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1. Temperature Effects Explain Continental Scale Distribution of Cyanobacterial Toxins

Author

Evanthia Mantzouki, Miquel Lürling, Jutta Fastner, Lisette de Senerpont Domis, Elżbieta Wilk-Woźniak, Judita Koreivienė, Laura Seelen, Sven Teurlincx, Yvon Verstijnen, Wojciech Krztoń, Edward Walusiak, Jūratė Karosienė, Jūratė Kasperovičienė, Ksenija Savadova, Irma Vitonytė, Carmen Cillero-Castro, Agnieszka Budzyńska, Ryszard Goldyn, Anna Kozak, Joanna Rosińska, Elżbieta Szeląg-Wasielewska, Piotr Domek, Natalia Jakubowska-Krepska, Kinga Kwasizur, Beata Messyasz, Aleksandra Pełechata, Mariusz Pełechaty, Mikolaj Kokocinski, Ana García-Murcia, Monserrat Real, Elvira Romans, Jordi Noguero-Ribes, David Parreño Duque, Elísabeth Fernández-Morán, Nusret Karakaya, Kerstin Häggqvist, Nilsun Demir, Meryem Beklioğlu, Nur Filiz, Eti E. Levi, Uğur Iskin, Gizem Bezirci, Ülkü Nihan Tavşanoğlu, Koray Özhan, Spyros Gkelis, Manthos Panou, Özden Fakioglu, Christos Avagianos, Triantafyllos Kaloudis, Kemal Çelik, Mete Yilmaz, Rafael Marcé, Nuria Catalán, Andrea G. Bravo, Moritz Buck, William Colom-Montero, Kristiina Mustonen, Don Pierson, Yang Yang, Pedro M. Raposeiro, Vítor Gonçalves, Maria G. Antoniou, Nikoletta Tsiarta, Valerie McCarthy, Victor C. Perello, Tõnu Feldmann, Alo Laas, Kristel Panksep, Lea Tuvikene, Ilona Gagala, Joana Mankiewicz-Boczek, Meral Apaydın Yağcı, Şakir Çınar, Kadir Çapkın, Abdulkadir Yağcı, Mehmet Cesur, Fuat Bilgin, Cafer Bulut, Rahmi Uysal, Ulrike Obertegger, Adriano Boscaini, Giovanna Flaim, Nico Salmaso, Leonardo Cerasino, Jessica Richardson, Petra M. Visser, Jolanda M. H. Verspagen, Tünay Karan, Elif Neyran Soylu, Faruk Maraşlıoğlu, Agnieszka Napiórkowska-Krzebietke, Agnieszka Ochocka, Agnieszka Pasztaleniec, Ana M. Antão-Geraldes, Vitor Vasconcelos, João Morais, Micaela Vale, Latife Köker, Reyhan Akçaalan, Meriç Albay, Dubravka Špoljarić Maronić, Filip Stević, Tanja Žuna Pfeiffer, Jeremy Fonvielle, Dietmar Straile, Karl-Otto Rothhaupt, Lars-Anders Hansson, Pablo Urrutia-Cordero, Luděk Bláha, Rodan Geriš, Markéta Fránková, Mehmet Ali Turan Koçer, Mehmet Tahir Alp, Spela Remec-Rekar, Tina Elersek, Theodoros Triantis, Sevasti-Kiriaki Zervou, Anastasia Hiskia, Sigrid Haande, Birger Skjelbred, Beata Madrecka, Hana Nemova, Iveta Drastichova, Lucia Chomova, Christine Edwards, Tuğba Ongun Sevindik, Hatice Tunca, Burçin Önem, Boris Aleksovski, Svetislav Krstić, Itana Bokan Vucelić, Lidia Nawrocka, Pauliina Salmi, Danielle Machado-Vieira, Alinne Gurjão de Oliveira, Jordi Delgado-Martín, David García, Jose Luís Cereijo, Joan Gomà, Mari Carmen Trapote, Teresa Vegas-Vilarrúbia, Biel Obrador, Magdalena Grabowska, Maciej Karpowicz, Damian Chmura, Bárbara Úbeda, José Ángel Gálvez, Arda Özen, Kirsten Seestern Christoffersen, Trine Perlt Warming, Justyna Kobos, Hanna Mazur-Marzec, Carmen Pérez-Martínez, Eloísa Ramos-Rodríguez, Lauri Arvola, Pablo Alcaraz-Párraga, Magdalena Toporowska, Barbara Pawlik-Skowronska, Michał Niedźwiecki, Wojciech Pęczuła, Manel Leira, Armand Hernández, Enrique Moreno-Ostos, José María Blanco, Valeriano Rodríguez, Jorge Juan Montes-Pérez, Roberto L. Palomino, Estela Rodríguez-Pérez, Rafael Carballeira, Antonio Camacho, Antonio Picazo, Carlos Rochera, Anna C. Santamans, Carmen Ferriol, Susana Romo, Juan Miguel Soria, Julita Dunalska, Justyna Sieńska, Daniel Szymański, Marek Kruk, Iwona Kostrzewska-Szlakowska, Iwona Jasser, Petar Žutinić, Marija Gligora Udovič, Anđelka Plenković-Moraj, Magdalena Frąk, Agnieszka Bańkowska-Sobczak, Michał Wasilewicz, Korhan Özkan, Valentini Maliaka, Kersti Kangro, Hans-Peter Grossart, Hans W. Paerl, Cayelan C. Carey, and Bas W. Ibelings

