Which processes drive the productivity benefits of biodiversity remain a critical, but unanswered question in ecology. We tested whether the soil microbiome mediates the diversity‐productivity relationships among late successional plant species. We found that productivity increased with plant richness in diverse soil communities, but not with low‐diversity mixtures of arbuscular mycorrhizal fungi or in pasteurised soils. Diversity‐interaction modelling revealed that pairwise interactions among species best explained the positive diversity‐productivity relationships, and that transgressive overyielding resulting from positive complementarity was only observed with the late successional soil microbiome, which was both the most diverse and exhibited the strongest community differentiation among plant species. We found evidence that both dilution/suppression from host‐specific pathogens and microbiome‐mediated resource partitioning contributed to positive diversity‐productivity relationships and overyielding. Our results suggest that re‐establishment of a diverse, late successional soil microbiome may be critical to the restoration of the functional benefits of plant diversity following anthropogenic disturbance.
This content will become publicly available on December 1, 2024
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.
more » « less- Award ID(s):
- 1738041
- NSF-PAR ID:
- 10489828
- Publisher / Repository:
- Nature Communications
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 14
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract -
more » « less
Abstract In many natural systems, diverse host communities can reduce disease risk, though less is known about the mechanisms driving this “dilution effect.” We relate feedback theory, which focuses on pathogen‐mediated coexistence, to mechanisms of dilution derived from epidemiological models, with the central goal of gaining insights into host–pathogen interactions in a community context. We first compare the origin, structure, and application of epidemiological and feedback models. We then explore the mechanisms of dilution, which are grounded in single‐pathogen, single‐host epidemiological models, from the perspective of feedback theory. We also draw on feedback theory to examine how coinfecting pathogens, and pathogens that vary along a host specialist–generalist continuum, apply to dilution theory. By identifying synergies among the feedback and epidemiological approaches, we reveal ways in which organisms occupying different trophic levels contribute to diversity–disease relationships. Additionally, using feedbacks to distinguish dilution in disease incidence from dilution in the net effect of disease on host fitness allows us to articulate conditions under which definitions of dilution may not align. After ascribing dilution mechanisms to macro‐ or microorganisms, we propose ways in which each contributes to diversity–disease and productivity–diversity relationships. Our analyses lead to predictions that can guide future research efforts.
-
more » « less
Abstract Although the importance of the soil microbiome in mediating plant community structures and functions has been increasingly emphasized in ecological studies, the biological processes driving crop diversity overyielding remain unexplained in agriculture. Based on the plant–soil feedback (PSF) theory and method, we quantified to what extent and how soil microbes contributed to intercropping overyielding.
Soils were collected as inocula and sequenced from a unique 10‐year field experiment, consisting of monoculture, intercropping and rotation planted with wheat (
Triticum aestivum) , maize (Zea mays) or faba bean (Vicia faba ). A PSF greenhouse study was conducted to test microbial effects on three crops' growth in monoculture or intercropping.In wheat & faba bean (W&F) and maize & faba bean (M&F) systems, soil microbes drove intercropping overyielding compared to monoculture, with 28%–51% of the overyielding contributed by microbial legacies. The overyielding effects resulted from negative PSFs in both systems, as crops, in particular faba bean grew better in soils conditioned by other crops than itself. Moreover, faba bean grew better in soils from intercropping or rotation than from the average of monocultures, indicating a strong positive legacy effect of multispecies cropping systems. However, with positive PSF and negative legacy benefit effect of intercropping/rotation, we did not observe significant overyielding in the W&M system.
