The role of plant-soil feedback in long-term species coexistence cannot be predicted from its effects on plant performance.

BACKGROUND: Despite many studies on the importance of competition and plants' associations with mutualists and pathogens on plant performance and community organization, the joint effects of these two factors remain largely unexplored. Even less is known about how these joint effects vary through a plant's life in different environmental conditions and how they contribute to the long-term coexistence of species. METHODS: We investigated the role of plant-soil feedback (PSF) in intra- and interspecific competition, using two co-occurring dry grassland species as models. A two-phase PSF experiment was used. In the first phase, soil was conditioned by the two plant species. In the second, we assessed the effect of soil conditioning, competition and drought stress on seedling establishment, plant growth in the first and second vegetation season, and fruit production. We also estimated effects of different treatments on overall population growth rates and predicted the species' potential coexistence. RESULTS: Soil conditioning played a more important role in the early stages of the plants' life (seedling establishment and early growth) than competition. Specifically, we found strong negative intraspecific PSF for biomass production in the first year in both species. Although the effects of soil conditioning persisted in later stages of plant's life, competition and drought stress became more important. Surprisingly, models predicting species coexistence contrasted with the effects on individual life stages, showing that our model species benefit from their self-conditioned soil in the long run. CONCLUSIONS: We provide evidence that the effects of PSF vary through plants' life stages. Our study suggests that we cannot easily predict the effects of soil conditioning on long-term coexistence of species using data only on performance at a single time as commonly done in PSF studies. We also show the importance of using as realistic environmental conditions as possible (such as drought stress experienced in dry grasslands) to draw reasonable conclusions on species coexistence.

Quasi-steady uptake and bacterial community assembly in a mathematical model of soil-phosphorus mobility.

We mathematically model the uptake of phosphorus by a soil community consisting of a plant and two bacterial groups: copiotrophs and oligotrophs. Four equilibrium states emerge, one for each of the species monopolising the resource and dominating the community and one with coexistence of all species. We show that the dynamics are controlled by the ratio of chemical adsorption to bacterial death permitting either oscillatory states or quasi-steady uptake. We show how a steady state can emerge which has soil and plant nutrient content unresponsive to increased fertilization. However, the additional fertilization supports the copiotrophs leading to community reassembly. Our results demonstrate the importance of time-series measurements in nutrient uptake experiments.

Co-occurring Fungal Functional Groups Respond Differently to Tree Neighborhoods and Soil Properties Across Three Tropical Rainforests in Panama.

Abiotic and biotic drivers of co-occurring fungal functional guilds across regional-scale environmental gradients remain poorly understood. We characterized fungal communities using Illumina sequencing from soil cores collected across three Neotropical rainforests in Panama that vary in soil properties and plant community composition. We classified each fungal OTU into different functional guilds, namely plant pathogens, saprotrophs, arbuscular mycorrhizal (AM), or ectomycorrhizal (ECM). We measured soil properties and nutrients within each core and determined the tree community composition and richness around each sampling core. Canonical correspondence analyses showed that soil pH and moisture were shared potential drivers of fungal communities for all guilds. However, partial the Mantel tests showed different strength of responses of fungal guilds to composition of trees and soils. Plant pathogens and saprotrophs were more strongly correlated with soil properties than with tree composition; ECM fungi showed a stronger correlation with tree composition than with soil properties; and AM fungi were correlated with soil properties, but not with trees. In conclusion, we show that co-occurring fungal guilds respond differently to abiotic and biotic environmental factors, depending on their ecological function. This highlights the joint role that abiotic and biotic factors play in determining composition of fungal communities, including those associated with plant hosts.

Beyond the rootzone: Unveiling soil property and biota gradients around plants.

