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      Invasive Plant Suppresses the Growth of Native Tree Seedlings by Disrupting Belowground Mutualisms

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          Abstract

          The impact of exotic species on native organisms is widely acknowledged, but poorly understood. Very few studies have empirically investigated how invading plants may alter delicate ecological interactions among resident species in the invaded range. We present novel evidence that antifungal phytochemistry of the invasive plant, Alliaria petiolata, a European invader of North American forests, suppresses native plant growth by disrupting mutualistic associations between native canopy tree seedlings and belowground arbuscular mycorrhizal fungi. Our results elucidate an indirect mechanism by which invasive plants can impact native flora, and may help explain how this plant successfully invades relatively undisturbed forest habitat.

          Abstract

          Experimental evidence reveals that an invasive species in North America--garlic mustard--negatively impacts the growth of native tree seedlings by disrupting native mycorrhizal mutualisms.

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          Most cited references47

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          VARIATION IN PLANT RESPONSE TO NATIVE AND EXOTIC ARBUSCULAR MYCORRHIZAL FUNGI

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            Mycorrhizae Influence Tropical Succession

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              Plant invasions--the role of mutualisms.

              Many introduced plant species rely on mutualisms in their new habitats to overcome barriers to establishment and to become naturalized and, in some cases, invasive. Mutualisms involving animal-mediated pollination and seed dispersal, and symbioses between plant roots and microbiota often facilitate invasions. The spread of many alien plants, particularly woody ones, depends on pollinator mutualisms. Most alien plants are well served by generalist pollinators (insects and birds), and pollinator limitation does not appear to be a major barrier for the spread of introduced plants (special conditions relating to Ficus and orchids are described). Seeds of many of the most notorious plant invaders are dispersed by animals, mainly birds and mammals. Our review supports the view that tightly coevolved, plant-vertebrate seed dispersal systems are extremely rare. Vertebrate-dispersed plants are generally not limited reproductively by the lack of dispersers. Most mycorrhizal plants form associations with arbuscular mycorrhizal fungi which, because of their low specificity, do not seem to play a major role in facilitating or hindering plant invasions (except possibly on remote islands such as the Galapagos which are poor in arbuscular mycorrhizal fungi). The lack of symbionts has, however, been a major barrier for many ectomycorrhizal plants, notably for Pinus spp. in parts of the southern hemisphere. The roles of nitrogen-fixing associations between legumes and rhizobia and between actinorhizal plants and Frankia spp. in promoting or hindering invasions have been virtually ignored in the invasions literature. Symbionts required to induce nitrogen fixation in many plants are extremely widespread, but intentional introductions of symbionts have altered the invasibility of many, if not most, systems. Some of the world's worst invasive alien species only invaded after the introduction of symbionts. Mutualisms in the new environment sometimes re-unite the same species that form partnerships in the native range of the plant. Very often, however, different species are involved, emphasizing the diffuse nature of many (most) mutualisms. Mutualisms in new habitats usually duplicate functions or strategies that exist in the natural range of the plant. Occasionally, mutualisms forge totally novel combinations, with profound implications for the behaviour of the introduced plant in the new environment (examples are seed dispersal mutualisms involving wind-dispersed pines and cockatoos in Australia; and mycorrhizal associations involving plant roots and fungi). Many ecosystems are becoming more susceptible to invasion by introduced plants because: (a) they contain an increasing array of potential mutualistic partners (e.g. generalist frugivores and pollinators, mycorrhizal fungi with wide host ranges, rhizobia strains with infectivity across genera); and (b) conditions conductive for the establishment of various alien/alien synergisms are becoming more abundant. Incorporating perspectives on mutualisms in screening protocols will improve (but not perfect) our ability to predict whether a given plant species could invade a particular habitat.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                pbio
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                May 2006
                25 April 2006
                : 4
                : 5
                : e140
                Affiliations
                [1] 1Harvard Forest, Harvard University, Petersham, Massachusetts, United States of America
                [2] 2Department of Integrative Biology, University of Guelph, Guelph, Ontario, Canada
                [3] 3Division of Biological Sciences, University of Montana, Missoula, Montana, United States of America
                [4] 4Department of Botany and Plant Pathology, Purdue University, West Lafayette, Indiana, United States of America
                [5] 5Department of Community Ecology, UFZ Centre for Environmental Research, Halle, Germany
                McGill University Canada
                Article
                10.1371/journal.pbio.0040140
                1440938
                16623597
                62aba5bd-27ec-4158-abd7-a170592cdebe
                Copyright: © 2006 Stinson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 5 December 2005
                : 1 March 2006
                Categories
                Research Article
                Ecology
                Yeast and Fungi
                Plants
                Eukaryotes

                Life sciences
                Life sciences

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