Subjects
microcystin, anatoxin, cylindrospermopsin, temperature, direct effects, indirect effects, spatial distribution, European Multi Lake Survey, Medicine
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.

Published
2018
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2. Stratification strength and light climate explain variation in chlorophyll a at the continental scale in a European multilake survey in a heatwave summer

Author

Christine Edwards, Yang Yang, Kinga Kwasizur, Agnieszka Napiórkowska-Krzebietke, Jeremy Fonvielle, David Parreño Duque, Mari Carmen Trapote, Triantafyllos Kaloudis, Magdalena Toporowska, Koray Ozhan, Marek Kruk, Pablo Urrutia-Cordero, Cayelan C. Carey, Joana Mankiewicz-Boczek, Judita Koreivienė, Andrea G. Bravo, Hana Nemova, Abdulkadir Yağcı, Eloísa Ramos-Rodríguez, Michał Niedźwiecki, Petar Žutinić, Carmen Cillero-Castro, Moritz Buck, Rodan Geriš, Maria G. Antoniou, Daphne Donis, Tunay Karan, Fuat Bilgin, Agnieszka Ochocka, Lea Tuvikene, Hans-Peter Grossart, Christos Avagianos, Boris Aleksovski, Roberto L. Palomino, Trine Perlt Warming, Kersti Kangro, Justyna Sieńska, Jessica Richardson, Meriç Albay, Rahmi Uysal, Elísabeth Fernández-Morán, João Morais, Valentini Maliaka, Daniel Szymański, Irma Vitonytė, Vítor Gonçalves, Burçin Önem, Jordi Noguero-Ribes, Mikołaj Kokociński, Biel Obrador, Edward Walusiak, Lisette N. de Senerpont Domis, Reyhan Akçaalan, Wojciech Pęczuła, Juan M. Soria, Kadir Çapkın, Meryem Beklioglu, J. A. Gálvez, Korhan Özkan, Petra M. Visser, Özden Fakioglu, Şakir Çinar, Leonardo Cerasino, Dominic Vachon, Victor C. Perello, Magdalena Grabowska, Laura Seelen, David García, Jolanda M. H. Verspagen, Svetislav Krstić, Sevasti-Kiriaki Zervou, Adriano Boscaini, Donald C. Pierson, Kerstin Häggqvist, Carmen Ferriol, Iwona Jasser, Anastasia Hiskia, Miquel Lürling, Elżbieta Wilk-Woźniak, Julita Dunalska, Núria Catalán, José María Blanco, Mehmet Ali Turan Koçer, Valerie McCarthy, Köker Latife, Jorge Juan Montes-Pérez, Itana Bokan Vucelić, Anđelka Plenković-Moraj, Tuğba Ongun Sevindik, Beata Madrecka-Witkowska, Kirsten Christoffersen, Pauliina Salmi, Estela Rodríguez-Pérez, Joanna Rosińska, Barbara Pawlik-Skowrońska, Ilona Gagala-Borowska, Wojciech Krztoń, Elvira Romans, Hans W. Paerl, Spela Remec-Rekar, Magdalena Frąk, Mete Yilmaz, Carmen Pérez-Martínez, Susana Romo, Nur Filiz, Luděk Bláha, Karl . Rothhaupt, Enrique Moreno-Ostos, Markéta Fránková, Iwona Kostrzewska-Szlakowska, Nikoletta Tsiarta, Mehmet Tahir Alp, Joan Gomà, Jūratė Karosienė, Agnieszka Pasztaleniec, Vitor Vasconcelos, Jūratė Kasperovičienė, Filip Stević, Hanna Mazur-Marzec, Maria J. van Herk, Alinne Gurjão de Oliveira, Agnieszka Bańkowska-Sobczak, Sigrid Haande, Ana Maria Antão-Geraldes, Birger Skjelbred, Jose Luis Cereijo, Anna Kozak, Uğur Işkın, Manthos Panou, Agnieszka Budzyńska, Faruk Maraşlıoğlu, Iveta Drastichova, Tanja Žuna Pfeiffer, Ksenija Savadova-Ratkus, R. Carballeira, Alo Laas, Giovanna Flaim, Lucia Chomova, Tina Elersek, Lauri Arvola, Dubravka Špoljarić Maronić, Justyna Kobos, Lars-Anders Hansson, Beata Messyasz, Daniel Frank Mcginnis, Valeriano Rodríguez, Monserrat Real, Spyros Gkelis, Nilsun Demir, Evanthia Mantzouki, Pablo Alcaraz-Párraga, Elżbieta Szeląg-Wasielewska, Micaela Vale, Carlos Rochera, Meral Apaydın Yağcı, Piotr Domek, Jordi Delgado-Martín, Tõnu Feldmann, Michał Wasilewicz, Hatice Tunca, Ülkü Nihan Tavşanoğlu, Marija Gligora Udovič, Ulrike Obertegger, Bárbara Úbeda, Elif Neyran Soylu, Aleksandra Pełechata, Kristiina Mustonen, Danielle Machado-Vieira, Hannah Cromie, Eti E. Levi, Maciej Karpowicz, Nusret Karakaya, Cafer Bulut, Kemal Celik, Lidia Nawrocka, Natalia Jakubowska-Krepska, Armand Hernández, Anna C. Santamans, Sven Teurlincx, Damian Chmura, Arda Özen, Pedro M. Raposeiro, Nico Salmaso, Bastiaan Willem Ibelings, Gizem Bezirci, Kristel Panksep, Antonio Camacho, Theodoros M. Triantis, Antonio Picazo, William Colom-Montero, Teresa Vegas-Vilarrúbia, Manel Leira, Ana García-Murcia, Mariusz Pełechaty, Yvon Verstijnen, Irene Gallego, Mehmet Cesur, Ryszard Gołdyn, Yılmaz, Mete, Ministerio de Ciencia, Innovación y Universidades (España), National Science Foundation (US), AKWA, Aquatic Ecology (AqE), Centre for Limnology (NIOO / CL), Freshwater and Marine Ecology (IBED, FNWI), IBED (FNWI), Fen Edebiyat Fakültesi, Lammi Biological Station, BAİBÜ, Mühendislik Fakültesi, Çevre Mühendisliği Bölümü, and Karakaya, Nusret

