Low doses of neonicotinoid pesticides in food rewards impair short-term olfactory memory in foraging-age honeybees.

Geraldine A Wright,Helen Earnshaw,Samantha Softley

doi:10.1038/srep15322

Abstract

Neonicotinoids are often applied as systemic seed treatments to crops and have reported negative impact on pollinators when they appear in floral nectar and pollen. Recently, we found that bees in a two-choice assay prefer to consume solutions containing field-relevant doses of the neonicotinoid pesticides, imidacloprid (IMD) and thiamethoxam (TMX), to sucrose alone. This suggests that neonicotinoids enhance the rewarding properties of sucrose and that low, acute doses could improve learning and memory in bees. To test this, we trained foraging-age honeybees to learn to associate floral scent with a reward containing nectar-relevant concentrations of IMD and TMX and tested their short (STM) and long-term (LTM) olfactory memories. Contrary to our predictions, we found that none of the solutions enhanced the rate of olfactory learning and some of them impaired it. In particular, the effect of 10 nM IMD was observed by the second conditioning trial and persisted 24 h later. In most other groups, exposure to IMD and TMX affected STM but not LTM. Our data show that negative impacts of low doses of IMD and TMX do not require long-term exposure and suggest that impacts of neonicotinoids on olfaction are greater than their effects on rewarding memories.

Highlights

Several previous studies have shown that honeybees exposed to neonicotinoids prior to learning and memory tasks exhibit slower rates of learning and poor memory formation[6,7,8,9]
Bees rewarded with sucrose containing IMD during both massed and spaced learning were less likely to learn to associate the odour with food (Fig. 1a,b, massed: repeated-measures lreg, χ 32 = 29.9, P < 0.001; spaced: repeated-measures lreg, χ 32 = 56.8, P < 0 .001)
Comparisons within groups revealed that bees conditioned with TMX in rewards were more likely to respond during the LTM test than the STM test. The premise of these experiments was to test whether low, field-relevant doses of the neonicotinoids, IMD and TMX, enhanced learning and memory when they were present in food rewards during olfactory conditioning

Summary

Introduction

Several previous studies have shown that honeybees exposed to neonicotinoids prior to learning and memory tasks exhibit slower rates of learning and poor memory formation[6,7,8,9]. We could find only one study in which bees were trained with food containing neonicotinoids during conditioning, and this was for a 1-trial olfactory learning task using a very high dose that did not examine the impact on learning[6]. We examined how nectar-relevant concentrations of IMD and TMX in sucrose rewards affected the rate of learning during olfactory conditioning of the PER. Massed conditioning (30 s inter-trial interval) was used to examine how IMD and TMX would affect learning as bees might experience it during foraging. Spaced conditioning (5 min inter-trial interval) was used to determine the extent to which IMD and TMX affected the formation of LTM

Methods

Results

Conclusion