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Neonicotinoid insecticides translocated in guttated droplets of seed-treated maize and wheat: a threat to honeybees?

An Erratum to this article was published on 14 September 2011


The immune system of bees is influenced by a diversity of factors, some of which have changed in the last 10 years such as the application of pesticides. In addition to pollen, nectar and dust, guttated water of seed-dressed plants might be a new source of contamination to bees. Our experiments demonstrated that guttated water of plants germinated from seeds dressed with neonicotinoids contains neonicotinoids. Maize seeds treated with clothianidin (Poncho® 0.5 mg/seed and Poncho® Pro 1.25 mg/seed) resulted in neonicotinoid concentrations up to 8,000 ng mL−1 in the guttated fluid. This concentration decreases rapidly, but remained detectable over several weeks. Seeds treated with Poncho® Pro did not result in higher concentrations in guttated droplets in the first stages of plant development, but the concentration decreased more slowly. Triticale seed treated with imidacloprid contained small quantities of this active agent (up to 13 ng mL−1) in the guttated fluid the following spring after overwintering. During the sampling of guttation fluid, no bees were observed collecting these droplets from triticale or maize. To evaluate the attractiveness of guttation fluid exuded from seed-treated plants under field conditions, more studies are required.

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  1. Butler, C.G. (1940) The choice of drinking water by the honeybee. J. Exp. Biol. 17, 253–261

    CAS  Google Scholar 

  2. Cutler, G.C., Scott-Dupree, C.D. (2007) Exposure to clothianidin seed-treated canola has no long-term impact on honey bees. J. Econ. Entomol. 100(3), 765–772

    PubMed  Article  CAS  Google Scholar 

  3. Decourtye, A., Devillers, J., Genecque, E., Le Menach, K., Budzinski, H., Cluzeau, S., Pham-Delègue, M.-H. (2005) Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis mellifera. Arch. Environ. Contam. Toxicol. 48, 242–250

    PubMed  Article  CAS  Google Scholar 

  4. Desneux, N., Decourtye, A., Delpuech, J.-M. (2007) The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52, 81–106

    PubMed  Article  CAS  Google Scholar 

  5. Halm, M.-P., Rortais, A., Arnold, G., Taséi, J.N., Rault, S. (2006) New risk assessment approach for systemic insecticides: the case of honey bees and imidacloprid (Gaucho). Environ. Sci. Technol. 40(7), 2448–2454

    PubMed  Article  CAS  Google Scholar 

  6. Harries, R.I. (1999) Guttation—the basis of an assay for evaluating formulation behaviour in vivo. Pestic. Sci. 55, 582–584

    Article  Google Scholar 

  7. Iwasa, T., Motoyama, N., Ambrose, J.T., Roe, R.M. (2004) (2003) Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Protection 23, 371–378

    Article  CAS  Google Scholar 

  8. Jeschke, P., Nauen, R. (2008) Neonicotinoids – from zero to hero in insecticide chemistry. Pest. Manag. Sci. 64, 1084–1098

    PubMed  Article  CAS  Google Scholar 

  9. Kühnholz, S., Seeley, T.D. (1997) The control of water collection in honey bee colonies. Behav. Ecol. Sociobiol. 41(6), 407–422

    Article  Google Scholar 

  10. Liu, M.Y., Lanford, J., Casida, J.E. (1993) Relevance of [3H]imidacloprid binding site in house fly head acetylcholine receptor to insecticidal activity of 2-nitromethylene-and 2-nitroimino-imidazolidines. Pestic. Biochem. Physiol. 46, 200–206

    Article  CAS  Google Scholar 

  11. Maienfisch, P., Angst, M., Brandl, F., Fischer, W., Hofen, D., Kayser, H., Kobel, W., Rindlisbacher, A., Senn, R., Steinemann, A., Widmer, H. (2001) Chemistry and biology of thiamethoxam: a second generation neonicotinoid. Pest. Manag. Sci. 57, 906–913

    PubMed  Article  CAS  Google Scholar 

  12. Oldroyd, B.P. (2007) What's killing American honey bees? PLoS Biol. 5, e168

    PubMed  Article  Google Scholar 

  13. Rosenkranz, P., Wallner, K. (2009) The chronology of honey bee losses in the Rhine Valley during spring 2008: an example of worst case scenario. Proceedings of the Third European Conference of Apidologie, Dublin, Ireland, 7–11 September 2008, 94–95

