The invasive ant Pheidole megacephala on an oceanic island: impact, control and community-level response to management

Alien invasive species are among the most important global conservation threats. Their management is one of the key conservation challenges that will have to be addressed in the next few decades. The study of real invasions and their management in natural ecosystems provides an opportunity to gain important information on theoretical and applied aspects of biological invasions. This project focuses on the broader ecological context of invasive ant management in an ecologically sensitive island habitat. The thesis has three main components: 1) assessing the role of the invasive ant Pheidole megacephala in the ecosystem and evaluating its threat to the system, 2) developing and evaluating a low-impact management program for the ant, and 3) using a community-level approach to assess ecosystem response to ant removal. A variety of survey methods were used to monitor the island ecosystem before, during and after the management program was initiated. The ant occupied almost 30% of the island's total land area and reached extremely high densities in some areas. Throughout the infested area the ant was associated with exotic hemipteran scale insects through trophobiotic mutualisms that facilitated high ant and hemipteran abundances. The highly destructive scale insect Pulvinaria urbicola was among the hemipterans that benefited from ant attendance. High levels of hemipteran feeding resulted in dieback of functionally important and threatened native Pisonia trees, which represented a significant threat to the forest ecosystem. A management program was initiated in response to this threat, consisting of baiting with selective hydramethylnon-based bait delivered in bait stations, accompanied by detailed pre-and post-baiting monitoring. The method was highly effective at suppressing the ants, whilst reducing the opportunity for bait uptake by non-target organisms. It was also cost-effective and adaptable to ant density in the field, but was only effective over short distances. The method may be applicable to other sensitive environments with similar challenges. After ant control, the ant-scale mutualism was decoupled and the Pu. urbicola population collapsed. There were broad and variable responses in different taxa to the removal of these highly abundant exotic species, the most important of which was the recovery in Pisonia trees. Shoot condition and foliage density improved and there was a decrease in sooty mold. Herbivory on Pisonia increased due to recovery of native canopy herbivores, but the overall impact was far less than that of the exotic hemipterans. Soil surface arthropods, a group that may have been vulnerable to the treatment method, were unaffected by baiting. Instead, they increased significantly after ant removal, confirming the ant's impact on other arthropods. Other ant diversity increased and there was recovery of the Seychelles endemic Pheidole flavens farquharensis in the baited areas after being at very low population levels before baiting. Non-ant arthropod abundance increased post-baiting, including some functionally important species such as the Indian cockroach. Natural enemies that interacted predictably with the mutualists were influenced by management. Predators of hemipterans increased significantly after ant removal and were instrumental in the scale population collapse, whereas parasitoids of hemipterans that benefited from the mutualism declined. Additionally, groups that were unrelated to the mutualism were indirectly influenced by management. The natural enemy assemblage as a whole showed recovery to pre-invasion conditions after management. The study shows how widely interconnected and influential the ant was in the ecosystem. It highlights the threat of the species in natural systems as well as the complex responses following invasive ant removal. Yet, it also demonstrates the potential to safely and effectively manage the species, thereby raising the opportunity for ecosystem recovery.

外来入侵物种是全球最重要的保护威胁之一，其防控管理是未来数十年亟需应对的核心保护挑战之一。对自然生态系统中的真实入侵事件及其防控措施开展研究，可为我们获取生物入侵的理论与应用维度的关键信息提供契机。本项目聚焦生态敏感岛屿生境中入侵蚁防控的更广泛生态背景。本研究包含三个核心组成部分：1）评估入侵蚁大头蚁（Pheidole megacephala）在生态系统中的作用，及其对该系统的威胁；2）研发并评估针对该蚁的低干扰防控方案；3）采用群落水平研究方法，评估生态系统对移除入侵蚁的响应。研究团队采用多种调查方法，在防控方案实施前、实施期间及实施后对该岛屿生态系统进行持续监测。该入侵蚁占据该岛屿总陆地面积近30%，部分区域种群密度极高。在整个受侵染区域，该蚁与外来半翅目介壳虫通过营养共生关系形成互利互作，显著促进了二者的种群丰度。其中，破坏性极强的介壳虫普尔维纳利亚蚧（Pulvinaria urbicola）便是得益于蚁类保护的类群之一。介壳虫取食强度过高导致具有重要生态功能且受保护的本土光叶桐（Pisonia）出现枯梢，对森林生态系统构成显著威胁。针对该威胁，研究团队启动了防控方案：采用置于诱饵站中的特异性伏蚁腙（hydramethylnon）诱饵进行诱杀，并辅以完善的诱饵前后监测流程。该方法对压制蚁群极为高效，同时大幅降低了非靶标生物取食诱饵的概率，且兼具成本效益与田间适应性，可根据实际蚁群密度灵活调整，但仅在短距离范围内起效。该方法或可推广应用于面临同类挑战的其他敏感生境。防控实施后，蚁-介壳虫的营养共生关系被打破，普尔维纳利亚蚧种群快速崩溃。不同类群对移除该高度丰富的外来物种产生了广泛且各异的响应，其中最显著的是本土光叶桐种群的恢复：枝条健康状况与叶密度均得到改善，煤污病发生率显著下降。本土冠层植食性昆虫种群恢复导致光叶桐的植食性取食有所增加，但整体影响远低于外来介壳虫造成的危害。地表节肢动物本可能受该防控方法影响，却未受到诱饵处理的显著干扰；反而在移除蚁群后种群丰度显著提升，证实了入侵蚁对其他节肢动物的负面影响。其他蚁类物种多样性有所提升，曾在诱饵处理前种群水平极低的塞舌尔特有种黄大头蚁法夸尔亚种（Pheidole flavens farquharensis）也在诱饵区域出现种群恢复。非蚁类节肢动物的丰度在诱饵后同样显著提升，包括一些具有重要生态功能的类群如印度蜚蠊。与该营养共生关系存在可预测互作的天敌类群同样受到防控措施的影响：介壳虫的捕食者种群在移除蚁群后显著增加，成为介壳虫种群崩溃的关键驱动因素；而得益于该共生关系的介壳虫寄生蜂种群则出现下降。此外，与该共生关系无关的类群也间接受到防控措施的影响。整体天敌群落在防控后恢复至入侵前的状态。本研究揭示了该入侵蚁在生态系统中极强的连通性与影响力，凸显了该物种对自然生态系统的威胁，以及移除入侵蚁后生态系统产生的复杂响应。同时，本研究也证实了可安全且高效地对该物种实施防控，为生态系统的恢复提供了可行路径。