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      Invasive Mutualists Erode Native Pollination Webs

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      PLoS Biology
      Public Library of Science

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          Abstract

          Plant–animal mutualisms are characterized by weak or asymmetric mutual dependences between interacting species, a feature that could increase community stability. If invasive species integrate into mutualistic webs, they may alter web structure, with consequences for species persistence. However, the effect of alien mutualists on the architecture of plant–pollinator webs remains largely unexplored. We analyzed the extent of mutual dependency between interacting species, as a measure of mutualism strength, and the connectivity of 10 paired plant–pollinator webs, eight from forests of the southern Andes and two from oceanic islands, with different incidences of alien species. Highly invaded webs exhibited weaker mutualism than less-invaded webs. This potential increase in network stability was the result of a disproportionate increase in the importance and participation of alien species in the most asymmetric interactions. The integration of alien mutualists did not alter overall network connectivity, but links were transferred from generalist native species to super-generalist alien species during invasion. Therefore, connectivity among native species declined in highly invaded webs. These modifications in the structure of pollination webs, due to dominance of alien mutualists, can leave many native species subject to novel ecological and evolutionary dynamics.

          Author Summary

          Plant–animal mutualisms are characterized by weak or asymmetric mutual dependences between interacting species, such that if a plant species depends strongly on an animal species, the animal typically depends weakly on the plant, and vice versa. This limited reciprocal dependency, or “mutualism strength,” might increase species persistence by buffering plant and animal species against the extinction of any of their partners. Many plant–pollinator networks include a fraction of alien species, and it is not clear how these invaders might affect the structure of pollination webs. We analyzed 10 paired plant–pollinator webs, eight from forests of the southern Andes and two from oceanic islands, with different incidences of alien species. Highly invaded webs exhibited, on average, weaker mutualistic interactions, and hence a potential increase in network stability, than less-invaded webs. This was due to a disproportionate increase in the participation of some alien species in the most asymmetric interactions and their role as central nodes in the structure of the most invaded pollination webs. The increase in alien dominance involves the usurpation of interaction links, decreasing connectivity among native mutualists. Thus, many native species that rely on native generalists for either reproduction or survivorship become highly dependent on these super-generalist alien mutualists.

          Abstract

          Alien mutualists can alter the structure of native pollination networks by usurping interaction links, thereby becoming central nodes of highly invaded webs.

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          Most cited references48

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          Habitat modification alters the structure of tropical host-parasitoid food webs.

          Global conversion of natural habitats to agriculture has led to marked changes in species diversity and composition. However, it is less clear how habitat modification affects interactions among species. Networks of feeding interactions (food webs) describe the underlying structure of ecological communities, and might be crucially linked to their stability and function. Here, we analyse 48 quantitative food webs for cavity-nesting bees, wasps and their parasitoids across five tropical habitat types. We found marked changes in food-web structure across the modification gradient, despite little variation in species richness. The evenness of interaction frequencies declined with habitat modification, with most energy flowing along one or a few pathways in intensively managed agricultural habitats. In modified habitats there was a higher ratio of parasitoid to host species and increased parasitism rates, with implications for the important ecosystem services, such as pollination and biological control, that are performed by host bees and wasps. The most abundant parasitoid species was more specialized in modified habitats, with reduced attack rates on alternative hosts. Conventional community descriptors failed to discriminate adequately among habitats, indicating that perturbation of the structure and function of ecological communities might be overlooked in studies that do not document and quantify species interactions. Altered interaction structure therefore represents an insidious and functionally important hidden effect of habitat modification by humans.
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            Interactive effects of habitat modification and species invasion on native species decline.

            Different components of global environmental change are often studied and managed independently, but mounting evidence points towards complex non-additive interaction effects between drivers of native species decline. Using the example of interactions between land-use change and biotic exchange, we develop an interpretive framework that will enable global change researchers to identify and discriminate between major interaction pathways. We formalise a distinction between numerically mediated versus functionally moderated causal pathways. Despite superficial similarity of their effects, numerical and functional pathways stem from fundamentally different mechanisms of action and have fundamentally different consequences for conservation management. Our framework is a first step toward building a better quantitative understanding of how interactions between drivers might mitigate or exacerbate the net effects of global environmental change on biotic communities in the future.
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              Biological invasions as disruptors of plant reproductive mutualisms.

              Invasive alien species affect the composition and functioning of invaded ecosystems in many ways, altering ecological interactions that have arisen over evolutionary timescales. Specifically, disruptions to pollination and seed-dispersal mutualistic interactions are often documented, although the profound implications of such impacts are not widely recognized. Such disruptions can occur via the introduction of alien pollinators, seed dispersers, herbivores, predators or plants, and we define here the many potential outcomes of each situation. The frequency and circumstances under which each category of mechanisms operates are also poorly known. Most evidence is from population-level studies, and the implications for global biodiversity are difficult to predict. Further insights are needed on the degree of resilience in interaction networks, but the preliminary picture suggests that invasive species frequently cause profound disruptions to plant reproductive mutualisms.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                pbio
                plbi
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                February 2008
                12 February 2008
                : 6
                : 2
                : e31
                Affiliations
                [1]Laboratorio Ecotono, Centro Regional Universitario Bariloche, Universidad Nacional del Comahue, Bariloche, Río Negro, Argentina
                University of Tennessee, United States of America
                Author notes
                * To whom correspondence should be addressed. E-mail: marcelo.aizen@ 123456gmail.com
                Article
                07-PLBI-RA-3165R2 plbi-06-02-05
                10.1371/journal.pbio.0060031
                2235906
                18271628
                85ca0895-bc1e-41a4-8b19-06b1e4fd49a6
                Copyright: © 2008 Aizen 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
                : 27 September 2007
                : 20 December 2007
                Page count
                Pages: 8
                Categories
                Research Article
                Ecology
                Plant Biology
                Custom metadata
                Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6(2): e31. doi: 10.1371/journal.pbio.0060031

                Life sciences
                Life sciences

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