A neonicotinoid impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults

Abstract

Xenobiotics such as the neonicotinoid pesticide, imidacloprid, are used globally, but their effects on native bee species are poorly understood. We studied the effects of sublethal doses of imidacloprid on olfactory learning in the native honey bee species, Apis cerana, an important pollinator of agricultural and native plants throughout Asia. We provide the first evidence that imidacloprid can impair learning in A. cerana workers exposed as adults or as larvae. Adults that ingested a single imidacloprid dose as low as 0.1 ng/bee had significantly reduced olfactory learning acquisition, which was 1.6-fold higher in control bees. Longer-term learning (1-17 h after the last learning trial) was also impaired. Bees exposed as larvae to a total dose of 0.24 ng/bee did not have reduced survival to adulthood. However, these larval-treated bees had significantly impaired olfactory learning when tested as adults: control bees exhibited up to 4.8-fold better short-term learning acquisition, though longer-term learning was not affected. Thus, sublethal cognitive deficits elicited by neonicotinoids on a broad range of native bee species deserve further study.

Figure 1. Effect of imidacloprid on olfactory PER learning in A. cerana bees treated when they were adults or brood.

The temporal design of the (a) short-term and (b) longer-term trials is shown. For bees treated and tested as adults, we show mean PER for (c) short-term learning acquisition (elapsed time from first trial shown) and (d) longer-term learning retention (elapsed time from the last reinforced learning trial, t5, shown). For bees treated when they were larvae and tested as adults, we show mean PER for (e) short-term and (f) longer-term learning. Lines link points with significant contrasts (*P < 0.05, **P ≤ 0.01, ***P ≤ 0.001, ****P ≤ 0.0001). Standard error bars are shown. The x-axes show time (h) and trial numbers.