. Biochemical sites important in insecticide action and resistance, Springer Verlag Berlin 2001; 77-105.
18. Guez D, Belzunces LP, Maleszka R. Effects of imidacloprid metabolites on habituation in honeybees suggest the existence of two subtypes of nicotinic receptors differentially expressed during adult development. Pharmacol Biochem Behav 2003; 75:217-222. (Pubitemid 36577597)
19. Suchail S, Guez D, Belzunces LP. Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environ Toxicol Chem 2001; 20:2482-2486. (Pubitemid 34117869)
20. Iwasa T, Motoyama N, Ambrose JT et al. Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Protect 2004; 23:371-378. (Pubitemid 38355801)
21. Schmuck R, Schöning R, Stork A et al. Risk posed to honeybees (Apis mellifera L, Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Manag Sci 2001; 57:225-238. (Pubitemid 32179089)
22. Decourtye A, Lacassie E, Pham-Delègue MH. Learning performances of honeybee (Apis mellifera L) are differentially affected by imidacloprid according to the season. Pest Manag Sci 2003; 59:269-278. (Pubitemid 36288082)
23. Ruzhong G, Rui C, Liangyan C. Evaluation on toxicity and safety of imidacloprid to environmental organisms. Pestic Sci Administration 1999; 20(3).
24. Wallner K. Test regarding effects of imidacloprid on honey bees. In: Belzunces LP, Pélissier C, Lewis G, eds. Proceedings of the 7th International Symposium "Hazards of pesticides to bees", Les Colloques de l'INRA 2001; 98:91-94.
25. Bonmatin JM, Moineau I, Charvet R et al. A LC/APCI-MS/MS method for analysis of imidacloprid in soil, in plants and in pollens. Anal Chem 2003; 75:2027-2033. (Pubitemid 36542340)
26. Aliouane Y, El Hassani AK, Gary V et al. Subchronic exposure of honeybees to sublethal doses of pesticides: Effects on behaviour. Environ Toxicol Chem 2009; 28(1):113-122.
27. Schmuck R. Effects of a chronic dietary exposure of the honeybee Apis mellifera (Hymenoptera: Apidae) to imidacloprid. Arch Environ Contam Toxicol 2004; 47:471-478. (Pubitemid 39506607)
28. Wilson EO. The insect societies. Cambridge: Harvard University Press 1971.
29. Dechaume-Moncharmont FX, Decourtye A, Hennequet C et al. Statistical analysis of the honeybee survival after chronic exposure to insecticides. Environ Toxicol Chem 2003; 22(12):3088-3094. (Pubitemid 37485243)
30. Decourtye A, Tisseur M, Taséi JN et al. Toxicité et risques liés à l'emploi de pesticides chez les pollinisateurs : Cas de l'abeille domestique. In: Regnault-Roger C. ed. Enjeux phytosanitaires pour l'agriculture et l'environnement au XXI° siècle. Tec et Doc Lavoisier, Paris 2005; 283-299.
31. Abbott VA, Nadeau JL, Higo HA et al. Lethal and sublethal effects of imidacloprid on Osmia lignaria and clothianidin on Megachile rotundata (Hymenoptera: Megachilidae). J Econ Entomol 2008; 101(3):784-796. (Pubitemid 351955940)
32. Taséi JN, Ripault G, Rivault E. Hazards of imidacloprid seed coating to Bombus terrestris (Hymenoptera: Apidea) when applied to sunflower. J Econ Entomol 2001; 94:623-627. (Pubitemid 33750039)
33. Medrzycki P, Montanari R, Bortolotti P et al. Effects of imidacloprid administered in sub-lethal doses on honey bee behaviour. Laboratory tests. Bull Insect 2003; 56(1):59-62.
34. Colin ME, Bonmatin JM, Moineau I et al. 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 2004; 47:387-395. (Pubitemid 39287465)
35. Lambin M, Armengaud C, Raymond S et al. Imidacloprid-induced facilitation of the proboscis extension reflex habituation in the honeybee. Arch Insect Biochem Physiol 2001; 4:129-134. (Pubitemid 33597326)
36. El Hassani AK, Dacher M, Gary V et al. Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honeybee (Apis mellifera). Arch Environ Contam Toxicol 2008; 54:653-661.
37. Menzel R, Greggers U, Hammer M. Functional organization of appetitive learning and memory in a generalist pollinator, the honey bee. In: Papaj DR, Lewis AC eds. Insect learning. New York: Chapman Hall 1993: 79-125.
38. Takeda K. Classical conditioned response in the honey bee. J Insect Physiol 1961; 6:168-179.
39. Desneux N, Decourtye A, Delpuech JM. The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 2007; 52:81-106. (Pubitemid 46133563)
40. Decourtye A, Devillers J, Cluzeau S et al. Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol Environ Saf 2004; 57(3):410-419. (Pubitemid 38376274)
41. Decourtye A, Armengaud C, Renou M et al. Imidacloprid impairs memory and brain metabolism in the honey bee (Apis mellifera L.). Pestic Biochem Physiol 2004; 78(2):83-92. (Pubitemid 38836702)
42. Decourtye A, Pham-Delègue MH. The proboscis extension response: Assessing the sublethal effects of pesticides on the honey bee. In: Devillers J, Pham-Delègue MH eds. Honey bees: Estimating the environmental impact of chemicals, Taylor and Francis publ., London 2002; 67-84.
43. Armengaud C, Causse N, Aït-Oubah J et al. Functional cytochrome oxidase histochemistry in the honeybee brain. Brain Research 2000; 859:390-393. (Pubitemid 30136117)
44. Guez D, Suchail S, Maleszka R et al. Contrasting effects of imidacloprid on habituation in 7-day and 8-day old honeybees. Neurobiol Learn Memory 2001; 76:183-191. (Pubitemid 32802851)
45. von Frisch K. The dance language and orientation of bees. Cambridge:Harvard University Press 1967.