Subjects
0106 biological sciences, Temperate, Aquatic Ecology and Water Quality Management, 010504 meteorology & atmospheric sciences, Chlorophyll a, CYANOBACTERIAL BLOOMS, Mediterranean, Oceanography, 01 natural sciences, Filamentous cyanobacteria, PHYTOPLANKTON DYNAMICS, Klimatforskning, Photosystem-II, Climate change, Phytoplankton biomass, chlorophyll, Temperature anomaly, Phytoplankton Dynamics, media_common, Filamentous Cyanobacteria, Ecology, plankton, TEMPERATE, Dissolved Organic-Matter, Plan_S-Compliant_NO, Art, Eutrophication, Biological Sciences, 6. Clean water, Europe, kesä, international, EUTROPHICATION, 1181 Ecology, evolutionary biology, articles, lämpötila, GREEN-ALGAE, Natural Sciences, LAKES, SHALLOW, klorofylli, Thermal stratificaiton, Climate Research, media_common.quotation_subject, multilake survey, Cyanobacterial Blooms, Aquatic Science, phytoplankton, European lakes, climate change, large scale, light, stratification, nutrients, järvet, Heat wave, limnologia, PHOTOSYSTEM-II, Settore BIO/07 - ECOLOGIA, ddc:570, Life Science, biomassa (ekologia), 0105 earth and related environmental sciences, Ekologi, Green-Algae, WIMEK, FILAMENTOUS CYANOBACTERIA, 010604 marine biology & hydrobiology, ilmastonmuutokset, mikrolevät, Aquatische Ecologie en Waterkwaliteitsbeheer, Surface temperature, Lakes, Shallow, 13. Climate action, DISSOLVED ORGANIC-MATTER, Phytoplankton, kerrostuneisuus, Humanities, valo
Abstract

The authors acknowledge COST Action ES 1105 "CYANOCOST Cyanobacterial blooms and toxins in water resources: Occurrence impacts and management" and COST Action Global Change Biology ES 1201 NETLAKE -Networking Lake Observatories in Europe" for contributing to this study through networking and knowledge sharing with European experts in the field. We acknowledge the members of the Global Lake Ecological Observatory Network (GLEON) for their collaborative spirit and enthusiasm that inspired the grassroots effort of the EMLS. E.M. was supported by a grant from the Swiss State Secretariat for Education, Research and Innovation to Bas Ibelings and by supplementary funding from University of Geneva. We thank Wendy Beekman for the nutrient analysis. We thank Pieter Slot for assisting with the pigment analysis. We thank Dr. Ian Jones for valuable feedback on an earlier version of the manuscript. We thank the Leibniz Institute of Freshwater Ecology and the Aquatic Microbial Ecology Group for logistic and technical support of J. Fonvielle and H.-P. Grossart, and the Leibniz Association for financial support. H.P. was supported by the US National Science Foundation (1840715, 1831096). A.C.'s work was funded by the Spanish Agencia Estatal de Investigacion and EU funds through the project CLIMAWET (CGL2015-69557-R). The collection of data for Lough Erne and Lough Neagh were funded by the Department of Agriculture, Environment and Rural Affairs, Northern Ireland. We are grateful to Kristiina Vuorio from the Freshwater Centre of the Finnish Environment institute for her help in organizing, collecting and analysing samples by the University of Jyvaskyla and to Gerald Dorflinger from the Water Development Department of Cyprus for his assistance with the sampling in Cyprus and for granting the CUT team permission to use WDD's equipment. Finally, we would like to thank the numerous other assistants that helped realizing each local survey. Open access funding provided by Universite de Geneve., To determine the drivers of phytoplankton biomass, we collected standardized morphometric, physical, and biological data in 230 lakes across the Mediterranean, Continental, and Boreal climatic zones of the European continent. Multilinear regression models tested on this snapshot of mostly eutrophic lakes (median total phosphorus [TP] = 0.06 and total nitrogen [TN] = 0.7 mg L-1), and its subsets (2 depth types and 3 climatic zones), show that light climate and stratification strength were the most significant explanatory variables for chlorophyll a (Chl a) variance. TN was a significant predictor for phytoplankton biomass for shallow and continental lakes, while TP never appeared as an explanatory variable, suggesting that under high TP, light, which partially controls stratification strength, becomes limiting for phytoplankton development. Mediterranean lakes were the warmest yet most weakly stratified and had significantly less Chl a than Boreal lakes, where the temperature anomaly from the long-term average, during a summer heatwave was the highest (+4 degrees C) and showed a significant, exponential relationship with stratification strength. This European survey represents a summer snapshot of phytoplankton biomass and its drivers, and lends support that light and stratification metrics, which are both affected by climate change, are better predictors for phytoplankton biomass in nutrient-rich lakes than nutrient concentrations and surface temperature., European Cooperation in Science and Technology (COST) ES 1105 ES 1201, Swiss State Secretariat for Education, Research and Innovation, University of Geneva, Leibniz Association, National Science Foundation (NSF) 1840715 1831096, Spanish Agencia Estatal de Investigacion, European Commission CGL2015-69557-R, Department of Agriculture, Environment and Rural Affairs, Northern Ireland

