Abstract
Several influential hypotheses in plant-herbivore and herbivore-predator interactions consider the interactive effects of plant quality, herbivore diet breadth, and predation on herbivore performance. Yet individually and collectively, these hypotheses fail to address the simultaneous influence of all three factors. Here we review existing hypotheses, and propose the tri-trophic interactions (TTI) hypothesis to consolidate and integrate their predictions. The TTI hypothesis predicts that dietary specialist herbivores (as compared to generalists) should escape predators and be competitively dominant due to faster growth rates, and that such differences should be greater on low quality (as compared to high quality) host plants. To provide a preliminary test of these predictions, we conducted an empirical study comparing the effects of plant (Baccharis salicifolia) quality and predators between a specialist (Uroleucon macolai) and a generalist (Aphis gossypii) aphid herbivore. Consistent with predictions, these three factors interactively determine herbivore performance in ways not addressed by existing hypotheses. Compared to the specialist, the generalist was less fecund, competitively inferior, and more sensitive to low plant quality. Correspondingly, predator effects were contingent upon plant quality only for the generalist. Contrary to predictions, predator effects were weaker for the generalist and on low-quality plants, likely due to density-dependent benefits provided to the generalist by mutualist ants. Because the TTI hypothesis predicts the superior performance of specialists, mutualist ants may be critical to A. gossypii persistence under competition from U. macolai. In summary, the integrative nature of the TTI hypothesis offers novel insight into the determinants of plant-herbivore and herbivore-predator interactions and the coexistence of specialist and generalist herbivores.
Highlights
For more than half a century, evolutionary ecologists have studied plant-herbivore interactions with the dual aims of understanding plant defense and dietary specialization by insect herbivores [1,2,3,4,5,6,7,8]
While a multi-trophic approach has been applied to many aspects of plant-herbivore interactions, here we address the dual influences of natural enemies and host plant quality on the relative performance and coexistence of dietary specialist and generalist herbivores
In the large literature on this topic, three long-standing hypotheses are especially relevant: The physiological efficiency [1], slow-growth/highmortality [11,20,21] and enemy-free space hypotheses [22,23]. These highly influential hypotheses are notable for their integrative nature, with each addressing the interactive effects of unique pairwise combinations of host-plant quality, natural enemies and herbivore diet breadth upon herbivore performance (Fig. 1, Table 1)
Summary
For more than half a century, evolutionary ecologists have studied plant-herbivore interactions with the dual aims of understanding plant defense and dietary specialization by insect herbivores [1,2,3,4,5,6,7,8]. In the large literature on this topic, three long-standing hypotheses are especially relevant: The physiological efficiency [1], slow-growth/highmortality [11,20,21] and enemy-free space hypotheses [22,23]. These highly influential hypotheses are notable for their integrative nature, with each addressing the interactive effects of unique pairwise combinations of host-plant quality, natural enemies and herbivore diet breadth upon herbivore performance (Fig. 1, Table 1)
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