Mounting evidence suggests that plant–soil feedbacks (PSF) may determine plant community structure. However, we still have a poor understanding of how predictions from short‐term PSF experiments compare with outcomes of long‐term field experiments involving competing plants. We conducted a reciprocal greenhouse experiment to examine how the growth of prairie grass species depended on the soil communities cultured by conspecific or heterospecific plant species in the field. The source soil came from monocultures in a long‐term competition experiment (LTCE; Cedar Creek Ecosystem Science Reserve, MN, USA). Within the LTCE, six species of perennial prairie grasses were grown in monocultures or in eight pairwise competition plots for 12 years under conditions of low or high soil nitrogen availability. In six cases, one species clearly excluded the other; in two cases, the pair appeared to coexist. In year 15, we gathered soil from all 12 soil types (monocultures of six species by two nitrogen levels) and grew seedlings of all six species in each soil type for 7 weeks. Using biomass estimates from this greenhouse experiment, we predicted coexistence or competitive exclusion using pairwise PSFs, as derived by Bever and colleagues, and compared model predictions to observed outcomes within the LTCE. Pairwise PSFs among the species pairs ranged from negative, which is predicted to promote coexistence, to positive, which is predicted to promote competitive exclusion. However, these short‐term PSF predictions bore no systematic resemblance to the actual outcomes of competition observed in the LTCE. Other forces may have more strongly influenced the competitive interactions or critical assumptions that underlie the PSF predictions may not have been met. Importantly, the pairwise PSF score derived by Bever et al. is only valid when the two species exhibit an internal equilibrium, corresponding to the Lotka–Volterra competition outcomes of stable coexistence and founder control. Predicting the other two scenarios, competitive exclusion by either species irrespective of initial conditions, requires measuring biomass in uncultured soil, which is methodologically challenging. Subject to several caveats that we discuss, our results call into question whether long‐term competitive outcomes in the field can be predicted from the results of short‐term PSF experiments.
Plant‐soil feedback (PSF) theory provides a powerful framework for understanding plant dynamics by integrating growth assays into predictions of whether soil communities stabilise plant–plant interactions. However, we lack a comprehensive view of the likelihood of feedback‐driven coexistence, partly because of a failure to analyse pairwise PSF, the metric directly linked to plant species coexistence. Here, we determine the relative importance of plant evolutionary history, traits, and environmental factors for coexistence through PSF using a meta‐analysis of 1038 pairwise PSF measures. Consistent with eco‐evolutionary predictions, feedback is more likely to mediate coexistence for pairs of plant species (1) associating with similar guilds of mycorrhizal fungi, (2) of increasing phylogenetic distance, and (3) interacting with native microbes. We also found evidence for a primary role of pathogens in feedback‐mediated coexistence. By combining results over several independent studies, our results confirm that PSF may play a key role in plant species coexistence, species invasion, and the phylogenetic diversification of plant communities.
more » « less- NSF-PAR ID:
- 10461228
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Ecology Letters
- Volume:
- 22
- Issue:
- 8
- ISSN:
- 1461-023X
- Page Range / eLocation ID:
- p. 1274-1284
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Plants affect associated biotic and abiotic edaphic factors, with reciprocal feedbacks from soil characteristics affecting plants. These two‐way interactions between plants and soils are collectively known as plant–soil feedbacks (PSFs). The role of phylogenetic relatedness and evolutionary histories have recently emerged as a potential driver of PSFs, although the strength and direction of feedbacks among sympatric congeners are not well‐understood. We examined plant–soil feedback responses of
Asclepias syriaca , a common clonal milkweed species, with several sympatric congeners across a gradient of increasing phylogenetic distances (A. tuberosa ,A. viridis ,A. sullivantii , andA. verticillata , respectively). Plant–soil feedbacks were measured through productivity and colonization by arbuscular mycorrhizal (AM) fungi.Asclepias syriaca produced less biomass in soils conditioned by the most phylogenetically distant species (A. verticillata ), relative to conspecific‐conditioned soils. Similarly, arbuscular mycorrhizal (AM) fungal colonization ofA. syriaca roots was reduced when grown in soils conditioned byA. verticillata , compared with colonization in plants grown in soil conditioned by any of the other threeAsclepias species, indicating mycorrhizal associations are a potential mechanism of observed positive PSFs. This display of differences between the most phylogenetically distant, but not close or intermediate, paring(s) suggests a potential phylogenetic threshold, although other exogenous factors cannot be ruled out. Overall, these results highlight the potential role of phylogenetic distance in influencing positive PSFs through mutualists. The role of phylogenetic relatedness and evolutionary histories have recently emerged as a potential driver of plant–soil feedbacks (PSFs), although the strength and direction of feedbacks among sympatric congeners are not well‐understood. Congeneric, sympatric milkweeds typically generated positive PSFs in terms of productivity and AM fungal colonization, suggesting the low likelihood of coexistence among tested pairs, with a strength of feedback increasing as the phylogenetic distance increases. -
