, Volume 42, Issue 5, pp 596–606 | Cite as

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

  • Jana E. ReetzEmail author
  • Sebastian Zühlke
  • Michael Spiteller
  • Klaus Wallner
Original article


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.


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



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.


  1. Butler, C.G. (1940) The choice of drinking water by the honeybee. J. Exp. Biol. 17, 253–261Google 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), 765–772PubMedCrossRefGoogle 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, 242–250PubMedCrossRefGoogle Scholar
  4. Desneux, N., Decourtye, A., Delpuech, J.-M. (2007) The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52, 81–106PubMedCrossRefGoogle 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), 2448–2454PubMedCrossRefGoogle Scholar
  6. Harries, R.I. (1999) Guttation—the basis of an assay for evaluating formulation behaviour in vivo. Pestic. Sci. 55, 582–584CrossRefGoogle 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, 371–378CrossRefGoogle Scholar
  8. Jeschke, P., Nauen, R. (2008) Neonicotinoids – from zero to hero in insecticide chemistry. Pest. Manag. Sci. 64, 1084–1098PubMedCrossRefGoogle Scholar
  9. Kühnholz, S., Seeley, T.D. (1997) The control of water collection in honey bee colonies. Behav. Ecol. Sociobiol. 41(6), 407–422CrossRefGoogle 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, 200–206CrossRefGoogle 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, 906–913PubMedCrossRefGoogle Scholar
  12. Oldroyd, B.P. (2007) What's killing American honey bees? PLoS Biol. 5, e168PubMedCrossRefGoogle 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, 94–95Google Scholar
  14. Schmuck, R. (1999) Imidacloprid - Kein Zusammenhang zwischen Saatgutbeizung mit Gaucho® in Sonnenblumen und Bienenschäden in Frankreich. Pflanzenschutz-Nachr. Bayer 52, 267–310Google 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, 471–478PubMedCrossRefGoogle Scholar
  16. Schmuck, R., Keppler, J. (2003) Clothianidin—ecotoxicological profile and risk assessment. Pflanzenschutz-Nachrichten Bayer 56, 26–58Google 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, 225–238PubMedCrossRefGoogle 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, 2482–2486PubMedGoogle 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, 1056–1062PubMedCrossRefGoogle 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, e6481PubMedCrossRefGoogle Scholar
  21. Villa, S., Vighi, M., Finizio, A., Serini, G.B. (2000) Risk assessment for honeybees from pesticide-exposed pollen. Ecotoxicology 9, 287–297CrossRefGoogle 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, 1089–1094CrossRefGoogle Scholar
  23. Wallner, K. (2006) Pflanzenschutzmitteleinsatz in blühende Kulturen und der Wirkstofftransport in Bienenvölker. BVL - Das “Bienensterben” im Winter 2002/2003 in Deutschland, 60–67Google Scholar
  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, 152–153Google Scholar

Copyright information

© INRA, DIB-AGIB and Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Jana E. Reetz
    • 1
    Email author
  • Sebastian Zühlke
    • 2
  • Michael Spiteller
    • 2
  • Klaus Wallner
    • 1
  1. 1.Apicultural State InstituteUniversity of HohenheimStuttgartGermany
  2. 2.Institute of Environmental Research (INFU)Technische Universität DortmundDortmundGermany

Personalised recommendations