Although the effects of plants on soil properties are well known, the effects of distance from plant roots to root-free soil on soil properties and associated soil organisms are much less studied. Previous research on the effects of distance from a plant explored specific soil organisms and properties, however, comparative studies across a wide range of plant-associated organisms and multiple model systems are lacking. We conducted a controlled greenhouse experiment using soil from two contrasting habitats. Within each soil type, we cultivated two plant species, individually and in combination, studying soil organisms and properties in the root centre, the root periphery, and the root-free zones. We showed that the distance from the cultivated plant (representing decreasing amount of plant roots) had a significant impact on the abiotic properties of the soil (pH and available P and N) and also on the composition of the fungal, bacterial, and nematode communities. The specific patterns, however, did not always match our expectations. For example, there was no significant relationship between the abundance of fungal pathogens and the distance from the cultivated plant compared to a strong decrease in the abundance of arbuscular mycorrhizal fungi. Changes in soil chemistry along the distance from the cultivated plant were probably one of the important drivers that affected bacterial communities. The abundance of nematodes also decreased with distance from the cultivated plant, and the rate of their responses reflected the distribution of their food sources. The patterns of soil changes along the gradient from plant to root-free soil were largely similar in two contrasting soil types and four plant species or their mixtures. This suggests that our results can be generalised to other systems and contribute to a better understanding of the mechanisms of soil legacy formation.

Host-specific soil microbes contribute to habitat restriction of closely related oaks (Quercus spp.).

Habitat divergence among close relatives is a common phenomenon. Studying the mechanisms behind habitat divergence is fundamental to understanding niche partitioning, species diversification, and other evolutionary processes. Recent studies found that soil microbes regulate the abundance and diversity of plant species. However, it remains unclear whether soil microbes can affect the habitat distributions of plants and drive habitat divergence. To fill in this knowledge gap, we investigated whether soil microbes might restrict habitat distributions of closely related oaks (Quercus spp.) in eastern North America. We performed a soil inoculum experiment using two pairs of sister species (i.e., the most closely related species) that show habitat divergence: Quercus alba (local species) vs. Q. michauxii (foreign), and Q. shumardii (local) vs. Q. acerifolia (foreign). To test whether host-specific soil microbes are responsible for habitat restriction, we investigated the impact of local sister live soil (containing soil microbes associated with local sister species) on the survival and growth of local and foreign species. Second, to test whether habitat-specific soil microbes are responsible for habitat restriction, we examined the effect of local habitat live soil (containing soil microbes within local sister's habitats, but not directly associated with local sister species) on the seedlings of local and foreign species. We found that local sister live soil decreased the survival and biomass of foreign species' seedlings while increasing those of local species, suggesting that host-specific soil microbes could potentially mediate habitat exclusion. In contrast, local habitat live soil did not differentially affect the survival or biomass of the local vs. foreign species. Our study indicates that soil microbes associated with one sister species can suppress the recruitment of the other host species, contributing to the habitat partitioning of close relatives. Considering the complex interactions with soil microbes is essential for understanding the habitat distributions of closely related plants.

Strong associations between plant genotypes and bacterial communities in a natural salt marsh.

Although microbial communities have been shown to vary among plant genotypes in a number of experiments in terrestrial ecosystems, relatively little is known about this relationship under natural conditions and outside of select model systems. We reasoned that a salt marsh ecosystem, which is characterized by twice-daily flooding by tides, would serve as a particularly conservative test of the strength of plant-microbial associations, given the high degree of abiotic regulation of microbial community assembly resulting from alternating periods of inundation and exposure. Within a salt marsh in the northeastern United States, we characterized genotypes of the foundational plant Spartina alterniflora using microsatellite markers, and bacterial metagenomes within marsh soil based on pyrosequencing. We found significant differences in bacterial community composition and diversity between bulk and rhizosphere soil, and that the structure of rhizosphere communities varied depending on the growth form of, and genetic variation within, the foundational plant S. alterniflora. Our results indicate that there are strong plant-microbial associations within a natural salt marsh, thereby contributing to a growing body of evidence for a relationship between plant genotypes and microbial communities from terrestrial ecosystems and suggest that principles of community genetics apply to this wetland type.

Facilitation between woody and herbaceous plants that associate with arbuscular mycorrhizal fungi in temperate European forests.