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Abstract The plant soil feedback (PSF) framework has been instrumental in understanding the impacts of soil microbes on plant fitness and species coexistence. PSFs develop when soil microbial communities are altered due to the identity and density of a particular plant species, which can then enhance or inhibit the local survival and growth of that plant species as well as different plant species. The recent extension of the PSF framework to aboveground microbiota, termed here as plant phyllosphere feedbacks (PPFs), can also help to determine the impact of aboveground microbes on plant fitness and species interactions. However, experimental tests of PPFs during early plant growth are nascent and the prevalence of PPFs across diverse plant species remains unknown. Additionally, it is unclear whether plant host characteristics, such as functional traits or phylogenetic distance, may help to predict the strength and direction of PPFs. To test for the prevalence of litter‐mediated PPFs, recently senesced plant litter from 10 native Asteraceae species spanning a range of life history strategies was used to inoculate seedlings of both conspecific and heterospecific species. We found that exposure to conspecific litter significantly reduced the growth of four species relative to exposure to heterospecific litter (i.e., significant negative PPFs), three species experienced marginally significant negative PPFs, and the PPF estimates for all 10 species were negative. However, neither plant functional traits, nor phylogenetic distance were predictive of litter feedbacks across plant species pairs, suggesting that other mechanisms or traits not measured may be driving conspecific negative PPFs. Our results indicate that negative, litter‐mediated PPFs are common among native Asteraceae species and that they may have substantial impacts on plant growth and plant species interactions, particularly during early plant growth.
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Abstract Plant–soil feedback (
PSF ) can structure plant communities, promoting coexistence (negativePSF ) or monodominance (positivePSF ). At higher trophic levels, predators can alter plant community structure by re‐allocating resources within habitats. When predator and plant species are spatially associated, predators may alter the outcome ofPSF . Here, I explore the influence of plant‐associated predators onPSF using a generalised cellular automaton model that tracks nutrients, plants, herbivores and predators. I explore key contingencies in plant–predator associations such as whether predators associate with live vs. senesced vegetation. Results indicate that plant‐associated predators shiftPSF to favour the host plant when predators colonise live vegetation, but the outcome ofPSF will depend upon plant dispersal distance when predators colonise dead vegetation. I apply the model to two spider‐associated invasive plants, finding that spider predators should shiftPSF dynamics in a way that inhibits invasion by one forest invader, but exacerbates invasion by another. -
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Abstract Plant–soil feedbacks (PSFs) drive plant community diversity via interactions between plants and soil microbes. However, we know little about how frequently PSFs affect plants at the seed stage, and the compositional shifts in fungi that accompany PSFs on germination.
We conducted a pairwise PSF experiment to test whether seed germination was differentially impacted by conspecific versus heterospecific soils for seven grassland species. We used metagenomics to characterize shifts in fungal community composition in soils conditioned by each plant species. To investigate whether changes in the abundance of certain fungal taxa were associated with multiple PSFs, we assigned taxonomy to soil fungi and identified putative pathogens that were significantly more abundant in soils conditioned by plant species that experienced negative or positive PSFs.
We observed negative, positive, and neutral PSFs on seed germination. Although conspecific and heterospecific soils for pairs with significant PSFs contained host‐specialized soil fungal communities, soils with specialized microbial communities did not always lead to PSFs. The identity of host‐specialized pathogens, that is, taxa uniquely present or significantly more abundant in soils conditioned by plant species experiencing negative PSFs, overlapped among plant species, while putative pathogens within a single host plant species differed depending on the identity of the heterospecific plant partner. Finally, the magnitude of feedback on germination was not related to the degree of fungal community differentiation between species pairs involved in negative PSFs.
Synthesis . Our findings reveal the potential importance of PSFs at the seed stage. Although plant species developed specialized fungal communities in rhizosphere soil, pathogens were not strictly host‐specific and varied not just between plant species, but according to the identity of plant partner. These results illustrate the complexity of microbe‐mediated interactions between plants at different life stages that next‐generation sequencing can begin to unravel.
