The tri-trophic interactions hypothesis: interactive effects of host plant quality, diet breadth and natural enemies on herbivores

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.

Figure 1. Predictions of the tri-trophic interactions (TTI) hypothesis for the interactive effects of natural enemies, host-plant quality and diet breadth on herbivores.

Three well-studied hypotheses – the physiological efficiency (PE), enemy free space (EFS) hypotheses, and slow-growth/high-mortality (SGHM) – each address unique, pairwise combinations of these factors. The physiological efficiency (PE) hypothesis predicts specialists should outperform generalists on shared host plants (e.g. a>b), and that generalists should be more sensitive to variation in host-plant quality than specialists (e.g. a–c

Figure 2. The dietary specialist herbivore Uroleucon macolai Blanchard (top) and the generalist Aphis gossypii Glover (bottom) feeding upon Baccharis salicifolia (Ruiz & Pav.) Pers.

Also shown are the predatory ladybird larvae (Coleoptera: Coccinelidae) (top) and the ant Linepithema humile (Mayr). Photo credits Kailen Mooney.

Figure 3. Treatment means from the bi-trophic experiment.

Effects of intra- vs. inter-specific competition and genetically based variation in host plant Baccharis salicifolia quality on the fecundity of a generalist (Aphis gossypii) and a specialist (Uroleucon macolai) herbivore. The effects of genetically based variation in host plant quality are tested by comparing herbivore fecundity between male and female plants (panels A, B) and among 14 plant genotypes (panels C, D). For effects of plant sex, means (± 1SE) are shown for each competition treatment. For effects of plant genotype, overall means (± 1SE) are shown for each competition treatment, and means for individual genotypes (error bars omitted for clarity) are indicated with solid (male) or dashed (female) lines. See Table 2 for statistics.

Figure 4. Treatment means from the tri-trophic experiment.

Effects of natural enemies and Baccharis salicifolia sex on the fecundity of a generalist, ant-tended herbivore (Aphis gossypii) and a specialist, untended herbivore (Uroleucon macolai). Least square means (±95% CI) for per capita daily growth are shown for each treatment controlling for initial aphid population size. See Table 3 for statistics.