The temporal development of plant-soil feedback is contingent on competition and nutrient availability contexts.

Summary Plant–soil feedbacks contribute to species invasions, the maintenance of biodiversity and climate change impacts on terrestrial ecosystems. Despite their far‐reaching importance, we lack a general understanding of the ecological and evolutionary determinants of plant–soil feedbacks. We conducted a large‐scale plant–soil feedback experiment using 49 co‐occurring plant species from southern Ontario, Canada, representing a wide phylogenetic range. We tested whether the effects of soil conditioning vary among these species and whether different focal species respond similarly to the same soil conditioning. Next, we investigated whether plant traits and soil feedbacks depend on phylogenetic similarity and which plant traits affect plant–soil feedbacks between pairs of plant species. Finally, we used our experimental results to test whether soil feedbacks affect co‐occurrence of species in the field. We found evidence of both strong positive and negative soil feedbacks between pairs of plant species. Our soil‐conditioning treatment explained nearly 20% of the variation in focal species performance. Phylogenetic relatedness and phenotypic similarity between plant species were unrelated to the strength of their soil feedback. However, numerous plant traits of the conditioning species influenced the strength of soil feedbacks on focal species, including specific leaf area and total above‐ground productivity. Trait differences between species were also predictive of plant–soil feedbacks, though for some pairs of species, increased trait differences were associated with positive plant–soil feedbacks and for others, trait differences were associated with negative plant–soil feedbacks. Plant species co‐occurrence in the field was related to their experimentally determined soil feedbacks but only for particular plant species. Synthesis. Our results illustrate how evolutionary history and phenotypic variation shape plant–soil feedbacks and highlight the need for trait‐based studies. Due to the unique evolutionary history of individual traits and the variability in their importance across all possible interacting species, we show that indices of overall phenotypic and phylogenetic relatedness are poor predictors of plant–soil feedbacks at large phylogenetic scales. We conclude that a detailed trait‐based approach can be used to predict plant–soil feedbacks, and laboratory measures of soil feedbacks can explain patterns of co‐occurrence in nature.

Most plant‒soil feedback studies have been conducted on the mechanism by which soil directly influences plant growth performance and mostly in indoor pot experiments; however, it is unclear how plant‒soil feedback is influenced by plant, soil and microbial diversity in grassland ecosystems in alpine meadows with high plant diversity. In this study, plant‒soil feedback patterns were investigated by analyzing plant, soil and microbial characteristics across seven gradients in the time series from light degradation to 10-years of recovery, classified into three categories: ecosystem multifunctionality, biotic and abiotic factors, and comparing the strength and magnitude of plant‒soil feedback in alpine meadows of degradation stages and years of recovery. The results showed that the plant-soil feedback relationships in alpine meadows differed significantly in three aspects: ecosystem multifunctionality, biotic and abiotic factors in the degradation stage and recovery years, and under the degradation gradient, ecosystem multifunctionality decreased from 0.34 to −0.99 with the deepening of degradation, biotic factors increased from −0.17 to 0.09, and abiotic factors increased from −0.17 to 0.15, while in the recovery gradient, ecosystem multifunctionality showed a trend of increasing and then decreasing with increasing recovery years, while biotic and abiotic factors showed fluctuating changes. The plant-soil feedback index indicated that the strength and direction of plant-soil interactions during degradation and recovery were different, and the positive feedback effect was 0.34 and 0.38 in the early stage of degradation and recovery, respectively, which were greater than the negative feedback effect. With the deepening of degradation, the negative feedback effect became more and more obvious, and at the stage of extreme degradation, the negative feedback effect reached −0.99, which was much larger than the positive feedback effect. However, with the increase of the recovery years, the positive feedback effect gradually weakened, and finally all of them were negative feedback effects at 10-years of recovery. This study provides a scientific basis for understanding plant-soil feedback in alpine meadow ecosystems and indicates the direction for the next scientific recovery of alpine meadows.

