Effects of Nosema ceranae (DISSOCIODIHAPLOPHASIDA: Nosematidae) and flupyradifurone on olfactory learning in honey bees, Apis mellifera (HYMENOPTERA: Apidae)

The health of insect pollinators, particularly the honey bee, <em>Apis mellifera </em>(Linnaeus, 1758), is a major concern for agriculture and ecosystem health. In response to mounting evidence supporting the detrimental effects of neonicotinoid pesticides on pollinators, a novel “bee safe” butenolide compound, flupyradifurone (FPF) has been registered for agricultural use. Although FPF is not a neonicotinoid, like neonicotinoids, it is an excitotoxic nicotinic acetylcholine receptor agonist. In addition, <em>A. mellifera</em> faces threats from pathogens, such as the microsporidian endoparasite,<em> Nosema ceranae</em> (Fries et al., 1996). We therefore sought (1) to increase our understanding of the potential effects of FPF on honey bees by focusing on a crucial behavior, the ability to learn and remember an odor associated with a food reward, and (2) to test for a potential synergistic effect on such learning by exposure to FPF and infection with <em>N. ceranae. </em>We found little evidence that FPF significantly alters learning and memory at short-term field-realistic doses. However, at high doses and at chronic, field-realistic exposure, FPF did reduce learning and memory in an olfactory conditioning task. Infection with <em>N. ceranae</em> also reduced learning, but there was no synergy (no significant interaction) between<em> N. ceranae</em> and exposure to FPF. These results suggest the importance of continued studies on the chronic effects of FPF.