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      Effect of plant root symbionts on performance of native woody species in competition with an invasive grass in multispecies microcosms

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          Abstract

          The majority of terrestrial plants form mutualistic associations with arbuscular mycorrhizal fungi (AMF) and rhizobia (i.e., nitrogen‐fixing bacteria). Understanding these associations has important implications for ecological theory and for restoration practice. Here, we tested whether the presence of AMF and rhizobia influences the performance of native woody plants invaded by a non‐native grass in experimental microcosms. We planted eight plant species (i.e., Acacia acuminata, A. microbotrya, Eucalyptus loxophleba subsp. loxophleba, E. astringens, Calothamnus quadrifidus, Callistemon phoeniceus, Hakea lissocarpha and H. prostrata) in microcosms of field‐conditioned soil with and without addition of AMF and rhizobia in a fully factorial experimental design. After seedling establishment, we seeded half the microcosms with an invasive grass Bromus diandrus. We measured shoot and root biomass of native plants and Bromus, and on roots, the percentage colonization by AMF, number of rhizobia‐forming nodules and number of proteaceous root clusters. We found no effect of plant root symbionts or Bromus addition on performance of myrtaceous, and as predicted, proteaceous species as they rely little or not at all on AMF and rhizobia. Soil treatments with AMF and rhizobia had a strong positive effect (i.e., larger biomass) on native legumes ( Amicrobotrya and A. acuminata). However, the beneficial effect of root symbionts on legumes became negative (i.e., lower biomass and less nodules) if Bromus was present, especially for one legume, i.e., A. acuminata, suggesting a disruptive effect of the invader on the mutualism. We also found a stimulating effect of Bromus on root nodule production in Amicrobotrya and AMF colonization in A. acuminata which could be indicative of legumes’ increased resource acquisition requirement, i.e., for nitrogen and phosphorus, respectively, in response to the Bromus addition. We have demonstrated the importance of measuring belowground effects because the aboveground effects gave limited indication of the effects occurring belowground.

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          Most cited references69

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          Plant nutrient-acquisition strategies change with soil age.

          Nitrogen (N) tends to limit plant productivity on young soils; phosphorus (P) becomes increasingly limiting in ancient soils because it gradually disappears through leaching and erosion. Plant traits that are regarded as adaptations to N- and P-limited conditions include mycorrhizas and cluster roots. Mycorrhizas 'scavenge' P from solution or 'mine' insoluble organic N. Cluster roots function in severely P-impoverished landscapes, 'mining' P fixed as insoluble inorganic phosphates. The 'scavenging' and 'mining' strategies of mycorrhizal species without and non-mycorrhizal species with cluster roots, respectively, allow functioning on soils that differ markedly in P availability. Based on recent advances in our understanding of these contrasting strategies of nutrient acquisition, we provide an explanation for the distribution of mycorrhizal species on less P-impoverished soils, and for why, globally, cluster-bearing species dominate on severely P-impoverished, ancient soils, where P sensitivity is relatively common.
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            What's new about old fields? Land abandonment and ecosystem assembly.

            Environmental and socio-economic changes are leading to increased levels of land abandonment worldwide. The assembly of plant communities on old fields has informed much ecological theory, which in turn has facilitated efforts at ecological restoration. The interaction of the cultivation legacy with inherent soil and vegetation characteristics will determine the dynamics of plant community assembly on old fields and indicate the level of effort required to restore historical vegetation states. The abandonment of traditional agricultural lands in some areas will create old fields that require limited or no restoration. Yet intensification of agriculture and rapid environmental change will lead to increasing numbers of old fields that show little recovery towards an historic vegetation state. The restoration of these old fields will pose significant scientific and policy challenges.
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              Janzen-Connell effects are widespread and strong enough to maintain diversity in grasslands.

              Crop rotation schemes are believed to work by preventing specialist soil-borne pests from depressing the future yields of similar crops. In ecology, such negative plant-soil feedbacks may be viewed as a type of Janzen-Connell effect, which promotes species coexistence and diversity by preventing the same species from repeatedly occupying a particular site. In a controlled greenhouse experiment with 24 plant species and using soils from established field monocultures, we reveal community-wide soil-based Janzen-Connell effects between the three major functional groups of plants in temperate European grasslands. The effects are much stronger and more prevalent if plants are grown in interspecific competition. Using several soil treatments (gamma irradiation, activated carbon, fungicide, fertilizer) we show that the mechanism of the negative feedback is the buildup of soil pathogens which reduce the competitive ability of nearly all species when grown on soils they have formerly occupied. We further show that the magnitude of the change in competitive outcome is sufficient to stabilize observed fitness differences between functional groups in reasonably large communities. The generality and strength of this negative feedback suggests that Janzen-Connell effects have been underestimated as drivers of plant diversity in temperate ecosystems.
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                Author and article information

                Contributors
                chbirnbaum@gmail.com , cbirnbaum@tulane.edu
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                02 August 2018
                September 2018
                : 8
                : 17 ( doiID: 10.1002/ece3.2018.8.issue-17 )
                : 8652-8664
                Affiliations
                [ 1 ] Environmental and Conservation Sciences School of Veterinary and Life Sciences Murdoch University Murdoch WA Australia
                [ 2 ] School of Biological Sciences The University of Western Australia Crawley WA Australia
                [ 3 ] Centre for Agri‐Environmental Research & Soil Research Centre School of Agriculture, Policy and Development University of Reading Reading UK
                [ 4 ] Centre for Plant Genetics and Breeding The University of Western Australia Crawley WA Australia
                Author notes
                [*] [* ] Correspondence

                Christina Birnbaum, Department of Ecology and Evolutionary Biology, Tulane University, 6823 St. Charles Avenue, New Orleans, LA 70118.

                Emails: chbirnbaum@ 123456gmail.com ; cbirnbaum@ 123456tulane.edu

                [†]

                These authors contributed equally to this work.

                [‡]

                These authors also contributed equally to this work.

                Author information
                http://orcid.org/0000-0002-2511-1845
                Article
                ECE34397
                10.1002/ece3.4397
                6157687
                30271534
                305c9bda-48a3-4ec3-bf39-26ce7ab7f8a6
                © 2018 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 02 August 2017
                : 30 April 2018
                : 17 June 2018
                Page count
                Figures: 5, Tables: 0, Pages: 13, Words: 8968
                Funding
                Funded by: University of Western Australia Research Development Award
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece34397
                September 2018
                Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.4.9 mode:remove_FC converted:26.09.2018

                Evolutionary Biology
                invasion,legumes,old‐field restoration,plant–soil interactions,symbiosis
                Evolutionary Biology
                invasion, legumes, old‐field restoration, plant–soil interactions, symbiosis

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