Honeybees fail to discriminate floral scents in a complex learning task after consuming a neonicotinoid pesticide.

Julie A Mustard,Anne Gott,Nancy L Chavarria,Geraldine A Wright,Jennifer Scott

doi:10.1242/jeb.217174

Abstract

ABSTRACTNeonicotinoids are pesticides used to protect crops but with known secondary influences at sublethal doses on bees. Honeybees use their sense of smell to identify the queen and nestmates, to signal danger and to distinguish flowers during foraging. Few behavioural studies to date have examined how neonicotinoid pesticides affect the ability of bees to distinguish odours. Here, we used a differential learning task to test how neonicotinoid exposure affects learning, memory and olfactory perception in foraging-age honeybees. Bees fed with thiamethoxam could not perform differential learning and could not distinguish odours during short- and long-term memory tests. Our data indicate that thiamethoxam directly impacts the cognitive processes involved in working memory required during differential olfactory learning. Using a combination of behavioural assays, we also identified that thiamethoxam has a direct impact on the olfactory perception of similar odours. Honeybees fed with other neonicotinoids (clothianidin, imidacloprid, dinotefuran) performed the differential learning task, but at a slower rate than the control. These bees could also distinguish the odours. Our data are the first to show that neonicotinoids have compound specific effects on the ability of bees to perform a complex olfactory learning task. Deficits in decision making caused by thiamethoxam exposure could mean that this is more harmful than other neonicotinoids, leading to inefficient foraging and a reduced ability to identify nestmates.

Highlights

Since the beginning of the 20th century, agriculture has increasingly relied on industrial chemicals that kill or repel insect pests, fungi, non-crop plants and plant pathogens
Honeybees fed for 48 h with a field-relevant concentration of a neonicotinoid pesticide, had difficulty performing the olfactory, differential learning task (Fig. 1)
We verified the results of the gustatory assay by testing each subject for its response to the sucrose solution and to the quinine solution; TMX exposure did not have a significant effect on the response to sucrose or quinine. These data are the first to show that the neonicotinoid TMX completely ablates the ability of bees to learn to associate odours with different outcomes. These bees generalized among odours during the 10 min and 24 h memory tests as if they could not distinguish the conditioned stimuli (CS)+ from the CS−, indicating that they could not learn the different odour–outcome associations or could not distinguish the odours

Summary

Introduction

Since the beginning of the 20th century, agriculture has increasingly relied on industrial chemicals that kill or repel insect pests, fungi, non-crop plants and plant pathogens. Pesticides are often applied to crops as a seed dressing; when the plant grows, the pesticides permeate the plant’s tissues. Compounds that cannot be applied to seeds as systemic pesticides are instead applied through water sources or sprayed topically While the main intention of the application of these substances to plants is to target pests, many of the compounds affect ‘non-target’ organisms such as pollinators like bees

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Results

Conclusion