Sub-lethal concentrations of neonicotinoid insecticides at the field level affect negatively honey yield: Evidence from a 6-year survey of Greek apiaries

The threats posed by neonicotinoid insecticides to bee populations have been the focus of considerable research. Previous work has shed new light on the effects of neonicotinoids on bees by uncovering pathways through which neonicotinoids affect bee population dynamics and the potential interactions they have with exogenous stressors. Yet, little is known about whether these effects translate in a field-relevant setting to substantial losses in honey yields for commercial beekeepers. Here, we used data from a 6-year survey of 60 apiaries in Greece and economic modelling to assess at the field level the effects of neonicotinoid insecticides on honey production. Based on production function estimates, we found that sub-lethal concentrations of two widely used neonicotinoid insecticides (imidacloprid and thiamethoxam) detected in the nectar of flowers resulted in substantial losses in honey production for commercial beekeepers in our sample. By simulating a scenario with ideal pathogenic and environmental conditions, we found that the magnitude of the neonicotinoid effects decreases significantly under ideal conditions providing evidence for possible synergies at the field between neonicotinoids and environmental and pathogenic factors. Moreover, in a replicated study with grouped apiaries, we found evidence that the marginal effects of neonicotinoids on honey production vary across apiaries facing different conditions.新烟碱类杀虫剂（neonicotinoid insecticides）对蜂群构成的威胁一直是相关研究的重点议题。既往研究通过揭示新烟碱类杀虫剂影响蜂群动态的作用通路，及其与外源胁迫因子的潜在交互作用，为阐明该类药剂对蜜蜂的效应提供了新的认知。然而，目前学界尚不清楚此类效应在田间实际场景中，是否会转化为商业养蜂场的显著蜂蜜产量损失。本研究依托对希腊60个养蜂场开展的为期6年的调查数据，并结合经济建模方法，从田块尺度评估了新烟碱类杀虫剂对蜂蜜生产的影响。基于生产函数估计结果，本研究发现：在花朵花蜜中检出的两种广泛使用的新烟碱类杀虫剂——吡虫啉（imidacloprid）和噻虫嗪（thiamethoxam）——的亚致死浓度，会导致本研究样本中的商业养蜂场出现显著的蜂蜜产量损失。通过模拟理想病原与环境条件的场景，本研究发现：新烟碱类杀虫剂的效应强度在理想条件下会显著降低，这为田间场景中新烟碱类杀虫剂与环境、病原因子间可能存在的协同作用提供了证据。此外，在一项针对分组养蜂场的重复研究中，本研究发现：新烟碱类杀虫剂对蜂蜜生产的边际效应，会因不同养蜂场所处的环境条件差异而有所不同。