Aboveground Competition and Herbivory Overpower Plant-Soil Feedback Contributions to Succession in a Remediated Grassland

Abstract

Plant-soil feedback (PSF) can provide a driving force during ecological succession by altering soil properties in ways that benefit or disadvantage other species in the successional sequence. Succession may be inevitable in disturbed sites remediated by planting early successional species, but information on PSF in such settings is lacking. We investigated whether gray birch (Betula populifolia), a native species but strong invader, alters succession from grassland to deciduous forest at a site contaminated with zinc, lead, and cadmium. We investigated PSF within the context of competition, herbivory, and soil contaminants, and evaluated whether gray birch, as a high metal accumulator, engages in elemental allelopathy, poisoning other species through its metal-contaminated leaf litter. We assessed the effects of gray birch on neighboring plant community structure, soil chemistry, fungal root symbionts, and the germination, growth, and herbivory of seedlings of black oak (Quercus velutina) and sugar maple (Acer saccharum), two tree species expected to follow gray birch in succession. Gray birch was associated with increased diversity in its neighborhood grassland community, increased herbivory on black oak seedlings, and influenced colonization by fungal root symbionts in both species. Seedling biomass was correlated with colonization by ectomycorrhizal fungi in black oak, but not with arbuscular mycorrhizal or dark septate fungal colonization in sugar maple. Gray birch had no effect on maple seedling performance or soil chemistry, and a small effect on black oak performance in the absence of aboveground competition. We found little evidence consistent with elemental allelopathy. Black oak and sugar maple seedlings responded more strongly to variation in soil nutrients than soil heavy metals, and they maintained leaf metal concentration profiles markedly different from those in their soils. We conclude that gray birch alters its environment in ways that could promote establishment and succession of woody species, potentially favoring those that are ectomycorrhizal, but most effects of PSF are overpowered by aboveground competition, herbivory, and/or existing abiotic soil factors. This study well illustrates why the potential for PSF to affect plant performance Dietterich et al. Plant-Soil Feedback and Succession in the Field and community structure must be examined within the context of other ecological processes. Such a broad understanding can inform decisions made in the remediation and management of disturbed sites, and our understanding of plant succession and coexistence in general.

Plant-soil feedback: incorporating untested influential drivers and reconciling terminology

“…It has been shown that herbivory by polyphagous caterpillars can alter soil fungal community composition possibly via changes to plant exudation patterns (Bezemer et al 2013), and that this modifies PSF dynamics in response plants (Kostenko et al 2012). Several studies suggest that herbivory may mask or alleviate PSF (Bennett et al 2020;Dietterich et al 2019;Heinze and Joshi 2018), and that the importance of PSF for plant species increases along a gradient of diminishing herbivory (Heinze et al 2019). In addition, a large-scale PSF study using 20 herbaceous plant species demonstrated that the individual PSFs experienced by plants exposed to herbivores during the conditioning phase were better predictors of plant landscape abundance and diversity than those of plants that were shielded from herbivory (Heinze et al 2020).…”

“…Types of secondary succession may vary depending on the ecosystem age or form(s) of disturbance. This can lead to disparities in strength and/or direction of PSF effects (Kardol et al 2022;van de Voorde et al 2011) and interactions with other factors (e.g., herbivory, water or nutrient availability, climate) that may override the feedback effects (de la Peña et al 2016;Dietterich et al 2019;Heinze and Joshi 2018;Yelenik and Levine 2011).…”

Resistance against tree encroachment is driven by richness and identity of herbaceous resident species

“…Betula is a shade‐intolerant, fast‐growing ectomycorrhizal species with small‐sized seeds (Northup et al., 1995; Hewitt, 1998; Lindahl & Tunlid, 2015). Both species frequently establish in unmanaged grasslands and old fields (Wagner et al., 2014; Dietterich et al., 2019). They also frequently encroach under electrical powerline rights‐of‐way in northeastern North America, where they are considered a nuisance requiring frequent control (Mercier et al., 2001; Wagner et al., 2014; Boivin et al., 2018).…”