  14. Schmuck, R. (1999) Imidacloprid - Kein Zusammenhang zwischen Saatgutbeizung mit Gaucho® in Sonnenblumen und Bienenschäden in Frankreich. Pflanzenschutz-Nachr. Bayer 52, 267–310

    CAS  Google Scholar 

  15. Schmuck, R. (2004) Effects of a chronic dietary exposure of the honeybee Apis mellifera (Hymenoptera: Apidae) to Imidaclorpid. Arch. Environ. Contam. Toxicol. 47, 471–478

    PubMed  Article  CAS  Google Scholar 

  16. Schmuck, R., Keppler, J. (2003) Clothianidin—ecotoxicological profile and risk assessment. Pflanzenschutz-Nachrichten Bayer 56, 26–58

    CAS  Google Scholar 

  17. Schmuck, R., Schöning, R., Stork, A., Schramel, O. (2001) Risk posed to honeybees (Apis mellifera L, Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest. Manag. Sci. 57, 225–238

    PubMed  Article  CAS  Google Scholar 

  18. Suchail, S., Guez, D., Belzunces, L.P. (2001) Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environ. Toxicol. Chem. 20, 2482–2486

    PubMed  CAS  Google Scholar 

  19. Suchail, S., de Sousa, G., Rahmani, R., Belzunces, L.P. (2004) In vivo distribution and metabolisation of 14C-imidacloprid in different compartments of Apis mellifera L. Pest Manag. Sci. 60, 1056–1062

    PubMed  Article  CAS  Google Scholar 

  20. VanEngelsdorp, D., Evans, J.D., Saegerman, C., Mullin, C., Haubruge, E., Nguyen, B.K., Frazier, M., Frazier, J., Cox-Foster, D., Chen, Y., Underwood, R., Tarpy, D.R., Pettis, J.S. (2009) Colony collapse disorder: a descriptive study. PLoS ONE 4, e6481

    PubMed  Article  Google Scholar 

  21. Villa, S., Vighi, M., Finizio, A., Serini, G.B. (2000) Risk assessment for honeybees from pesticide-exposed pollen. Ecotoxicology 9, 287–297

    Article  CAS  Google Scholar 

  22. Visscher, P.K., Crailsheim, K., Sherman, G. (1996) How do honey bees (Apis mellifera) fuel their water foraging flights? J. Insect. Physiol. 42, 1089–1094

    Article  CAS  Google Scholar 

  23. Wallner, K. (2006) Pflanzenschutzmitteleinsatz in blühende Kulturen und der Wirkstofftransport in Bienenvölker. BVL - Das “Bienensterben” im Winter 2002/2003 in Deutschland, 60–67

  24. Wallner, K. (2009) Sprayed and seed dressed pesticides in pollen, nectar and honey of treated oil seed rape. Hazard of pesticides to bees. Julius Kühn-Archiv 423, 152–153

    Google Scholar 

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The authors thank the staff members of the field site Heidfeldhof for assistance and providing us experimental sites. Furthermore, we thank Dr. Helen M. Thompson for proofreading the manuscript.

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Corresponding author

Correspondence to Jana E. Reetz.

Additional information

Présence d'insecticides néonicotinoïdes dans les gouttelettes exsudées par guttation sur les plants de maïs et de blé issus de graines traitées par enrobage: une menace pour les abeilles?

Graines traitées par enrobage / néonicotinoïdes/guttation / Apis mellifera / LC-HR-MS

Freisetzung neonicotinoider Insektizide aus der Saatgutbeizung in Guttationstropfen bei Mais und Getreide: Eine Gefahr für Honigbienen?

Saatgutbeizung / Neonicotinoide / Guttationswasser / Apis mellifera / LC-HR-MS

An erratum to this article can be found at

Manuscript editor: Monique Gauthier

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Reetz, J.E., Zühlke, S., Spiteller, M. et al. Neonicotinoid insecticides translocated in guttated droplets of seed-treated maize and wheat: a threat to honeybees?. Apidologie 42, 596–606 (2011).

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  • seed coating
  • neonicotinoids
  • guttated fluid
  • Apis mellifera
  • LC-HR-MS