Plants interact with a variety of soil biota; the accumulation of which can affect their growth and that of subsequent plants. This plant–soil feedback (PSF) can both positively and negatively affect plant populations. Diverse plant communities should dilute pathogens and increase beneficial soil biota, which can mitigate negative PSF. Plant dominance, conversely, should result in reduced microbial diversity and increased pathogens or mutualists of the dominant plant, enhancing negative or positive PSF. Genetic diversity within the dominant species may dilute PSF, yet it is unclear whether species and genetic diversity can have additive effects. Using field‐conditioned soils from Medicago sativa production systems varying in dominance and species diversity, we inoculated multiple plant species and Medicago cultivars to assess effects on PSF. In the field, we measured multiple aspects of the biotic and abiotic environment, including sequencing bacteria, fungi, arbuscular mycorrhizal fungi and oomycetes. Using structural equation modelling, we linked the dominance and diversity of the plant community to intraspecific and interspecific (community‐wide) means and variances in PSF via changes in microbiome community composition and diversity. Intraspecific PSF was more negative and variable as Medicago dominance increased, whereas the mean and variance in interspecific PSF were largely unlinked to plant composition. While the microbiome was strongly linked to both the mean and variance of intra‐ and interspecific PSF, only the oomycete community had similar effects within and among species, suggesting they are important generalist pathogens and drivers of plant population and community dynamics. Nonetheless, each microbiome component was linked to the mean PSF of either the community or Medicago. The diversity of the eukaryotic microbiome, however, was more important for determining variability in PSF within and among species. Synthesis. Plant dominance had stronger effects on microbiome assembly and plant–soil feedback (PSF) than plant diversity. Although plant diversity did not reduce negative PSF, independent variation in PSF within and among species suggests additive benefits of genetic and species diversity for dilution of plant responses to pathogens. Understanding this variation, however, requires quantifying microbiome components beyond bacteria and fungi.

Mounting evidence suggests that reciprocal interactions between plants and the soil microbiota can be a primary force that generates key macroscopic patterns of plant communities (coexistence, dominance, and succession) in forest ecosystems. The aim of this article is to review empirical and theoretical perspectives of plant–soil feedback research in the context of forest community ecology. I first use a simple theoretical model to get insights into an array of the dynamics generated by plant–soil feedback: negative plant–soil feedback maintains plant species diversity and reduces plant growth, while positive plant–soil feedback drives plant growth of certain species and hence their dominance. I then describe how ecologists have unveiled the enormously complex plant‐microbiota interaction (i.e., the soil conditioning experiment) and review the linkage of plant–soil feedback with three key plant community patterns: (i) dominance, (ii) spatial structure and (iii) succession. I highlight one belowground plant trait (mycorrhizal type) that can mediate these linkages: arbuscular mycorrhizal species tend to exhibit negative plant–soil feedback while ectomycorrhizal species tend to exhibit positive plant–soil feedback. Although mycorrhizal plant–soil feedback potentially explains the patterns of tree diversity from local to global scales, many questions remain. Future studies should expand plant–soil feedback theory to incorporate numerous other feedback mechanisms and test how mycorrhizal types mediate the net feedback effects that could propagate to shape large‐scale forest structures and dynamics.

