Department of Biology, University of Texas Rio Grande Valley, Brownsville, TX 78520, USA.
Institute of Neuroscience, Newcastle University, Newcastle upon Tyne NE2 4HH, UK.
J Exp Biol. 2020 Feb 28;223(Pt 5):jeb217174. doi: 10.1242/jeb.217174.
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 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.
新烟碱类杀虫剂被用于保护作物,但在亚致死剂量下对蜜蜂有已知的次要影响。蜜蜂利用嗅觉来识别蜂王和巢内同伴,发出危险信号,并在觅食时区分花朵。迄今为止,很少有行为研究检查新烟碱类杀虫剂如何影响蜜蜂区分气味的能力。在这里,我们使用差异学习任务来测试新烟碱类杀虫剂暴露如何影响觅食期蜜蜂的学习、记忆和嗅觉感知。喂食噻虫嗪的蜜蜂无法进行差异学习,也无法在短期和长期记忆测试中区分气味。我们的数据表明,噻虫嗪直接影响差异嗅觉学习过程中所需的工作记忆的认知过程。通过结合行为测定,我们还发现噻虫嗪对类似气味的嗅觉感知有直接影响。喂食其他新烟碱类杀虫剂(噻虫胺、吡虫啉、噻虫呋)的蜜蜂完成了差异学习任务,但速度比对照组慢。这些蜜蜂也能区分气味。我们的数据首次表明,新烟碱类杀虫剂对蜜蜂执行复杂嗅觉学习任务的能力有特定的复合影响。噻虫嗪暴露导致的决策能力下降可能意味着它比其他新烟碱类杀虫剂更有害,导致觅食效率降低,识别巢内同伴的能力降低。