Abstract

Although decades of research have typically demonstrated a positive correlation between biodiversity of primary producers and associated trophic levels, the ecological drivers of this association are poorly understood. Recent evidence suggests that the plant microbiome, or the fungi and bacteria found on and inside plant hosts, may be cryptic yet important drivers of important processes, including primary production and trophic interactions. Here, using high-throughput sequencing, we characterized foliar fungal community diversity, composition, and function from 15 broadleaved tree species (N = 545) in a recently established, large-scale temperate tree diversity experiment using over 17,000 seedlings. Specifically, we tested whether increases in tree richness and phylogenetic diversity would increase fungal endophyte diversity (the “Diversity Begets Diversity” hypothesis), as well as alter community composition (the “Tree Diversity–Endophyte Community” hypothesis) and function (the “Tree Diversity–Endophyte Function” hypothesis) at different spatial scales. We demonstrated that increasing tree richness and phylogenetic diversity decreased fungal species and functional guild richness and diversity, including pathogens, saprotrophs, and parasites, within the first three years of a forest diversity experiment. These patterns were consistent at the neighborhood and tree plot scale. Our results suggest that fungal endophytes, unlike other trophic levels (e.g., herbivores as well as epiphytic bacteria), respond negatively to increasing plant diversity.

Highlights

  • Rapid environmental and anthropogenic changes are altering patterns of biodiversity worldwide, degrading ecosystem productivity, function, and services [1,2]

  • For all fungal species accumulation curves, many samples appear to be somewhat close to approaching an asymptote, suggesting that our sequencing depth is relatively close to encompassing a large extent of endophyte exact sequence variants (ESVs) richness in communities among diversity treatments (Figure S1)

  • We highlight the importance of plant diversity and its interaction with the plant microbiome and explore how these interactions may impact plant performance early in forest stand development

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Summary

Introduction

Rapid environmental and anthropogenic changes are altering patterns of biodiversity worldwide, degrading ecosystem productivity, function, and services [1,2]. Declining biodiversity will likely have important implications for human wellbeing, as decades of research in land and seascapes have demonstrated a positive relationship between biodiversity and critical ecosystem services (e.g., increasing plant productivity, supporting diverse faunal communities, regulating nutrient cycles, and buffering ecosystems against climate change; reviewed by [7,8]). Endophytes, or the microbes that live inside plant tissues, colonize all of the world’s plant species and mediate multiple tree performance metrics – which, in turn, may have implications for BEF [12,13,16,20,21]. Griffin et al [12,13] demonstrated that applying antibiotics to sapling foliage in situ either decreased or increased seedling growth of multiple tree species by up to

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