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.

中文翻译：

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互补资源的限制会影响大黄蜂的群体生长、觅食行为和繁殖

农业景观中许多生物的资源可用性受到干扰，包括传粉物种。花卉可用性的丰富性和多样性有益于蜜蜂种群，但是，对于哪些蛋白质或碳水化合物资源可能会限制其生长和繁殖性能知之甚少。在这里，我们使用补充喂养方法测试补充资源限制的假设。我们将这一假设应用于大黄蜂 (Bombus terrestris)，假设蜂群生长和繁殖性能应取决于碳水化合物和蛋白质的持续供应，分别通过采食花蜜和花粉。我们沿着半自然栖息地的景观梯度放置野生捕获的大黄蜂群，并监测群的重量，整个群体周期中的觅食活动和繁殖性能。我们将补充喂养作为景观资源限制的一个指标，使用由添加糖水（碳水化合物，补充或不补充）与花粉（蛋白质，补充或不补充）交叉组成的析因设计。大黄蜂群体动态显示出明显的季节性模式，先是增长期，后是停滞期。半自然栖息地的丰度更高导致两个时期花粉觅食者相对于所有觅食者的比例减少，并提高了熊蜂的繁殖性能。有趣的是，糖水的补充喂养对停滞期的菌落重量产生了积极的影响，而花粉的补充喂养减轻了对花粉收集投资的景观影响。糖水和花粉的单一和联合补充增加了半自然栖息地对繁殖性能的积极影响。这项研究揭示了影响熊蜂觅食行为和繁殖性能的花粉和花蜜资源的潜在共同限制，并表明即使在半自然栖息地比例较高的混合农业景观中，熊蜂种群也面临资源限制。我们得出的结论是，在保护中必须考虑花卉资源的季节性管理，以支持农田的熊蜂种群和授粉服务。糖水和花粉的单一和联合补充增加了半自然栖息地对繁殖性能的积极影响。这项研究揭示了影响熊蜂觅食行为和繁殖性能的花粉和花蜜资源的潜在共同限制，并表明即使在半自然栖息地比例较高的混合农业景观中，熊蜂种群也面临资源限制。我们得出的结论是，在保护中必须考虑花卉资源的季节性管理，以支持农田的熊蜂种群和授粉服务。糖水和花粉的单一和联合补充增加了半自然栖息地对繁殖性能的积极影响。这项研究揭示了影响熊蜂觅食行为和繁殖性能的花粉和花蜜资源的潜在共同限制，并表明即使在半自然栖息地比例较高的混合农业景观中，熊蜂种群也面临资源限制。我们得出的结论是，在保护中必须考虑花卉资源的季节性管理，以支持农田的熊蜂种群和授粉服务。并表明即使在半自然栖息地比例较高的混合农业景观中，熊蜂种群也面临资源限制。我们得出的结论是，在保护中必须考虑花卉资源的季节性管理，以支持农田的熊蜂种群和授粉服务。并表明即使在半自然栖息地比例较高的混合农业景观中，熊蜂种群也面临资源限制。我们得出的结论是，在保护中必须考虑花卉资源的季节性管理，以支持农田的熊蜂种群和授粉服务。