Kailen A. Mooney

Birds as predators in tropical agroforestry systems.

Insectivorous birds reduce arthropod abundances and their damage to plants in some, but not all, studies where predation by birds has been assessed. The variation in bird effects may be due to characteristics such as plant productivity or quality, habitat complexity, and/or species diversity of predator and prey assemblages. Since agroforestry systems vary in such characteristics, these systems provide a good starting point for understanding when and where we can expect predation by birds to be important. We analyze data from bird exclosure studies in forests and agroforestry systems to ask whether birds consistently reduce their arthropod prey base and whether bird predation differs between forests and agroforestry systems. Further, we focus on agroforestry systems to ask whether the magnitude of bird predation (1) differs between canopy trees and understory plants, (2) differs when migratory birds are present or absent, and (3) correlates with bird abundance and diversity. We found that, across all studies, birds reduce all arthropods, herbivores, carnivores, and plant damage. We observed no difference in the magnitude of bird effects between agroforestry systems and forests despite simplified habitat structure and plant diversity in agroforests. Within agroforestry systems, bird reduction of arthropods was greater in the canopy than the crop layer. Top-down effects of bird predation were especially strong during censuses when migratory birds were present in agroforestry systems. Importantly, the diversity of the predator assemblage correlated with the magnitude of predator effects; where the diversity of birds, especially migratory birds, was greater, birds reduced arthropod densities to a greater extent. We outline potential mechanisms for relationships between bird predator, insect prey, and habitat characteristics, and we suggest future studies using tropical agroforests as a model system to further test these areas of ecological theory.

Interactions among predators and the cascading effects of vertebrate insectivores on arthropod communities and plants

Theory on trophic interactions predicts that predators increase plant biomass by feeding on herbivores, an indirect interaction called a trophic cascade. Theory also predicts that predators feeding on predators, or intraguild predation, will weaken trophic cascades. Although past syntheses have confirmed cascading effects of terrestrial arthropod predators, we lack a comprehensive analysis for vertebrate insectivores—which by virtue of their body size and feeding habits are often top predators in these systems—and of how intraguild predation mediates trophic cascade strength. We report here on a meta-analysis of 113 experiments documenting the effects of insectivorous birds, bats, or lizards on predaceous arthropods, herbivorous arthropods, and plants. Although vertebrate insectivores fed as intraguild predators, strongly reducing predaceous arthropods (38%), they nevertheless suppressed herbivores (39%), indirectly reduced plant damage (40%), and increased plant biomass (14%). Furthermore, effects of vertebrate insectivores on predatory and herbivorous arthropods were positively correlated. Effects were strongest on arthropods and plants in communities with abundant predaceous arthropods and strong intraguild predation, but weak in communities depauperate in arthropod predators and intraguild predation. The naturally occurring ratio of arthropod predators relative to herbivores varied tremendously among the studied communities, and the skew to predators increased with site primary productivity and in trees relative to shrubs. Although intraguild predation among arthropod predators has been shown to weaken herbivore suppression, we find this paradigm does not extend to vertebrate insectivores in these communities. Instead, vertebrate intraguild preda-tion is associated with strengthened trophic cascades, and insectivores function as dominant predators in terrestrial plant-arthropod communities.

Plant Genotype Shapes Ant‐Aphid Interactions: Implications for Community Structure and Indirect Plant Defense

Little is known about the mechanisms by which plant genotype shapes arthropod community structure. In a field experiment, we measured the effects of milkweed (Asclepias syriaca) genotype and ants on milkweed arthropods. Populations of the ant‐tended aphid Aphis asclepiadis and the untended aphid Myzocallis asclepiadis varied eight‐ to 18‐fold among milkweed genotypes, depending on aphid species and whether ants were present. There was no milkweed effect on predatory arthropods. Ants increased Aphis abundance 59%, decreased Myzocallis abundance 52%, and decreased predator abundance 56%. Milkweed genotype indirectly influenced ants via direct effects on Aphis and Myzocallis abundance. Milkweed genotype also modified ant‐aphid interactions, influencing the number of ants attracted per Aphis and Myzocallis. While ant effects on Myzocallis were consistently negative, effects on Aphis ranged from antagonistic to mutualistic among milkweed genotypes. As a consequence of milkweed effects on ant‐aphid interactions, ant abundance varied 13‐fold among milkweed genotypes, and monarch caterpillar survival was negatively correlated with genetic variation in ant abundance. We speculate that heritable variation in milkweed phloem sap drives these effects on aphids, ants, and caterpillars. In summary, milkweed exerts genetic control over the interactions between aphids and an ant that provides defense against foliage‐feeding caterpillars.

