Insect herbivores cause substantial changes in the leaves they attack, but their effects on the ecophysiology of neighbouring, nondamaged leaves have never been quantified in natural canopies. We studied how winter moth (Operophtera brumata), a common herbivore in temperate forests, affects the photosynthetic and isoprene emission rates of its host plant, the pedunculate oak (Quercus robur). Through a manipulative experiment, we measured leaves on shoots damaged by caterpillars or mechanically by cutting, or left completely intact. To quantify the effects at the canopy scale, we surveyed the extent and patterns of leaf area loss in the canopy. Herbivory reduced photosynthesis both in damaged leaves and in their intact neighbours. Isoprene emission rates significantly increased after mechanical leaf damage. When scaled up to canopy-level, herbivory reduced photosynthesis by 48 ± 10%. The indirect effects of herbivory on photosynthesis in undamaged leaves (40%) were much more important than the direct effects of leaf area loss (6%). If widespread across other plant-herbivore systems, these findings suggest that insect herbivory has major and previously underappreciated influences in modifying ecosystem carbon cycling, with potential effects on atmospheric chemistry.

No abstract

Climate is changing faster now than it has in the last 2000 years (IPCC, 2021), and ecological communities are being reshuffled as a consequence (Davis & Shaw, 2001;Parmesan & Yohe, 2003).Predicting which types of species are likely to suffer or benefit from changing climate and species interactions is needed for accurate estimates of future community composition and ecosystem function.How plant species respond to environmental change depends on their eco-physiological properties (Beyschlag & Ryel, 2007).

By feeding on plant tissue, insect herbivores can change several characteristics of their hosts. These changes have the potential to alter the quality of the plant for other herbivore species, potentially altering the structure of the community of species attacking the plant at a later point in time. We tested whether herbivory early in the season changes host plant performance, polyphenol chemistry, and the community structure of sessile herbivores later in the season. We experimentally manipulated densities of early-season moth caterpillars on a set of young oak trees and measured tree growth, reproduction, leaf chemistry, and the abundance and community composition of leafmining and galling species later in the season. The experimental manipulations of early-season herbivores did not affect late-season leaf chemistry or tree performance. Early-season herbivores had a weak negative effect on the abundance of gallers and a positive, tree-dependent effect on the overall diversity of late-season sessile herbivores. The chemical composition of leaves covaried with the species composition of the late-season leafmining and galling community. Both the chemical composition of the host tree and the late-season insect community structure were strongly affected by the growth location of the tree. Our results suggest that plant-mediated indirect effects between herbivores might play a limited role in this system, whereas the underlying variation in plant chemistry is an important factor structuring the associated insect community. Our results emphasize that factors other than prior herbivory can be important determinants of plant chemistry and the community composition of herbivores.