Data from: Economy of scale: third partner strengthens a keystone ant-plant mutualism

While foundation species can stabilize ecosystems at landscape scales, their ability to persist is often underlain by keystone interactions occurring at smaller scales. Acacia drepanolobium is a foundation tree, comprising >95% of woody cover in East African black-cotton savanna ecosystems. Its dominance is underlain by a keystone mutualistic interaction with several symbiotic ant species in which it provides housing (swollen thorns) and carbohydrate-rich nectar from extra-floral nectaries (EFN). In return, it gains protection from catastrophic damage from mega-herbivores. Crematogaster mimosae is the ecologically dominant symbiotic ant in this system, also providing the highest protection services. In addition to tending EFN, C. mimosae tend scale insects for carbohydrate-rich honeydew. We investigated the role of scale insects in this specialized ant-plant interaction. Specifically, does this putatively redundant third partner strengthen the ant-plant mutualism by making the ant a better protector of the tree? Or does it weaken the mutualism by being costly to the tree while providing no additional benefit to the ant-plant mutualism? We coupled observational surveys with two scale-manipulation experiments and found evidence that this third partner strengthens the ant-plant mutualism. Trees with scale insects experimentally removed experienced a 2.5X increase in elephant damage compared to trees with scale insects present over 10 months. Reduced protection was driven by scale removal causing a decrease in ant colony size and per capita baseline activity and defensive behavior. We also found that ants increased scale-tending and the density of scale insects on trees when EFN were experimentally reduced. Thus, in this system, scale insects and EFN are likely complementary, rather than redundant, resources with scale insects benefitting ants when EFN production is low (such as during annual dry periods in this semi-arid ecosystem). This study reveals that a third-partner strengthens an ant-plant mutualism that serves to stabilize a whole ecosystem.

尽管建群种（foundation species）能够在景观尺度（landscape scales）上稳定生态系统，但其存续能力往往依托于更小尺度下发生的关键互作（keystone interactions）。镰刺金合欢（Acacia drepanolobium）是一种建群乔木，在东非黑棉土稀树草原生态系统（East African black-cotton savanna ecosystems）中，其木本盖度（woody cover）占比超过95%。该树种的优势地位依赖于与多种共生蚁类（symbiotic ant species）的关键互利互作（keystone mutualistic interaction）：它为蚂蚁提供膨大刺（swollen thorns）作为栖息场所，以及来自花外蜜腺（extra-floral nectaries, EFN）的富碳水化合物花蜜，作为回报，树木得以避免遭受大型植食动物（mega-herbivores）的毁灭性破坏。

含羞草举腹蚁（Crematogaster mimosae）是该系统中生态优势最显著的共生蚁，同时也是提供保护服务最优的蚁种。除了取食花外蜜腺，含羞草举腹蚁还会抚育介壳虫（scale insects）以获取其分泌的富碳水化合物蜜露（honeydew）。本研究探究了介壳虫在这一特化蚁植互作（ant-plant interaction）中的角色：其一，这个看似冗余的第三伙伴，是否会通过让蚂蚁成为更出色的树木保护者，强化蚁植互利共生（ant-plant mutualism）？其二，它是否会因给树木带来额外成本，且未给蚁植互利共生提供额外收益，反而削弱该共生体系？

本研究结合野外观测调查与两组介壳虫操控实验，结果表明该第三伙伴确实强化了蚁植互利共生。在10个月的观测周期内，人工移除介壳虫的树木遭受大象破坏的程度较保留介壳虫的树木升高2.5倍。保护能力的下降源于介壳虫移除导致蚁群规模缩小，且蚂蚁的个体基础活动与防御行为均有所减弱。此外，研究还发现，当实验性抑制花外蜜腺分泌时，蚂蚁会提升对介壳虫的抚育行为，且树木上的介壳虫密度也会升高。由此可见，在该系统中，介壳虫与花外蜜腺并非冗余资源，而是互补资源：在该半干旱生态系统的年度旱季等花外蜜腺产量较低的时期，介壳虫可为蚂蚁提供额外的碳水补给。本研究揭示，第三伙伴能够强化支撑整个生态系统稳定的蚁植互利共生关系。