Neonicotinoids interfere with specific components of navigation in honeybees

PLoS One. 2014 Mar 19;9(3):e91364. doi: 10.1371/journal.pone.0091364. eCollection 2014.


Three neonicotinoids, imidacloprid, clothianidin and thiacloprid, agonists of the nicotinic acetylcholine receptor in the central brain of insects, were applied at non-lethal doses in order to test their effects on honeybee navigation. A catch-and-release experimental design was applied in which feeder trained bees were caught when arriving at the feeder, treated with one of the neonicotinoids, and released 1.5 hours later at a remote site. The flight paths of individual bees were tracked with harmonic radar. The initial flight phase controlled by the recently acquired navigation memory (vector memory) was less compromised than the second phase that leads the animal back to the hive (homing flight). The rate of successful return was significantly lower in treated bees, the probability of a correct turn at a salient landscape structure was reduced, and less directed flights during homing flights were performed. Since the homing phase in catch-and-release experiments documents the ability of a foraging honeybee to activate a remote memory acquired during its exploratory orientation flights, we conclude that non-lethal doses of the three neonicotinoids tested either block the retrieval of exploratory navigation memory or alter this form of navigation memory. These findings are discussed in the context of the application of neonicotinoids in plant protection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bees / drug effects*
  • Bees / physiology
  • Exploratory Behavior / drug effects
  • Exploratory Behavior / physiology
  • Feeding Behavior / physiology
  • Flight, Animal / physiology
  • Guanidines / pharmacology
  • Homing Behavior / drug effects*
  • Homing Behavior / physiology
  • Imidazoles / pharmacology
  • Memory / drug effects*
  • Memory / physiology
  • Neonicotinoids
  • Nicotinic Agonists / pharmacology*
  • Nitro Compounds / pharmacology
  • Orientation / drug effects*
  • Orientation / physiology
  • Pyridines / pharmacology
  • Radar
  • Receptors, Nicotinic / metabolism
  • Spatial Navigation / drug effects*
  • Spatial Navigation / physiology
  • Thiazines / pharmacology
  • Thiazoles / pharmacology


  • Guanidines
  • Imidazoles
  • Neonicotinoids
  • Nicotinic Agonists
  • Nitro Compounds
  • Pyridines
  • Receptors, Nicotinic
  • Thiazines
  • Thiazoles
  • clothianidin
  • imidacloprid
  • thiacloprid

Grants and funding

The studies were financially supported by the following institutions: Deutsche Forschungsgemeinschaft (DFG grant ME 365/34-2 to RM), Hertie Gemeinnützige Stiftung (RM), Dr. Klaus Tschira Stiftung (RM, UG), and by the EU and the Land Hessen, Hessisches Ministerium für Umwelt, Ernährung, Landwirtschaft und Verbraucherschutz (BG). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.