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Negative effects of an allelopathic invader on AM fungal plant species drive community-level responses.

ABSTRACT: The mechanisms causing invasive species impact are rarely empirically tested, limiting our ability to understand and predict subsequent changes in invaded plant communities. Invader disruption of native mutualistic interactions is a mechanism expected to have negative effects on native plant species. Specifically, disruption of native plant-fungal mutualisms may provide non-mycorrhizal plant invaders an advantage over mycorrhizal native plants. Invasive Alliaria petiolata (garlic mustard) produces secondary chemicals toxic to soil microorganisms including mycorrhizal fungi, and is known to induce physiological stress and reduce population growth rates of native forest understory plant species. Here, we report on a 11-yr manipulative field experiment in replicated forest plots testing if the effects of removal of garlic mustard on the plant community support the mutualism disruption hypothesis within the entire understory herbaceous community. We compare community responses for two functional groups: the mycorrhizal vs. the non-mycorrhizal plant communities. Our results show that garlic mustard weeding alters the community composition, decreases community evenness, and increases the abundance of understory herbs that associate with mycorrhizal fungi. Conversely, garlic mustard has no significant effects on the non-mycorrhizal plant community. Consistent with the mutualism disruption hypothesis, our results demonstrate that allelochemical producing invaders modify the plant community by disproportionately impacting mycorrhizal plant species. We also demonstrate the importance of incorporating causal mechanisms of biological invasion to elucidate patterns and predict community-level responses.

SUBMITTER: Roche MD

PROVIDER: S-EPMC7816256 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Negative effects of an allelopathic invader on AM fungal plant species drive community-level responses.

Roche Morgan D MD Pearse Ian S IS Bialic-Murphy Lalasia L Kivlin Stephanie N SN Sofaer Helen R HR Kalisz Susan S

Ecology 20201104 1

The mechanisms causing invasive species impact are rarely empirically tested, limiting our ability to understand and predict subsequent changes in invaded plant communities. Invader disruption of native mutualistic interactions is a mechanism expected to have negative effects on native plant species. Specifically, disruption of native plant-fungal mutualisms may provide non-mycorrhizal plant invaders an advantage over mycorrhizal native plants. Invasive Alliaria petiolata (garlic mustard) produc ...[more]

PMID: 32970846

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Project description:Many studies have reported the phytotoxicity of allelopathic compounds under controlled conditions. However, more field studies are required to provide realistic evidences for the significance of allelopathic interference in natural communities. We conducted a 2-years field experiment in a semiarid plant community (NE Spain). Specifically, we planted juvenile individuals and sowed seeds of Salsola vermiculata L., Lygeum spartum L. and Artemisia herba-alba Asso. (three co-dominant species in the community) beneath adult individuals of the allelopathic shrub A. herba-alba, and assessed the growth, vitality, seed germination and seedling survival of those target species with and without the presence of chemical interference by the incorporation of activated carbon (AC) to the soil. In addition, juveniles and seeds of the same three target species were planted and sown beneath the canopy of adults of S. vermiculata (a shrub similar to A. herba-alba, but non-allelopathic) and in open bare soil to evaluate whether the allelopathic activity of A. herba-alba modulates the net outcome of its interactions with neighboring plants under contrasting abiotic stress conditions. We found that vitality of A. herba-alba juveniles was enhanced beneath A. herba-alba individuals when AC was present. Furthermore, we found that the interaction outcome in A. herba-alba microsite was neutral, whereas a positive outcome was found for S. vermiculata microsite, suggesting that allelopathy may limit the potential facilitative effects of the enhanced microclimatic conditions in A. herba-alba microsite. Yet, L. spartum juveniles were facilitated in A. herba-alba microsite. The interaction outcome in A. herba-alba microsite was positive under conditions of very high abiotic stress, indicating that facilitative interactions predominated over the interference of allelopathic plants under those conditions. These results highlight that laboratory studies can overestimate the significance of allelopathy in nature, and consequently, results obtained under controlled conditions should be interpreted carefully.

Project description:Facilitation among plants mediated by grazers occurs when an unpalatable plant extends its protection against grazing to another plant. This type of indirect facilitation impacts species coexistence and ecosystem functioning in a large array of ecosystems worldwide. It has nonetheless generally been understudied so far in comparison with the role played by direct facilitation among plants. We aimed at providing original data on indirect facilitation at the community scale to determine the extent to which indirect facilitation mediated by grazers can shape plant communities. Such experimental data are expected to contribute to refining the conceptual framework on plant-plant-herbivore interactions in stressful environments. We set up a 2-year grazing exclusion experiment in tropical alpine peatlands in Bolivia. Those ecosystems depend entirely on a few, structuring cushion-forming plants (hereafter referred to as "nurse" species), in which associated plant communities develop. Fences have been set over two nurse species with different strategies to cope with grazing (direct vs. indirect defenses), which are expected to lead to different intensities of indirect facilitation for the associated communities. We collected functional traits which are known to vary according to grazing pressure (LDMC, leaf thickness, and maximum height), on both the nurse and their associated plant communities in grazed (and therefore indirect facilitation as well) and ungrazed conditions. We found that the effect of indirectly facilitated on the associated plant communities depended on the functional trait considered. Indirect facilitation decreased the effects of grazing on species relative abundance, mean LDMC, and the convergence of the maximum height distribution of the associated communities, but did not affect mean height or cover. The identity of the nurse species and grazing jointly affected the structure of the associated plant community through indirect facilitation. Our results together with the existing literature suggest that the "grazer-nurse-beneficiary" interaction module can be more complex than expected when evaluated in the field.

Project description:Invasive plants can negatively affect belowground processes and alter soil microbial communities. For native plants that depend on soil resources from root fungal symbionts (RFS), invasion could compromise their resource status and subsequent ability to manufacture and store carbohydrates. Herbaceous perennials that depend on RFS-derived resources dominate eastern North American forest understories. Therefore, we predict that forest invasion by Alliaria petiolata, an allelopathic species that produces chemicals that are toxic to RFS, will diminish plant carbon storage and fitness. Over a single growing season, the loss of RFS could reduce a plant's photosynthetic physiology and carbon storage. If maintained over multiple growing seasons, this could create a condition of carbon stress and declines in plant vital rates. Here we characterize the signals of carbon stress over a short timeframe and explore the long-term consequence of Alliaria invasion using Maianthemum racemosum, an RFS-dependent forest understory perennial. First, in a greenhouse experiment, we treated the soil of potted Maianthemum with fresh leaf tissue from either Alliaria or Hesperis matronalis (control) for a single growing season. Alliaria-treated plants exhibit significant overall reductions in total non-structural carbohydrates and have 17 % less storage carbohydrates relative to controls. Second, we monitored Maianthemum vital rates in paired experimental plots where we either removed emerging Alliaria seedlings each spring or left Alliaria at ambient levels for 7 years. Where Alliaria is removed, Maianthemum size and vital rates improve significantly: flowering probability increases, while the probability of plants regressing to non-flowering stages or entering prolonged dormancy are reduced. Together, our results are consistent with the hypothesis that disruption of a ubiquitous mutualism following species invasion creates symptoms of carbon stress for species dependent on RFS. Disruption of plant-fungal mutualisms may generally contribute to the common, large-scale declines in forest biodiversity observed in the wake of allelopathic invaders.

Dataset Information

Negative effects of an allelopathic invader on AM fungal plant species drive community-level responses.

Publications

Negative effects of an allelopathic invader on AM fungal plant species drive community-level responses.

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