Negative plant–soil feedbacks can impair seedling survival near conspecific trees and may enhance forest diversity. However, the reciprocal aspect of this relationship, the influence of tree diversity on the strengths of plant–soil feedbacks is unknown. We examined whether tree diversity can affect plant–soil feedbacks of two common temperate tree species, beech (Fagus sylvatica) and sessile oak (Quercus petraea). Soils were collected from adjacent to beech and oak trees growing in a manipulative tree diversity field experiment and used as inocula in a greenhouse experiment to determine whether increasing tree diversity could moderate the strengths of plant–soil feedbacks. We also compared plant–soil feedback responses between Q. petraea and F. sylvatica to test the hypothesis that stronger negative feedbacks contribute to the relative rarity of Q. petraea. Negative plant–soil feedbacks on seedling emergence were observed for both tree species. Emergence increased with increasing distance of the soil inocula from established trees in the field, but only for inocula taken from the low‐diversity treatment (monocultures) and irrespective of the inoculum source (i.e., from conspecific vs. heterospecific trees). In contrast, tree diversity had no influence on the biomass responses of seedlings for either tree species. Quercus petraea seedlings experienced negative plant–soil feedbacks in their biomass responses which cascaded up to higher trophic levels, i.e., leaf pathogen infection. Fagus sylvatica biomass responses suggested positive plant–soil feedbacks, supporting the hypothesis that the abundance of this species is less limited by interactions with natural enemies. Our results suggest that distance‐dependent seedling emergence in temperate forests may depend on the diversity of tree communities and that plant–soil feedbacks may cascade up to higher trophic levels and change with the life history stage of the seedlings involved. An increased focus on the surrounding communities would help to judge the importance and context‐dependency of plant–soil feedbacks as a mechanism for stabilizing forest diversity.

Negative plant–soil feedback (PSF) has been widely considered to be a primary mechanism maintaining plant diversity. Previous studies have shown that rare species suffer stronger negative conspecific PSF than common species, but it remains unclear how rare species persist if they are more strongly self‐limited. Here, we used shade‐house and field experiments to test soil feedback effects of phylogenetically related species on seedling growth, with seven species of contrasting local abundance, in a subtropical forest, China. We quantified the PSF of conspecifics and heterospecifics and assessed the phylogenetic dependence of the feedback. Both experiments showed that although rare species suffered strong negative PSF in soils of conspecifics or phylogenetically close heterospecifics, no such feedback was found in the soils of phylogenetically distant heterospecifics. In contrast, common species had no or weak negative conspecific PSF but strong heterospecific soil PSF. Synthesis. The variation in the phylogenetically dependent PSF among rare and common species evidenced in this study ensures that rare species would grow well in the neighbourhood of phylogenetically distant heterospecifics but do poorly under their own or close relatives, while common species perform relatively well in their own neighbourhood but poorly in other's neighbourhood. This phylogenetically dependent PSF facilitates the rare–common species coexistence in communities.

Increasing evidence suggest that plant–soil interactions play an essential role in plant community assembly processes. Empirical investigations show that plant species abundance in the field is often related to plant–soil biota interactions; however, the direction of these relations have yielded inconsistent results. We combined unique 31‐year long field data on species abundances from a species‐rich mountain meadow with single time point plant–soil feedback greenhouse experiments of 24 co‐occurring plant species. We tested whether these relations were dynamic in time, whether coupled increases and decreases in abundance between years were related to plant–soil feedback and whether these changes were underlain by years in which manuring was applied. The prevailingly negative relationship between plant–soil feedback and plant relative abundance in the field was significantly time‐dependent, which may reconcile the contrasting results in literature. Furthermore, significantly coupled oscillations appeared between species relative abundance changes and plant–soil feedback, which were likely moderated by years in which manuring was applied. Our results are consistent with the notion that the more abundant species are stabilised by negative plant–soil feedback, and the less abundant species co‐vary with the fluctuations of these more competitive species. Synthesis . Our results project plant–soil feedback as an important regulatory mechanism in plant communities, operating in conjunction with species' competitive ability and soil nutrient availability. We suggest that negative feedback is particularly prominent in more abundant plant species that profit from more readily available soil nutrients than less abundant species with positive feedback. Negative plant–soil feedback may thus prevent more abundant plant species from out‐competing less abundant plant species, facilitating stable species co‐existence.

