Limitation of complementary resources affects colony growth, foraging behavior, and reproduction in bumble bees

Resource availability has been disturbed for many organisms in agricultural landscapes including pollinator species. Abundance and diversity in flower availability benefit bee populations, however, little is known about which of protein or carbohydrate resources may limit their growth and reproductive performance. Here, we test the hypothesis of complementary resource limitation using a supplemental feeding approach. We applied this assumption with bumble bees (Bombus terrestris), assuming that colony growth and reproductive performance should depend on the continuous supply of carbohydrates and proteins, through the foraging for nectar and pollen respectively. We placed wild-caught bumble bee colonies along a landscape gradient of semi-natural habitats, and monitored the colonies’ weight, foraging activity and reproductive performance during the whole colony cycle. We performed supplemental feeding as an indicator of landscape resource limitation, using a factorial design consisting of the addition of sugar-water (carbohydrate, supplemented or not) crossed by pollen (protein, supplemented or not). Bumble bee colony dynamics showed a clear seasonal pattern with a period of growth followed by a period of stagnation. Higher abundance of semi-natural habitats resulted in reducing the proportion of pollen foragers relative to all foragers in both periods, and in improving the reproductive performance of bumble bees. Interestingly, the supplemental feeding of sugar-water positively affected the colony weight during the stagnation period, while the supplemental feeding of pollen mitigated the landscape effect on pollen collection investment. Single and combined supplementation of sugar-water and pollen increased the positive effect of semi-natural habitats on reproductive performance. This study reveals a potential co-limitation in pollen and nectar resources affecting foraging behavior and reproductive performance in bumble bees, and indicates that even in mixed agricultural landscapes with higher proportions of semi-natural habitats, bumble bee populations face resource limitations. We conclude that the seasonal management of floral resources must be considered in conservation to support bumble bee populations and pollination services in farmlands.

农业景观中包括传粉昆虫在内的诸多生物的资源可获得性均已受到干扰。尽管花资源的丰度与多样性可惠及蜂群，但目前学界尚不清楚蛋白质或碳水化合物资源中，究竟哪一种会限制它们的生长与繁殖表现。本研究采用补充饲喂的实验方法，验证互补性资源限制假说。我们以野外捕获的熊蜂（Bombus terrestris）蜂群为研究对象，假设其蜂群生长与繁殖表现分别依赖于通过觅食花蜜获取碳水化合物、通过觅食花粉获取蛋白质的持续供给。我们将熊蜂蜂群放置在沿半自然生境梯度布设的景观样地中，并在整个蜂群生命周期内监测其体重、觅食活动与繁殖表现。本研究以补充饲喂作为景观资源限制的指示指标，采用析因实验设计：设置糖水（碳水化合物，添加/不添加）与花粉（蛋白质，添加/不添加）的交叉处理。熊蜂蜂群动态呈现出清晰的季节模式：先经历生长阶段，随后进入停滞阶段。半自然生境占比更高的景观样地，可在两个监测阶段均降低所有觅食蜂中花粉采集蜂的占比，并提升熊蜂的繁殖表现。值得注意的是，在停滞阶段补充饲喂糖水可正向提升蜂群体重，而补充饲喂花粉则可缓解景观因素对花粉采集投入的影响。单独或联合补充糖水与花粉，均能增强半自然生境对熊蜂繁殖表现的正向效应。本研究揭示了花粉与花蜜资源可能存在共同限制效应，该效应会影响熊蜂的觅食行为与繁殖表现；同时表明，即便在半自然生境占比较高的混合农业景观中，熊蜂种群仍面临资源限制问题。综上，在农田生态系统的保护实践中，需考虑花资源的季节性管理策略，以支撑熊蜂种群存续与农田传粉服务功能。