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Toxins 2018, 10(4), 156; https://doi.org/10.3390/toxins10040156

Temperature Effects Explain Continental Scale Distribution of Cyanobacterial Toxins

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Department F.-A. Forel for Environmental and Aquatic Sciences, University of Geneva, 1205 Geneva, Switzerland
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Department of Environmental Sciences, Wageningen University & Research, 6700 Wageningen, The Netherlands
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Department of Aquatic Ecology, Netherlands Institute of Ecology (NIOO-KNAW), 6700 Wageningen, The Netherlands
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German Environment Agency, Unit Drinking Water Resources and Water Treatment, Corrensplatz 1, 14195 Berlin, Germany
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Institute of Nature Conservation, Polish Academy of Sciences, 31-120 Krakow, Poland
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Institute of Botany, Nature Research Centre, Vilnius 08412, Lithuania
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R&D Department Environmental Engineering, 3edata, 27004 Lugo, Spain
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Department of Water Protection, Adam Mickiewicz University, 61614 Poznan, Poland
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Department of Hydrobiology, Adam Mickiewicz University, 61614 Poznan, Poland
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Department of Limnology and Water Quality, AECOM U.R.S, 08036 Barcelona, Spain
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Department of Environmental Engineering, Abant Izzet Baysal University, 14280 Bolu, Turkey
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Department of Science and Engineering, Åbo Akademi University, 20520 Åbo, Finland
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Department of Fisheries and Aquaculture, Ankara University, 6100 Ankara, Turkey
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Department of biology, Middle East Technical University, 6800 Ankara, Turkey
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Institute of Marine Sciences, Department of Oceanography, Middle East Technical University, 06800 Ankara, Turkey
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Department of Botany, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
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Department of Basic Science, Ataturk University, 25240 Erzurum, Turkey
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Water Quality Department, Athens Water Supply and Sewerage Company, 11146 Athens, Greece
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Department of Biology, Balikesir University, 10145 Balikesir, Turkey
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Department of Bioengineering, Bursa Technical University, 16310 Bursa, Turkey
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Catalan Institute for Water Research (ICRA), 17003 Girona, Spain
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Department of Ecology and Genetics, Limnology, Uppsala University, 75236 Uppsala, Sweden
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Department of Ecology and Genetics, Erken Laboratory, Uppsala University, 76173 Norrtalje, Sweden
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Research Center in Biodiversity and Genetic Resources (CIBIO-Azores), InBIO Associated Laboratory, Faculty of Sciences and Technology, University of the Azores, 9501-801 Ponta Delgada, Portugal
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Department of Environmental Science and Technology, Cyprus University of Technology, 3036 Lemesos, Cyprus
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Centre for Freshwater and Environmental Studies, Dundalk Institute of Technology, A91 K584 Dundalk, Ireland
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Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, 51014 Tartu, Estonia
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European Regional Centre for Ecohydrology of the Polish Academy of Sciences, 90364 Lodz, Poland
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Republic of Turkey Ministry of Food Agriculture, Fisheries Research Institute, 32500 Eğirdir, Isparta, Turkey
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Department of Sustainable Ecosystems and Bioresources, Fondazione Edmund Mach, 38010 San Michele all’Adige, Italy
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Department of Biological and Environmental Sciences, University of Stirling, Stirling FK9 4LA, UK