Plant-soil feedbacks (PSFs), soil-mediated plant effects on conspecific or heterospecific successors, are a major driver of vegetation development. It has been proposed that specialist plant antagonists drive differences in PSF responses between conspecific and heterospecific plants, whereas contributions of generalist plant antagonists to PSFs remain understudied. Here we examined PSFs among nine annual and nine perennial grassland species to test whether poorly defended annuals accumulate generalist-dominated plant antagonist communities, causing equally negative PSFs on conspecific and heterospecific annuals, whereas well-defended perennial species accumulate specialist-dominated antagonist communities, predominantly causing negative conspecific PSFs. Annuals exhibited more negative PSFs than perennials, corresponding to differences in root-tissue investments, but this was independent of conditioning plant group. Overall, conspecific and heterospecific PSFs did not differ. Instead, conspecific and heterospecific PSF responses in individual species' soils were correlated. Soil fungal communities were generalist dominated but could not robustly explain PSF variation. Our study nevertheless suggests an important role for host generalists as drivers of PSFs.

Interactions among plant species and their soil biota drive plant-soil feedbacks (PSFs) that play a major role in the dynamics and diversity of plant communities. Among the different components of the soil community, pathogens are considered to be the main drivers of negative PSFs. Despite this, the number of studies that have experimentally quantified the contribution of soil pathogens to PSFs remains considerably low. Here we conducted a greenhouse experiment with oomycete-specific fungicide to quantify the contribution of soil pathogens, and particularly oomycete pathogens, to individual and pairwise PSFs in forest communities. We used as a case study Mediterranean mixed forests dominated by Quercus suber and invaded by the oomycete pathogen Phytophthora cinnamomi. The fungicide treatment was crossed with a competition treatment to explore how conspecific neighbors might modify pathogen effects. To place the results of the experiment in a wider context, we also conducted a systematic review of published papers that explicitly used fungicide to explore the role of pathogens in PSF experiments. Our experimental results showed that oomycete pathogens were the main drivers of individual PSFs in the study forests. Oomycete effects varied among tree species according to their susceptibility to P.cinnamomi, driving negative PSFs in the highly susceptible Q.suber but not in the coexistent Olea europaea. Oomycete-driven PSFs were not modified by intraspecific competition. Oomycete pathogens were also major contributors to negative pairwise PSFs assumed to promote species coexistence. Results from the systematic review supported the novelty of our experimental results, since only three studies had previously used oomycete-specific fungicide in a PSF context and none in systems invaded by exotic oomycetes. Overall, our results provide novel evidence of oomycete pathogens (including the exotic P.cinnamomi) as fundamental drivers of negative individual and pairwise PSFs with implications for species coexistence in invaded communities. Although in the short-term invasive pathogens might contribute to species coexistence by causing self-limitation in dominant species, strong inter-specific variation in self-limitation might undermine coexistence in the long-term. Because of the increasing number of exotic oomycetes worldwide, further attention should be given to oomycetes as drivers of PSFs in plant communities.

Plant-soil feedback (PSF) occurs when plants change the biota and physicochemical properties of the soil, and these changes affect future survival or growth of plants. PSF depends on several factors such as plant functional attributes (e.g., life cycle or photosynthetic metabolism) and the environment. PSF often turn positive under dry conditions because soil biota confers drought tolerance. Conspecifics and close relatives share pathogens and consume similar resources, exerting negative PSF on each other. These ideas have mostly been tested under controlled conditions, while field studies remain scarce. To reevaluate these findings in nature, we analyzed plant-soil feedbacks over a drought-stress gradient in a phosphorus-limited semiarid grassland. We planted seedlings of 17 species in plots where community composition had been monitored for six years. To determine PSF intensity, we measured how seedling longevity was affected by previous occupancy of conspecifics and heterospecifics. The previous occupancy-survival relationship (OSR) was used as a proxy for PSF. Evidence for OSRs was found in one-third of the species pairs, with inconclusive evidence for the rest suggesting weak feedbacks. This is in line with the expectation that PSFs in the field are weaker than under controlled conditions. As expected, positive PSFs were more frequent as drought stress increased. The strongest OSRs were caused in dry plots by C4 perennial grasses, which had very positive OSRs on several C3 annual forbs, but negative effects on each other. Well-documented differences between these two functional groups may explain this result: C3 plants are more sensitive to drought, and thus may be favored by tolerance-conferring microbiota; in contrast, water-efficient C4 perennial grasses compete for phosphorus strongly, perhaps driving strong negative PSFs between them. Finally, close relatives had more negative OSRs on each other than on distant relatives as expected, although only in dry plots. This pattern was mostly due to the negative effects of closely related C4 grasses under dry conditions, and their positive effects on distantly related dicots. Our results highlight the importance of plant traits and of the environmental context in determining the direction and strength of PSFs under field conditions.

