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

Neonicotinoids 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 use 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 decition-making caused by thiamethoxam exposure could be more harmful than other neonicotinoids, leading to inefficient foraging and a reduced ability to identify nestmates.

新烟碱类杀虫剂（neonicotinoids）是一类用于作物保护的药剂，但已有研究证实其在亚致死剂量下会对蜜蜂产生明确的次生影响。蜜蜂依靠嗅觉识别蜂王与同伴、传递危险信号，并在觅食过程中区分不同花朵。迄今为止，鲜有行为学研究探讨新烟碱类杀虫剂如何影响蜜蜂的气味识别能力。本研究采用辨别学习范式，探究新烟碱类药剂暴露对觅食适龄蜜蜂的学习、记忆及嗅觉感知能力的影响。饲喂噻虫嗪（thiamethoxam）的蜜蜂无法完成辨别学习任务，且在短时记忆与长时记忆测试中均无法区分气味。本研究数据表明，噻虫嗪会直接干扰辨别性嗅觉学习过程中工作记忆所需的认知过程。结合行为学实验手段，本研究还证实噻虫嗪会直接影响蜜蜂对相似气味的嗅觉感知能力。饲喂其他新烟碱类药剂——噻虫胺（clothianidin）、吡虫啉（imidacloprid）、呋虫胺（dinotefuran）——的蜜蜂虽可完成辨别学习任务，但完成速率慢于对照组，且同样能够区分气味。本研究数据首次证实，新烟碱类药剂对蜜蜂完成复杂嗅觉学习任务的能力存在化合物特异性影响。噻虫嗪暴露引发的决策能力缺陷，其危害或甚于其他新烟碱类药剂，会导致觅食效率低下以及识别同伴的能力下降。