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Department of Freshwater and Marine Ecology, University of Amsterdam, 1090 GE Amsterdam, The Netherlands
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Department of Molecular Biology and Genetics, Gaziosmanpasa University, 60250 Merkez, Turkey
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Department of Biology, Giresun University, 28100 Giresun, Turkey
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Department of Biology, Hitit University, 19040 Corum, Turkey
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Department of Icthyology, Hydrobiology and Aquatic Ecology, Inland Fisheries Institute, 10719 Olsztyn, Poland
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Department of Freshwater Protection, Institute of Environmental Protection- National Research Institute, 01-692 Warsaw, Poland
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Centro de Investigação da Montanha, Instituto Politécnico de Bragança, Campus de Santa Apolónia, 5300-253 Bragança, Portugal
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Interdisciplinary Centre of Marine and Environmental Research (CIIMAR) and University of Porto, 4450-208 Matosinhos, Portugal
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Department of Freshwater Resource and Management, Faculty of Aquatic Sciences, Istanbul University, 34134 Istanbul, Turkey
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Department of Biology, Josip Juraj Strossmayer University of Osijek, 31000 Osijek, Croatia
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Department of Experimental Limnology, Leibniz Institute of Freshwater Ecology and Inland Fisheries, 16775 Stechlin, Germany
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Department of Biology, Limnological Institute, University of Konstanz, 78464 Konstanz, Germany
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Department of Biology, Lund University, 22362 Lund, Sweden
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RECETOX, Faculty of Science, Masaryk University, 62500 Brno, Czech Republic
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Department of Hydrobiology, Morava Board Authority, 60200 Brno, Czech Republic
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Laboratory of Paleoecology, Institute of Botany, The Czech Academy of Sciences, 60200 Brno, Czech Republic
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Department of Environment and Resource Management, Mediterranean Fisheries Research Production and Training Institute, 7090 Antalya, Turkey
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Faculty of Aquaculture, Mersin University, 33160 Mersin, Turkey
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Department of Water Quality, Slovenian Environmental Agency, 1000 Ljubljana, Slovenia
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Department of Genetic Toxicology and Cancer Biology, National Institute of Biology, 1000 Ljubljana, Slovenia
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Institute of Nanoscience and Nanotechnology, National Center for Scientific Research «DEMOKRITOS», 15341 Attiki, Greece
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Department of Freshwater Ecology, Norwegian Institute for Water Research, 0349 Oslo, Norway
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Institute of Environmental Engineering, Poznan University of Technology, 60965 Poznan, Poland
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National Reference Center for Hydrobiology, Public Health Authority of the Slovak Republic, 82645 Bratislava, Slovakia
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School of Pharmacy and Life Sciences, Robert Gordon University, Aberdeen AB10 7GJ, UK
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Department of Biology, Sakarya University, 54187 Sakarya, Turkey
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Faculty of Natural Sciences and Mathematics, SS Cyril and Methodius University, 1000 Skopje, Macedonia
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Department for Ecotoxicology, Teaching Institute of Public Health of Primorje-Gorski Kotar County, 51000 Rijeka, Croatia
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Institute of Technology, The State University of Applied Sciences, 82300 Elblag, Poland
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Department of Biological and Environmental Science, University of Jyväskylä, 40014 Jyväskylä, Finland
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Departamento de Sistemática e Ecologia, Universidade Federal da Paraíba, 58059-970 Paraíba, Brasil