Published
2021

3. Temperature effects explain continental scale distribution of cyanobacterial toxins

Author

Sigrid Haande, Christos Avagianos, Vítor Gonçalves, Lisette N. de Senerpont Domis, Carlos Rochera, Ana García-Murcia, Kerstin Häggqvist, Reyhan Akçaalan, Jordi Noguero-Ribes, Mariusz Pełechaty, Wojciech Krztoń, Hans-Peter Grossart, Jutta Fastner, Bárbara Úbeda, Wojciech Pęczuła, Nur Filiz, Justyna Kobos, Juan M. Soria, Elif Neyran Soylu, Lars-Anders Hansson, Filip Stević, Luděk Bláha, Hanna Mazur-Marzec, Jolanda M. H. Verspagen, Burçin Önem, Karl-Otto Rothhaupt, Nico Salmaso, Abdulkadir Yağcı, David Parreño Duque, Ksenija Savadova, Nusret Karakaya, Aleksandra Pełechata, Yvon Verstijnen, Carmen Pérez-Martínez, Pauliina Salmi, Gizem Bezirci, Tuğba Ongun Sevindik, Svetislav Krstić, Rahmi Uysal, Laura Seelen, Eloísa Ramos-Rodríguez, Spela Remec-Rekar, Sven Teurlincx, Monserrat Real, Meriç Albay, Donald C. Pierson, Susana Romo, Kristiina Mustonen, Kirsten Christoffersen, Valentini Maliaka, Estela Rodríguez-Pérez, Joanna Rosińska, Nilsun Demir, Mehmet Tahir Alp, Elvira Romans, João Morais, Daniel Szymański, Danielle Machado-Vieira, Damian Chmura, Evanthia Mantzouki, Teresa Vegas-Vilarrúbia, Antonio Picazo, Mikołaj Kokociński, Anastasia Hiskia, Christine Edwards, Yang Yang, Irma Vitonytė, Mehmet Cesur, Agnieszka Bańkowska-Sobczak, Iwona Kostrzewska-Szlakowska, Nikoletta Tsiarta, Anđelka Plenković-Moraj, Miquel Lürling, Ryszard Gołdyn, Kristel Panksep, Kemal Celik, Anna Kozak, Jose Luis Cereijo, Pablo Urrutia-Cordero, Petra M. Visser, Rodan Geriš, Uğur Işkın, Leonardo Cerasino, Kadir Çapkın, Victor C. Perello, Carmen Cillero-Castro, Arda Özen, Manel Leira, Enrique Moreno-Ostos, Şakir Çinar, Agnieszka Budzyńska, Faruk Maraşlıoğlu, Pedro M. Raposeiro, Theodoros M. Triantis, Agnieszka Pasztaleniec, Sevasti-Kiriaki Zervou, Elżbieta Wilk-Woźniak, Edward Walusiak, Kersti Kangro, Jorge Juan Montes-Pérez, Triantafyllos Kaloudis, Mari Carmen Trapote, Pablo Alcaraz-Párraga, José María Blanco, Marek Kruk, Hans W. Paerl, Lidia Nawrocka, Meryem Beklioglu, Antonio Camacho, Moritz Buck, Biel Obrador, Ilona Gagala, Lauri Arvola, Elżbieta Szeląg-Wasielewska, Petar Žutinić, Giovanna Flaim, Núria Catalán, R. Carballeira, Alinne Gurjão de Oliveira, Magdalena Frąk, Alo Laas, Magdalena Grabowska, Dubravka Špoljarić