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

ABSTRACT: 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.

SUBMITTER: Wang G

PROVIDER: S-EPMC10728191 | biostudies-literature | 2023 Dec

REPOSITORIES: biostudies-literature

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

Wang Guangzhou G Burrill Haley M HM Podzikowski Laura Y LY Eppinga Maarten B MB Zhang Fusuo F Zhang Junling J Schultz Peggy A PA Bever James D JD

Nature communications 20231218 1

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 pathog ...[more]

PMID: 38110413

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Project description:Diversity-productivity relationships can differ between forests dominated by different mycorrhizal types and be modulated by specialist and generalist pathogens. However, little is known about how these factors interact to modulate biodiversity effects. We addressed this knowledge gap with a 2-year experiment combining the manipulation of plant richness (one, two, four, eight species) and mycorrhizal tree type (arbuscular mycorrhizal [AM] tree-dominated; ecto-mycorrhizal [ECM] tree-dominated) with fungicide application for leaf pathogens (added or control). Biodiversity effects were quantified for community productivity and its two components (shoots and roots). We observed nonlinear diversity-productivity relationships, with the productivity of ECM tree-dominated communities increasing at low to intermediate diversity and declining at the highest species richness. Foliar fungicide application reduced positive complementarity effects and increased productivity in both ECM tree monocultures as well as eight-species mixtures. This finding suggests that the dilution effects of specialized pathogens may dominate at low diversity, while the spillover effects of generalist pathogens may become dominant at high diversity, resulting in unimodal diversity-productivity relationships. In AM tree-dominated communities, aboveground productivity strongly increased in response to leaf pathogen suppression in eight-species mixtures, and the release from leaf pathogens benefited most of the species that were most productive in fungicide-treated monocultures. This agrees with the prediction that spillover effects of generalist pathogens in diverse plant communities could differentially suppress highly productive species due to the trade-off between growth and defense. In addition, positive biodiversity effects on root production were significantly stronger in AM tree- than ECM tree-dominated communities. Our results demonstrate that relationships between plant diversity and productivity can be nonlinear due to the combined effects of specialized and generalized plant-fungal interactions, depend on plant mycorrhizal type, and differ between aboveground and belowground compartments.

Project description:BackgroundThe different hypotheses proposed to explain positive species richness-productivity relationships, i.e. selection effect and complementarity effect, imply that plant functional characteristics are at the core of a mechanistic understanding of biodiversity effects.Methodology/principal findingsWe used two community-wide measures of plant functional composition, (1) community-weighted means of trait values (CWM) and (2) functional trait diversity based on Rao's quadratic diversity (FD(Q)) to predict biomass production and measures of biodiversity effects in experimental grasslands (Jena Experiment) with different species richness (2, 4, 8, 16 and 60) and different functional group number and composition (1 to 4; legumes, grasses, small herbs, tall herbs) four years after establishment. Functional trait composition had a larger predictive power for community biomass and measures of biodiversitity effects (40-82% of explained variation) than species richness per se (<1-13% of explained variation). CWM explained a larger amount of variation in community biomass (80%) and net biodiversity effects (70%) than FD(Q) (36 and 38% of explained variation respectively). FD(Q) explained similar proportions of variation in complementarity effects (24%, positive relationship) and selection effects (28%, negative relationship) as CWM (27% of explained variation for both complementarity and selection effects), but for all response variables the combination of CWM and FD(Q) led to significant model improvement compared to a separate consideration of different components of functional trait composition. Effects of FD(Q) were mainly attributable to diversity in nutrient acquisition and life-history strategies. The large spectrum of traits contributing to positive effects of CWM on biomass production and net biodiversity effects indicated that effects of dominant species were associated with different trait combinations.Conclusions/significanceOur results suggest that the identification of relevant traits and the relative impacts of functional identity of dominant species and functional diversity are essential for a mechanistic understanding of the role of plant diversity for ecosystem processes such as aboveground biomass production.

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

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

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