The pesticide flupyradifurone impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults

Abstract

Relatively little attention has focused on how pesticides may affect Asian honey bees, which provide vital crop pollination services and are key native pollinators. We therefore studied the effects of a relatively new pesticide, flupyradifurone (FLU), which has been developed, in part, because it appears safer for honey bees than neonicotinoids. We tested the effects of FLU on Apis cerana olfactory learning in larvae (lower dose of 0.033 µg/larvae/day over 6 days) and, in a separate experiment, adults (lower dose of 0.066 µg/adult bee/day) at sublethal, field-realistic doses given over 3 days. A worst-case field-realistic dose is 0.44 µg/bee/day. Learning was tested in adult bees. The lower larval dose did not increase mortality, but the lower adult dose resulted in 20% mortality. The lower FLU doses decreased average olfactory learning by 74% (larval treatment) and 48% (adult treatment) and reduced average memory by 48% (larval treatment) and 22% (adult treatment) as compared to controls. FLU at higher doses resulted in similar learning impairments. The effects of FLU, a pesticide that is reported to be safer than neonicotinoids for honey bees, thus deserve greater attention.

Figure 1

Effects of flupyradifurone on the survival of (A) larvae and (B) adults. Proportions were calculated based upon the number of initially treated larvae. The P-values are from Fisher’s Exact tests, with dashed lines connecting the groups being compared.

Figure 2

Effect of flupyradifurone (FLU) on olfactory learning and memory (PER) in A. cerana bees treated as larvae or adults. The temporal design of the (A) learning and (B) memory trials is shown. For bees treated when they were larvae and tested as adults, we show mean PER for (C) learning (elapsed time from first trial shown in h) and (D) memory (elapsed time from the last rewarded learning trial, t5, shown). For bees treated and tested as adults (foragers), we also show mean PER for (E) learning and (F) memory. Dashed lines with stars link points that are significantly different (Tukey HSD tests, P < 0.05). Standard error bars are shown. The legend shows the FLU dose that each bee (larva or forager) received per day (see Table 1 for details).