In late-successional environments, low in available nutrient such as the forest understory, herbaceous plant individuals depend strongly on their mycorrhizal associates for survival. We tested whether in temperate European forests arbuscular mycorrhizal (AM) woody plants might facilitate the establishment of AM herbaceous plants in agreement with the mycorrhizal mediation hypothesis. We used a dataset spanning over 400 vegetation plots in the Weser-Elbe region (northwest Germany). Mycorrhizal status information was obtained from published resources, and Ellenberg indicator values were used to infer environmental data. We carried out tests for both relative richness and relative abundance of herbaceous plants. We found that the subset of herbaceous individuals that associated with AM profited when there was a high cover of AM woody plants. These relationships were retained when we accounted for environmental filtering effects using path analysis. Our findings build on the existing literature highlighting the prominent role of mycorrhiza as a coexistence mechanism in plant communities. From a nature conservation point of view, it may be possible to promote functional diversity in the forest understory through introducing AM woody trees in stands when absent.

Root Foraging Performance and Life-History Traits.

Plants use their roots to forage for nutrients in heterogeneous soil environments, but different plant species vastly differ in the intensity of foraging they perform. This diversity suggests the existence of constraints on foraging at the species level. We therefore examined the relationships between the intensity of root foraging and plant body traits across species in order to estimate the degree of coordination between plant body traits and root foraging as a form of plant behavior. We cultivated 37 perennial herbaceous Central European species from open terrestrial habitats in pots with three different spatial gradients of nutrient availability (steep, shallow, and no gradient). We assessed the intensity of foraging as differences in root placement inside pots with and without a spatial gradient of resource supply. For the same set of species, we retrieved data about body traits from available databases: maximum height at maturity, mean area of leaf, specific leaf area, shoot lifespan, ability to self-propagate clonally, maximal lateral spread (in clonal plants only), realized vegetative growth in cultivation, and realized seed regeneration in cultivation. Clonal plants and plants with extensive vegetative growth showed considerably weaker foraging than their non-clonal or slow-growing counterparts. There was no phylogenetic signal in the amount of expressed root foraging intensity. Since clonal plants foraged less than non-clonals and foraging intensity did not seem to be correlated with species phylogeny, we hypothesize that clonal growth itself (i.e., the ability to develop at least partly self-sustaining ramets) may be an answer to soil heterogeneity. Whereas unitary plants use roots as organs specialized for both resource acquisition and transport to overcome spatial heterogeneity in resource supply, clonal plants separate these two functions. Becoming a clonal plant allows higher specialization at the organ level, since a typical clonal plant can be viewed as a network of self-sustainable harvesting units connected together with specialized high-throughput connection organs. This may be an effective alternative for coping with spatial heterogeneity in resource availability.

Mycorrhizas influence functional traits of two tallgrass prairie species.

Over the past decade, functional traits that influence plant performance and thus, population, community, and ecosystem biology have garnered increasing attention. Generally lacking, however, has been consideration of how ubiquitous arbuscular mycorrhizas influence plant allometric and stoichiometric functional traits. We assessed how plant dependence on and responsiveness to mycorrhizas influence plant functional traits of a warm-season, C4 grass, Andropogon gerardii Vitman, and the contrasting, cool-season, C3 grass, Elymus canadensis L. We grew both host species with and without inoculation with mycorrhizal fungi, across a broad gradient of soil phosphorus availabilities. Both host species were facultatively mycotrophic, able to grow without mycorrhizas at high soil phosphorus availability. A. gerardii was most dependent upon mycorrhizas and E. canadensis was weakly dependent, but highly responsive to mycorrhizas. The high dependence of A. gerardii on mycorrhizas resulted in higher tissue P and N concentrations of inoculated than noninoculated plants. When not inoculated, E. canadensis was able to take up both P and N in similar amounts to inoculated plants because of its weak dependence on mycorrhizas for nutrient uptake and its pronounced ability to change root-to-shoot ratios. Unlike other highly dependent species, A. gerardii had a high root-to-shoot ratio and was able to suppress colonization by mycorrhizal fungi at high soil fertilities. E. canadensis, however, was unable to suppress colonization and had a lower root-to shoot ratio than A. gerardii. The mycorrhiza-related functional traits of both host species likely influence their performance in nature: both species attained the maximum responsiveness from mycorrhizas at soil phosphorus availabilities similar to those of tallgrass prairies. Dependence upon mycorrhizas affects performance in the absence of mycorrhizas. Responsiveness to mycorrhizal fungi is also a function of the environment and can be influenced by both mycorrhizal fungus species and soil fertility.

