Pollinator diversity and abundance in North America have been at a steep decline over the last two decades due to the combinatorial effects of several environmental and anthropogenic stressors. In particular, managed honey bees (Apis mellifera) face multiple health risks including nutritional stress, exposure to pests and pathogens, poor queen quality, and pesticide contamination, which cause problems at the individual and colony levels. One of the gravest problems faced by honey bees is parasitization by the mite Varroa destructor, which is typically controlled through the application of miticides such as tau-fluvalinate, coumaphos, and amitraz. In addition to miticides, colonies are also exposed to pesticides brought by foragers from agricultural settings, including the fungicide chlorothalonil and the insecticide chlorpyrifos. Here, we explored whether exposure of wax to combinations of these pesticides during development affects honey bee queen physiology and worker behavior. To do this, we reared queens in plastic cups coated with molten beeswax that was either pesticide-free or containing field-relevant concentrations of tau-fluvalinate and coumaphos, amitraz, or chlorothalonil and chlorpyrifos. Once queens mated naturally, we placed them in observation hives to measure egg-laying rate and worker retinue size. We then dissected the queens and used the contents of their mandibular glands to measure worker attractiveness in caged bioassays and to analyze their chemical components using GC-MS. Exposure of wax to field-relevant concentrations of the tested pesticides during queen development significantly lowered the adult queens’ egg-laying rate and worker retinue size. Miticide exposure during development also lowered the attractiveness of queen mandibular gland contents to workers and affected the relative amounts of the glands’ chemical components. Our results support the ideas that mandibular gland pheromones act as honest indicators of queen reproductive fitness and that pesticide exposure of wax during bee development is an important and concerning factor impairing honey bee health. Pollinator health is currently being threatened by multiple environmental factors, including poor nutrition, habitat fragmentation, and pesticide contamination. In particular, honey bee health is facing challenges caused by combinations of these factors, leading to an annual mortality of over 30% of all managed colonies in the USA. The conditions in which honey bee queens are reared can cause severe physiological and behavioral effects in adults, which in turn can affect the behavior of workers that tend to those queens, thus affecting colony productivity, growth, and survival. In this study, we show that queens reared in beeswax contaminated with miticides or agrochemicals lay fewer eggs over time and exhibit mandibular gland pheromone profiles that differ from those of queens reared in pesticide-free wax. Workers discern these differences, preferentially investigating the gland contents and forming larger retinues (thus performing more tending behaviors) for queens reared in pesticide-free wax. These results indicate that pesticide contamination of the queen-rearing wax directly affects queen physiology and behavior and further affirm that queen mandibular pheromones seem to act as honest indicators to workers of a queen’s reproductive capacity and overall health.

中文翻译：

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蜂王 (Apis mellifera) 信息素和生殖行为在发育过程中受到农药暴露的影响

由于几种环境和人为压力因素的组合影响，北美的传粉媒介多样性和丰度在过去二十年中急剧下降。特别是，受管理的蜜蜂 (Apis mellifera) 面临多种健康风险，包括营养压力、接触害虫和病原体、蜂王质量差以及农药污染，这会在个体和群体层面造成问题。蜜蜂面临的最严重的问题之一是螨破坏瓦螨的寄生，通常通过使用 tau-fluvalinate、香豆磷和双甲脒等杀螨剂来控制。除了杀螨剂外，菌落还会接触到来自农业环境的觅食者带来的杀虫剂，包括杀菌剂百菌清和杀虫剂毒死蜱。这里，我们探讨了在发育过程中蜡接触这些杀虫剂的组合是否会影响蜂王的生理和工蜂行为。为此，我们将蜂王放在涂有熔融蜂蜡的塑料杯中饲养，这些蜂蜡不含农药或含有田间相关浓度的 tau-fluvalinate 和香豆磷、双甲脒或百菌清和毒死蜱。一旦蜂王自然交配，我们将它们放在观察蜂箱中以测量产卵率和工人随从的大小。然后，我们解剖了蜂王，并使用它们下颌腺的内容物在笼式生物测定中测量工人的吸引力，并使用 GC-MS 分析它们的化学成分。在蜂王发育期间将蜡暴露于与田间相关浓度的测试杀虫剂中，显着降低了成年蜂王的产卵率和工人随从的大小。在发育过程中接触杀螨剂也降低了蜂王下颌腺内容物对工蚁的吸引力，并影响了腺体化学成分的相对含量。我们的结果支持下颌腺信息素作为蜂王生殖健康的可靠指标的观点，并且在蜜蜂发育过程中接触农药的蜡是损害蜜蜂健康的一个重要且相关的因素。传粉者的健康目前正受到多种环境因素的威胁，包括营养不良、栖息地破碎和农药污染。尤其是，蜜蜂健康正面临由这些因素共同造成的挑战，导致美国所有管理蜂群的年死亡率超过 30%。蜜蜂蜂王的饲养条件会对成虫造成严重的生理和行为影响，进而影响照料蜂王的工蜂的行为，从而影响蜂群生产力、生长和存活。在这项研究中，我们表明，随着时间的推移，在被杀螨剂或农用化学品污染的蜂蜡中饲养的蜂王产卵较少，并且其下颌腺信息素谱与在无农药蜂蜡中饲养的蜂蜡不同。工蚁辨别这些差异，优先研究腺体内容物，并为在无农药蜡中饲养的蜂王形成更大的随从（从而表现出更多的抚育行为）。