Maronić, Meral Apaydın Yağcı, Itana Bokan Vucelić, Ana Maria Antão-Geraldes, Tõnu Feldmann, Natalia Jakubowska-Krepska, Trine Perlt Warming, Armand Hernández, Anna C. Santamans, Fuat Bilgin, Cayelan C. Carey, Joana Mankiewicz-Boczek, Elísabeth Fernández-Morán, Mete Yilmaz, Iwona Jasser, Boris Aleksovski, Michał Wasilewicz, Agnieszka Ochocka, David García, Lea Tuvikene, Roberto L. Palomino, B.W. Ibelings, Hatice Tunca, Birger Skjelbred, Joan Gomà, Jūratė Karosienė, Maria G. Antoniou, Vitor Vasconcelos, Mehmet Ali Turan Koçer, Eti E. Levi, Markéta Fránková, Beata Madrecka, Barbara Pawlik-Skowrońska, Jeremy Fonvielle, Korhan Özkan, Maciej Karpowicz, Özden Fakioglu, Lucia Chomova, Magdalena Toporowska, Ülkü Nihan Tavşanoğlu, Jūratė Kasperovičienė, Latife Köker, Kinga Kwasizur, Koray Ozhan, Valeriano Rodríguez, William Colom-Montero, Ulrike Obertegger, Micaela Vale, Spyros Gkelis, Michał Niedźwiecki, Tunay Karan, Piotr Domek, Judita Koreivienė, Andrea G. Bravo, Justyna Sieńska, Jessica Richardson, Hana Nemova, Cafer Bulut, Jordi Delgado-Martín, Tanja Žuna Pfeiffer, Marija Gligora Udovič, Manthos Panou, Dietmar Straile, Rafael Marcé, Valerie McCarthy, Iveta Drastichova, Agnieszka Napiórkowska-Krzebietke, J. A. Gálvez, Tina Elersek, Beata Messyasz, Adriano Boscaini, Carmen Ferriol, Julita Dunalska, Freshwater and Marine Ecology (IBED, FNWI), BAİBÜ, Mühendislik Fakültesi, Çevre Mühendisliği Bölümü, Karakaya, Nusret, Universitat de Barcelona, Fakülteler, Fen - Edebiyat Fakültesi, Biyoloji Bölümü, Soylu, Elif Neyran, European Cooperation in Science and Technology, Université de Genève, Tokat Gaziosmanpaşa Üniversitesi, Lammi Biological Station, Doctoral Programme in Atmospheric Sciences, CIIMAR - Centro Interdisciplinar de Investigação Marinha e Ambiental, Yılmaz, Mete, Institute of Agricultural and Environmental Sciences, Mantzouki, Evanthia, Ibelings, Bastiaan Willem, Mantzouki, E, Lurling, M, Fastner, J, Domis, LD, Wilk-Wozniak, E, Koreiviene, J, Seelen, L, Teurlincx, S, Verstijnen, Y, Krzton, W, Walusiak, E, Karosiene, J, Kasperoviciene, J, Savadova, K, Vitonyte, I, Cillero-Castro, C, Budzynska, A, Goldyn, R, Kozak, A, Rosinska, J, Szelag-Wasielewska, E, Domek, P, Jakubowska-Krepska, N, Kwasizur, K, Messyasz, B, Pelechata, A, Pelechaty, M, Kokocinski, M, Garcia-Murcia, A, Real, M, Romans, E, Noguero-Ribes, J, Duque, DP, Fernandez-Moran, E, Karakaya, N, Haggqvist, K, Demir, N, Beklioglu, M, Filiz, N, Levi, EE, Iskin, U, Bezirci, G, Tavsanoglu, UN, Ozhan, K, Gkelis, S, Panou, M, Fakioglu, O, Avagianos, C, Kaloudis, T, Celik, K, Yilmaz, M, Marce, R, Catalan, N, Bravo, AG, Buck, M, Colom-Montero, W, Mustonen, K, Pierson, D, Yang, Y, Raposeiro, PM, Goncalves, V, Antoniou, MG, Tsiarta, N, McCarthy, V, Perello, VC, Feldmann, T, Laas, A, Panksep, K, Tuvikene, L, Gagala, I, Mankiewicz-Boczek, J, Yagci, MA, Cinar, S, Capkin, K, Yagci, A, Cesur, M, Bilgin, F, Bulut, C, Uysal, R, Obertegger, U, Boscaini, A, Flaim, G, Salmaso, N, Cerasino, L, Richardson, J, Visser, PM, Verspagen, JMH, Karan, T, Soylu, EN, Maraslioglu, F, Napiorkowska-Krzebietke, A, Ochocka, A, Pasztaleniec, A, Antao-Geraldes, AM, Vasconcelos, V, Morais, J, Vale, M, Koker, L, Akcaalan, R, Albay, M, Maronic, DS, Stevic, F, Pfeiffer, TZ, Fonvielle, J, Straile, D, Rothhaupt, KO, Hansson, LA, Urrutia-Cordero, P, Blaha, L, Geris, R, Frankova, M, Kocer, MAT, Alp, MT, Remec-Rekar, S, Elersek, T, Triantis, T, Zervou, SK, Hiskia, A, Haande, S, Skjelbred, B, Madrecka, B, Nemova, H, Drastichova, I, Chomova, L, Edwards, C, Sevindik, TO, Tunca, H, Onem, B, Aleksovski, B, Krstic, S, Vucelic, IB, Nawrocka, L, Salmi, P, Machado-Vieira, D, de Oliveira, AG, Delgado-Martin, J, Garcia, D, Cereijo, JL, Goma, J, Trapote, MC, Vegas-Vilarrubia, T, Obrador, B, Grabowska, M, Karpowicz, M, Chmura, D, Ubeda, B, Galvez, JA, Ozen, A, Christoffersen, KS, Warming, TP, Kobos, J, Mazur-Marzec, H, Perez-Martinez, C, Ramos-Rodriguez, E, Arvola, L, Alcaraz-Parraga, P, Toporowska, M, Pawlik-Skowronska, B, Niedzwiecki, M, Peczula, W, Leira, M, Hernandez, A, Moreno-Ostos, E, Blanco, JM, Rodriguez, V, Montes-Perez, JJ, Palomino, RL, Rodriguez-Perez, E, Carballeira, R, Camacho, A, Picazo, A, Rochera, C, Santamans, AC, Ferriol, C, Romo, S, Soria, JM, Dunalska, J, Sienska, J, Szymanski, D, Kruk, M, Kostrzewska-Szlakowska, I, Jasser, I, Zutinic, P, Udovic, MG, Plenkovic-Moraj, A, Frak, M, Bankowska-Sobczak, A, Wasilewicz, M, Ozkan, K, Maliaka, V, Kangro, K, Grossart, HP, Paerl, HW, Carey, CC, Ibelings, BW, Sakarya Üniversitesi/Fen-Edebiyat Fakültesi/Biyoloji Bölümü, Ongun Sevindik, Tuğba, Tunca, Hatice, Hitit Üniversitesi, Fen Edebiyat Fakültesi, Biyoloji Bölümü, and Fen Edebiyat Fakültesi

