Sensitivity to AMF species is greater in late‐successional than early‐successional native or nonnative grassland plants

Abstract

Sensitivity of plant species to individual arbuscular mycorrhizal (AM) fungal species is of primary importance to understanding the role of AM fungal diversity and composition in plant ecology. Currently, we do not have a predictive framework for understanding which plant species are sensitive to different AM fungal species. In two greenhouse studies, we tested for differences in plant sensitivity to different AM fungal species and mycorrhizal responsiveness across 17 grassland plant species of North America that varied in successional stage, native status, and plant family by growing plants with different AM fungal treatments including eight single AM fungal isolates, diverse mixtures of AM fungi, and non-inoculated controls. We found that late successional grassland plant species were highly responsive to AM fungi and exhibited stronger sensitivity in their response to individual AM fungal taxa compared to nonnative or early successional native grassland plant species. We confirmed these results using a meta-analysis that included 13 experiments, 37 plant species, and 40 fungal isolates (from nine publications and two greenhouse experiments presented herein). Mycorrhizal responsiveness and sensitivity of response (i.e., variation in plant biomass response to different AM fungal taxa) did not differ by the source of fungal inocula (i.e., local or not local) or plant family. Sensitivity of plant response to AM fungal species was consistently correlated with the average mycorrhizal response of that plant species. This study identifies that AM fungal identity is more important to the growth of late successional plant species than early successional or nonnative plant species, thereby predicting that AM fungal composition will be more important to plant community dynamics in late successional communities than in early successional or invaded plant communities.

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

“…Additionally, we saw that the native whole‐soil treatment had either no effect or a positive effect on plant performance, which suggests that soil mutualists were an important component of the whole prairie soil. The strong positive effects of native AM fungi on annual species in our work are in contrast to other studies that show early successional species to have relatively little response to AM fungal additions or sensitivity to AM fungal composition (Cheeke et al., 2019; Koziol & Bever, 2015, 2016). Major positive effects of native AM fungal additions (or native whole‐soil additions) have been primarily found in studies of longer living perennial plants (House & Bever, 2019; Koziol & Bever, 2017; Koziol et al., 2018; Middleton & Bever, 2012; Middleton et al., 2015).…”

“…Similarly, Chamaecrista is found primarily in disturbed areas, including recently burned or animal‐disturbed parts of prairies and roadside habitat (Galloway & Fenster, 2000). Native AM fungi are less likely to benefit the growth of plant species with low coefficients of conservatism (Bauer, Koziol, & Bever, 2018; Koziol & Bever, 2015); such plant species are also less sensitive to AM fungal identity (Cheeke et al., 2019; Koziol & Bever, 2016).…”

“…AM fungal species are, however, not always mutualists. The degree to which a particular plant–AM fungal interaction is mutualistic or pathogenic depends on the plant species, AM fungal species, and abiotic factors such as soil nutrient and water availability (Cheeke, Zheng, Koziol, Gurholt, & Bever, 2019; Hoeksema et al., 2018; Johnson, Graham, & Smith, 1997; Jones & Smith, 2004). Most work on plant–AM fungal interactions has focused on agronomic plants; there have been fewer studies of the effects of AM fungi on demography of wild plants.…”

“…Notably, work by Koide and coauthors has demonstrated that the presence of AM fungi can have large positive effects on plant reproduction, seed size, and germination of Abutilon theoprasti (Koide & Dickie, 2002; Stanley, Koide, & Shumway, 1993). While the identity of AM fungal species has been shown to have large effects on plant growth (Cheeke et al., 2019; Koziol & Bever, 2016), less is known on the importance of AM fungal species composition on elements of plant demography.…”

“…Reintroduction of these native prairie soil microbes, through either inoculation with AM fungi or whole‐soil additions, can be important in establishing prairie plants in restoration sites in degraded postagricultural soils (Koziol et al., 2018; Lubin, Schultz, Bever, & Alexander, 2019; Middleton & Bever, 2012). Late successional native plant species have been found to be sensitive to AM fungal species composition and particularly benefit from reintroduction of native AM fungi (Cheeke et al., 2019; House & Bever, 2019; Koziol & Bever, 2016, 2017; Middleton et al., 2015).…”