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      Linking Cascading Effects of Fish Predation and Zooplankton Grazing to Reduced Cyanobacterial Biomass and Toxin Levels Following Biomanipulation

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          Abstract

          Eutrophication has been one of the largest environmental problems in aquatic ecosystems during the past decades, leading to dense, and often toxic, cyanobacterial blooms. In a way to counteract these problems many lakes have been subject to restoration through biomanipulation. Here we combine 13 years of monitoring data with experimental assessment of grazing efficiency of a naturally occurring zooplankton community and a, from a human perspective, desired community of large Daphnia to assess the effects of an altered trophic cascade associated with biomanipulation. Lake monitoring data show that the relative proportion of Daphnia spp. grazers in June has increased following years of biomanipulation and that this increase coincides with a drop in cyanobacterial biomass and lowered microcystin concentrations compared to before the biomanipulation. In June, the proportion of Daphnia spp. (on a biomass basis) went from around 3% in 2005 (the first year of biomanipulation) up to around 58% in 2012. During months when the proportion of Daphnia spp. remained unchanged (July and August) no effect on lower trophic levels was observed. Our field grazing experiment revealed that Daphnia were more efficient in controlling the standing biomass of cyanobacteria, as grazing by the natural zooplankton community never even compensated for the algal growth during the experiment and sometimes even promoted cyanobacterial growth. Furthermore, although the total cyanobacterial toxin levels remained unaffected by both grazer communities in the experimental study, the Daphnia dominated community promoted the transfer of toxins to the extracellular, dissolved phase, likely through feeding on cyanobacteria. Our results show that biomanipulation by fish removal is a useful tool for lake management, leading to a top-down mediated trophic cascade, through alterations in the grazer community, to reduced cyanobacterial biomass and lowered cyanobacterial toxin levels. This improved water quality enhances both the ecological and societal value of lakes as units for ecosystem services.

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          Predation, Body Size, and Composition of Plankton.

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            Evolution of phosphorus limitation in lakes.

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              Eutrophication of freshwater and coastal marine ecosystems: a global problem.

              Humans now strongly influence almost every major aquatic ecosystem, and their activities have dramatically altered the fluxes of growth-limiting nutrients from the landscape to receiving waters. Unfortunately, these nutrient inputs have had profound negative effects upon the quality of surface waters worldwide. This review examines how eutrophication influences the biomass and species composition of algae in both freshwater and costal marine systems. An overview of recent advances in algae-related eutrophication research is presented. In freshwater systems, a summary is presented for lakes and reservoirs; streams and rivers; and wetlands. A brief summary is also presented for estuarine and coastal marine ecosystems. Eutrophication causes predictable increases in the biomass of algae in lakes and reservoirs; streams and rivers; wetlands; and coastal marine ecosystems. As in lakes, the response of suspended algae in large rivers to changes in nutrient loading may be hysteretic in some cases. The inhibitory effects of high concentrations of inorganic suspended solids on algal growth, which can be very evident in many reservoirs receiving high inputs of suspended soils, also potentially may occur in turbid rivers. Consistent and predictable eutrophication-caused increases in cyanobacterial dominance of phytoplankton have been reported worldwide for natural lakes, and similar trends are reported here both for phytoplankton in turbid reservoirs, and for suspended algae in a large river A remarkable unity is evident in the global response of algal biomass to nitrogen and phosphorus availability in lakes and reservoirs; wetlands; streams and rivers; and coastal marine waters. The species composition of algal communities inhabiting the water column appears to respond similarly to nutrient loading, whether in lakes, reservoirs, or rivers. As is true of freshwater ecosystems, the recent literature suggests that coastal marine ecosystems will respond positively to nutrient loading control efforts. Our understanding of freshwater eutrophication and its effects on algal-related water quality is strong and is advancing rapidly. However, our understanding of the effects of eutrophication on estuarine and coastal marine ecosystems is much more limited, and this gap represents an important future research need. Although coastal systems can be hydrologically complex, the biomass of marine phytoplankton nonetheless appears to respond sensitively and predictably to changes in the external supplies of nitrogen and phosphorus. These responses suggest that efforts to manage nutrient inputs to the seas will result in significant improvements in coastal zone water quality. Additional new efforts should be made to develop models that quantitatively link ecosystem-level responses to nutrient loading in both freshwater and marine systems.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                19 November 2014
                : 9
                : 11
                : e112956
                Affiliations
                [1 ]Lund University, Department of Biology, Ecology Building, SE-223 62, Lund, Sweden
                [2 ]Lund University, Center for Environmental and Climate Research, Ecology Building, SE-223 62, Lund, Sweden
                University of Connecticut, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: ME LAH. Performed the experiments: ME PUC LAH. Analyzed the data: ME PUC. Contributed reagents/materials/analysis tools: LAH ME PUC. Contributed to the writing of the manuscript: ME LAH PUC.

                Article
                PONE-D-14-26304
                10.1371/journal.pone.0112956
                4237340
                25409309
                3551a148-7250-4c31-9a89-6835e522a560
                Copyright @ 2014

                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 June 2014
                : 30 September 2014
                Page count
                Pages: 10
                Funding
                This work was funded by the European Union Interreg IV A project “Algae be gone!” and by the ERA-Net BiodivERsA, with the national funders FORMAS, part of the 2012 BiodivERsA call for research proposals (LIMNOTIP). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Ecology
                Freshwater Ecology
                Limnetic Ecosystems
                Food Chains
                Restoration Ecology
                Earth Sciences
                Marine and Aquatic Sciences
                Aquatic Environments
                Freshwater Environments
                Lakes
                Limnology
                Ecology and Environmental Sciences
                Environmental Management
                Natural Resources
                Water Resources
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. Data are available within the Supporting Information files. Data regarding the lake monitoring are available in forms of yearly reports on: http://www.ringsjon.se/usok_rapport.asp.

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