Evolutionary trade-offs in plants mediate the strength of trophic cascades.

Trophic Trade-Offs There have been many attempts to document and explain the effects of predators on plant biomass in so-called “trophic cascades.” Theory suggests that fast-growing plants are relatively undefended and suffer more from herbivory, which implies a functional trade-off between investment in traits relating to growth and defensive strategies. Mooney et al. (p. 1642; see the Perspective by Hambäck) compared responses to fertilization and aphid predators in 16 milkweed species. As predicted, interspecific variation in the strength of top-down control in terms of a tradeoff with growth was observed. The effect of herbivore predators on plant biomass depends on a trade-off between plant growth and resistance to herbivores. Predators determine herbivore and plant biomass via so-called trophic cascades, and the strength of such effects is influenced by ecosystem productivity. To determine whether evolutionary trade-offs among plant traits influence patterns of trophic control, we manipulated predators and soil fertility and measured impacts of a major herbivore (the aphid Aphis nerii) on 16 milkweed species (Asclepias spp.) in a phylogenetic field experiment. Herbivore density was determined by variation in predation and trade-offs between herbivore resistance and plant growth strategy. Neither herbivore density nor predator effects on herbivores predicted the cascading effects of predators on plant biomass. Instead, cascade strength was strongly and positively associated with milkweed response to soil fertility. Accordingly, contemporary patterns of trophic control are driven by evolutionary convergent trade-offs faced by plants.

TRITROPHIC EFFECTS OF BIRDS AND ANTS ON A CANOPY FOOD WEB, TREE GROWTH, AND PHYTOCHEMISTRY

Insectivorous birds and ants co-occur in most terrestrial communities, and theory predicts that emergent properties (i.e., nonadditive effects) can determine their combined influence on arthropods and plants. In a three-year factorial experiment, I investigated whether the effects of birds on pine and its arthropods differed based on the presence of ants that were predators of most arthropods, but mutualists with tended aphid species. Birds and ants reduced the abundance of most herbivorous and carnivorous arthropods in an additive fashion, with the effects of ants being stronger than those of birds. In sharp contrast, the opposing influences of birds and ants on tended aphid species interacted strongly; ants only increased tended aphid abundance in the absence of birds, while birds only reduced their abundance in the presence of ants. This interaction was mirrored in total herbivore abundance because tended aphids dominated the herbivore community. I develop a novel lexicon to discuss the emergent properties from these effects of opposing sign (predation, mutualism). Despite having emergent effects on herbivores, birds indirectly increased pine wood and foliage growth to a similar extent whether or not ants were present, while ants had no detectable effects. Birds also indirectly increased the abundance of some pine phloem monoterpenes, but these effects differed based on the presence or absence of ants. Thus, I report on a novel yet possibly widespread indirect interaction between intraguild predators, herbivore mutualists, and plant traits (growth, secondary chemistry) mediated through a species-rich community of arthropods.

TEMPORAL AND SPATIAL VARIATION TO ANT OMNIVORY IN PINE FORESTS

To understand omnivore function in food webs, we must know the contributions of resources from different trophic levels and how resource use changes through space and time. We investigated the spatial and temporal dynamics of pine (Pinus ponderosa) food webs that included the omnivorous ant, Formica podzolica, using direct observation and stable isotopes. Formica podzolica is a predator of herbivorous and predatory arthropods, and a mutualist with some aphids. Observations in 2001 of foragers showed that in early summer (June) ants fed upon equal parts non-mutualist herbivores (31% prey biomass), mutualist aphids (27%), and predators (42%); ant trophic position was thus between that of primary and secondary predator (trophic level = 3.4). In late summer (September), ant feeding remained relatively constant upon non-mutualist herbivores (53%) and mutualist aphids (43%), but ant feeding upon predators fell (4%), thus shifting ant trophic position to that of a primary predator (trophic level = 3.0). Feeding ...

