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

Abstract

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.

Inoculation with native grassland soils improves native plant species germination in highly disturbed soil

“…Furthermore, restoration strategies to eradicate nonnative plants often include mechanical or chemical removal of the invasive species, and these intensive management practices may also impede germination of native species (Hu et al, 2021; McManamen et al, 2018; Wagner & Nelson, 2014). While it is well documented that anthropogenic disturbances have adverse effects on soil microbial communities, the importance of re‐establishing native microbial communities is seldom considered in ecological restorations (Koziol et al, 2021), and few studies have assessed effective strategies to enhance germination of desirable species in highly degraded soils.…”

“…However, inoculating with remnant NG soil is not practical for large‐scale restorations, as collection and transfer of enough native topsoil are highly destructive to the very ecosystems that we are trying to restore and protect. To address these challenges, improved methods to re‐establish soil microbiomes are currently being developed and there is much promise regarding the culturing of beneficial microbiota for landscape‐scale applications (Koziol et al, 2021; Vahter et al, 2020). For example, out‐planting “nurse” plants inoculated with local native soil or laboratory‐cultured AM fungi from the same local grassland sites significantly improved restoration establishment of late‐successional native grass and forb species (Koziol et al, 2021; Middleton & Bever, 2012), while minimizing the need for large quantities of native soil inocula to improve germination in large‐scale restorations.…”

“…To address these challenges, improved methods to re‐establish soil microbiomes are currently being developed and there is much promise regarding the culturing of beneficial microbiota for landscape‐scale applications (Koziol et al, 2021; Vahter et al, 2020). For example, out‐planting “nurse” plants inoculated with local native soil or laboratory‐cultured AM fungi from the same local grassland sites significantly improved restoration establishment of late‐successional native grass and forb species (Koziol et al, 2021; Middleton & Bever, 2012), while minimizing the need for large quantities of native soil inocula to improve germination in large‐scale restorations. As native soil inocula can spread as far as 2 m a year (Koziol & Bever, 2017), single plant inoculation and out‐planting may restore altered soil microbiomes across large areas.…”

“…Successful restoration of this site is exceedingly difficult as Bothriochloa spp. have been shown to exert direct and indirect effects on native soil, plant, and animal communities (Bhandari et al, 2018; Duell et al, 2022; Gabbard & Fowler, 2007; Hickman et al, 2006; Koziol et al, 2021), and soil legacy effects of herbicides used to control invasive plants have been known to limit native plant establishment (Cornish & Burgin, 2005; Lekberg et al, 2017). The specific objectives of our study are to (1) determine the effects of B. ischaemum and eradication control management on native plant germination, relative to germination in NG soil, and (2) assess if native soil inoculation improves germination success of 16 species of NG grasses and forbs, compared to germination in degraded soils without inoculation.…”

Arbuscular Mycorrhizal Fungi Taxa Show Variable Patterns of Micro-Scale Dispersal in Prairie Restorations

“…To compare the effects of pure AMF inocula to inocula containing the full suite of soil microbes, we collected and created a "whole soil" treatment for our experiment. We collected whole soil inocula at remnant prairies ranging from 0 to 25 km from each field site (Koziol et al, 2021). At remnant prairies, we collected 0.5 L for each of the five randomized samples of field soil to a depth of approximately 10 cm.…”