Insect defoliation is linked to a decrease in soil ectomycorrhizal biomass and shifts in needle endophytic communities

Abstract

Insect outbreaks of increasing frequency and severity in forests are predicted due to climate change. Insect herbivory is known to promote physiological changes in forest trees. However, little is known about whether these plant phenotypic adjustments have cascading effects on tree microbial symbionts such as fungi in roots and foliage. We studied the impact of defoliation by the pine processionary moth in two infested Pinus nigra forests through a multilevel sampling of defoliated and non-defoliated trees. We measured tree growth, nutritional status and carbon allocation to chemical defenses. Simultaneously, we analyzed the putative impact of defoliation on the needle endophytes and on the soil fungal communities. Higher concentrations of chemical defenses were found in defoliated trees, likely as a response to defoliation; however, no differences in non-structural carbohydrate reserves were found. In parallel to the reductions in tree growth and changes in chemical defenses, we observed shifts in the composition of needle endophytic and soil fungal communities in defoliated trees. Defoliated trees consistently corresponded with a lower biomass of ectomycorrhizal fungi in both sites, and a higher alpha diversity and greater relative abundance of belowground saprotrophs and pathogens. However, ectomycorrhizal alpha diversity was similar between non-defoliated and defoliated trees. Specific needle endophytes in old needles were strongly associated with non-defoliated trees. The potential role of these endophytic fungi in pine resistance should be further investigated. Our study suggests that lower biomass of ectomycorrhizal fungi in defoliated trees might slow down tree recovery since fungal shifts might affect tree-mycorrhizal feedbacks and can potentially influence carbon and nitrogen cycling in forest soils.

J.J.C. acknowledges the support of the CGL2015-69186-C2-1-R and RTI2018-096884-B-C31 projects (Spanish Ministry of Science), and L.S. and R.Z. acknowledge support from MCIU/AEI/FEDER/UE grants FUTURPIN AGL2015-68274-C3-2-R and RESILPINE RTI2018-094691-B-C33 and from Xunta de Galicia‐GAIN grant IN607A2016/013. J.O. and J.G.A. were supported by a Ramón y Cajal fellowship (RYC-2015-17459; RYC-2016-20528, respectively) and J.A.B. was supported by the Serra-Hunter Program-Generalitat de Catalunya.