Honey bee (Apis mellifera L.) populations have undergone a dramatic decline as an outcome of an increasing incidence of colony collapse disorder (CCD). The honey bee is a unique keystone species because its pollination activities are not only necessary for the viability of many flowering plant species in the wild, but are also necessary for many human agricultural practices. The increasing prevalence of CCD is a threat to the economic and nutritional security of all societies that rely on efficient pollination for large monoculture crops. Although there is ample evidence that Varroa mites, pesticides, disease, and climate change contribute to CCD, only a few studies have investigated the contribution of synergism across multiple factors to the development of CCD and CCD-like symptoms. However, there is increasing acknowledgement in the scientific community that synergism across different factors affects honey bee colony health and behavior. Here, we provide evidence that sub-lethal levels of imidacloprid neonicotinoid pesticide reduce learning and memory capabilities. Synergistic effects become apparent when Varroa mites together with imidacloprid exposure to individual bees more than doubled average mortality and attrition per trial.

蜜蜂（Apis mellifera L.）由于菌落崩溃障碍（CCD）的发病率上升，导致种群数量急剧下降。蜜蜂是独特的基石种，因为它的授粉活性不仅对野生许多开花植物物种的生存能力是必需的，而且对许多人类农业实践也是必需的。CCD的日益流行对所有依靠大型单作作物进行有效授粉的社会的经济和营养安全构成威胁。尽管有足够的证据表明瓦螨，杀虫剂，疾病和气候变化对CCD有影响，但只有少数研究调查了多种因素对CCD和CCD样症状发展的协同作用。然而，科学界越来越认识到，不同因素之间的协同作用会影响蜜蜂群体的健康和行为。在这里，我们提供证据表明亚吡虫啉新烟碱类农药的亚致死水平会降低学习和记忆能力。当Varroa螨虫与吡虫啉对个体蜜蜂的接触加在一起时，协同效应变得很明显，每项试验的平均死亡率和减员率翻了一番以上。