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      Downsizing of animal communities triggers stronger functional than structural decay in seed-dispersal networks

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          Abstract

          Downsizing of animal communities due to defaunation is prevalent in many ecosystems. Yet, we know little about its consequences for ecosystem functions such as seed dispersal. Here, we use eight seed-dispersal networks sampled across the Andes and simulate how downsizing of avian frugivores impacts structural network robustness and seed dispersal. We use a trait-based modeling framework to quantify the consequences of downsizing—relative to random extinctions—for the number of interactions and secondary plant extinctions (as measures of structural robustness) and for long-distance seed dispersal (as a measure of ecosystem function). We find that downsizing leads to stronger functional than structural losses. For instance, 10% size-structured loss of bird species results in almost 40% decline of long-distance seed dispersal, but in less than 10% of structural loss. Our simulations reveal that measures of the structural robustness of ecological networks underestimate the consequences of animal extinction and downsizing for ecosystem functioning.

          Abstract

          Species loss from ecological networks can impair network stability and ecosystem function. Here the authors simulate animal extinctions in interaction networks between plants and avian frugivores, showing that frugivore extinctions have comparatively weak effects on network structure, but strongly reduce seed-dispersal distance.

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          Most cited references52

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          Mechanisms of long-distance seed dispersal.

          Growing recognition of the importance of long-distance dispersal (LDD) of plant seeds for various ecological and evolutionary processes has led to an upsurge of research into the mechanisms underlying LDD. We summarize these findings by formulating six generalizations stating that LDD is generally more common in open terrestrial landscapes, and is typically driven by large and migratory animals, extreme meteorological phenomena, ocean currents and human transportation, each transporting a variety of seed morphologies. LDD is often associated with unusual behavior of the standard vector inferred from plant dispersal morphology, or mediated by nonstandard vectors. To advance our understanding of LDD, we advocate a vector-based research approach that identifies the significant LDD vectors and quantifies how environmental conditions modify their actions.
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            Extinction order and altered community structure rapidly disrupt ecosystem functioning.

            By causing extinctions and altering community structure, anthropogenic disturbances can disrupt processes that maintain ecosystem integrity. However, the relationship between community structure and ecosystem functioning in natural systems is poorly understood. Here we show that habitat loss appeared to disrupt ecosystem functioning by affecting extinction order, species richness and abundance. We studied pollination by bees in a mosaic of agricultural and natural habitats in California and dung burial by dung beetles on recently created islands in Venezuela. We found that large-bodied bee and beetle species tended to be both most extinction-prone and most functionally efficient, contributing to rapid functional loss. Simulations confirmed that extinction order led to greater disruption of function than predicted by random species loss. Total abundance declined with richness and also appeared to contribute to loss of function. We demonstrate conceptually and empirically how the non-random response of communities to disturbance can have unexpectedly large functional consequences.
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              The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour.

              Species extinctions pose serious threats to the functioning of ecological communities worldwide. We used two qualitative and quantitative pollination networks to simulate extinction patterns following three removal scenarios: random removal and systematic removal of the strongest and weakest interactors. We accounted for pollinator behaviour by including potential links into temporal snapshots (12 consecutive 2-week networks) to reflect mutualists' ability to 'switch' interaction partners (re-wiring). Qualitative data suggested a linear or slower than linear secondary extinction while quantitative data showed sigmoidal decline of plant interaction strength upon removal of the strongest interactor. Temporal snapshots indicated greater stability of re-wired networks over static systems. Tolerance of generalized networks to species extinctions was high in the random removal scenario, with an increase in network stability if species formed new interactions. Anthropogenic disturbance, however, that promote the extinction of the strongest interactors might induce a sudden collapse of pollination networks.
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                Author and article information

                Contributors
                isa.donoso.cuadrado@gmail.com
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                27 March 2020
                27 March 2020
                2020
                : 11
                : 1582
                Affiliations
                [1 ]Senckenberg Biodiversity and Climate Research Centre (SBiK-F), Senckenberganlage 25, 60325 Frankfurt am Main, Germany
                [2 ]ISNI 0000 0004 1936 8198, GRID grid.34429.38, Department of Integrative Biology, , University of Guelph, ; Guelph, 50 Stone Road East, N1G 2W1 Ontario, Canada
                [3 ]ISNI 0000 0004 1936 9721, GRID grid.7839.5, Department of Biological Sciences, , Goethe University Frankfurt, ; Max-von-Laue-Str. 9, 60438 Frankfurt am Main, Germany
                [4 ]ISNI 0000000121496664, GRID grid.108162.c, Instituto de Ecología Regional, , Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) - Universidad Nacional de Tucumán, ; CC 34, 4107 Yerba Buena, Tucumán, Argentina
                [5 ]ISNI 0000000084992262, GRID grid.7177.6, Institute for Biodiversity and Ecosystem Dynamics (IBED), , University of Amsterdam, ; P.O. Box 94240, 1090 GE Amsterdam, The Netherlands
                Author information
                http://orcid.org/0000-0002-5556-0502
                http://orcid.org/0000-0002-2130-9934
                http://orcid.org/0000-0002-7274-6755
                http://orcid.org/0000-0001-9305-7716
                http://orcid.org/0000-0001-9426-045X
                Article
                15438
                10.1038/s41467-020-15438-y
                7101352
                32221279
                280fd373-2917-4807-947e-323d90c120c2
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 4 June 2019
                : 3 March 2020
                Funding
                Funded by: FundRef https://doi.org/10.13039/100005156, Alexander von Humboldt-Stiftung (Alexander von Humboldt Foundation);
                Funded by: FundRef https://doi.org/10.13039/501100010409, Netherlands Organisation for Scientific Research | Nationaal Regieorgaan Praktijkgericht Onderzoek SIA (Nationaal Regieorgaan Praktijkgericht Onderzoek);
                Award ID: 824.15.007
                Award Recipient :
                Funded by: University of Amsterdam Faculty Research Cluster ‘Global Ecology’
                Funded by: FundRef https://doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft (German Research Foundation);
                Award ID: PAK 825/1
                Award ID: FOR2730
                Award ID: PAK 825/1
                Award Recipient :
                Funded by: (DFG) in the framework of the Research Bundle 823–825 “Platform for Biodiversity and Ecosystem Monitoring and Research in South Ecuador” (PAK 825/1) and the Research Unit FOR2730 “Environmental changes in biodiversity hotspot ecosystems of South Ecuador: RESPonse and feedback effECTs”
                Funded by: FundRef https://doi.org/10.13039/501100001646, Robert Bosch Stiftung (Robert Bosch Foundation);
                Categories
                Article
                Custom metadata
                © The Author(s) 2020

                Uncategorized
                ecological modelling,ecological networks,community ecology
                Uncategorized
                ecological modelling, ecological networks, community ecology

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