Tritrophic Interactions at a Community Level: Effects of Host Plant Species Quality on Bird Predation of Caterpillars

Effects of plant traits on herbivore-carnivore interactions are well documented in component communities but are not well understood at the level of large, complex communities. We report on a 2-year field experiment testing mechanisms by which variation in food quality among eight temperate forest tree species alters avian suppression of an assemblage of dietary generalist caterpillars. Plant quality and bird effects varied dramatically among tree species; high-quality plants yielded herbivores of 50% greater mass than those on low-quality plants, and bird effects ranged from near 0% to 97% reductions in caterpillar density. We also find evidence for two mechanisms linking host plant quality to bird effects. If caterpillar density was statistically controlled for, birds had relatively strong effects on the herbivores of low-quality plants, as predicted by the slow-growth/high-mortality hypothesis. At the same time, caterpillar density increased with plant quality, and bird effects were density dependent. Consequently, the net effect of birds was strongest on the herbivores of high-quality plants, a dynamic we call the high-performance/high-mortality hypothesis. Host plant quality thus changes highly generalized herbivore-carnivore interactions by two complementary but opposing mechanisms. These results highlight the interrelatedness of plant-herbivore and herbivore-carnivore interactions and thus the importance of a tritrophic perspective.

The Tri-Trophic Interactions Hypothesis: Interactive Effects of Host Plant Quality, Diet Breadth and Natural Enemies on Herbivores

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.

Plant diversity effects on insect herbivores and their natural enemies: current thinking, recent findings, and future directions

A rich body of theory has been developed to predict the effects of plant diversity on communities at higher trophic levels and the mechanisms underpinning such effects. However, there are currently a number of key gaps in knowledge that have hindered the development of a predictive framework of plant diversity effects on consumers. For instance, we still know very little about how the magnitude of plant trait variation (e.g. intra-specific vs. inter-specific), as well as the identity and combined effects of plant, herbivore and natural enemy traits, mediate plant diversity effects on consumers. Moreover, the fine-scale mechanisms (e.g. changes in consumer behaviour or recruitment responses) underlying such diversity effects in many cases remain elusive or have been overlooked. In addition, most studies of plant diversity effects on associated consumers have been developed under a static, unidirectional (bottom-up) framework of effects on herbivores and predators without taking into account the potential for dynamic feedbacks across trophic levels. Here we seek to address these key gaps in knowledge as well as to capitalize on recent advances and emerging frameworks in plant biodiversity research. In doing so, we provide new insights as well as recommendations which will stimulate new research and advance this field of study.

Herbivore diet breadth mediates the cascading effects of carnivores in food webs

Significance This study shows the far-reaching effects of herbivore dietary specialization on the ecological and evolutionary dynamics of carnivore–herbivore–plant interactions. First, we test the long-standing hypothesis that dietary specialization of insect herbivores mediates the strength of bird predation on herbivores. Accounting for phylogenetic nonindependence of herbivores and plants, we show for the first time (to our knowledge) that dietary specialization of herbivore species is associated with reduced bird predation across an herbivore phylogeny, and that dietary specialization of herbivores increases the antipredator effects of camouflage and aposematism. Second, this study develops and finds support for the novel hypothesis that the proportion of dietary specialist species in a plant’s herbivore community predicts the degree of antiherbivore protection birds provide to plants. Predicting the impact of carnivores on plants has challenged community and food web ecologists for decades. At the same time, the role of predators in the evolution of herbivore dietary specialization has been an unresolved issue in evolutionary ecology. Here, we integrate these perspectives by testing the role of herbivore diet breadth as a predictor of top-down effects of avian predators on herbivores and plants in a forest food web. Using experimental bird exclosures to study a complex community of trees, caterpillars, and birds, we found a robust positive association between caterpillar diet breadth (phylodiversity of host plants used) and the strength of bird predation across 41 caterpillar and eight tree species. Dietary specialization was associated with increased enemy-free space for both camouflaged (n = 33) and warningly signaled (n = 8) caterpillar species. Furthermore, dietary specialization was associated with increased crypsis (camouflaged species only) and more stereotyped resting poses (camouflaged and warningly signaled species), but was unrelated to caterpillar body size. These dynamics in turn cascaded down to plants: a metaanalysis (n = 15 tree species) showed the beneficial effect of birds on trees (i.e., reduced leaf damage) decreased with the proportion of dietary specialist taxa composing a tree species’ herbivore fauna. We conclude that herbivore diet breadth is a key functional trait underlying the trophic effects of carnivores on both herbivores and plants.