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Plant-soil feedbacks promote negative frequency dependence in the coexistence of two aridland grasses.

ABSTRACT: Understanding the mechanisms of species coexistence is key to predicting patterns of species diversity. Historically, the ecological paradigm has been that species coexist by partitioning resources: as a species increases in abundance, self-limitation kicks in, because species-specific resources decline. However, determining coexistence mechanisms has been a particular puzzle for sedentary organisms with high overlap in their resource requirements, such as plants. Recent evidence suggests that plant-associated microbes could generate the stabilizing self-limitation (negative frequency dependence) that is required for species coexistence. Here, we test the key assumption that plant-microbe feedbacks cause such self-limitation. We used competition experiments and modelling to evaluate how two common groups of soil microbes (rhizospheric microbes and biological soil crusts) influenced the self-limitation of two competing desert grass species. Negative feedbacks between the dominant plant competitor and its rhizospheric microbes magnified self-limitation, whereas beneficial interactions between both plant species and biological soil crusts partly counteracted this stabilizing effect. Plant-microbe interactions have received relatively little attention as drivers of vegetation dynamics in dry land ecosystems. Our results suggest that microbial mechanisms can contribute to patterns of plant coexistence in arid grasslands.

SUBMITTER: Chung YA

PROVIDER: S-EPMC4971199 | biostudies-literature | 2016 Jul

REPOSITORIES: biostudies-literature

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Plant-soil feedbacks promote negative frequency dependence in the coexistence of two aridland grasses.

Chung Y Anny YA Rudgers Jennifer A JA

Proceedings. Biological sciences 20160701 1835

Understanding the mechanisms of species coexistence is key to predicting patterns of species diversity. Historically, the ecological paradigm has been that species coexist by partitioning resources: as a species increases in abundance, self-limitation kicks in, because species-specific resources decline. However, determining coexistence mechanisms has been a particular puzzle for sedentary organisms with high overlap in their resource requirements, such as plants. Recent evidence suggests that p ...[more]

PMID: 27466448

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Project description:BACKGROUND: Biological invasions are fundamentally biogeographic processes that occur over large spatial scales. Interactions with soil microbes can have strong impacts on plant invasions, but how these interactions vary among areas where introduced species are highly invasive vs. naturalized is still unknown. In this study, we examined biogeographic variation in plant-soil microbe interactions of a globally invasive weed, Centaurea solstitialis (yellow starthistle). We addressed the following questions (1) Is Centaurea released from natural enemy pressure from soil microbes in introduced regions? and (2) Is variation in plant-soil feedbacks associated with variation in Centaurea's invasive success? METHODOLOGY/PRINCIPAL FINDINGS: We conducted greenhouse experiments using soils and seeds collected from native Eurasian populations and introduced populations spanning North and South America where Centaurea is highly invasive and noninvasive. Soil microbes had pervasive negative effects in all regions, although the magnitude of their effect varied among regions. These patterns were not unequivocally congruent with the enemy release hypothesis. Surprisingly, we also found that Centaurea generated strong negative feedbacks in regions where it is the most invasive, while it generated neutral plant-soil feedbacks where it is noninvasive. CONCLUSIONS/SIGNIFICANCE: Recent studies have found reduced below-ground enemy attack and more positive plant-soil feedbacks in range-expanding plant populations, but we found increased negative effects of soil microbes in range-expanding Centaurea populations. While such negative feedbacks may limit the long-term persistence of invasive plants, such feedbacks may also contribute to the success of invasions, either by having disproportionately negative impacts on competing species, or by yielding relatively better growth in uncolonized areas that would encourage lateral spread. Enemy release from soil-borne pathogens is not sufficient to explain the success of this weed in such different regions. The biogeographic variation in soil-microbe effects indicates that different mechanisms may operate on this species in different regions, thus establishing geographic mosaics of species interactions that contribute to variation in invasion success.

Project description: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.

Project description:Backgrounds and aimsNegative plant-soil feedbacks (PSFs) are thought to promote species coexistence, but most evidence is derived from theoretical models and data from plant monoculture experiments.MethodsWe grew Anthoxanthum odoratum and Centaurea jacea in field plots in monocultures and in mixtures with three ratios (3:1, 2:2 and 1:3) for three years. We then tested in a greenhouse experiment the performance of A. odoratum and C. jacea in pots planted with monocultures and 1:1 mixtures and filled with live and sterile soils collected from the field plots.ResultsIn the greenhouse experiment, C. jacea produced less aboveground biomass in soil conditioned by C. jacea monocultures than in soil conditioned by A. odoratum monocultures, while the aboveground biomass of A. odoratum in general did not differ between the two monospecific soils. The negative PSF effect was greater in the 1:1 plant mixture than in plant monocultures for A. odoratum but did not differ for C. jacea. In the greenhouse experiment, the performance of C. jacea relative to A. odoratum in the 1:1 plant mixture was negatively correlated to the abundance of C. jacea in the field plot where the soil was collected from. This relationship was significant both in live and sterile soils. However, there was no relationship between the performance of A. odoratum relative to C. jacea in the 1:1 plant mixture in the greenhouse experiment and the abundance of A. odoratum in the field plots.ConclusionsThe response of a plant to PSF depends on whether the focal species grows in monocultures or in mixtures and on the identity of the species. Interspecific competition can exacerbate the negative plant-soil feedbacks compared to intraspecific competition when a plant competes with a stronger interspecific competitor. Moreover, the abundance of a species in mixed plant communities, via plant-soil feedback, negatively influences the relative competitiveness of that species when it grows later in interspecific competition, but this effect varies between species. This phenomenon may contribute to the coexistence of competing plants under natural conditions through preventing the dominance of a particular plant species.

Project description:Intraspecific negative feedback effects, where performance is reduced on soils conditioned by conspecifics, are widely documented in plant communities. However, interspecific feedbacks are less well studied, and their direction, strength, causes, and consequences are poorly understood. If more closely related species share pathogens, or have similar soil resource requirements, plants may perform better on soils conditioned by more distant phylogenetic relatives. There have been few empirical tests of this prediction across plant life stages, and none of which attempt to account for soil chemistry. Here, we test the utility of phylogeny for predicting soil feedback effects on plant survival and performance (germination, seedling survival, growth rate, biomass). We implement a full factorial experiment growing species representing five families on five plant family-specific soil sources. Our experiments exploit soils that have been cultured for over 30 years in plant family-specific beds at Oxford University Botanic Gardens. Plant responses to soil source were idiosyncratic, and species did not perform better on soils cultured by phylogenetically more distant relatives. The magnitude and sign of feedback effects could, however, be explained by differences in the chemical properties of "home" and "away" soils. Furthermore, the direction of soil chemistry-related plant-soil feedbacks was dependent on plant life stage, with the effects of soil chemistry on germination success and accumulation of biomass inversely related. Our results (1) suggest that the phylogenetic distance between plant families cannot predict plant-soil feedbacks across multiple life stages, and (2) highlight the need to consider changes in soil chemistry as an important driver of population responses. The contrasting responses at plant life stages suggest that studies focusing on brief phases in plant demography (e.g., germination success) may not give a full picture of plant-soil feedback effects.

Dataset Information

Plant-soil feedbacks promote negative frequency dependence in the coexistence of two aridland grasses.

Publications

Plant-soil feedbacks promote negative frequency dependence in the coexistence of two aridland grasses.

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