Background and aimsThe concept of plant-soil feedback is increasingly used to explain plant community assembly processes. Soil nutrient availability can be expected to play a critical role on these processes. However, little is known about the effects of nutrient availability on feedback direction and strength.MethodsA plant-soil feedback experiment was performed with the grasses Anthoxanthum odoratum and Festuca rubra, and the forbs Leontodon hispidus and Plantago lanceolata, on soil with either low or high nutrient availability. Additionally, we tested if plant-soil feedback of the two forbs under these conditions changed by inoculation of the soil with spores of an arbuscular mycorrhizal fungus.ResultsIncreased nutrient availability neutralised plant-soil feedback based on shoot biomass independent of its negative or positive direction, whereas the effects on root biomass were either not altered or turned negative. Mycorrhizal fungi spore addition decreased negative feedback and increased positive feedback.ConclusionsOur results suggest that negative plant-soil feedback on low nutrient soil can be overcome with nutrient addition, and that positive soil biota associations on low nutrient soil may become superfluous with nutrient increase. We hypothesize that species-specific, microbial mediated plant community assembly processes occur in low rather than high nutrient environments.

Plant–soil feedbacks (PSF) play a central role in determining forest community dynamics, with trees associated with arbuscular mycorrhizal fungi (AMF) often experiencing negative PSFs, while those associated with ectomycorrhizal fungi (EMF) experience positive PSFs. PSFs are driven by the difference between seedling performance in both conspecific and heterospecific soil, and thus the mycorrhizal match or mismatch of the heterospecific soil to the focal seedling could drive PSFs. Furthermore, functional traits and light environments could influence seedling responses. To understand how mycorrhizal type and seedling functional traits influence PSFs, we conducted a greenhouse experiment with five temperate tree species (3 AM, 2 EM) in soils from six adult tree species (3 AM, 3 EM). Seedlings were grown for 12 weeks under three light levels. Mycorrhizal colonization and defence/recovery traits (phenolics, lignin, non‐structural carbohydrates) were assessed at 3 weeks, and survival was measured over 12 weeks. AM seedlings generally experienced negative PSFs, with lower survival in AM‐cultured soils, while EM seedlings had positive PSFs and higher survival in EM soils. However, negative PSFs in AM trees and positive PSFs in EM trees occurred only when the heterospecific tree culturing the soil had a mismatched mycorrhizal type relative to the focal seedling PSFs occurred under all light levels, but their magnitude was strongest at low light, where AM seedlings showed the most negative PSFs and EM seedlings the most positive. Mycorrhizal colonization and functional trait values increased under high light and were often elevated in conspecific soils (with the exception of non‐structural carbohydrates). These enhancements in traits tended to neutralize PSFs in both AM and EM seedlings. Mycorrhizal type match/mismatches between adults and seedlings influenced seedling survivorship and PSFs, likely shaping seedling recruitment patterns and long‐term forest composition, diversity, and resilience. Read the free Plain Language Summary for this article on the Journal blog.

