Costa-Silva Vitor M, De-Freitas Iasmim, Del-Claro Kleber, Moreira Xoaquín
Graduate Program in Entomology, Department of Biology, Universidade de São Paulo. Ribeirão Preto, SP, Brazil.
Graduate Program in Ecology and Conservation of Natural Resources, Institute of Biology, Universidade Federal de Uberlândia, Uberlândia, MG, Brazil.
Ann Bot. 2025 Jul 17. doi: 10.1093/aob/mcaf156.
Protection mutualisms involve plants receiving defence against herbivores from predators such as ants and insectivorous birds in exchange for food resources. Ants can reduce herbivory by actively patrolling plants with extrafloral nectaries (EFNs) or by tending trophobiotic insects that provide them with food rewards. Insectivorous birds also contribute to herbivore suppression but may simultaneously reduce ant activity through predation. While both ants and birds can enhance plant performance, few studies have explored how the availability of multiple ant-associated resources influences herbivore suppression, or how bird predation on ants affects these ant-plant mutualisms. These gaps limit our understanding of the dynamics in complex multitrophic interactions.
We investigated how the availability of multiple food resources for ants and the predation exerted by insectivorous birds on ants influence the performance of the tropical shrub Banisteriopsis malifolia. To address this, we conducted two field experiments. The first manipulated the individual and combined presence of mutualistic ant resources-EFNs, myrmecophilous caterpillars, and treehoppers. The second experiment manipulated the presence or absence of both ants and birds to assess their interactive effects. Plant performance was evaluated by measuring leaf herbivore damage, fruit number, and fruit weight.
Our findings show that B. malifolia plants offering a full complement of mutualistic food resources for ants-including EFN and trophobiotic insects-experienced significantly lower leaf herbivory and higher fruit production compared to plants lacking these resources. Bird exclusion resulted in increased herbivore damage and reduced fruit output, with these negative effects being even more pronounced when both birds and ants were excluded.
Our findings highlight the complexity of multi-trophic interactions in ant-plant mutualisms. They emphasize the importance of considering multiple trophic levels in plant defence strategies and underscore the cascading effects of predator interactions within natural ecosystems.
保护共生关系是指植物通过为蚂蚁和食虫鸟类等捕食者提供食物资源，从而获得抵御食草动物的保护。蚂蚁可以通过积极巡逻带有花外蜜腺（EFN）的植物，或照料能为它们提供食物奖励的共生昆虫，来减少食草动物的侵害。食虫鸟类也有助于抑制食草动物，但可能同时通过捕食减少蚂蚁的活动。虽然蚂蚁和鸟类都能提高植物的性能，但很少有研究探讨多种与蚂蚁相关的资源的可利用性如何影响食草动物的抑制，或者鸟类对蚂蚁的捕食如何影响这些蚂蚁与植物的共生关系。这些空白限制了我们对复杂多营养级相互作用动态的理解。
我们研究了蚂蚁的多种食物资源的可利用性以及食虫鸟类对蚂蚁的捕食如何影响热带灌木马利筋叶巴豆的性能。为了解决这个问题，我们进行了两个田间实验。第一个实验操纵了互利共生蚂蚁资源——花外蜜腺、嗜蚁毛虫和角蝉的单独和组合存在情况。第二个实验操纵了蚂蚁和鸟类的存在与否，以评估它们的交互作用。通过测量叶片食草动物损害、果实数量和果实重量来评估植物性能。
我们的研究结果表明，与缺乏这些资源的植物相比，为蚂蚁提供完整互利共生食物资源（包括花外蜜腺和共生昆虫）的马利筋叶巴豆植物遭受的叶片食草动物损害显著更低，果实产量更高。排除鸟类导致食草动物损害增加和果实产量降低，当同时排除鸟类和蚂蚁时，这些负面影响更加明显。
我们的研究结果突出了蚂蚁与植物共生关系中多营养级相互作用的复杂性。它们强调了在植物防御策略中考虑多个营养级的重要性，并强调了自然生态系统中捕食者相互作用的级联效应。
