Subchronic exposure of honeybees to sublethal doses of pesticides: Effects on behavior

Environmental Toxicology and Chemistry

Volumn 28, Issue 1, 2009, Pages 113-122

  Aliouane, Yassine ^a   El Hassani, Adessalam K ^a   Gary, Vincent ^a   Armengaud, Catherine ^a   Lambin, Michel ^a   Gauthier, Monique ^a  

^a Université de Toulouse 3 Paul Sabatier   (France)

Author keywords

Behavior; Chronic; Honeybee; Pesticides; Sublethal

Indexed keywords

BEHAVIOR; CHRONIC EXPOSURE; COGNITIVE FUNCTIONS; CONTACT TREATMENT; FIPRONIL; IN-FIELD; LABORATORY BIOASSAY; LEARNING PERFORMANCE; LETHAL DOSE; NEONICOTINOIDS; SUBCHRONIC EXPOSURE; SUBLETHAL DOSE; SUCROSE CONCENTRATION; THIAMETHOXAM;

INSECTICIDES; RISKS; SUGAR (SUCROSE);

AGRICULTURAL CHEMICALS;

ACETAMIPRID; FIPRONIL; PESTICIDE; THIAMETHOXAM; UNCLASSIFIED DRUG;

BEHAVIORAL RESPONSE; BIOASSAY; DOSE-RESPONSE RELATIONSHIP; ECOTOXICOLOGY; HONEYBEE; INSECTICIDE; MORTALITY; POLLUTION EXPOSURE; RISK ASSESSMENT; SUBLETHAL EFFECT; SUCROSE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR CHANGE; CHRONIC TOXICITY; CONTROLLED STUDY; HONEYBEE; LD 50; MORTALITY; NONHUMAN; PRIORITY JOURNAL; RISK ASSESSMENT; ANIMAL; BEE; DRUG EFFECT; PHYSIOLOGY;

APIS MELLIFERA;

ANIMALS; BEES; BEHAVIOR, ANIMAL; LETHAL DOSE 50; PESTICIDES;

EID: 65449170134     PISSN: 07307268     EISSN: 15528618     Source Type: Journal    
DOI: 10.1897/08-110.1     Document Type: Article

References (41)