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Department of Civil Engineering, University of A Coruña, 15192 A Coruña, Spain
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Department of Evolutionary Biology, Ecology, and Environmental Sciences, University of Barcelona, 08028 Barcelona, Spain
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Department of Hydrobiology, University of Bialystok, 15245 Bialystok, Poland
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Institute of Environmental Protection and Engineering, University of Bielsko-Biala, 43309 Bielsko-Biala, Poland
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Department of Biology, University of Cádiz, 11510 Puerto Real, Cádiz, Spain
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Department of Forest Engineering, University of Cankiri Karatekin, 18200 Cankiri, Turkey
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Freshwater Biological Laboratory, Department of Biology, University of Copenhagen, 2100 Copenhagen, Denmark
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Department of Marine Biotechnology, University of Gdansk, 81378 Gdynia, Poland
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Department of Ecology, University of Granada, 18071 Granada, Spain
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Lammi Biological Station, University of Helsinki, 16900 Lammi, Finland
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Department of Animal Biology, Plant Biology and Ecology, University of Jaen, 23701 Jaen, Spain
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Department of Hydrobiology and Protection of Ecosystems, University of Life Sciences in Lublin, 20262 Lublin, Poland
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Instituto Dom Luiz, University of Lisbon, 1749016 Lisbon, Portugal
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Institute of Earth Sciences Jaume Almera, ICTJA, CSIC, 08028 Barcelona, Spain
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Department of Ecology, University of Malaga, 29071 Malaga, Spain
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Centro de Investigacións Cientificas Avanzadas (CICA), Facultade de Ciencias, Universidade da Coruña, 15071 A Coruña, Spain
79
Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, 46980 Paterna Valencia, Spain
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Department of Microbiology and Ecology, University of Valencia, 46100 Burjassot, Spain
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Department of Water Protection Engineering, University of Warmia and Mazury, 10-720 Olsztyn, Poland
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Department of Tourism, Recreation and Ecology, University of Warmia and Mazury, 10-720 Olsztyn, Poland
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Faculty of Biology, University of Warsaw, 02-096 Warsaw, Poland
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Department of Plant Ecology and Environmental Conservation, Faculty of Biology, University of Warsaw, 02-089 Warsaw, Poland
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Department of Biology, Faculty of Science, University of Zagreb, 10000 Zagreb, Croatia
86
Department of Environmental Improvement, Faculty of Civil and Environmental Engineering, Warsaw University of Life Sciences—SGGW, 02-787 Warsaw, Poland
87
Department of Hydraulic Engineering, Faculty of Civil and Environmental Engineering, Warsaw University of Life Sciences—SGGW, 02-787 Warsaw, Poland
88
Institute of Marine Sciences, Marine Biology and Fisheries, Middle East Technical University, 06800 Ankara, Turkey
89
Society for the Protection of Prespa, 53077 Agios Germanos, Greece
90
Institute for Water and Wetland Research, Department of Aquatic Ecology and Environmental Biology, Radboud University Nijmegen, 6525 AJ Nijmegen, The Netherlands
91
Tartu Observatory, Faculty of Science and Technology, University of Tartu, 61602 Tartu, Estonia
92
Institute of Biochemistry and Biology, Potsdam University, 14469 Potsdam, Germany
93
Institute of Marine Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC 28557, USA
94
Department of Biological Sciences, Virginia Tech, Blacksburg, VA 24061, USA
*
Author to whom correspondence should be addressed.
Received: 15 February 2018 / Revised: 27 March 2018 / Accepted: 29 March 2018 / Published: 13 April 2018
Full-Text   |   PDF [16409 KB, uploaded 3 May 2018]   |  

Abstract

