Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure

1. Insect pollination is a vital ecosystem service that maintains biodiversity and sustains agricultural crop yields. Social bees are essential insect pollinators so it is concerning that their populations are in global decline. 2. Although pesticide exposure has been implicated as a possible cause for bee declines, we currently have a limited understanding of the risk these chemicals pose. Whilst environmental exposure to pesticides typically has non-lethal effects on individual bees, recent reports suggest that sublethal exposure can affect important behavioural traits such as foraging. However, at present we know comparatively little about how natural foraging behaviour is impaired and the relative impacts of acute and chronic effects. 3. Using Radio Frequency Identification (RFID) tagging technology we examined how the day-to-day foraging patterns of bumblebees (Bombus terrestris) were affected when exposed to either a neonicotinoid (imidacloprid) and/or a pyrethroid (λ-cyhalothrin) independently and in combination over a four week period. This is the first study to provide data on the impacts of combined and individual pesticide exposure on the temporal dynamics of foraging behaviour in the field over a prolonged period of time. 4. Our results show that neonicotinoid exposure has both acute and chronic effects on overall foraging activity. While foragers from control colonies improved their pollen foraging performance as they gained experience, the performance of bees exposed to imidacloprid became worse: chronic behavioural impairment. We also found evidence suggesting that pesticide exposure can change forager preferences for the flower types from which they collect pollen. 5. Our findings highlight the importance of considering prolonged exposure (which happens in the field) when assessing the risk that pesticides pose to bees. The effects of chronic pesticide exposure could have serious detrimental consequences for both colony survival and also the pollination services provided by these essential insect pollinators.

1. 昆虫传粉是维持生物多样性、保障农作物产量的关键生态系统服务。社会性蜜蜂作为核心昆虫传粉者，其全球种群数量下降的现状令人担忧。
2. 尽管农药暴露被认为可能是蜜蜂种群衰减的诱因之一，但当前学界对这类化学物质带来的风险仍缺乏充分认知。环境中的农药暴露通常仅对单个蜜蜂产生非致死效应，但近期研究表明，亚致死剂量的暴露会影响其觅食等重要行为性状。然而，目前我们对自然觅食行为受损的具体机制，以及急性与慢性影响的相对强度，仍知之甚少。
3. 本研究借助射频识别（Radio Frequency Identification, RFID）标记技术，在为期四周的实验中，分别及联合检测了新烟碱类杀虫剂吡虫啉（imidacloprid）与拟除虫菊酯类杀虫剂氯氟氰菊酯（λ-cyhalothrin）对熊蜂（Bombus terrestris）日常觅食模式的影响。本研究首次提供了长期野外环境下，农药单独及联合暴露对觅食行为时间动态影响的相关数据。
4. 研究结果显示，新烟碱类药物暴露对整体觅食活动兼具急性与慢性影响。对照组蜂群的觅食者随着经验积累，花粉觅食绩效逐步提升；而暴露于吡虫啉的蜜蜂其觅食绩效却持续恶化，表现出慢性行为损伤。此外，我们还发现证据表明，农药暴露会改变觅食者采集花粉的花卉类型偏好。
5. 本研究结果凸显了在评估农药对蜜蜂的风险时，需考虑野外实际存在的长期暴露场景的重要性。慢性农药暴露可能对蜂群存活以及这类关键传粉昆虫所提供的传粉服务均造成严重的不利影响。