Pesticide-exposed bees fail to thermoregulate leading to cold colonies with consequences for offspring development

Insects face multiple environmental stressors, including widespread pesticide exposure under climate change. Thermoregulation is a critical adaptive response to changing environmental temperatures, but if pesticide exposure were to impair this homeostatic process, reproduction and population viability may be at risk. This is of significant relevance to the ecologically important social insects, as multiple individuals must act collectively to maintain brood temperature for the successful rearing of offspring. In this study, we tested if pesticide exposure affects the ability of bumblebee individuals to maintain body temperature, whether such impact translates to reduced colony-level function (brood care and nest thermal homeostasis), and if this consequently impacts offspring development. Conducting three complementary experiments exposing bumblebees to a neonicotinoid pesticide under different temperature challenges, we show: first, that pesticide-exposed individuals cannot maintain a stable thorax temperature especially at lower temperatures. Second, individual reductions in body temperature are accompanied by behavioural changes and that pesticide-exposed colonies fail to maintain appropriate brood temperatures. Third, the impairment to brood thermoregulation (and not the pesticide toxicity to offspring per se) leads to delayed pupal development and reduced adult population growth rate. We provide a valid mechanistic explanation for why terrestrial insects requiring brood thermoregulation have shown signs of decline over the past few decades. With pesticide exposure landscapes being commonplace, and extreme weather events forecasted to become more frequent, our findings have concerning implications for the ability of populations to adequately respond, persist, and grow under current pesticide use regimes with ramifications on pollination services.

昆虫面临多重环境胁迫，包括气候变化背景下广泛存在的农药暴露。体温调节（thermoregulation）是应对环境温度变化的关键适应性响应，但倘若农药暴露损害这一稳态（homeostatic）过程，生殖与种群存续便可能面临风险。这一问题对生态意义重大的社会性昆虫尤为关键，因这类昆虫需依靠多个个体协同维持巢内幼虫发育温度，方可成功抚育后代。

本研究开展三项互补实验，在不同温度胁迫条件下将熊蜂（bumblebee）暴露于新烟碱类农药（neonicotinoid pesticide），结果显示：其一，接触农药的个体无法稳定维持胸部体温，在低温环境下该缺陷尤为显著；其二，个体体温降低伴随行为改变，且接触农药的蜂群无法维持适宜的幼虫抚育温度；其三，幼虫体温调节功能受损（而非农药直接对幼虫产生的毒性）会导致蛹发育延迟、成虫种群增长率下降。

本研究为过去数十年间依赖幼虫体温调节的陆生昆虫种群衰退现象提供了合理的机理性解释。当前农药暴露场景已极为普遍，且极端天气事件预计将愈发频繁，我们的研究结果警示：在现行农药使用模式下，种群能否有效应对环境变化、维持存续并实现增长令人担忧，该结论也将对授粉服务产生连锁影响。