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

Abstract

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.ecological specialization | host specificity | plant-herbivore interactions | tritrophic interactions | trophic cascade P redicting the strength of trophic interactions is a major goal in ecology. Because most natural ecosystems contain numerous coexisting species at each trophic level, achieving this goal necessarily involves the integration of theory in evolutionary, community, and food web ecology. In this context, evolutionary ecology explains how traits of organisms adapt them to a fundamental trade-off between resource acquisition and mortality risk from natural enemies (1, 2); community ecology theory links the many patterns and consequences of species interactions to the diversity of traits of those species (2); and food web ecology subsumes this diversity into patterns of trophic structure and dynamics, such as a trophic cascade (3). The recognition that functional traits of species can drive the indirect positive effect of carnivores on plant biomass [trophic cascades broadly defined (4, 5)] provides important insight into the causes of variation in these dynamics (1,6). An emerging understanding of the functional traits mediating trophic cascade strength includes traits of herbivores that facilitate predator avoidance (7-10), or provide constitutive (11, 12) or induced resistance to predation (13). These examples identify antipredator traits of herbivores as an important mediator of top-down effects on plants within individual tritrophic food chains. However, the role of antipredator (or other) traits of herbivores is curr...

Costs and benefits of plant allelochemicals in herbivore diet in a multi enemy world

“…Besides differences in plant defence chemicals, it is also possible that 460 the two host plant species differ nutritionally, which can affect the performance of the larvae and 461 also their immunological defence (Singer et al 2014) 462 Overall, this study shows that P. plantaginis larvae are able to take up some amount of the …”

The costs and effectiveness of chemical defenses in herbivorous insects: a meta‐analysis

“…Several case studies found that larvae of specialist lepidoptera were better protected against predatory ants (Dyer 1995), paper wasps (Bernays 1988), and birds (Singer et al 2014) compared with generalist species. however, the cited papers consider both chemically defended and non-defended prey species.…”

A Genomic Perspective on the Generation and Maintenance of Genetic Diversity in Herbivorous Insects

“…Host plant-specialized herbivores have either gained the ability to sequester plant-produced chemicals to defend themselves against attack by the third trophic level—often advertised through aposematic coloration—or they employ detoxification mechanisms and evasive strategies such as camouflage or mimicry (Farkas et al 2013; Petschenka and Agrawal 2016). Although the genomic consequences of these combinations of selection pressures are just starting to be explored (Joron et al 2011; Heliconius Genome Consortium 2012; Kunte et al 2014; Soria-Carrasco et al 2014; Zhan et al 2014), it seems probable that top-down forces, including generalist predators such as birds, are especially important (Bernays and Graham 1988; Singer et al 2014). …”