Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees

Proc Biol Sci. 2016 Apr 13;283(1828):20160246. doi: 10.1098/rspb.2016.0246.


Learning and memory are crucial functions which enable insect pollinators to efficiently locate and extract floral rewards. Exposure to pesticides or infection by parasites may cause subtle but ecologically important changes in cognitive functions of pollinators. The potential interactive effects of these stressors on learning and memory have not yet been explored. Furthermore, sensitivity to stressors may differ between species, but few studies have compared responses in different species. Here, we show that chronic exposure to field-realistic levels of the neonicotinoid clothianidin impaired olfactory learning acquisition in honeybees, leading to potential impacts on colony fitness, but not in bumblebees. Infection by the microsporidian parasite Nosema ceranae slightly impaired learning in honeybees, but no interactive effects were observed. Nosema did not infect bumblebees (3% infection success). Nevertheless, Nosema-treated bumblebees had a slightly lower rate of learning than controls, but faster learning in combination with neonicotinoid exposure. This highlights the potential for complex interactive effects of stressors on learning. Our results underline that one cannot readily extrapolate findings from one bee species to others. This has important implications for regulatory risk assessments which generally use honeybees as a model for all bees.

Keywords: Apis mellifera; Bombus terrestris; Nosema ceranae; clothianidin; pollination; proboscis extension response.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bees / drug effects*
  • Bees / parasitology
  • Bees / physiology
  • Guanidines / toxicity*
  • Insecticides / toxicity*
  • Learning / drug effects
  • Neonicotinoids
  • Nosema / physiology
  • Risk Assessment
  • Smell / drug effects
  • Species Specificity
  • Thiazoles / toxicity*


  • Guanidines
  • Insecticides
  • Neonicotinoids
  • Thiazoles
  • clothianidin

Associated data

  • Dryad/10.5061/dryad.15264