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      What Can Interaction Webs Tell Us About Species Roles?

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          Abstract

          The group model is a useful tool to understand broad-scale patterns of interaction in a network, but it has previously been limited in use to food webs, which contain only predator-prey interactions. Natural populations interact with each other in a variety of ways and, although most published ecological networks only include information about a single interaction type ( e.g., feeding, pollination), ecologists are beginning to consider networks which combine multiple interaction types. Here we extend the group model to signed directed networks such as ecological interaction webs. As a specific application of this method, we examine the effects of including or excluding specific interaction types on our understanding of species roles in ecological networks. We consider all three currently available interaction webs, two of which are extended plant-mutualist networks with herbivores and parasitoids added, and one of which is an extended intertidal food web with interactions of all possible sign structures (+/+, -/0, etc.). Species in the extended food web grouped similarly with all interactions, only trophic links, and only nontrophic links. However, removing mutualism or herbivory had a much larger effect in the extended plant-pollinator webs. Species removal even affected groups that were not directly connected to those that were removed, as we found by excluding a small number of parasitoids. These results suggest that including additional species in the network provides far more information than additional interactions for this aspect of network structure. Our methods provide a useful framework for simplifying networks to their essential structure, allowing us to identify generalities in network structure and better understand the roles species play in their communities.

          Author Summary

          Ecological interactions are highly diverse even when considering a single species: the species might feed on a first, disperse the seeds of a second, and pollinate a third. Here we extend the group model, a method for identifying broad patterns of interaction across a food web, to networks which contain multiple types of interactions. Using this new method, we ask whether the traditional approach of building a network for each type of interaction (food webs for consumption, pollination webs, seed-dispersal webs, host-parasite webs) can be improved by merging all interaction types in a single network. In particular, we test whether combining different interaction types leads to a better definition of the roles species play in ecological communities. We find that, although having more information necessarily leads to better results, the improvement is only incremental if the linked species remain unchanged. However, including a new interaction type that attaches new species to the network substantially improves performance. This method provides insight into possible implications of merging different types of interactions and allows for the study of coarse-grained structure in any signed network, including ecological interaction webs, gene regulation networks, and social networks.

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          Most cited references20

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          Food-web structure and network theory: The role of connectance and size.

          Networks from a wide range of physical, biological, and social systems have been recently described as "small-world" and "scale-free." However, studies disagree whether ecological networks called food webs possess the characteristic path lengths, clustering coefficients, and degree distributions required for membership in these classes of networks. Our analysis suggests that the disagreements are based on selective use of relatively few food webs, as well as analytical decisions that obscure important variability in the data. We analyze a broad range of 16 high-quality food webs, with 25-172 nodes, from a variety of aquatic and terrestrial ecosystems. Food webs generally have much higher complexity, measured as connectance (the fraction of all possible links that are realized in a network), and much smaller size than other networks studied, which have important implications for network topology. Our results resolve prior conflicts by demonstrating that although some food webs have small-world and scale-free structure, most do not if they exceed a relatively low level of connectance. Although food-web degree distributions do not display a universal functional form, observed distributions are systematically related to network connectance and size. Also, although food webs often lack small-world structure because of low clustering, we identify a continuum of real-world networks including food webs whose ratios of observed to random clustering coefficients increase as a power-law function of network size over 7 orders of magnitude. Although food webs are generally not small-world, scale-free networks, food-web topology is consistent with patterns found within those classes of networks.
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            Compartmentalization increases food-web persistence.

            It has recently been noted that empirical food webs are significantly compartmentalized; that is, subsets of species exist that interact more frequently among themselves than with other species in the community. Although the dynamic implications of compartmentalization have been debated for at least four decades, a general answer has remained elusive. Here, we unambiguously demonstrate that compartmentalization acts to increase the persistence of multitrophic food webs. We then identify the mechanisms behind this result. Compartments in food webs act directly to buffer the propagation of extinctions throughout the community and augment the long-term persistence of its constituent species. This contribution to persistence is greater the more complex the food web, which helps to reconcile the simultaneous complexity and stability of natural communities.
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              Parasites dominate food web links.

              Parasitism is the most common animal lifestyle, yet food webs rarely include parasites. The few earlier studies have indicated that including parasites leads to obvious increases in species richness, number of links, and food chain length. A less obvious result was that adding parasites slightly reduced connectance, a key metric considered to affect food web stability. However, reported reductions in connectance after the addition of parasites resulted from an inappropriate calculation. Two alternative corrective approaches applied to four published studies yield an opposite result: parasites increase connectance, sometimes dramatically. In addition, we find that parasites can greatly affect other food web statistics, such as nestedness (asymmetry of interactions), chain length, and linkage density. Furthermore, whereas most food webs find that top trophic levels are least vulnerable to natural enemies, the inclusion of parasites revealed that mid-trophic levels, not low trophic levels, suffered the highest vulnerability to natural enemies. These results show that food webs are very incomplete without parasites. Most notably, recognition of parasite links may have important consequences for ecosystem stability because they can increase connectance and nestedness.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                PLoS Comput. Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, CA USA )
                1553-734X
                1553-7358
                July 2015
                21 July 2015
                : 11
                : 7
                : e1004330
                Affiliations
                [1 ]Department of Ecology & Evolution, University of Chicago, Chicago, Illinois, United States of America
                [2 ]Computation Institute, University of Chicago, Chicago, Illinois, United States of America
                University of North Carolina at Wilmington, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: ELS SA. Performed the experiments: ELS SA. Analyzed the data: ELS. Wrote the paper: ELS SA JTW. Contributed Data: JTW.

                Article
                PCOMPBIOL-D-14-02237
                10.1371/journal.pcbi.1004330
                4511233
                26197151
                cce51f38-928a-4042-b803-d5b69f0bfa31
                Copyright @ 2015

                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
                : 12 December 2014
                : 11 May 2015
                Page count
                Figures: 10, Tables: 0, Pages: 22
                Funding
                This work was supported by the NSF (graduate fellowship to ELS, DEB-1148867 to SA, DEB 09-19420 and OCE 04-52678 to JTW) and the University of Chicago Hinds Fund (to ELS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                Code is available at https://github.com/esander91/SignedGroupModel. Network and taxonomic data for the Tatoosh network is available on Dryad at http://datadryad.org/review?doi=doi:10.5061/dryad.39jv1

                Quantitative & Systems biology
                Quantitative & Systems biology

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