With more bacterial and fungal dissimilarities by metabarcoding in heterospecific than its own soil, the better it improved faba bean growth. More detailed analysis showed faba bean monoculture soil accumulated more putative pathogens with higher
Fusarium relative abundance and moreFusarium oxysporum gene copies by qPCR, while in heterospecific soils, there were less pathogenic effects when cereals were engaged. Further analysis in maize/faba bean intercropping also showed an increase of rhizobia relative abundance.Synthesis and applications . Our results demonstrate a soil microbiome‐mediated advantage in intercropping through suppression of the negative PSF of pathogens and increasing beneficial microbes. As microbial mediation of overyielding is context‐dependent, we conclude that the dynamics of both beneficial and pathogenic microbes should be considered in designing cropping systems for sustainable agriculture, particularly including combinations of legumes and cereals. -
more » « less
Abstract Litter decomposition facilitates the recycling of often limiting resources, which may promote plant productivity responses to diversity, that is, overyielding. However, the direct relationship between decomposition,
k , and overyielding remains underexplored in grassland diversity manipulations.We test whether local adaptation of microbes, that is, home‐field advantage (HFA), N‐priming from plant inputs or precipitation drive decomposition and whether decomposition generates overyielding. Within a grassland diversity‐manipulation, altering plant richness (1, 2, 3 and 6 species), composition (communities composed of plants from a single‐family or multiple‐families) and precipitation (50% and 150% ambient growing season precipitation), we conducted a litter decomposition experiment. In spring 2020, we deployed four replicate switchgrass,
Panicum virgatum , litter bags (1.59 mm mesh opening), collecting them over 7 months to estimate litterk .Precipitation was a strong, independent driver of decomposition. Switchgrass decomposition accelerated with grass richness and decelerated as phylogenetic dissimilarity from switchgrass increased, suggesting decomposition is fastest at ‘home’. However, decomposition slowed with switchgrass density. In plots that contained switchgrass, we observed no relationship between decomposition and fungal saprotroph dissimilarity from switchgrass. However, in plots without switchgrass, decomposition slowed with increasing saprotroph dissimilarity from switchgrass. Combined these findings suggest that HFA is strongest when closely related neighbours, that is, heterospecific neighbours, are present in the community, rather than other individuals of the same species, that is, conspecifics. Legumes accelerated decomposition with more litter N remaining in those plots, suggesting that N‐inputs from planted legumes are priming decomposition of litter C. However, decomposition and overyielding were unrelated in legume communities. While in grass communities, overyielding and decomposition were positively related and the relationship was strongest in plots with low densities of switchgrass, that is, with heterospecific neighbours.
Combined these findings suggest that plant species richness and community composition stimulate litter decomposition through multiple mechanisms, including N‐priming, but only HFA from local adaptation of microbes on closely related species correlates with overyielding, likely through resource recycling. Our results link diversity with ecosystem processes facilitating above‐ground productivity. Whether diversity loss will affect litter decomposition, productivity or both is contingent on resident plant traits and whether a locally adapted soil microbiome is maintained.
Read the free
Plain Language Summary for this article on the Journal blog. -
more » « less
Abstract Plant productivity often increases with species richness, but the mechanisms explaining this diversity–productivity relationship are not fully understood. We tested if plant–soil feedbacks (PSF) can help to explain how biomass production changes with species richness. Using a greenhouse experiment, we measured all 240 possible PSFs for 16 plant species. At the same time, 49 plant communities with diversities ranging from one to 16 species were grown in replicated pots. A suite of plant community growth models, parameterized with (PSF) or without PSF (Null) effects, was used to predict plant growth observed in the communities. Selection effects and complementarity effects in modeled and observed data were separated. Plants created soils that increased or decreased subsequent plant growth by 25%
± 10%, but because PSFs were negative for C3and C4grasses, neutral for forbs, and positive for legumes, the net effect of all PSFs was a 2%± 17% decrease in plant growth. Experimental plant communities with 16 species produced 37% more biomass than monocultures due to complementarity. Null models incorrectly predicted that 16‐species communities would overyield due to selection effects. Adding PSF effects to Null models decreased selection effects, increased complementarity effects, and improved correlations between observed and predicted community biomass. PSF models predicted 26% of overyielding caused by complementarity observed in experimental communities. Relative to Null models, PSF models improved the predictions of the magnitude and mechanism of the diversity–productivity relationship. Results provide clear support for PSFs as one of several mechanisms that determine diversity–productivity relationships and help close the gap in understanding how biodiversity enhances ecosystem services such as biomass production.
