Abstract

Pesticides, including neonicotinoids, typically target pest insects by being neurotoxic. Inadvertent exposure to foraging insect pollinators is usually sub-lethal, but may affect cognition. One cognitive trait, spatial working memory, may be important in avoiding previously-visited flowers and other spatial tasks such as navigation. To test this, we investigated the effect of acute thiamethoxam exposure on spatial working memory in the bumblebee Bombus terrestris, using an adaptation of the radial-arm maze (RAM). We first demonstrated that bumblebees use spatial working memory to solve the RAM by showing that untreated bees performed significantly better than would be expected if choices were random or governed by stereotyped visitation rules. We then exposed bees to either a high sub-lethal positive control thiamethoxam dose (2.5 ng−1 bee), or one of two low doses (0.377 or 0.091 ng−1) based on estimated field-realistic exposure. The high dose caused bees to make more and earlier spatial memory errors and take longer to complete the task than unexposed bees. For the low doses, the negative effects were smaller but statistically significant, and dependent on bee size. The spatial working memory impairment shown here has the potential to harm bees exposed to thiamethoxam, through possible impacts on foraging efficiency or homing.

Highlights

  • Pesticides, including neonicotinoids, typically target pest insects by being neurotoxic

  • Analysis of the final training bout showed that bees displayed a moderate tendency to travel to the nearest neighbouring flower (“contiguity preference”), and in addition, transition frequency between neighbouring flower pairs was negatively correlated with angle from vertical between flowers (Spearman’s rho =−​0.87) implying an additional preference to fly vertically upwards

  • We tested bees treated with a high dose of the neonicotinoid thiamethoxam as a positive control and observed negative effects on bumblebee spatial working memory

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Summary

Introduction

Pesticides, including neonicotinoids, typically target pest insects by being neurotoxic. Inadvertent exposure to foraging insect pollinators is usually sub-lethal, but may affect cognition. We investigated the effect of acute thiamethoxam exposure on spatial working memory in the bumblebee Bombus terrestris, using an adaptation of the radial-arm maze (RAM). The spatial working memory impairment shown here has the potential to harm bees exposed to thiamethoxam, through possible impacts on foraging efficiency or homing. Animal pollinators are key ecosystem service providers across most terrestrial landscapes They pollinate around 87.5% of flowering plants worldwide[1], and economically are responsible for approximately 9.5% of the value of global food production[2]. Olfactory learning and memory have been shown to be impaired by sub-lethal neonicotinoid exposure in honeybees[21,22] and bumblebees[23]. We investigate the effect of pesticide exposure on spatial working memory in a key pollinator, Bombus terrestris L. We investigate the effect of pesticide exposure on spatial working memory in a key pollinator, Bombus terrestris L. (Fig. 1a)

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