Plant invader alters root fungal microbiome, physiology and biomass allocation in native understory species

Abstract

Plant invaders that produce novel antimicrobial compounds can alter local soil properties and below‐ground microbial communities, including both arbuscular mycorrhizal (AM) and pathogenic fungi. Such changes can inhibit the critical nutritional mutualism between native plants and AM fungi and in turn influence the acquisition and allocation of resources by native plants. However, we know little about how root fungal‐mediated changes to plant resource economies affect native plant traits and performance, especially across species that vary in reliance on AM fungi. We established a common garden experiment in a forest by transplanting replicates of 10 common native herbaceous understory species (eight mycorrhizal and two non‐mycorrhizal species) into an area previously uninvaded by the widespread invader, Alliaria petiolata (garlic mustard). We seeded Alliaria in half of the plots and measured native plant physiology and leaf traits three times over the course of the experiment. After 5–6 years, we quantified the effects of Alliaria on soil nutrients, the root fungal community (AM and pathogenic) and plant above‐ and below‐ground biomass. Alliaria addition reduced colonization and changed AM fungi community composition within mycorrhizal species' roots. Native species grown with Alliaria received relatively less leaf nitrogen from AM fungal partners, indicating depressed nutritional function of the plant‐AM fungal mutualism. Alliaria addition also increased photosynthetic capacity for three mycorrhizal species, by 83%–215%, and increased total leaf area twofold overall. Interestingly, Alliaria addition increased above‐ground biomass and reduced root‐shoot ratio in both mycorrhizal and non‐mycorrhizal plants. Alliaria‐driven increases in leaf area were mediated by shifts in the composition of AM root fungal microbiomes. Synthesis. Together, these changes indicate increased investment in photosynthetic function of native understory plants in response to Alliaria invasion, which may arise from shifts in the root fungal microbiome that reduce nutritional function and increase carbon allocation to plant–fungal symbioses. Our findings provide mechanistic insight into how invaders such as Alliaria that produce novel antimicrobial compounds can influence native understory plants and potentially contribute to native species declines over time.