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  1. 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.

     
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    Free, publicly-accessible full text available December 1, 2024
  2. Abstract

    Soil microbes impact plant community structure and diversity through plant–soil feedbacks. However, linking the relative abundance of plant pathogens and mutualists to differential plant recruitment remains challenging. Here, we tested for microbial mediation of pairwise feedback using a reciprocal transplant experiment in a lowland tropical forest in Panama paired with amplicon sequencing of soil and roots. We found evidence that plant species identity alters the microbial community, and these changes in microbial composition alter subsequent growth and survival of conspecific plants. We also found that greater community dissimilarity between species in their arbuscular mycorrhizal and nonpathogenic fungi predicted increased positive feedback. Finally, we identified specific microbial taxa across our target functional groups that differentially accumulated under conspecific settings. Collectively, these findings clarify how soil pathogens and mutualists mediate net feedback effects on plant recruitment, with implications for management and restoration.

     
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  3. Abstract

    Meeting restoration targets may require active strategies to accelerate natural regeneration rates or overcome the resilience associated with degraded ecosystem states. Introducing desired ecosystem patches in degraded landscapes constitutes a promising active restoration strategy, with various mechanisms potentially causing these patches to become foci from which desired species can re‐establish throughout the landscape. This study considers three mechanisms previously identified as potential drivers of introduced patch dynamics: autocatalytic nucleation, directed dispersal, and resource concentration. These mechanisms reflect qualitatively different positive feedbacks. We developed an ecological model framework that compared how the occurrence of each mechanism was reflected in spatio‐temporal patch dynamics. We then analyzed the implications of these relationships for optimal restoration design. We found that patch expansion accelerated over time when driven by the autocatalytic nucleation mechanism, while patch expansion driven by the directed dispersal or resource concentration mechanisms decelerated over time. Additionally, when driven by autocatalytic nucleation, patch expansion was independent of patch position in the landscape. However, the proximity of other patches affected patch expansion either positively or negatively when driven by directed dispersal or resource concentration. For autocatalytic nucleation, introducing many small patches was a favorable strategy, provided that each individual patch exceeded a critical patch size. Introducing a single patch or a few large patches was the most effective restoration strategy to initiate the directed dispersal mechanism. Introducing many small patches was the most effective strategy for reaching restored ecosystem states driven by a resource concentration mechanism. Our model results suggest that introducing desirable patches can substantially accelerate ecosystem restoration, or even induce a critical transition from an otherwise stable degraded state toward a desired ecosystem state. However, the potential of this type of restoration strategy for a particular ecosystem may strongly depend on the mechanism driving patch dynamics. In turn, which mechanism drives patch dynamics may affect the optimal spatial design of an active restoration strategy. Each of the three mechanisms considered reflects distinct spatio‐temporal patch dynamics, providing novel opportunities for empirically identifying key mechanisms, and restoration designs that introduce desired patches in degraded landscapes according to these patch dynamics.

     
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  4. Abstract

    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.

     
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  5. Abstract

    Plant–microbe interactions play an important role in structuring plant communities. Arbuscular mycorrhizal fungi (AMF) are particularly important. Nonetheless, increasing anthropogenic disturbance will lead to novel plant–AMF interactions, altering longstanding co‐evolutionary trajectories between plants and their associated AMF. Although emerging work shows that plant–AMF response can evolve over relatively short time scales due to anthropogenic change, little work has evaluated how plant AMF responsespecificitymay evolve due to novel plant–mycorrhizal interactions. Here, we examine changes in plant–AMF interactions in novel grassland systems by comparing the mycorrhizal response of plant populations from unplowed native prairies with populations from post‐agricultural grasslands to inoculation with both native prairie AMF and non‐native novel AMF. Across four plant species, we find support for evolution of differential responses to mycorrhizal inocula types, that is, mycorrhizal response specificity, consistent with expectations of local adaptation, with plants from native populations responding most to native AMF and plants from post‐agricultural populations responding most to non‐native AMF. We also find evidence of evolution of mycorrhizal response in two of the four plant species, as overall responsiveness to AMF changed from native to post‐agricultural populations. Finally, across all four plant species, roots from native prairie populations had lower levels of mycorrhizal colonization than those of post‐agricultural populations. Our results report on one of the first multispecies assessment of local adaptation to AMF. The consistency of the responses in our experiment among four species provides evidence that anthropogenic disturbance may have unintended impacts on native plant species' association with AMF, causing evolutionary change in the benefit native plant species gain from native symbioses.

