Dilution of specialist pathogens drives productivity benefits from diversity in plant mixtures.

Productivity benefits from diversity can arise when compatible pathogen hosts are buffered by unrelated neighbors, diluting pathogen impacts. However, the generality of pathogen dilution has been controversial and rarely tested within biodiversity manipulations. Here, we test whether soil pathogen dilution generates diversity- productivity relationships using a field biodiversity-manipulation experiment, greenhouse assays, and feedback modeling. We find that the accumulation of specialist pathogens in monocultures decreases host plant yields and that pathogen dilution predicts plant productivity gains derived from diversity. Pathogen specialization predicts the strength of the negative feedback between plant species in greenhouse assays. These feedbacks significantly predict the overyielding measured in the field the following year. This relationship strengthens when accounting for the expected dilution of pathogens in mixtures. Using a feedback model, we corroborate that pathogen dilution drives overyielding. Combined empirical and theoretical evidence indicate that specialist pathogen dilution generates overyielding and suggests that the risk of losing productivity benefits from diversity may be highest where environmental change decouples plant-microbe interactions.

Rapid differentiation of soil and root microbiomes in response to plant composition and biodiversity in the field.

Research suggests that microbiomes play a major role in structuring plant communities and influencing ecosystem processes, however, the relative roles and strength of change of microbial components have not been identified. We measured the response of fungal, arbuscular mycorrhizal fungal (AMF), bacteria, and oomycete composition 4 months after planting of field plots that varied in plant composition and diversity. Plots were planted using 18 prairie plant species from three plant families (Poaceae, Fabaceae, and Asteraceae) in monoculture, 2, 3, or 6 species richness mixtures and either species within multiple families or one family. Soil cores were collected and homogenized per plot and DNA were extracted from soil and roots of each plot. We found that all microbial groups responded to the planting design, indicating rapid microbiome response to plant composition. Fungal pathogen communities were strongly affected by plant diversity. We identified OTUs from genera of putatively pathogenic fungi that increased with plant family, indicating likely pathogen specificity. Bacteria were strongly differentiated by plant family in roots but not soil. Fungal pathogen diversity increased with planted species richness, while oomycete diversity, as well as bacterial diversity in roots, decreased. AMF differentiation in roots was detected with individual plant species, but not plant family or richness. Fungal saprotroph composition differentiated between plant family composition in plots, providing evidence for decomposer home-field advantage. The observed patterns are consistent with rapid microbiome differentiation with plant composition, which could generate rapid feedbacks on plant growth in the field, thereby potentially influencing plant community structure, and influence ecosystem processes. These findings highlight the importance of native microbial inoculation in restoration.

Effects of the soil microbiome on the demography of two annual prairie plants.

Both mutualistic and pathogenic soil microbes are known to play important roles in shaping the fitness of plants, likely affecting plants at different life cycle stages.In order to investigate the differential effects of native soil mutualists and pathogens on plant fitness, we compared survival and reproduction of two annual tallgrass prairie plant species (Chamaecrista fasciculata and Coreopsis tinctoria) in a field study using 3 soil inocula treatments containing different compositions of microbes. The soil inocula types included fresh native whole soil taken from a remnant prairie containing both native mutualists and pathogens, soil enhanced with arbuscular mycorrhizal (AM) fungi derived from remnant prairies, and uninoculated controls.For both species, plants inoculated with native prairie AM fungi performed much better than those in uninoculated soil for all parts of the life cycle. Plants in the native whole prairie soil were either generally similar to plants in the uninoculated soil or had slightly higher survival or reproduction.Overall, these results suggest that native prairie AM fungi can have important positive effects on the fitness of early successional plants. As inclusion of prairie AM fungi and pathogens decreased plant fitness relative to prairie AM fungi alone, we expect that native pathogens also can have large effects on fitness of these annuals. Our findings support the use of AM fungi to enhance plant establishment in prairie restorations.