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Effects of Sublethal Doses of Acetamiprid and Thiamethoxam on the Behavior of the Honeybee (Apis mellifera)

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Abstract

Acetamiprid and thiamethoxam are insecticides introduced for pest control, but they can also affect non-target insects such as honeybees. In insects, these neonicotinoid insecticides are known to act on acetylcholine nicotinic receptors but the behavioral effects of low doses are not yet fully understood. The effects of acetamiprid and thiamethoxam were studied after acute sublethal treatment on the behavior of the honeybee (Apis mellifera) under controlled laboratory conditions. The drugs were either administered orally or applied topically on the thorax. After oral consumption acetamiprid increased sensitivity to antennal stimulation by sucrose solutions at doses of 1 μg/bee and impaired long-term retention of olfactory learning at the dose of 0.1 μg/bee. Acetamiprid thoracic application induced no effect in these behavioral assays but increased locomotor activity (0.1 and 0.5 μg/bee) and water-induced proboscis extension reflex (0.1, 0.5, and 1 μg/bee). Unlike acetamiprid, thiamethoxam had no effect on bees’ behavior under the conditions used. Our results suggest a particular vulnerability of honeybee behavior to sublethal doses of acetamiprid.

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References

  • Armengaud C, Lambin M, Gauthier M (2002) Effects of imidacloprid on the neural processes of memory in honeybee. In: Devillers J, Pham-Délègue MH (eds) Honey bees: estimating the environmental impact of chemicals. CRC Press, Boca Raton, FL, pp 85–100

    Google Scholar 

  • Bicker G (1999) Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microsc Res Tech 45:174–183

    Article  CAS  Google Scholar 

  • Braun G, Bicker G (1992) Habituation of an appetitive reflex in the honeybee. J Neurophysiol 67:588–598

    CAS  Google Scholar 

  • Breer H (1987) Neurochemical aspects of cholinergic synapses in the insect brain. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure and functions. Wiley, New York, pp 415–437

    Google Scholar 

  • Brunet JL, Badiou A, Belzunces LP (2005) In vivo metabolic fate of [14C]-acetamiprid in six biological compartments of the honeybee, Apis mellifera L. Pest Manage Sci 61:742–748

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Claudianos C, Ranson H, Johnson RM, Biswas S, Schuler MA, Berenbaum MR, Feyereisen R, Oakeshott JG (2006) A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Mol Biol 15:615–636

    Article  CAS  Google Scholar 

  • Dacher M, Lagarrigue A, Gauthier M (2005) Antennal tactile learning in the honeybee: effect of nicotinic antagonists on memory dynamics. Neuroscience 130:37–50

    Article  CAS  Google Scholar 

  • Decourtye A, Armengaud C, Renou M, Devillers J, Cluzeau S, Gauthier M, Pham-Délègue MH (2004) Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.) Pest Biochem Physiol 78:83–92

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Erber J (1975a) The dynamics of learning in the honeybee (Apis mellifica carnica). I. The time dependence of the choice reaction. J Comp Physiol A 99:231–242

    Google Scholar 

  • Erber J (1975b) The dynamics of learning in the honeybee (Apis mellifica carnica). II. Principles of information processing. J Comp Physiol A 99:243–255

    Google Scholar 

  • European Commission (2004) European Commission Acetamiprid SANCO/1392/2001—Final. Available at: http://www.ec.europa.eu/food/plant/protection/evaluation/newactive/acetamiprid.pdf

  • Gauthier M, Dacher M, Thany SH, Niggebrugge C, Déglise 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

    Article  CAS  Google Scholar 

  • Gerber B, Wustenberg D, Schutz A, Menzel R (1998) Temporal determinants of olfactory long-term retention in honeybee classical conditioning: nonmonotonous effects of the training trial interval. Neurobiol Learn Mem 69:71–78

    Article  CAS  Google Scholar 

  • Guez D, Belzunces LP, Maleszka R (2003) 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 75:217–222

    Article  CAS  Google Scholar 

  • Iwasa T, Motoyama N, Ambrose JT, Roe MR (2004) Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Protect 23:371–378

    Article  CAS  Google Scholar 

  • Jones AK, Raymond-Delpech V, Thany SH, Gauthier M, Sattelle DB (2006) The nicotinic acetylcholine receptor gene family of the honey bee, Apis mellifera. Genome Res 16:1422–1430

    Article  CAS  Google Scholar 

  • Kayser H, Lee C, Decock A, Baur M, Haettenschwiler J, Maienfisch P (2004) Comparative analysis of neonicotinoid binding to insect membranes: I. A structure-activity study of the mode of [3H] imidacloprid displacement in Myzus persicae and Aphis craccivora. Pest Manage Sci 60:945–958

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Mamood AN, Waller GD (1990) Recovery of learning responses by honeybees following a sublethal exposure to permethrin. Physiol Enthomol 15:55–60

    Article  CAS  Google Scholar 

  • Michelsen DB, Braun GH (1987) Circling behavior in honey bees. Brain Res 421:14–20

    Article  CAS  Google Scholar 

  • 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 Manage Sci 57:577–586

    Article  CAS  Google Scholar 

  • Nauen R, Ebbinghaus-Kintscher U, Salgado VL, Kaussmann M (2003) Thiamethoxam is a neonicotinoid precursor converted to clothianidin in insects and plants. Pest Biochem Physiol 76:55–69

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Pankiw T, Waddington KD, Page RE (2001) Modulation of sucrose response thresholds in honeybees (Apis mellifera): influence of genotype, feeding and foraging experience. J Comp Physiol A 187:293–301

    Article  CAS  Google Scholar 

  • Pham-Délègue MH, Decourtye A, Kaiser L, Devillers J (2002) Behavioural methods to assess the effects of pesticides on honey bees. Apidology 33:425–432

    Article  Google Scholar 

  • Scheidler A, Kaulen P, Brüning G, Erber J (1990) Quantitative autoradiographic localization of 125I α-bungarotoxin binding sites in the honeybee brain. Brain Res 534:332–335

    Article  CAS  Google Scholar 

  • Tan J, Galligan JJ, Hollingworth RM (2007) Agonist actions of neonicotinoids on nicotinic acetylcholine receptors expressed by cockroach neurons. Neurotoxicology 28:829–842

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Tomizawa M, Casida JE (2003) Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. Annu Rev Entomol 48:339–364

    Article  CAS  Google Scholar 

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Acknowledgment

This work was supported by a French Agriculture Ministry grant to M. Dacher, A. K. El Hassani, and V. Garry (Grant 407 ONIFLHOR).

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Authors and Affiliations

  1. Centre de Recherches sur la Cognition Animale, Université Paul Sabatier Toulouse III, CNRS UMR 5169, 118 Route de Narbonne, 31062, Toulouse Cedex 04, France

    Abdessalam Kacimi El Hassani, Matthieu Dacher, Vincent Gary, Michel Lambin, Monique Gauthier & Catherine Armengaud

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  1. Abdessalam Kacimi El Hassani
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  2. Matthieu Dacher
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  3. Vincent Gary
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  4. Michel Lambin
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  5. Monique Gauthier
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  6. Catherine Armengaud
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Correspondence to Catherine Armengaud.

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El Hassani, A.K., 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 54, 653–661 (2008). https://doi.org/10.1007/s00244-007-9071-8

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  • DOI: https://doi.org/10.1007/s00244-007-9071-8

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