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.

Integrating quality and quantity of mutualistic service to contrast ant species protecting Ferocactus wislizeni.

Generalized, facultative mutualisms are often characterized by great variation in the benefits provided by different partner species. This variation may be due to differences among species in the quality and quantity of their interactions, as well as their phenology. Many plant species produce extrafloral nectar, a carbohydrate-rich resource, to attract ant species that can act as "bodyguards" against a plant's natural enemies. Here, we explore differences in the quality and quantity of protective service that ants can provide a plant by contrasting the four most common ant visitors to Ferocactus wislizeni, an extrafloral nectary-bearing cactus in southern Arizona. The four species differ in abundance when tending plants, and in the frequency at which they visit plants. By adding surrogate herbivores (Manduca sexta caterpillars) to plants, we demonstrate that all four species recruit to and attack potential herbivores. However, their per capita effectiveness in deterring herbivores (measured as the inverse of the number of workers needed to remove half of the experimentally added caterpillars) differs. Using these among-species differences in quality (per capita effectiveness) and quantity (number of workers that visit a plant and frequency of visitation), we accurately predicted the variation in fruit production among plants with different histories of ant tending. We found that plant benefits (herbivore removal and maturation of buds and fruits) typically saturated at high levels of ant protection, although plants could be "well defended" via different combinations of interaction frequency, numbers of ant workers per interaction, and per capita effects. Our study documents variation among prospective mutualists, distinguishes the components of this variation, and integrates these components into a predictive measure of protection benefit to the plant. The method we used to average saturating benefits over time could prove useful for quantifying overall service in other mutualisms.

Forest edges and fire ants alter the seed shadow of an ant-dispersed plant.

Exotic species invade fragmented, edge-rich habitats readily, yet the distinct impacts of habitat edges and invaders on native biota are rarely distinguished. Both appear detrimental to ant-dispersed plants such as bloodroot, Sanguinaria canadensis. Working in northeastern Georgia (USA), an area characterized by a rich ant-dispersed flora, fragmented forests, and invasions by the red imported fire ant, Solenopsis invicta, I monitored the interactions between ants and S. canadensis seeds in uninvaded forest interiors, uninvaded forest edges, invaded forest interiors, and invaded forest edges. I observed 95% of the seed dispersal events that occurred within the 60-min observation intervals. Seed collection rates were similar among all four (habitat x invasion) groups. The presence of invasive ants had a strong effect on seed dispersal distance: S. invicta collected most seeds in invaded sites, but was a poorer disperser than four of five native ant taxa. Habitat type (interior versus edge) had no effect on seed dispersal distance, but it had a strong effect on seed dispersal direction. Dispersal towards the edge was disproportionately rare in uninvaded forest edges, and ants in those habitats moved the average dispersed seed approximately 70 cm away from that edge. Dispersal direction was also skewed away from the edge in uninvaded forest interiors and invaded forest edges, albeit non-significantly. This biased dispersal may help explain the rarity of myrmecochorous plants in younger forests and edges, and their poor ability to disperse between fragments. This is the first demonstration that forest edges and S. invicta invasion influence seed dispersal destination and distance, respectively. These forces act independently.

Catalpa bignonioides alters extrafloral nectar production after herbivory and attracts ant bodyguards.

Inducible anti-herbivore defenses are found within many plant taxa, but there are fewer examples of inducible indirect defenses that incorporate the third trophic level. This study links caterpillar foraging, herbivore-induced changes in extrafloral nectar production, and the attraction of ants to vulnerable leaves and plants. Catalpa bignonioides Walter (Bignoniaceae) uses extrafloral nectar to attract ant (Forelius pruinosus(Roger)) bodyguards in response to Ceratomia catalpae (Boisduval)(Lepidoptera: Sphingidae) herbivory. Ant density per leaf increased with the sugar content of extrafloral nectar excreted by sampled leaves, suggesting that increased nectar production could attract or retain beneficial arthropods. The masses of sucrose, fructose, glucose and all three sugars combined in the extrafloral nectar increased two- to three-fold on attacked leaves within 36 h of the experimental addition of caterpillars. Production rates for neighboring non-attacked leaves and non-attacked leaves on adjacent plants did not differ over the same time period. Ant attendance at caterpillar-attacked leaves increased two- to three-fold within 24 h of herbivory, relative to attendance at neighboring, undamaged leaves. These attacked leaves attracted the fewest ants prior to the onset of herbivory, suggesting the specialist caterpillar may avoid or be excluded from leaves with more bodyguards. The removal of leaf tissue with scissors did not alter ant attendance at damaged leaves. Mean ant attendance per leaf on attacked plants increased 6- to 10-fold after caterpillar introduction, relative to adjacent unattacked plants. The plant's biotic defense thus operates at two scales; the number of bodyguards (ant workers) on the plant increases after attack, and this increased workforce is biased towards attacked leaves within plants. Fewer caterpillars remained on plants that attracted greater numbers of ants, suggesting these bodyguards benefit the plant.