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Plants link interactions between aboveground and belowground organisms. Herbivore-induced changes in plant chemistry are hypothesized to impact entire food webs by changing the strength of trophic cascades. Yet, few studies have explored how belowground herbivores affect the behaviors of generalist predators, nor how such changes may act through diverse changes to the plant metabolome. Using a factorial experiment, we tested whether herbivory by root-knot nematodes (Meloidogyne incognita) affected the aboveground interaction among milkweed plants (Asclepias fascicularis or Asclepias speciosa), oleander aphids (Aphis nerii), and aphid-tending ants (Linepithema humile). We quantified the behaviors of aphid-tending ants, and we measured the effects of herbivore treatments on aphid densities and on phytochemistry. Unexpectedly, ants tended aphids primarily on the leaves of uninfected plants, whereas ants tended aphids primarily at the base of the stem of nematode-infected plants. In nematode-infected plants, aphids excreted more sugar per capita in their ant-attracting honeydew. Additionally, although plant chemistry was species-specific, nematode infection generally decreased the richness of plant secondary metabolites while acting as a protein sink in the roots. Path analysis indicated that the ants' behavioral change was driven in part by indirect effects of nematodes acting through changes in plant chemistry. We conclude that belowground herbivores can affect the behaviors of aboveground generalist ant predators by multiple paths, including changes in phytochemistry, which may affect the attractiveness of aphid honeydew rewards.

Tolerance is the ability of a plant to regrow or reproduce following damage. While experimental studies typically measure tolerance in response to the intensity of herbivory (i.e., the amount of leaf tissue removed in one attack), the impact of how many times plants are attacked during a growing season (i.e., the frequency of damage) is virtually unexplored. Using experimental defoliations that mimicked patterns of attack by leaf-cutter ants (Atta spp.), we examined how the frequency of herbivory influenced plant tolerance traits in six tree species in Brazil's Cerrado. For 2 years we quantified how monthly and quarterly damage influenced individual survivorship, relative growth rate, plant architecture, flowering, and foliar chemistry. We found that the content of leaf nitrogen (N) increased among clipped individuals of most species, suggesting that Atta influences the allocation of resources in damaged plants. Furthermore, our clipping treatments affected tree architecture in ways thought to promote tolerance. However, none of our focal species exhibited a compensatory increase in growth (increment in trunk diameter) in response to herbivory as relative growth rates were significantly lower in clipped than in unclipped individuals. In addition, the probability of survival was much lower for clipped plants, and lower for plants clipped monthly than those clipped quarterly. For plants that did survive, simulated herbivory dramatically reduced the probability of flowering. Our results were similar across a phylogenetically distinct suite of species, suggesting a potential extendability of these findings to other plant species in this system.