Drought history affects grassland plant and microbial carbon turnover during and after a subsequent drought event.

Drought periods are projected to become more severe and more frequent in many European regions. While effects of single strong droughts on plant and microbial carbon (C) dynamics have been studied in some detail, impacts of recurrent drought events are still little understood.We tested whether the legacy of extreme experimental drought affects responses of plant and microbial C and nitrogen (N) turnover to further drought and rewetting. In a mountain grassland, we conducted a 13C pulse-chase experiment during a naturally occurring drought and rewetting event in plots previously exposed to experimental droughts and in ambient controls (AC). After labelling, we traced 13C below-ground allocation and incorporation into soil microbes using phospholipid fatty acid biomarkers.Drought history (DH) had no effects on the standing shoot and fine root plant biomass. However, plants with experimental DH displayed decreased shoot N concentrations and increased fine root N concentrations relative to those in AC. During the natural drought, plants with DH assimilated and allocated less 13C below-ground; moreover, fine root respiration was reduced and not fuelled by fresh C compared to plants in AC.Regardless of DH, microbial biomass remained stable during natural drought and rewetting. Although microbial communities initially differed in their composition between soils with and without DH, they responded to the natural drought and rewetting in a similar way: gram-positive bacteria increased, while fungal and gram-negative bacteria remained stable. In soils with DH, a strongly reduced uptake of recent plant-derived 13C in microbial biomarkers was observed during the natural drought, pointing to a smaller fraction of active microbes or to a microbial community that is less dependent on plant C. Synthesis. Drought history can induce changes in above- vs. below-ground plant N concentrations and affect the response of plant C turnover to further droughts and rewetting by decreasing plant C uptake and below-ground allocation. DH does not affect the responses of the microbial community to further droughts and rewetting, but alters microbial functioning, particularly the turnover of recent plant-derived carbon, during and after further drought periods.

More closely related plants have more distinct mycorrhizal communities.

Neighbouring plants are known to vary from having similar to dissimilar arbuscular mycorrhizal fungal (AMF) communities. One possibility is that closely related plants have more similar AMF communities than more distantly related plants, an indication of phylogenetic host specificity. Here, we investigated the structure of AMF communities among dominant grassland plants at three sites in the Northern Great Plains to test whether the pairwise phylogenetic distance among plant species was correlated with pairwise AMF community dissimilarity. For eight dominant and co-occurring grassland plant species, we reconstructed a phylogeny based on DNA data and characterized the AMF communities of their roots at each site. Community analyses revealed that AMF communities varied among sites and among plant species. Contrary to expectations for phylogenetic host specificity, we found that within a site more closely related plants had more distinct AMF communities despite their having similar phenologies. Associations with unique AMF communities may enhance the functional complementarity of related species and promote their coexistence.

Microbial community composition explains soil respiration responses to changing carbon inputs along an Andes-to-Amazon elevation gradient.

1. The Andes are predicted to warm by 3-5 °C this century with the potential to alter the processes regulating carbon (C) cycling in these tropical forest soils. This rapid warming is expected to stimulate soil microbial respiration and change plant species distributions, thereby affecting the quantity and quality of C inputs to the soil and influencing the quantity of soil-derived CO2 released to the atmosphere. 2. We studied tropical lowland, premontane and montane forest soils taken from along a 3200-m elevation gradient located in south-east Andean Peru. We determined how soil microbial communities and abiotic soil properties differed with elevation. We then examined how these differences in microbial composition and soil abiotic properties affected soil C-cycling processes, by amending soils with C substrates varying in complexity and measuring soil heterotrophic respiration (RH). 3. Our results show that there were consistent patterns of change in soil biotic and abiotic properties with elevation. Microbial biomass and the abundance of fungi relative to bacteria increased significantly with elevation, and these differences in microbial community composition were strongly correlated with greater soil C content and C:N (nitrogen) ratios. We also found that RH increased with added C substrate quality and quantity and was positively related to microbial biomass and fungal abundance. 4. Statistical modelling revealed that RH responses to changing C inputs were best predicted by soil pH and microbial community composition, with the abundance of fungi relative to bacteria, and abundance of gram-positive relative to gram-negative bacteria explaining much of the model variance. 5. Synthesis. Our results show that the relative abundance of microbial functional groups is an important determinant of RH responses to changing C inputs along an extensive tropical elevation gradient in Andean Peru. Although we do not make an experimental test of the effects of climate change on soil, these results challenge the assumption that different soil microbial communities will be 'functionally equivalent' as climate change progresses, and they emphasize the need for better ecological metrics of soil microbial communities to help predict C cycle responses to climate change in tropical biomes.