     
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  6. Abstract

    Arbuscular mycorrhizal fungi (AMF; Glomeromycota) are difficult to culture; therefore, establishing a robust amplicon-based approach to taxa identification is imperative to describe AMF diversity. Further, due to low and biased sampling of AMF taxa, molecular databases do not represent the breadth of AMF diversity, making database matching approaches suboptimal. Therefore, a full description of AMF diversity requires a tool to determine sequence-based placement in the Glomeromycota clade. Nonetheless, commonly used gene regions, including the SSU and ITS, do not enable reliable phylogenetic placement. Here, we present an improved database and pipeline for the phylogenetic determination of AMF using amplicons from the large subunit (LSU) rRNA gene. We improve our database and backbone tree by including additional outgroup sequences. We also improve an existing bioinformatics pipeline by aligning forward and reverse reads separately, using a universal alignment for all tree building, and implementing a BLAST screening prior to tree building to remove non-homologous sequences. Finally, we present a script to extract AMF belonging to 11 major families as well as an amplicon sequencing variant (ASV) version of our pipeline. We test the utility of the pipeline by testing the placement of known AMF, known non-AMF, andAcaulosporasp. spore sequences. This work represents the most comprehensive database and pipeline for phylogenetic placement of AMF LSU amplicon sequences within the Glomeromycota clade.

     
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  7. Abstract

    Microbiomes have profound effects on host fitness, yet we struggle to understand the implications for host ecology. Microbiome influence on host ecology has been investigated using two independent frameworks. Classical ecological theory powerfully represents mechanistic interactions predicting environmental dependence of microbiome effects on host ecology, but these models are notoriously difficult to evaluate empirically. Alternatively, host–microbiome feedback theory represents impacts of microbiome dynamics on host fitness as simple net effects that are easily amenable to experimental evaluation. The feedback framework enabled rapid progress in understanding microbiomes’ impacts on plant ecology, and can also be applied to animal hosts. We conceptually integrate these two frameworks by deriving expressions for net feedback in terms of mechanistic model parameters. This generates a precise mapping between net feedback theory and classic population modelling, thereby merging mechanistic understanding with experimental tractability, a necessary step for building a predictive understanding of microbiome influence on host ecology.

     
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  8. Summary

    Many plant species simultaneously interact with multiple symbionts, which can, but do not always, generate synergistic benefits for their host. We ask if plant life history (i.e. annual vs perennial) can play an important role in the outcomes of the tripartite symbiosis of legumes, arbuscular mycorrhizal fungi (AMF), and rhizobia.

    We performed a meta‐analysis of 88 studies examining outcomes of legume–AMF–rhizobia interactions on plant and microbial growth.

    Perennial legumes associating with AMF and rhizobia grew larger than expected based on their response to either symbiont alone (i.e. their response to co‐inoculation was synergistic). By contrast, annual legume growth with co‐inoculation did not differ from additive expectations. AMF and rhizobia differentially increased phosphorus (P) and nitrogen (N) tissue concentration. Rhizobium nodulation increased with mycorrhizal fungi inoculation, but mycorrhizal fungi colonization did not increase with rhizobium inoculation. Microbial responses to co‐infection were significantly correlated with synergisms in plant growth.

    Our work supports a balanced plant stoichiometry mechanism for synergistic benefits. We find that synergisms are in part driven by reinvestment in complementary symbionts, and that time‐lags in realizing benefits of reinvestment may limit synergisms in annuals. Optimization of microbiome composition to maximize synergisms may be critical to productivity, particularly for perennial legumes.

     
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  9. Abstract

    Soil-borne pathogens structure plant communities, shaping their diversity, and through these effects may mediate plant responses to climate change and disturbance. Little is known, however, about the environmental determinants of plant pathogen communities. Therefore, we explored the impact of climate gradients and anthropogenic disturbance on root-associated pathogens in grasslands. We examined the community structure of two pathogenic groups—fungal pathogens and oomycetes—in undisturbed and anthropogenically disturbed grasslands across a natural precipitation and temperature gradient in the Midwestern USA. In undisturbed grasslands, precipitation and temperature gradients were important predictors of pathogen community richness and composition. Oomycete richness increased with precipitation, while fungal pathogen richness depended on an interaction of precipitation and temperature, with precipitation increasing richness most with higher temperatures. Disturbance altered plant pathogen composition and precipitation and temperature had a reduced effect on pathogen richness and composition in disturbed grasslands. Because pathogens can mediate plant community diversity and structure, the sensitivity of pathogens to disturbance and climate suggests that degradation of the pathogen community may mediate loss, or limit restoration of, native plant diversity in disturbed grasslands, and may modify plant community response to climate change.

     
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  10. Abstract

    The theory of alternate stable states provides an explanation for rapid ecosystem degradation, yielding important implications for ecosystem conservation and restoration. However, utilizing this theory to initiate transitions from degraded to desired ecosystem states remains a significant challenge. Applications of the alternative stable states framework may currently be impeded by a mismatch between local‐scale driving processes and landscape‐scale emergent system transitions. We show how nucleation theory provides an elegant bridge between local‐scale positive feedback mechanisms and landscape‐scale transitions between alternate stable ecosystem states. Geometrical principles can be used to derive a critical patch radius: a spatially explicit, local description of an unstable equilibrium point. This insight can be used to derive an optimal patch size that minimizes the cost of restoration, and to provide a framework to measure the resilience of desired ecosystem states to the synergistic effects of disturbance and environmental change.

     
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