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Title: Native plant abundance, diversity, and richness increases in prairie restoration with field inoculation density of native mycorrhizal amendments
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Award ID(s):
1738041 1656006
NSF-PAR ID:
10456973
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Restoration Ecology
Volume:
28
Issue:
S4
ISSN:
1061-2971
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
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  1. Perennial polyculture cropping systems are a novel agroecological approach used to mirror some of the ecological benefits provided by native perennial ecosystems including increased carbon and nitrogen storage, more stable soils, and reduced anthropogenic input. Plants selected for perennial agroecosystems are often closely related to native perennials known to be highly dependent on microbiome biota, such as arbuscular mycorrhizal (AM) fungi. However, most plantings take place in highly disturbed soils where tillage and chemical use may have rendered the AM fungal communities less abundant and ineffective. 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 the response of 19 crop plant species to a native mycorrhizal fungal community in a greenhouse and field experiment. In our field experiment, we chose eight different densities of AM fungal amendment, ranging from 0 to 8192 kg/hectare, representing conventional agricultural practices (no AM fungi addition), commercial product density recommendations, and higher densities more typical of past scientific investigation. We found that plant species that benefited from native mycorrhizal inocula in the greenhouse also benefited from inoculation in the field polyculture planting. However, the densities of mycorrhizal inocula suggested on commercial mycorrhizal products were ineffective, and higher concentrations were required to detect significant benefit plant growth and survival. These data suggest that higher concentrations of mycorrhizal amendment or perhaps alternative distribution methods may be required to utilize native mycorrhizal amendment in agroecology systems. 
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  2. 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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  3. Although several studies have shown increased native plant establishment with native microbe soil amendments, few studies have investigated how microbes can alter seedling recruitment and establishment in the presence of a non-native competitor. In this study, the effect of microbial communities on seedling biomass and diversity was assessed by seeding pots with both native prairie seeds and a non-native grass that commonly invades US grassland restorations, Setaria faberi. Soil in the pots was inoculated with whole soil collections from ex-arable land, late successional arbuscular mycorrhizal (AM) fungi isolated from a nearby tallgrass prairie, with both prairie AM fungi and ex-arable whole soil, or with a sterile soil (control). We hypothesized (1) late successional plants would benefit from native AM fungi, (2) that non-native plants would outcompete native plants in ex-arable soils, and (3) early successional plants would be unresponsive to microbes. Overall, native plant abundance, late successional plant abundance, and total diversity were greatest in the native AM fungi+ ex-arable soil treatment. These increases led to decreased abundance of the non-native grass S. faberi. These results highlight the importance of late successional native microbes on native seed establishment and demonstrate that microbes can be harnessed to improve both plant community diversity and resistance to invasion during the nascent stages of restoration. 
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    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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    Arbuscular mycorrhizal (AM) fungi are root symbionts that can facilitate plant growth and influence plant communities by altering plant interactions with herbivores. Therefore, AM fungi could be critical for the conservation of certain rare plants and herbivores. For example, North American milkweed species are crucial hosts for monarch butterflies (Danaus plexippus). Understanding how mycorrhizal composition affects milkweeds will have direct impacts on the conservation and restoration of both increasingly threatened guilds. We present data from three studies on the effect of AM fungal composition on milkweed growth, latex production, and establishment. First, we grew seven milkweed species with and without a mixture of native mycorrhizal fungi. We assessed how important fungal composition is to milkweed growth and latex production by growing four milkweed species with seven fungal compositions, as single‐species inoculations with four native fungi, a mixture of native fungi, a single commercial fungus of presumably non‐native origin, and noninoculated controls. Finally, we assessed the field establishment of two milkweed species with and without native mycorrhizal inoculation. Milkweed species grew 98% larger and produced 82% more latex after inoculation with native mycorrhizae. Milkweeds were strongly affected by fungal composition; milkweeds were inhibited by commercial fungi (average of −14% growth) and showed variable but positive responses to native fungal species (average of +3% to +38% biomass). Finally, we found that restoration establishment was dependent on inoculation with native fungi and milkweed species. Overall, our findings indicate that some milkweed species (i.e.,Asclepias syriacaandA. incarnata) are not responsive to mycorrhizal fungal presence or sensitive to mycorrhizal composition while others are, including endangered species (A. meadii) and species of high conservation value (A. tuberosa). We conclude that the reintroduction of native AM fungi could improve the establishment of desirable milkweed species and should be considered within strategies for plantings for monarch conservation.

     
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