Indirect benefits of symbiotic coccoids for an ant-defended myrmecophytic tree

Abstract

Abstract. The net benefits of mutualism depend directly on the costs and effectiveness of mutualistic services and indirectly on the interactions that affect those services. We examined interactions among Cordia alliodora myrmecophytic trees, their symbiotic ants Azteca pittieri, coccoid hemipterans, and foliar herbivores in two Neotropical dry forests. The tree makes two investments in symbiotic ants: it supplies nesting space, as domatia, and it provides phloem to coccoids, which then produce honeydew that is consumed by ants. Although higher densities of coccoids should have higher direct costs for trees, we asked whether higher densities of coccoids can also have higher indirect benefits for trees by increasing the effectiveness of ant defense against foliar herbivores. We found that trees benefited from ant defense against herbivores. Ants defended trees effectively only when colonies reached high densities within trees, and ant and coccoid densities within trees were strongly positively correlated. The benefits of reduced foliar herbivory by larger ant colonies were therefore indirectly controlled by the number of coccoids. Coccoid honeydew supply also affected per capita ant aggression against tree herbivores. Ants experimentally fed a carbohydrate-rich diet, analogous to sugar obtained from coccoids, were more aggressive against caterpillars per capita than ants fed a carbohydrate-poor diet. Ant defense was more effective on more valuable and vulnerable young leaves than on older leaves. Young domatia, associated with young leaves, contained higher coccoid densities than older domatia, which suggests that coccoids may also drive spatially favorable ant defense of the tree. If higher investments by one mutualistic partner are tied to higher benefits received from the other, there may be positive feedback between partners that will stabilize the mutualism. These results suggest that higher investment by trees in coccoids leads to more effective defense by ants against the tree's foliar herbivores.

Mixed effects of ant–aphid mutualism on plants across different spatial scales

“…The heterogeneous distribution of resources over different parts within a certain scale can shape the outcome of ant-plant interaction. In the direct ant-plant interaction, some high-quality rewards for ants only occur on young leaves, twigs, or larger segments within a tree (Miller 2014;Pringle, Dirzo, & Gordon 2011). In some cases, ant densities on larger trees are lower than the densities on smaller ones, which can lead to the varied effects of ants on plants on different-sized trees (Palmer & Brody 2013;Palmer et al 2010;Pringle, Dirzo, & Gordon 2012).…”

Trait-mediated indirect interactions in invasions: unique behavioral responses of an invasive ant to plant nectar

“…For example, Grover et al (2007) found that both activity levels and intraspecific aggression of L. humile were higher for lab colonies that were fed a diet rich in carbohydrates than under a proteinrich diet. Similarly, Pringle et al (2010) showed that native plant-inhabiting ants in a neotropical lowland rainforest were more aggressive towards plant-feeding herbivores when fed a diet rich in carbohydrates. However, Kay et al (2010) examined the aggression exerted by L. humile towards heterospecific ants and found no influence of diet, although carbohydrate-rich diets resulted in greater colony growth (a densitymediated effect).…”

Harnessing ant defence at fruits reduces bruchid seed predation in a symbiotic ant–plant mutualism

“…Cordia alliodora is found throughout the neotropics, from Mexico to Argentina, and the quality of ant defence varies throughout this range [52]. Ants are particularly good defenders at the Chamela site studied here [11]. Interestingly, A. atkinsoni, which was by far the most abundant bruchid seed predator in this study, is endemic to Jalisco, Mexico [35], and is replaced by different species of Amblycerus farther south [36].…”

“…Because a given ant colony associates with a single plant throughout its lifetime, but partners disperse separately, symbiotic ant-plant mutualisms are predicted to be good examples of 'short-term' (within-generation) partner fidelity feedback [4]. Consistent with this prediction, recent empirical studies of ant-plant symbioses have demonstrated positive feedback between plant rewards and ant defence [7,10,11]. However, ants may reduce herbivory or even increase plant growth without necessarily increasing plant fitness [12], and direct evidence that ants increase plant reproductive output is relatively scarce [but see 13 -16].…”

“…bruchid beetle larvae throughout its Middle American range [34 -36]. Previous studies have shown that ants can effectively defend C. alliodora leaves [11,37,38]. To the best of my knowledge, this is the first study to investigate ant defence of reproductive structures in this system.…”