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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 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.

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Project description:Spatial patterns of trait variation across a species' range have implications for population success and evolutionary change potential, particularly in range-expanding and weedy species that encounter distinct selective pressures at large and small spatial scales simultaneously. We investigated intraspecific trait variation in a common garden experiment with giant ragweed (Ambrosia trifida), a highly variable agricultural weed with an expanding geographic range and broad ecological amplitude. Our study included paired populations from agricultural and natural riparian habitats in each of seven regions ranging east to west from the core of the species' distribution in central Ohio to southeastern Minnesota, which is nearer the current invasion front. We observed trait variation across both large- and small-scale putative selective gradients. At large scales, giant ragweed populations from the westernmost locations were nearly four times more fecund and had a nearly 50% increase in reproductive allocation compared to populations from the core. The degree of surface texture on fruits also declined from east to west. Greater fecundity in the west represents a putative trade-off between fruit size and fruit number across the study region, although no such trade-off was found across individual plants. This pattern may effectively result in greater propagule pressure closer to the invasion front. At smaller spatial scales, plants from agricultural populations emerged later and were smaller than plants from riparian populations. However, because plants from agricultural populations allocated more biomass to reproduction, total fecundity did not differ across habitats. Our emergence data are consistent with previous observations showing delayed emergence in agricultural compared to natural populations; thus evolutionary change may be predictable as giant ragweed continues spreading into agricultural fields throughout North America. These shifts in life-history strategy apparently bear no fecundity cost, suggesting that giant ragweed's success can be attributed at least in part to its substantial adaptive potential.

Dataset Information

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

Publications

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

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