Oak dieback strongly influences the diversity, composition and network structure of soil microbial communities with feedbacks on regeneration

Abstract

Forested landscapes are rapidly being transformed by increasing rates of tree mortality caused by global-change factors such as exotic pathogens or extreme droughts. Disturbance of tree communities can have cascading impacts on biodiversity at all organization levels. However, how soil microorganisms respond to tree dieback and the implications for ecosystem recovery is largely unknown. Here we combined spatially-explicit neighborhood models, DNA metabarcoding, and a field experiment to explore how the decline of the Mediterranean tree Quercus suber altered the diversity, composition and network structure of belowground fungal communities in forests invaded by the exotic pathogen Phytophthora cinnamomi, and whether such changes had cascading impacts on Q. suber recruitment. We found that Q. suber dieback caused a reduction of the taxonomic diversity of soil fungal communities but increased their phylogenetic diversity, likely due to the colonization of unhealthy soils by rare taxa not present in healthy soils. Tree neighborhoods dominated by defoliated or dead oaks had soil fungal communities with higher relative abundance of saprophytic and pathogenic fungi, lower abundance of ectomycorrhizal fungi, and very distinct network structure (e.g. lower modularity) than healthy neighborhoods. Such changes had negative feedbacks on Q. suber regeneration, since seedling performance was negatively related to fungal phylogenetic diversity but positively influenced by ectomycorrhizal abundance. Our results showed that oak dieback exerted a strong influence on the diversity and structure of soil fungal networks, promoting new assemblages impoverished in mutualistic taxa. This implies that oak dieback has far-reaching multi-trophic effects that may affect regeneration and ecosystem recovery