For ant-protected plants, the best defense is a hungry offense

Animal foraging has been characterized as an attempt to maximize the intake of carbon and nitrogen at appropriate ratios. Plant species in over 90 families produce carbohydrate-rich extrafloral nectar (EFN), a resource attractive to ants and other omnivorous insects. This attraction can benefit the plant if those arthropods subsequently attack herbivores. This protective response has been attributed to the increased visitation and "ownership" of plants that provide a predictable source of fuel. Here, we propose and test an alternative (but non-mutually exclusive) hypothesis, that access to C-rich carbohydrates increases the ants' desire for N-rich protein and hence the likelihood that they will attack herbivorous insects on the host plant. This "deficit hypothesis" would be rejected if (1) EFN were itself a sufficiently balanced food source in terms of C and N, (2) ant dietary preferences were similar in the presence vs. absence of EFN, (3) protein-hungry ants were not more predaceous, or (4) ants provided access to protein were more aggressive toward potential prey items than were ants provided access to carbohydrates. We test these predictions in a protective mutualism between a guild of desert ants and the barrel cactus Ferocactus wislizeni. C:N ratios of EFN exceeded that of ants or potential prey items by an order of magnitude (i.e., EFN is an N-poor food for ants). Baiting studies demonstrated that plant-tending ant species recruited more workers to N-rich protein baits than to C-rich sugar baits; this difference was more pronounced when the ants had access to F. wislizeni EFN. From these data, we infer that protein is a valuable resource and that its relative value increases when carbohydrates are readily available. Moreover, ant colonies provided access to supplemental carbohydrates responded more aggressively to surrogate herbivores than did control colonies (to which no additional resources were provided) or colonies provided protein. These results support the predictions of the "deficit" hypothesis, wherein plant protection is elicited by plant-mediated dietary imbalances.