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

   https://doi.org/10.1002/ece3.6341  

   Reynolds, Hannah S. ; Wagner, Rebekah ; Wang, Guangzhou ; Burrill, Haley M. ; Bever, James D. ; Alexander, Helen M. ( June 2020 , Ecology and Evolution)

   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 fasciculataandCoreopsis 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.

    

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2. Manipulating plant microbiomes in the field: Native mycorrhizae advance plant succession and improve native plant restoration

   https://doi.org/10.1111/1365-2664.14036  

   Koziol, Liz ; Bauer, Jonathan T. ; Duell, Eric B. ; Hickman, Karen ; House, Geoffrey L. ; Schultz, Peggy A. ; Tipton, Alice G. ; Wilson, Gail W. T. ; Bever, James D. ( October 2021 , Journal of Applied Ecology)

   The plant microbiome is critical to plant health and is degraded with anthropogenic disturbance. However, the value of re‐establishing the native microbiome is rarely considered in ecological restoration. Arbuscular mycorrhizal (AM) fungi are particularly important microbiome components, as they associate with most plants, and later successional grassland plants are strongly responsive to native AM fungi.

   With five separate sites across the United States, we inoculated mid‐ and late successional plant seedlings with one of three types of native microbiome amendments: (a) whole rhizosphere soil collected from local old‐growth, undisturbed grassland communities in Illinois, Kansas or Oklahoma, (b) laboratory cultured AM fungi from these same old‐growth grassland sites or (c) no microbiome amendment. We also seeded each restoration with a diverse native seed mixture. Plant establishment and growth was followed for three growing seasons.

   The reintroduction of soil microbiome from native ecosystems improved restoration establishment.

   Including only native arbuscular mycorrhizal fungal communities produced similar improvements in plant establishment as what was found with whole soil microbiome amendment. These findings were robust across plant functional groups.

   Inoculated plants (amended with either AM fungi or whole soil) also grew more leaves and were generally taller during the three growing seasons.

   Synthesis and applications. Our research shows that mycorrhizal fungi can accelerate plant succession and that the reintroduction of both whole soil and laboratory cultivated native mycorrhizal fungi can be used as tools to improve native plant restoration following anthropogenic disturbance.

    

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3. Native arbuscular mycorrhizal fungi promote native grassland diversity and suppress weeds 4 years following inoculation

   https://doi.org/10.1111/rec.13772  

   Koziol, Liz ; McKenna, Thomas P. ; Crews, Timothy E. ; Bever, James D. ( August 2022 , Restoration Ecology)

   Restoration quality of native prairie can be improved by reintroducing key organisms from the native plant microbiome such as arbuscular mycorrhizal (AM) fungi. Here, we assess whether the positive effects of a native mycorrhizal inoculation observed during the first growing season remained at the end of the fourth growing season. In 2016, an experiment was initiated that assessed the response of a restored tallgrass prairie to an inoculation density gradient of native mycorrhizal fungi ranging from 0 to 8,192 kg/ha. First year results indicated that native plant establishment benefited from high but not low densities of native mycorrhizal inocula, resulting in improvements in native plant abundance, richness, and diversity. To assess whether these effects persist in later growing seasons, we resampled the prairie restoration in 2020 and analyzed the data similarly. Results from the fourth growing season indicated that the pattern of responses had persisted; the positive effects of inoculation observed during the first growing season remained after four growing seasons as demonstrated by improvements in total and native plant diversity and reduced non‐native abundance. Additionally, the low densities of mycorrhizal amendment that were not initially effective were found to reduce non‐native abundance in the fourth growing season, suggesting that low densities of mycorrhizal amendment can be amplified via positive plant‐AM fungal feedback to suppress weeds following the introduction of lesser amounts of AM fungi.

    

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4. Inoculation with native soil improves seedling survival and reduces non‐native reinvasion in a grassland restoration

   https://doi.org/10.1111/rec.13685  

   Duell, Eric B. ; O'Hare, Anna ; Wilson, Gail W. T. ( April 2022 , Restoration Ecology)

   Losses of grasslands have been largely attributed to widespread land‐use changes, such as conversion to row‐crop agriculture. The remaining tallgrass prairie faces further losses due to biological invasions by non‐native plant species, often with resultant ecosystem degradation. Of critical concern for conservation, restoration of native grasslands has been met with little success following eradication of non‐native plants. In addition to the direct and indirect effects of non‐native invasive plants on beneficial soil microbes, management practices targeting invasive species may also negatively affect subsequent restoration efforts. To assess mechanisms limiting germination and survival of native species and to improve native species establishment, we established six replicate plots of each of the following four treatments: (1) inoculated with freshly collected prairie soil with native seeds; (2) inoculated with steam‐pasteurized soil with native seeds; (3) noninoculated with native seeds; or (4) noninoculated/nonseeded control. Inoculation with whole soil did not improve seed germination; however, addition of whole soil significantly improved native species survival, compared to pasteurized soil or noninoculated treatments. Inoculation with whole soil significantly decreased reestablishment of non‐native invasiveBothriochloa bladhii(Caucasian bluestem); at the end of the growing season, plots receiving whole soil consisted of approximately 30%B. bladhiicover, compared to approximately 80% in plots receiving no soil inoculum. Our results suggest invasion and eradication efforts negatively affect arbuscular mycorrhizal hyphal and spore abundances and soil aggregate stability, and inoculation with locally adapted soil microbial communities can improve metrics of restoration success, including plant species richness and diversity, while decreasing reinvasion by non‐native species.

    

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5. Native plant abundance, diversity, and richness increases in prairie restoration with field inoculation density of native mycorrhizal amendments

   https://doi.org/10.1111/rec.13151  

   Koziol, Liz ; Crews, Timothy E. ; Bever, James D. ( April 2020 , Restoration Ecology)

   Ecological restoration efforts can increase the diversity and function of degraded areas. However, current restoration practices cannot typically reestablish the full diversity and species composition of remnant plant communities. Restoration quality can be improved by reintroducing key organisms from the native plant microbiome. In particular, root symbionts called arbuscular mycorrhizal (AM) fungi are critical in shaping grassland communities, but are sensitive to anthropogenic disturbance, which may pose a problem for grassland restoration. Studies of mycorrhizal amendments include inoculation densities of 2–10,000 kg of inocula per hectare. These studies report variable results that may depend on inocula volume, composition, or nativeness. Here we test eight different densities of native AM fungal amendment, ranging from 0 to 8,192 kg/ha in a newly installed prairie restoration. We found that native plant establishment benefited from native mycorrhizal inocula, resulting in improvements in native plant abundance, richness, and community diversity. Moreover, the application of very low densities of native mycorrhizal inocula, as suggested on commercial mycorrhizal products, were ineffective, and higher concentrations were required to benefit native plant abundance and community diversity. These data suggest that higher densities of mycorrhizal amendment or perhaps alternative distribution methods may be required to maximize benefits of native mycorrhizal amendments in restoration practices.

    

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