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.

There is growing evidence for the influence of plant intraspecific variation on associated multi-trophic communities, but the traits driving such effects are largely unknown. We conducted a field experiment with selected genetic lines of the dioecious shrub Baceharis salicifolia to investigate the effects of plant growth rate (two-fold variation) and gender (males vs. females of the same growth rate) on above- and belowground insect and fungal associates. We documented variation in associate density to test for effects occurring through plant-based habitat quality (controlling for effects of plant size) as well as variation in associate abundance to test for effects occurring through both habitat quality and abundance (including effects of plant size). Whereas the dietary specialist aphid Uroleucon macaolai was unaffected by plant sex and growth rate, the generalist aphid Aphis gossypii and its tending ants (Linepithema humile) had higher abundances and densities on male (vs. female) plants, suggesting males provide greater habitat quality. In contrast, Aphis and ant abundance and density were unaffected by plant growth rate, while Aphis parasitoids were unaffected by either plant sex or growth rate. Arbuscular mycorrhizal fungi had higher abundance and density (both marginally significant) on females (vs. males), suggesting females provide greater habitat quality, but lower abundances (marginally significant) and higher densities on slow- (vs. fast-) growing genotypes, suggesting slow-growing genotypes provided lower resource abundance but greater habitat quality. Overall, plant sex and growth rate effects on associates acted independently (i.e., no interactive effects), and these effects were of a greater magnitude than those coming from other axes of plant genetic variation. These findings thus demonstrate that plant genetic effects on associated communities may be driven by a small number of trait-specific mechanisms.

A plant's performance and interactions with other trophic levels are recorgnized to be contingent upon plant diversity and underlying associational dynamics, but far less is known about the plant traits driving such phenomena. We manipulated diversity in plant traits using pairs of plant and a substitutive design to elucidate the mechanisms underlying diversity effects operating at a fine spatial scale. Specifically, we measured the effects of diversity in sex (sexual monocultures vs. male and female genotypes together) and growth rate (growth rate monocultures vs. fast- and slow-growing genotypes together) on growth of the shrub Baccharis salicifolia and on above- and belowground consumers associated with this plant. We compared effects on associate abundance (# associates per plant) vs. density (# associates per kg plant biomass) to elucidate the mechanisms underlying diversity effects; effects on abundance but not density suggest diversity effects are mediated by resource abundance (i.e. plant biomass) alone, whereas effects on density suggest diversity effects are mediated by plant-based heterogeneity or quality. Sexual diversity increased root growth but reduced the density (but not abundance) of the dietary generalist aphid Aphis gossypii and its associated aphid-tending ants, suggesting sex mixtures were of lower quality to this herbivore (e.g. via reduced plant quality), and that this effect indirectly influenced ants. Sexual diversity had no effect on the abundance or density of parasitoids attacking A. gossypii, the dietary specialist aphid Uroleucon macolai, or mycorrhizae. In contrast, growth rate diversity did not influence plant growth or any associates except for the dietary specialist aphid U. macolai, which increased in both abundance and density at high diversity, suggesting growth rate mixtures were of higher quality to this herbivore. These results highlight that plant associational and diversity effects on consumers are contingent upon the source of plant trait variation, and that the nature of such dynamics may vary both within and among trophic levels.

Although species interactions are often proposed to be stronger at lower latitudes and elevations, few studies have evaluated the mechanisms driving such patterns. In this study, we assessed whether, and by which mechanisms, abiotic changes associated with elevation altered the outcome of an ant–aphid protection mutualism. To do so, we characterized the multi-trophic interactions among the ant Formica podzolica, the aphid Aphis varians, and aphid natural enemies occurring on the plant Chamerion angustifolium within replicate high and low elevation valleys. Low (versus high) elevation sites had longer summers (snowmelt 13 days earlier) and were on average 1.1°C warmer and 41% drier throughout the year. At low elevations, individual ant colonies consumed approximately double the volume of carbohydrate baits, likely due to a higher foraging tempo, and possibly due to a greater demand for sugar- versus protein-rich resources (as indicated by stable isotope analysis). Wild aphid colonies at low elevations were visited by 1.4-fold more natural enemies (controlling for variation in aphid abundance), while experimental aphid colonies on potted plants were tended 52% more frequently by ants. As a result, ants increased aphid colony survival by 66% at low elevations but had no detectable effect at high elevations; at low (versus high) elevations aphid colonies without ants had lower survival, demonstrating stronger predator effects, while aphid colonies with ants had higher survival, demonstrating even stronger ant benefits. Analyses for the effects of mean summer temperature yielded qualitatively identical results to those based on elevation. Collectively, these findings support predictions for a greater sensitivity of higher trophic levels to warming and demonstrate how species interactions can vary across environmental gradients due to simultaneous changes in species traits and abundances across multiple trophic levels.

Global declines in bird and arthropod abundance highlights the importance of understanding the role of food limitation and arthropod community composition for the performance of insectivorous birds. In this study, we link data on nestling diet, arthropod availability and nesting performance for the Coastal Cactus Wren (Campylorhynchus brunneicapillus sandiegensis), an at-risk insectivorous bird native to coastal southern California and Baja Mexico. We used DNA metabarcoding to characterize nestling diets and monitored 8 bird territories over two years to assess the relationship between arthropod and vegetation community composition and bird reproductive success. We document a discordance between consumed prey and arthropod biomass within nesting territories, in which Diptera and Lepidoptera were the most frequently consumed prey taxa but were relatively rare in the environment. In contrast other Orders (e.g., Hemiptera, Hymenoptera)were abundant in the environment but were absent from nestling diets. Accordingly, variation in bird reproductive success among territories was positively related to the relative abundance of Lepidoptera (but not Diptera), which were most abundant on 2 shrub species (Eriogonum fasciculatum, Sambucus nigra) of the 9 habitat elements characterized (8 dominant plant species and bare ground). Bird reproductive success was in turn negatively related to two invasive arthropods whose abundance was not associated with preferred bird prey, but instead possibly acted through harassment (Linepithema humile; Argentine ants) and parasite transmission or low nutritional quality (Armadillidium vulgare; "pill-bug"). These results demonstrate how multiple aspects of arthropod community structure can influence bird performance through complementary mechanisms, and the importance of managing for arthropods in bird conservation efforts.