Honey bee introductions displace native bees and decrease pollination of a native wildflower

Introduced species can have cascading effects on ecological communities,
but indirect effects of species introductions are rarely the focus of
ecological studies. For example, managed honey bees (Apis mellifera) have
been widely introduced outside their native range and are increasingly
dominant floral visitors. Multiple studies have documented how honey bees
impact native bee communities through floral resource competition, but few
have quantified how these competitive interactions indirectly affect
pollination and plant reproduction. Such indirect effects are hard to
detect because honey bees are themselves pollinators and may directly
impact pollination through their own floral visits. The potentially huge
but poorly understood impacts that non-native honey bees have on native
plant populations combined with increased pressure from beekeepers to
place hives in U.S. National Parks and Forests makes exploring the impacts
of honey bee introductions on native plant pollination of pressing
concern. In this study, we used experimental hive additions, field
observations, as well as single-visit and multiple-visit pollination
effectiveness trials across multiple years to untangle the direct and
indirect impacts of increasing honey bee abundance on the pollination of
an ecologically important wildflower, Camassia quamash. We found
compelling evidence that honey bee introductions indirectly decrease
pollination by reducing nectar and pollen availability and competitively
excluding visits from more effective native bees. In contrast, the direct
impact of honey bee visits on pollination was negligible, and, if
anything, negative. Honey bees were ineffective pollinators and increasing
visit quantity could not compensate for inferior visit quality. Indeed,
although the effect was not statistically significant, increased honey bee
visits had a marginally negative impact on seed production. Thus, honey
bee introductions may erode longstanding plant-pollinator mutualisms, with
negative consequences for plant reproduction. Our study calls for a more
thorough understanding of the indirect effects of species introductions
and more careful coordination of hive placements.

引入物种可能对生态群落产生级联效应，但物种引入的间接效应却很少成为生态学研究的焦点。例如，人工饲养的意大利蜜蜂（Apis mellifera）已被广泛引入其原生分布区以外的区域，且日益成为优势传粉者。多项研究已记录蜜蜂如何通过花资源竞争影响本地蜜蜂群落，但很少有研究量化这些竞争相互作用如何间接影响传粉和植物繁殖。这类间接效应难以检测，因为蜜蜂自身也是传粉者，可能通过其自身的访花行为直接影响传粉。非本地蜜蜂对本地植物种群潜在的巨大但知之甚少的影响，加上养蜂人将蜂箱放置在美国国家公园和森林中的压力日益增加，使得探索蜜蜂引入对本地植物传粉的影响成为一个迫切关注的问题。本研究通过多年的实验性添加蜂箱、野外观察以及单次和多次访花传粉有效性试验，厘清了蜜蜂数量增加对一种具有生态重要性的野花——卡马夏花（Camassia quamash）传粉的直接和间接影响。我们发现有力证据表明，引入蜜蜂通过降低花蜜和花粉的可获得性以及竞争排斥更有效的本地蜜蜂访花，间接减少了传粉。相比之下，蜜蜂访花对传粉的直接影响可忽略不计，甚至可能是负面的。蜜蜂是低效的传粉者，增加访花数量无法弥补其访花质量的不足。事实上，尽管该效应在统计上不显著，但蜜蜂访花增加对种子产量有轻微负面影响。因此，引入蜜蜂可能侵蚀长期存在的植物-传粉者共生关系，对植物繁殖产生负面后果。本研究呼吁更深入理解物种引入的间接效应，并更谨慎地协调蜂箱放置。