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Range-expanding populations of a globally introduced weed experience negative plant-soil feedbacks.

ABSTRACT: 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.

SUBMITTER: Andonian K

PROVIDER: S-EPMC3100334 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Range-expanding populations of a globally introduced weed experience negative plant-soil feedbacks.

Andonian Krikor K Hierro José L JL Khetsuriani Liana L Becerra Pablo P Janoyan Grigor G Villarreal Diego D Cavieres Lohengrin L Fox Laurel R LR Callaway Ragan M RM

PloS one 20110523 5

<h4>Background</h4>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 foll ...[more]

PMID: 21629781

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Project description:Plant-soil feedback (PSF) results from the net legacy effect that plants leave in the composition of soil communities and abiotic soil properties. PSF is induced by the rhizosphere and by litter inputs into the soil, however, we have little understanding of their individual contributions. Here, we examine feedback effects from the rhizosphere of living plants, decomposing litter and their combination.We used four pairs of climate warming-induced range-expanding plant species and congeneric natives, and examined PSF effects on plant biomass production, as well as on decomposition in their new range.We tested the hypothesis that the plant rhizosphere provides less negative feedback to range-expanders than to the congeneric natives, and that feedback mediated by litter decomposition does not provide such a difference because decomposers might be less specialized than pathogens. To determine PSF, we used soil from the congener species within each pair as an 'away' soil to indicate whether range-expanders may have lost their specialized soil biota upon arrival in the novel range.Our results show that although range-expanding plant species and their congeneric natives developed neutral PSF in both rhizosphere- and litter-conditioned soils, two of the four range-expanders produced more biomass than natives in soils conditioned by litter, that is, soils with high nutrient content. Shoot litter from two out of four range-expanding species decomposed more than that of natives, but decomposition was unaffected by soil conditioning. Synthesis. We compared PSF effects of range-expanders and congeneric natives mediated via both the rhizosphere and litter using the congeneric species as a control. Under those conditions, PSF effects were neutral and not affected by plant origin. Therefore, we conclude that studies not comparing within plant genera may overestimate the impact of plant origin on PSF. Still, even under those conditions range-expanders appeared to benefit more from high soil nutrient availability than natives, thus providing a possible advantage over congeneric natives.

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:Current climate warming enables plant species and soil organisms to expand their range to higher latitudes and altitudes. At the same time, climate change increases the incidence of extreme weather events such as drought. While it is expected that plants and soil organisms originating from the south are better able to cope with drought, little is known about the consequences of their range shifts on soil functioning under drought events.Here, we test how range-expanding plant species and soil communities may influence soil functioning under drought. We performed a full-factorial outdoor mesocosm experiment with plant communities of range expanders or related natives, with soil inocula from the novel or the original range, with or without summer drought. We measured litter decomposition, carbon mineralization and enzyme activities, substrate-induced respiration and the relative abundance of soil saprophytic fungi immediately after drought and at 6 and 12 weeks after rewetting.Drought decreased all soil functions regardless of plant and soil origin except one; soil respiration was less reduced in soils of range-expanding plant communities, suggesting stronger resistance to drought. After rewetting, soil functioning responses depended on plant and soil origin. Soils of native plant communities with a history of drought had more litter mass loss and higher relative abundance of saprophytic fungi than soils without drought and soils of range expanders. Functions of soil from range expanders recovered in a more conservative manner than soils of natives, as litter mass loss did not exceed the control rates. At the end of the experiment, after rewetting, most soil functions in mesocosms with drought history did not differ anymore from the control.We conclude that functional consequences of range-expanding plants and soil biota may interact with effects of drought and that these effects are most prominent during the first weeks after rewetting of the soil. A free http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13453/suppinfo can be found within the Supporting Information of this article.

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Range-expanding populations of a globally introduced weed experience negative plant-soil feedbacks.

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Range-expanding populations of a globally introduced weed experience negative plant-soil feedbacks.

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