Urbanization Increases Pathogen Pressure on Feral and Managed Honey Bees

Given the role of infectious disease in global pollinator decline, there is a need to understand factors that shape pathogen susceptibility and transmission in bees. Here we ask how urbanization affects the immune response and pathogen load of feral and managed colonies of honey bees (Apis mellifera Linnaeus), the predominant economically important pollinator worldwide. Using quantitative real-time PCR, we measured expression of 4 immune genes and relative abundance of 10 honey bee pathogens. We also measured worker survival in a laboratory bioassay. We found that pathogen pressure on honey bees increased with urbanization and management, and the probability of worker survival declined 3-fold along our urbanization gradient. The effect of management on pathogens appears to be mediated by immunity, with feral bees expressing immune genes at nearly twice the levels of managed bees following an immune challenge. The effect of urbanization, however, was not linked with immunity; instead, urbanization may favor viability and transmission of some disease agents. Feral colonies, with lower disease burdens and stronger immune responses, may illuminate ways to improve honey bee management. The previously unexamined effects of urbanization on honey-bee disease are concerning, suggesting that urban areas may favor problematic diseases of pollinators.

鉴于传染病在全球传粉昆虫种群衰退中发挥的关键作用，学界亟需阐明影响蜜蜂病原体易感性与传播的各类因素。本研究聚焦于城市化如何影响野生与养殖西方蜜蜂（Apis mellifera Linnaeus）——这一全球范围内兼具重要经济价值的优势传粉昆虫——的免疫反应与病原体载荷。我们通过实时定量PCR（quantitative real-time PCR）检测了4种免疫基因的表达水平，以及10种蜜蜂病原体的相对丰度；此外还在实验室生物测定中统计了工蜂的存活率。研究结果显示，蜜蜂承受的病原体压力随城市化水平与蜂群管理模式的提升而升高，且工蜂存活概率沿本次研究设置的城市化梯度下降至初始水平的1/3。蜂群管理对病原体的影响似乎由免疫反应介导：在经受免疫激发后，野生蜂群的免疫基因表达量几乎达到养殖蜂群的两倍。但城市化的影响并未与免疫反应产生关联；与之相反，城市化或可提升部分病原体的存活能力与传播效率。野生蜂群具有更低的病原体载荷与更强的免疫反应，其相关研究结果或可为优化蜜蜂养殖管理提供可行思路。此前尚未得到系统探究的城市化对蜜蜂病害的影响令人担忧，这表明城市环境或许会助长传粉昆虫的致病性病害问题。