Insight into how environmental change determines the production and distribution of cyanobacterial toxins is necessary for risk assessment. Management guidelines currently focus on hepatotoxins (microcystins). Increasing attention is given to other classes, such as neurotoxins (e.g., anatoxin-a) and cytotoxins (e.g., cylindrospermopsin) due to their potency. Most studies examine the relationship between individual toxin variants and environmental factors, such as nutrients, temperature and light. In summer 2015, we collected samples across Europe to investigate the effect of nutrient and temperature gradients on the variability of toxin production at a continental scale. Direct and indirect effects of temperature were the main drivers of the spatial distribution in the toxins produced by the cyanobacterial community, the toxin concentrations and toxin quota. Generalized linear models showed that a Toxin Diversity Index (TDI) increased with latitude, while it decreased with water stability. Increases in TDI were explained through a significant increase in toxin variants such as MC-YR, anatoxin and cylindrospermopsin, accompanied by a decreasing presence of MC-LR. While global warming continues, the direct and indirect effects of increased lake temperatures will drive changes in the distribution of cyanobacterial toxins in Europe, potentially promoting selection of a few highly toxic species or strains. View Full-Text
Keywords: microcystin; anatoxin; cylindrospermopsin; temperature; direct effects; indirect effects; spatial distribution; European Multi Lake Survey microcystin; anatoxin; cylindrospermopsin; temperature; direct effects; indirect effects; spatial distribution; European Multi Lake Survey
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Mantzouki, E.; Lürling, M.; Fastner, J.; de Senerpont Domis, L.; Wilk-Woźniak, E.; Koreivienė, J.; Seelen, L.; Teurlincx, S.; Verstijnen, Y.; Krztoń, W.; Walusiak, E.; Karosienė, J.; Kasperovičienė, J.; Savadova, K.; Vitonytė, I.; Cillero-Castro, C.; Budzyńska, A.; Goldyn, R.; Kozak, A.; Rosińska, J.; Szeląg-Wasielewska, E.; Domek, P.; Jakubowska-Krepska, N.; Kwasizur, K.; Messyasz, B.; Pełechata, A.; Pełechaty, M.; Kokocinski, M.; García-Murcia, A.; Real, M.; Romans, E.; Noguero-Ribes, J.; Duque, D.P.; Fernández-Morán, E.; Karakaya, N.; Häggqvist, K.; Demir, N.; Beklioğlu, M.; Filiz, N.; Levi, E.E.; Iskin, U.; Bezirci, G.; Tavşanoğlu, Ü.N.; Özhan, K.; Gkelis, S.; Panou, M.; Fakioglu, Ö.; Avagianos, C.; Kaloudis, T.; Çelik, K.; Yilmaz, M.; Marcé, R.; Catalán, N.; Bravo, A.G.; Buck, M.; Colom-Montero, W.; Mustonen, K.; Pierson, D.; Yang, Y.; Raposeiro, P.M.; Gonçalves, V.; Antoniou, M.G.; Tsiarta, N.; McCarthy, V.; Perello, V.C.; Feldmann, T.; Laas, A.; Panksep, K.; Tuvikene, L.; Gagala, I.; Mankiewicz-Boczek, J.; Yağcı, M.A.; Çınar, Ş.; Çapkın, K.; Yağcı, A.; Cesur, M.; Bilgin, F.; Bulut, C.; Uysal, R.; Obertegger, U.; Boscaini, A.; Flaim, G.; Salmaso, N.; Cerasino, L.; Richardson, J.; Visser, P.M.; Verspagen, J.M.H.; Karan, T.; Soylu, E.N.; Maraşlıoğlu, F.; Napiórkowska-Krzebietke, A.; Ochocka, A.; Pasztaleniec, A.; Antão-Geraldes, A.M.; Vasconcelos, V.; Morais, J.; Vale, M.; Köker, L.; Akçaalan, R.; Albay, M.; Špoljarić Maronić, D.; Stević, F.; Žuna Pfeiffer, T.; Fonvielle, J.; Straile, D.; Rothhaupt, K.-O.; Hansson, L.-A.; Urrutia-Cordero, P.; Bláha, L.; Geriš, R.; Fránková, M.; Koçer, M.A.T.; Alp, M.T.; Remec-Rekar, S.; Elersek, T.; Triantis, T.; Zervou, S.-K.; Hiskia, A.; Haande, S.; Skjelbred, B.; Madrecka, B.; Nemova, H.; Drastichova, I.; Chomova, L.; Edwards, C.; Sevindik, T.O.; Tunca, H.; Önem, B.; Aleksovski, B.; Krstić, S.; Vucelić, I.B.; Nawrocka, L.; Salmi, P.; Machado-Vieira, D.; de Oliveira, A.G.; Delgado-Martín, J.; García, D.; Cereijo, J.L.; Gomà, J.; Trapote, M.C.; Vegas-Vilarrúbia, T.; Obrador, B.; Grabowska, M.; Karpowicz, M.; Chmura, D.; Úbeda, B.; Gálvez, J.Á.; Özen, A.; Christoffersen, K.S.; Warming, T.P.; Kobos, J.; Mazur-Marzec, H.; Pérez-Martínez, C.; Ramos-Rodríguez, E.; Arvola, L.; Alcaraz-Párraga, P.; Toporowska, M.; Pawlik-Skowronska, B.; Niedźwiecki, M.; Pęczuła, W.; Leira, M.; Hernández, A.; Moreno-Ostos, E.; Blanco, J.M.; Rodríguez, V.; Montes-Pérez, J.J.; Palomino, R.L.; Rodríguez-Pérez, E.; Carballeira, R.; Camacho, A.; Picazo, A.; Rochera, C.; Santamans, A.C.; Ferriol, C.; Romo, S.; Soria, J.M.; Dunalska, J.; Sieńska, J.; Szymański, D.; Kruk, M.; Kostrzewska-Szlakowska, I.; Jasser, I.; Žutinić, P.; Gligora Udovič, M.; Plenković-Moraj, A.; Frąk, M.; Bańkowska-Sobczak, A.; Wasilewicz, M.; Özkan, K.; Maliaka, V.; Kangro, K.; Grossart, H.-P.; Paerl, H.W.; Carey, C.C.; Ibelings, B.W. Temperature Effects Explain Continental Scale Distribution of Cyanobacterial Toxins. Toxins 2018, 10, 156.

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