BackgroundStudying plant–soil feedback (PSF) is of great significance to understanding plant community dynamics.AimsWe aimed to determine the temporal variation in PSF at different stages of grassland community succession and the influencing factors.MethodsWe conducted a 3‐year experiment to examine how PSF changes during different successional stages (early‐, mid‐ and late‐). Setaria viridis, Stipa bungeana and Bothriochloa ischaemum were selected as representative and dominant early‐, mid‐ and late‐species, respectively, in the semiarid grassland of the Loess Plateau, China.ResultsThe temporal variation in the PSF pattern was found to be species‐specific. Negative and neutral PSF patterns in early‐ and mid‐species, respectively, were found within the 3‐year growth periods. A positive PSF pattern for late‐species was found in the second growth period, and a negative PSF pattern was found in the third growth period. The shoot biomass of early‐species was overall positively correlated with soil nutrients and enzyme activity in the soil of the three species. However, the shoot biomass of late‐species was overall negatively correlated with soil nutrients and enzyme activity in early‐species soil.ConclusionsWe suggest that the negative PSF of early‐species over the growing period explains why the advantage of these early colonizers is temporary. In contrast, the positive PSF of late‐species likely contributes to their successful colonization and the entire community succession process. Our results indicated that PSF plays an important role in the progression of plant community succession.

Plants influence numerous soil biotic factors that can alter the performance of later growing plants-defined as plant-soil feedback (PSF). Here, we investigate whether PSF effects are linked with the temporal changes in root exudate diversity and the rhizosphere microbiome of two common grassland species (Holcus lanatus and Jacobaea vulgaris). Both plant species were grown separately establishing conspecific and heterospecific soils. In the feedback phase, we determined plant biomass, measured root exudate composition, and characterised rhizosphere microbial communities weekly (eight time points). Over time, we found a strong negative conspecific PSF on J. vulgaris in its early growth phase which changed into a neutral PSF, whereas H. lanatus exhibited a more persistent negative PSF. Root exudate diversity increased considerably over time for both plant species. Rhizosphere microbial communities were distinct in conspecific and heterospecific soils and showed strong temporal patterns. Bacterial communities converged over time. Using path models, PSF effects could be linked to the temporal dynamics of root exudate diversity, whereby shifts in rhizosphere microbial diversity contributed to temporal variation in PSF to a lesser extent. Our results highlight the importance of root exudates and rhizosphere microbial communities in driving temporal changes in the strength of PSF effects.

Plant–soil feedbacks (PSFs) are key drivers of plant community dynamics. However, our understanding of the factors moderating PSFs remains limited. We examined how plant phylogenetic relatedness and functional traits determine PSFs via their influence on rhizosphere fungal communities, especially arbuscular mycorrhizal fungi (AMF) and fungal pathotrophs. We conducted a glasshouse PSF experiment using 21 temperate grassland plant species, where each focal species was exposed to soils conditioned by heterospecific plants of increasing phylogenetic dissimilarity. We tested whether phylogenetic distance between plant species, functional traits or the degree to which species associate with AMF or fungal pathotrophs, explained the magnitude and direction of PSF responses. None of the measured plant traits explained PSFs, although the relative abundance of AMF was weakly and positively related to PSFs. Across all plant species, phylogenetic relatedness did not explain PSFs. However, species‐specific effects of phylogenetic relatedness on the outcome of PSFs were detected. In particular, significant relationships with phylogenetic relatedness were observed only for species characterised by the highest rhizosphere relative abundance of AMF or fungal pathotrophs. For Centaurea nigra and Vicia cracca (both high AMF abundance) and Anthoxanthum odoratum (high pathotroph abundance), we found that PSF became more positive with increased phylogenetic distance between focal and conditioning species, showing a shift towards increased performance in conspecific than heterospecific soils. Meanwhile, as phylogenetic dissimilarity between Poa trivialis (high pathotroph abundance) and the soil conditioning species increased, more negative PSFs were observed, indicating improved performance in soils conditioned by increasingly distant heterospecific species. Synthesis. Our results suggest that plant traits and phylogenetic relatedness are poor predictors of plant–soil feedbacks (PSFs) among temperate grassland plant species. Hence, despite known effects of these factors in shaping rhizosphere microbial communities, the way plant species respond to these microbial communities is not related to the same characteristics. The occurrence of significant relationships between phylogenetic distance and PSFs in species with high relative abundances of mycorrhizal or pathogenic fungi suggests that the tendency to accumulate fungal mutualists or pathotrophs may be an important moderator of the relationship between plant phylogenetic relatedness and the magnitude and direction of PSFs.