Water Stress Strengthens Mutualism Among Ants, Trees, and Scale Insects

Abstract

Abiotic environmental variables strongly affect the outcomes of species interactions. For example, mutualistic interactions between species are often stronger when resources are limited. The effect might be indirect: water stress on plants can lead to carbon stress, which could alter carbon-mediated plant mutualisms. In mutualistic ant–plant symbioses, plants host ant colonies that defend them against herbivores. Here we show that the partners' investments in a widespread ant–plant symbiosis increase with water stress across 26 sites along a Mesoamerican precipitation gradient. At lower precipitation levels, Cordia alliodora trees invest more carbon in Azteca ants via phloem-feeding scale insects that provide the ants with sugars, and the ants provide better defense of the carbon-producing leaves. Under water stress, the trees have smaller carbon pools. A model of the carbon trade-offs for the mutualistic partners shows that the observed strategies can arise from the carbon costs of rare but extreme events of herbivory in the rainy season. Thus, water limitation, together with the risk of herbivory, increases the strength of a carbon-based mutualism. The strength of ecological interactions, measured as the costs or benefits sustained by each species, depends on the environmental context in which the interaction occurs. Stressful environmental conditions should favor trading between species that can produce a given resource or service at the lowest cost. Mutualisms, in which both interacting species incur a net benefit, may thus strengthen under stressful conditions. Here we examine an ant–plant mutualism, in which plants provide food and housing for ants and ants defend plants against leaf-eating insects, along a four-fold annual precipitation gradient comprising tropical sites in Mexico and Central America. We show that the strength of the mutualism, in terms of carbon investment by plants and leaf defense by ants, increases as water availability decreases. Carbon shortages are more frequent where water is scarce and increase the risk that plants will die if all of their leaves are eaten by herbivores. Trees appear to invest more in ant defenders when water is scarce to insure themselves against extreme herbivory. Water availability thus indirectly determines the outcomes of this ant–plant mutualism, which suggests that the increasing frequency of extreme climate events in the tropics will have important ecological consequences.