Department of Biology, University of Florida, Gainesville, Florida, USA.
Mpala Research Centre, Nanyuki, Kenya.
Ecology. 2017 Dec;98(12):3034-3043. doi: 10.1002/ecy.2008.
Ant-plant protection symbioses, in which plants provide food and/or shelter for ants in exchange for protection from herbivory, are model systems for understanding the ecology of mutualism. While interactions between ants, host plants, and herbivores have been intensively studied, we know little about how plant-plant interactions influence the dynamics of these mutualisms, despite strong evidence that plants compete for resources, that hosting ants can be costly, and that host-plant provisioning to ants can therefore be constrained by resource availability. We used field experiments in a semiarid Kenyan savanna to examine interactions between the ant-plant Acacia drepanolobium, neighboring grasses, and two species of symbiotic acacia-ants with divergent behaviors: Crematogaster mimosae, an aggressive symbiont that imposes high costs to host trees via consumption of extrafloral nectar, and Tetraponera penzigi, a less-protective symbiont that imposes lower costs because it does not consume nectar. We hypothesized that by competing with acacias for resources, neighboring grasses (1) reduce hosts' ability to support costly C. mimosae, while having little or no effect on the ability of hosts to support low-cost T. penzigi, and (2) reduce sapling growth rates irrespective of ant occupant. We factorially manipulated the presence/absence of grasses and the identity of ant occupants on saplings and evaluated effects on colony survivorship and sapling growth rates over 40 weeks. Contrary to prediction, the high-cost/high-reward nectar-dependent mutualist C. mimosae had higher colony-survival rates on saplings with grass neighbors present. Grasses appear to have indirectly facilitated the survival of C. mimosae by reducing water stress on host plants; soils under saplings shaded by grasses had higher moisture content, and these saplings produced more active nectaries than grass-removal saplings. Consistent with prediction, survival of low-cost/low-reward T. penzigi did not differ significantly between grass-removal treatments. Saplings occupied by low-cost/low-reward T. penzigi grew 100% more on average than saplings occupied by high-cost/high-reward C. mimosae, demonstrating that mutualist-partner identity strongly and differentially influences demographic rates of young plants. In contrast, contrary to prediction, grass neighbors had no significant net impact on sapling growth rates. Our results suggest that neighboring plants can exert strong and counterintuitive effects on ant-plant protection symbioses, highlighting the need to integrate plant-plant interactions into our understanding of these mutualisms.
植物与蚂蚁的互惠共生关系，即植物为蚂蚁提供食物和/或庇护所，而蚂蚁则为植物提供免受食草动物侵害的保护，是理解共生关系生态的模型系统。尽管有强有力的证据表明植物之间存在资源竞争，饲养蚂蚁可能代价高昂，并且宿主植物向蚂蚁提供食物可能会受到资源可用性的限制，但我们对植物-植物相互作用如何影响这些互惠共生关系知之甚少。我们在肯尼亚半干旱稀树草原进行了野外实验，以研究与蚂蚁-植物金合欢属（Acacia drepanolobium）、邻近的草以及两种具有不同行为的共生金合欢蚂蚁之间的相互作用：Crematogaster mimosae，一种侵略性共生体，通过消耗额外的花蜜对宿主树造成高昂的代价；以及 Tetraponera penzigi，一种保护作用较低的共生体，因为它不消耗花蜜，所以代价较低。我们假设，通过与金合欢竞争资源，邻近的草（1）降低宿主支持高成本 C. mimosae 的能力，而对宿主支持低成本 T. penzigi 的能力几乎没有影响，（2）无论蚂蚁居住者的情况如何，都会降低幼树的生长速度。我们在幼树上人为地操纵草的有无和蚂蚁居住者的身份，并在 40 周内评估对蚁群存活率和幼树生长速度的影响。与预测相反，高成本/高回报的依赖花蜜的共生体 C. mimosae 在有草邻居的情况下，蚁群的存活率更高。草似乎通过减少宿主植物的水分胁迫，间接地促进了 C. mimosae 的生存；在被草遮蔽的幼树下的土壤中，水分含量更高，并且这些幼树比去除草的幼树产生更多活跃的蜜腺。与预测一致，低成本/低回报的 T. penzigi 的存活率在去除草的处理之间没有显著差异。由低成本/低回报的 T. penzigi 占据的幼树平均增长了 100%，而由高成本/高回报的 C. mimosae 占据的幼树，这表明共生伙伴的身份强烈且不同地影响幼树的种群增长率。相比之下，与预测相反，草邻居对幼树的生长速度没有显著的净影响。我们的研究结果表明，邻近的植物可以对蚂蚁-植物保护共生关系产生强烈而直觉相悖的影响，这凸显了将植物-植物相互作用纳入我们对这些共生关系的理解的必要性。