Intraspecific plant-soil feedback and intraspecific overyielding in Arabidopsis thaliana.

Understanding the mechanisms of community coexistence and ecosystem functioning may help to counteract the current biodiversity loss and its potentially harmful consequences. In recent years, plant-soil feedback that can, for example, be caused by below-ground microorganisms has been suggested to play a role in maintaining plant coexistence and to be a potential driver of the positive relationship between plant diversity and ecosystem functioning. Most of the studies addressing these topics have focused on the species level. However, in addition to interspecific interactions, intraspecific interactions might be important for the structure of natural communities. Here, we examine intraspecific coexistence and intraspecific diversity effects using 10 natural accessions of the model species Arabidopsis thaliana (L.) Heynh. We assessed morphological intraspecific diversity by measuring several above- and below-ground traits. We performed a plant-soil feedback experiment that was based on these trait differences between the accessions in order to determine whether A. thaliana experiences feedback at intraspecific level as a result of trait differences. We also experimentally tested the diversity-productivity relationship at intraspecific level. We found strong differences in above- and below-ground traits between the A. thaliana accessions. Overall, plant-soil feedback occurred at intraspecific level. However, accessions differed in the direction and strength of this feedback: Some accessions grew better on their own soils, some on soils from other accessions. Furthermore, we found positive diversity effects within A. thaliana: Accession mixtures produced a higher total above-ground biomass than accession monocultures. Differences between accessions in their feedback response could not be explained by morphological traits. Therefore, we suggest that they might have been caused by accession-specific accumulated soil communities, by root exudates, or by accession-specific resource use based on genetic differences that are not expressed in morphological traits. Synthesis. Our results provide some of the first evidence for intraspecific plant-soil feedback and intraspecific overyielding. These findings may have wider implications for the maintenance of variation within species and the importance of this variation for ecosystem functioning. Our results highlight the need for an increased focus on intraspecific processes in plant diversity research to fully understand the mechanisms of coexistence and ecosystem functioning.

Coexistence and relative abundance in plant communities are determined by feedbacks when the scale of feedback and dispersal is local.

1. Negative plant-soil feedback occurs when the presence of an individual of a particular species at a particular site decreases the relative success of individuals of the same species compared to those other species at that site. This effect favors heterospecifics thereby facilitating coexistence and maintaining diversity. Empirical work has demonstrated that the average strengths of these feedbacks correlate with the relative abundance of species within a community, suggesting that feedbacks are an important driver of plant community composition. Understanding what factors contribute to the generation of this relationship is necessary for diagnosing the dynamic forces that maintain diversity in plant communities. 2. We used a spatially explicit, individual-based computer simulation to test the effects of dispersal distance, the size of feedback neighbourhoods, the strength of pairwise feedbacks and community wide variation of feedbacks, community richness, as well as life-history differences on the dependence of relative abundance on strength of feedback. 3. We found a positive dependence of relative abundance of a species on its average feedback for local scale dispersal and feedback. However, we found that the strength of this dependence decreased as either the spatial scale of dispersal and/or the spatial scale of feedback increased. We also found that for spatially local (i.e. relatively small) scale interaction and dispersal, as the mean strength of feedbacks in the community becomes less negative, the greater the increase in abundance produced by a comparable increase in species-specific average feedback. We found that life-history differences such as mortality rate did not generate a pattern with abundance, nor did they affect the relationship between abundance and average feedback. 4.Synthesis. Our results support the claim that empirical observations of a positive correlation between relative abundance and strength of average feedback serves as evidence that local scale negative feedbacks play a prominent role in structuring plant communities. We also identify that this relationship depends upon local scale plant dispersal and feedback which generates clumping and magnifies the negative feedbacks.