46. Menzel R, Geiger K, Joerges J et al. Bees travel novel homeward routes by integrating separately acquired vector memories. Anim Behav 1998; 55:139-152. (Pubitemid 28165201)
47. Capaldi EA, Dyer FC. The role of orientation flights on homing performance in honeybees. J Exp Biol 1999; 202:1655-1666. (Pubitemid 29321699)
48. Collett TS, Fry SN, Wehner R. Sequence learning by honey bees. J Comp Physiol A 1993; 172, 693-706.
49. Zhang SW, Bartsch K, Srinivasan MV. Maze learning by honeybees. Neurobiol Learn Mem 1996; 66:267-282. (Pubitemid 26404585)
50. Tan J, Galligan JJ, Hollingworth RM. Agonist actions of neonicotinoids on nicotinic acetylcholine receptors expressed by cockroach neurons. Neurotoxicol 2007; 28:829-842. (Pubitemid 47058581)
51. Nauen R, Ebbinghaus-Kintscher U, Salgado V et al. Thiamethoxam is neonicotinoid precursor converted to clothianidin in insects and plants. Pest Biochem Physiol 2003; 76:55-69. (Pubitemid 36893198)
52. Lindauer M. Time-compensated sun orientation in bees. Cold Spring Harbor Symp quant Bio 1960; 25:371-377.
53. Bortolotti L, Montanari R, Marcelino J et al. Effect of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees. Bull Insect 2003; 56:63-67.
54. Yang EC, Chuang YC, Chen YL et al. Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J Econ Entomol 2008; 101(6):1743-1748.
55. Rortais A, Arnold G, Halm MP et al. Modes of honeybees exposure to systemic insecticides: Estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 2005; 36:71-83. (Pubitemid 40560983)
56. Haynes KF. Sublethal effects of neurotoxic insecticides on insect behavior. Annu Rev Entomol 1988; 33:149-68.
57. Colombo A, Buonocore E. Effetto di trattamenti al terreno con imidacloprid sull'attività dei bombi. L'Informatore Agrario 1997; 53(38):85-87.
58. Alarcón AL, Cánovas M, Senn R et al. The safety of thiamethoxam to pollinating bumble bees (Bombus terrestris L.) when applied to tomato plants through drip irrigation. Commun Agric Appl Biol Sci 2005; 70(4):569-79.
59. Morandin LA, Winston ML. Effects of novel pesticides on bumble bee (Hymenoptera: Apidae) colony health and foraging ability. Environ Entomol 2003; 32:555-563. (Pubitemid 36821570)
60. Franklin MT, Winston ML, Morandin LA. Effects of clothianidin on Bombus impatiens (Hymenoptera: Apidae) colony health and foraging ability. J Econ Entomol 2004; 97(2):369-73. (Pubitemid 38583413)
61. Cutler GC, Scott-Dupree CD. Exposure to clothianidin seed-treated canola has no long-term impact on honey bees. J Econ Entomol 2007; 100(3):765-72. (Pubitemid 46960174)
62. Schmuck R. No causal relationship between Gaucho® seed dressing in sunflowers and the French bee malady. Pflanzenschutz-Nachrichten Bayer 1999; 52:267-309.
63. Mayer DF, Lunden JD. Effects of imidacloprid insecticide on three bee pollinators. Hortic Sci 1997; 29:93-97.
64. Kirchner WH. Mad-bee-disease? Sublethal effects of Imidacloprid ("Gaucho") on the behaviour of honey-bees. Apidologie 1999; 30:422.
65. Díaz S, Tilman D, Fargione J et al. Biodiversity regulation of ecosystem services. In: Hassan R, Scholes R, Ash N, eds. Ecosystems and human well-being: Current state and trends: Findings of the Condition and Trends Working Group Washington DC: Island Press 2005; 297-329.
66. Biesmeijer JC, Roberts SPM, Reemer M et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 2006; 313:351-354. (Pubitemid 44480959)
67. Gallai N, Salles JM, Settele J et al. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 2009; 68:810-821.
68. Thompson HM, Maus C. The relevance of sublethal effects in honey bee testing for pesticide risk assessment. Pest Manag Sci 2007; 63:1058-1061. (Pubitemid 350033349)
69. Curé G, Schmidt HW, Schmuck R. Results of a comprehensive field research programme with the systemic insecticide imidacloprid (Gaucho). In: Belzunces LP, Pelissier C, Lewis GB, eds. Proceedings of the 7th International Symposium "Hazards of pesticides to bees", Les Colloques de l'INRA 2001; 98:49-59.
70. Bonmatin JM, Marchand PA, Charvet R et al. Quantification of imidacloprid uptake in maize crops. J Agric Food Chem 2005; 53:5336-5341. (Pubitemid 40994843)
71. Laurent FM, Rathahao E. Distribution of [14C]imidacloprid in sunflower (Helianthus annuus) following seed treatment. J Agric Food Chem 2003; 51: 8005-8010.
72. Stadler T, Martinez Ginés D, Buteler M. Long-term toxicity assessment of imidacloprid to evaluate side effects on honey bees exposed to treated sunflower in Argentina, Bull Insect 2003; 56:77-81.
73. Faucon JP, Aurières C, Drajnudel P et al. Experimental study on the toxicity of imidacloprid given in syrup to honey bee (Apis mellifera) colonies, Pest Manag Sci 2005; 61:111-125. (Pubitemid 40115981)