Bottom-up and top-down effects of tree species diversity on leaf insect herbivory

The diversity of plant neighbors commonly results in direct, bottom-up effects on herbivore ability to locate their host, and in indirect effects on herbivores involving changes in plant traits and a top-down control by their enemies. Yet, the relative contribution of bottom-up and top-down forces remains poorly understood. We also lack knowledge on the effect of abiotic constraints such as summer drought on the strength and direction of these effects. We measured leaf damage on pedunculate oak (Quercus robur), alone or associated with birch, pine or both in a long-term tree diversity experiment (ORPHEE), where half of the plots were irrigated while the other half remained without irrigation and received only rainfall. We tested three mechanisms likely to explain the effects of oak neighbors on herbivory: (1) Direct bottom-up effects of heterospecific neighbors on oak accessibility to herbivores, (2) indirect bottom-up effects of neighbors on the expression of leaf traits, and (3) top-down control of herbivores by predators. Insect herbivory increased during the growth season but was independent of neighbor identity and irrigation. Specific leaf area, leaf toughness, and thickness varied with neighbor identity while leaf dry matter content or C:N ratio did not. When summarized in a principal component analysis (PCA), neighbor identity explained 87% of variability in leaf traits. PCA axes partially predicted herbivory. Despite greater rates of attack on dummy caterpillars in irrigated plots, avian predation, and insect herbivory remained unrelated. Our study suggests that neighbor identity can indirectly influence insect herbivory in mixed forests by modifying leaf traits. However, we found only partial evidence for these trait-mediated effects and suggest that more attention should be paid to some unmeasured plant traits such as secondary metabolites, including volatile organic compounds, to better anticipate the effects of climate change on plant-insect interactions in the future.