Higher probability of tick infestation reveals a hidden cost of army ant-following in Amazonian birds

The foraging specialization of army-ant-following birds has long intrigued ecologists and provided numerous questions such as why, how, and when did this foraging guild specialization arise and evolve. Many of the answers to these questions have focused on ecological interactions such as predation and competition, whereas little has been done to study the potential effects of host-parasite interactions among members of this foraging guild. Using 1,177 Amazonian birds from 187 species, we studied the probability of tick infestation in relation to attendance of birds at army-ant swarms. We demonstrate that the probability of tick infestation was higher among professional and occasional ant-followers than in bird species that do not follow army ants to prey upon leaf-litter flushed arthropods. Moreover, occasional ant-followers harbored a greater diversity of nymphal ticks. We argue that although the evolutionary transition toward specialized ant-following behavior has a genetic basis, a trade-off between the cost of evolution of this trait and its fitness benefits might exist. In this case, the cost is in the form of higher parasite pressure. Therefore, parasites may impose a selective pressure not only during foraging but also through the allocation of resources for an immunological response. Our results of an analysis of tick parasitism on Amazonian birds emphasizes the importance of parasitic organisms on ecology and evolution of behavioural traits of their hosts. Considering the effects imposed by parasite pressure is essential for understanding the evolution and maintenance of behavioral and life-history traits.

长期以来，跟随行军蚁的鸟类（army-ant-following birds）的觅食特化现象一直令生态学家着迷，并催生了诸多核心研究问题：这类觅食功能群（foraging guild）特化是如何起源、为何演化，以及其演化的时间节点为何？过往针对这些问题的解答多聚焦于捕食与竞争等生态相互作用，而鲜有研究探讨该觅食功能群内部宿主-寄生虫相互作用（host-parasite interactions）可能带来的影响。本研究使用了来自187个物种的1177只亚马逊地区鸟类样本，分析了鸟类参与行军蚁群活动与蜱虫侵染（tick infestation）概率之间的关联。研究结果显示，专职与偶见的行军蚁跟随鸟类的蜱虫侵染概率，显著高于不以跟随行军蚁捕食凋落物惊起的节肢动物为食的鸟类类群。此外，偶见的行军蚁跟随鸟类所携带的蜱虫若虫（nymphal ticks）多样性更高。我们认为，尽管向特化行军蚁跟随行为的演化过渡存在遗传基础，但该性状的演化成本与适合度收益（fitness benefits）之间可能存在权衡（trade-off）关系。在此情境下，该演化成本表现为更高的寄生虫压力。因此，寄生虫不仅会在觅食过程中施加选择压力，还会通过宿主为免疫应答分配资源的方式施加选择压力。本研究针对亚马逊鸟类蜱虫寄生情况的分析结果，凸显了寄生物对宿主行为性状的生态与演化过程的重要意义。考量寄生虫压力所带来的影响，对于理解行为与生活史性状的演化与维持机制至关重要。