1. Tomizawa M, Casida JE. 2005. Neonicotinoid insecticide toxicology: Mechanisms of selective action. Annu Rev Pharmacol Toxicol 45:247-268.
2. Buckingham SD, Biggin PC, Sattelle BM, Brown LA, Sattelle DB. 2005. Insect GABA receptors: Splicing, editing, and targeting by antiparasitic and insecticides. Mol Pharmacol 68:942-951.
3. Matsuda K, Buckingham SD, Kleier D, Rauhh JJ, Grauso M, Sattelle DB. 2001. Neonicotinoid insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 22:573-580.
4. Barbara GS, Zube C, Rybak J, Gauthier M, Grünewald B. 2005. Acetylcholine, GABA and glutamate induce ionic currents in cultured antennal lobe neurons of the honeybee, Apis mellifera. J Comp Physiol A 191:823-836.
5. Barbara GS, Grünewald B, Paute S, Gauthier M, Raymond-Delpech V. 2007. Cholinergic currents of cultured antennal lobe neurones from adult honeybees' brains. Invertebr Neurosci 8:19-29.
6. Déglise P, Grünewald B, Gauthier M. 2002. The insecticide imidacloprid is a partial agonist of the nicotinic receptor of honeybee Kenyon cells. Neurosci Lett 321:13-16.
7. Nauen R, Ebbinghaus-Kintscher U, Schmuck R. 2001. Toxicity and nicotinic acetylcholine receptor interaction of imidacloprid and its metabolites in Apis mellifera (Hymenoptera: Apidae). Pest Manag Sci 57:577-586.
8. Gauthier M, Dacher M, Thany SH, Niggebrugge C, Deglise P, Kljucevic P, Armengaud C, Grünewald B. 2006. Involvement of alpha-bungarotoxin-sensitive nicotinic receptors in long-term memory formation in the honeybee (Apis mellifera). Neurobiol Learn Mem 86:164-174.
9. Cano Lozano V, Bonnard E, Gauthier M, Richard D. 1996. Mecamylamine-induced impairment of acquisition and retrieval of olfactory conditioning in the honeybee. Behav Brain Res 81:215-222.
10. Cano Lozano V, Armengaud C, Gauthier M. 2001. Memory impairment induced by cholinergic antagonists injected into the mushroom bodies of the honeybee. J Comp Physiol A 187:249-254.
11. Dacher M, Lagarrigue A, Gauthier M. 2005. Antennal tactile learning in the honeybee: Effect of nicotinic antagonists on memory dynamics. Neuroscience 130:37-50.
12. Thany SH, Gauthier M. 2005. Nicotine injected into the antennal lobes induces a rapid modulation of sucrose threshold and improves short-term memory in the honeybee Apis mellifera. Brain Res 1039:216-219.
13. Janssen D, Derst C, Buckinx R, Van den Eynden J, Rigo JM, VanKerkhove E. 2007. Dorsal unpaired median neurons of Locusta migratoria express ivermectin- and fipronil-sensitive glutamate-gated chloride channels. J Neurophysiol 97:2642-2650.
14. Narahashi T, Zhao X, Ikeda T, Nagat K, Yeh JZ. 2007. Differential actions of insecticides on target sites: Basis for selective toxicity. Hum Exp Toxicol 26:361-366.
15. Bicker G, Schäfer S, Kingan T. 1985. Mushroom body feedback interneurons in the honeybee show GABA-like immunoreactivity. Brain Res 360:394-397.
16. Stopfer M, Bhagavan S, Smith B, Laurent G. 1997. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 990:70-74.
17. Sachse S, Galizia CG. 2002. Role of inhibition for temporal and spatial odor representation in olfactory output neurons: A calcium imaging study. J Neurophysiol 87:1106-1117.
18. Collet C, Belzunces L. 2007. Excitable properties of adult skeletal muscle fibers from the honeybee Apis mellifera. J Exp Biol 210: 454-464.
19. Marrus SB, Portman SL, Allen MJ, Moffat KG, DiAntonnio A. 2004. Differential localization of glutamate receptor subunits at the Drosophila neuromuscular junction. J Neurosci 24:1406-1415.
20. El Hassani AK, Dacher M, Gary V, Lambin M, Gauthier M, Armengaud C. 2008. Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honeybee (Apis mellifera). Arch Environ Contam Toxicol 54:653-661.
21. El Hassani AK, Dacher M, Gauthier M, Armengaud C. 2005. Effects of sublethal doses of fipronil on the behavior of the honeybee (Apis mellifera). Pharmacol Biochem Behav 82:30-39.
22. Halm MP, Rortais A, Arnold G, Taséi JN, Rault S. 2006. New risk assessment approach for systemic insecticides: The case of the honey bees and imidacloprid (Gaucho). Environ Sci Technol 40:2448-2454.
23. Aajoud A, Raveton M, Aouadi H, Tissut M, Ravanel P. 2006. Uptake and xylem transport of fipronil in sun flowers. J Agric Food Chem 54:5055-5060.
24. Decourtye A, Lacassie E, Pham-Délègue MH. 2003. Learning performances of honeybees (Apis mellifera L.) are differentially affected by imidacloprid according to the season. Pest Manag Sci 59:269-278.
25. Decourtye A, Devillers J, Genecque E, Le Menach K, Budzinski H, Cluzeau S, Pham-Délègue MH. 2005. Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis mellifera. Arch Environ Contam Toxicol 48: 242-250.
26. European and Mediterranean Plant Protection Organism. 1992. Guideline on test methods for evaluating the side-effects of plant protection products on honeybees. EPPO Bull 22:203-215.
27. 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 4:129-134.
28. Levene H. 1960. Robust tests for equality of variances. In Olkin I, Ghurye SG, Hoeffding W, Madow WG, Mann HB, eds, Contributions to Probability and Statistics: Essays in Honor of Harold Hotelling. Stanford University Press, Menlo Park, CA, USA, pp 278-292.
29. Eliasziv M, Donner A. 1991. Application of the McNemar test to non-independent matched pair-data. Stat Med 10:1981-1991.
30. Schmuck R. 2004. Effects of a chronic dietary exposure of the honeybee Apis mellifera (Hymenoptera: Apidae) to imidacloprid. Arch Environ Contam Toxicol 47:471-478.
31. Page RE, Erber J, Fondrk MK. 1998. The effects of genotype on response thresholds to sucrose and foraging behavior of honeybees (Apis mellifera). J Comp Physiol A 182:489-500.
32. Scheiner R, Page RE, Erber J. 2001. The effects of genotype, foraging role, and sucrose responsiveness on the tactile learning performance of honeybees (Apis mellifera L.). Neurobiol Learn Mem 76:138-150.
33. Humphries MA, Fondrk MK, Page RE. 2005. Locomotion and the pollen hoarding behavioral syndrome of the honeybee (Apis mellifera L.). J Comp Physiol A 191:669-674.
34. Pankiw T, Page RE. 1999. The effect of genotype, age, sex, and caste on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). J Comp Physiol A 185:207-213.
35. Guerrieri F, Schubert M, Sandoz JC, Giurfa M. 2005. Perceptual and neural olfactory similarity in honeybees. PLoS Biology 3: e60.
36. Zhao X, Yeh JZ, Salgado VL, Narahashi T. 2005. Sulfone metabolite of fipronil blocks γ-amino acid- and glutamate-activated chloride channels in mammalian and insect neurons. J Pharmacol Exp Ther 314:363-373.
37. Tan J, Galligan JJ, Hollingworth RM. 2007. Agonists actions of neonicotinoids on nicotinic acetylcholine receptors expressed by cockroach neurons. Neurotoxicology 28:829-842.
38. Tomiza M, Casida JE. 2000. Imidacloprid, Thiacloprid, and their imine derivatives up-regulate the α4β2 nicotinic receptor in M10 cells. Toxicol Applied Pharmacol 169:114-120.
39. Marszalec W, Yeh JZ, Narahashi T. 2005. Desensitization of nicotine acetylcholine receptors: Modulation by kinase activation and phosphatase inhibition. Eur J Pharmacol 514:83-90.
40. Nauen R, Ebbinghaus-Kintscher U, Salgado V, Kaussman M. 2003. Thiamethoxam is a neonicotinoid precursor converted to clothianidin in insects and plants. Pest Biochem Physiol 76:55-69.
41. Iwasa T, Motoyama N, Ambrose JT, Roe MR. 2004. Mechanism for the differential toxicity of neonicotinoid insecticides in the honeybee, Apis mellifera. Crop Prot 23:371-378.