Indirect plant defense depends on ant behavior in protection mutualisms with aphids

Plants attract natural enemies for indirect defense against herbivory. However, indirect defense can be altered by interactions at other trophic levels. For instance, many herbivorous hemipterans engage in mutualisms with ants, which protect hemipterans against natural enemies in exchange for sugar-rich rewards. As a result, shifts in ant-hemipteran mutualisms over space and time alter the outcomes of indirect plant defense. Here, we report on a series of studies, in which we demonstrate that shifts in ant identity and behavior have strong impacts on the abundance of mutualist hemipterans, particularly within the context of global change. We found that in response to a warming climate, aphid natural enemy abundance increases (140%), and so does their negative effects on aphid population growth (-250%). However, this is counteracted by an even greater increase in ant activity (230%), causing a net increase in aphid abundance (75%) in response to warming. Such effects may be further strengthened by ant associative learning of plant odors, which we have shown to increase ant recruitment (57%) to sugar-rich resources on plants, as well as by ant diversity, which increases the duration of aphid attendance and aphid colony fitness (100%). Overall, these studies demonstrate that shifts in the identity and behavior of herbivore mutualists can sometimes have stronger effects on indirect plant defense than shifts in the abundance of natural enemies themselves. As a result, it is essential to consider the multi-trophic context to better understand sources of contingency in the outcomes of indirect plant defense.