Combined effects of drought and insect herbivory on oak leaf endophytic communities and performance

Leaf-associated microbiota are considered sensitive indicators of how plants respond to their environment. Yet, plants can be exposed to a wide range of biotic and abiotic stresses whose independent and combined effects on plant microbiota remain poorly understood, as do their cumulative consequences for plant performance. We conducted an experiment to expose saplings of four oak species to drought and herbivory by a piercing–sucking insect. We assessed the effect of water deficit on herbivory, as well as the individual and combined effects of water deficit and herbivory on fungal endophytic communities. To evaluate the cumulative impacts of biotic and abiotic stresses on plant performance, and the potential of the fungal endophytic communities as an indicator of plant responses to stress, we measured photosynthetic capacity, growth, and the accumulation of non-structural carbohydrates in twigs at the end of the growing season. Water deficit had no effect on insect herbivory but induced a decrease in the diversity of the leaf-associated fungal community. In contrast, herbivory shifted the composition of fungal communities through species replacement or addition depending on oak species. Herbivory altered photosynthesis, whereas drought but not herbivory reduced oak growth. None of these stresses influenced the storage of non-structural carbohydrates. Leaf-associated fungi responded to both stresses. However, the underlying mechanisms appeared to differ and the association with oak performance was weak. Overall, our study suggests a certain degree of resilience in trees subjected to interacting stresses, while also highlighting vulnerabilities that may have implications for tree health over the long term.