The neonicotinoid imidacloprid alone alters the cognitive behavior in Apis mellifera L. and the combined exposure of imidacloprid and Varroa destructor mites synergistically contributes to trial attrition

Abstract

Honey bee (Apis mellifera L.) populations have undergone a dramatic decline as an outcome of an increasing incidence of colony collapse disorder (CCD). The honey bee is a unique keystone species because its pollination activities are not only necessary for the viability of many flowering plant species in the wild, but are also necessary for many human agricultural practices. The increasing prevalence of CCD is a threat to the economic and nutritional security of all societies that rely on efficient pollination for large monoculture crops. Although there is ample evidence that Varroa mites, pesticides, disease, and climate change contribute to CCD, only a few studies have investigated the contribution of synergism across multiple factors to the development of CCD and CCD-like symptoms. However, there is increasing acknowledgement in the scientific community that synergism across different factors affects honey bee colony health and behavior. Here, we provide evidence that sub-lethal levels of imidacloprid neonicotinoid pesticide reduce learning and memory capabilities. Synergistic effects become apparent when Varroa mites together with imidacloprid exposure to individual bees more than doubled average mortality and attrition per trial.