Subjects
light climate, 0106 biological sciences, thermocline, Bacterial toxins, toksiinit, limit of quantitation, Toxines bacterianes, Microcystin-LR, Toxicology, 01 natural sciences, Anatoxin-a, analogs and derivatives, BLOOMS, Direct Effects, uracil, Water Pollutants, chemistry.chemical_classification, Temperatures, FRESH-WATER, latitude, maximum buoyancy frequency, 6. Clean water, climate change, Indirect effects, EUTROPHICATION, microcystin RR, articles, GROWTH, lämpötila, LAKES, microcystin, anatoxin, cylindrospermopsin, temperature, direct effects, indirect effects, spatial distribution, European Multi Lake Survey, epilimnetic temperature, ta1172, cyanobacteria, lakes, climate warming, microcystin, Zoology, Article, water pollutant, MICROCYSTIS-AERUGINOSA, Alkaloids, Settore BIO/07 - ECOLOGIA, NATURAL SCIENCES. Biology, Spatial distribution, Microcystis aeruginosa, Uracil, lake, syanobakteerit, Indirect Effects, liquid chromatography-mass spectrometry, 1172 Environmental sciences, Ekologi, nutrient, 010604 marine biology & hydrobiology, lcsh:R, microbiology, Climatic changes, microcystin LR, Anatoxin, Lakes, Spatial Distribution, chemistry, nodularin, microbial diversity, phytoplankton, ta1181, Cylindrospermopsin, Tropanes, Cyanobacteria, Aquatic Ecology and Water Quality Management, analysis, Health, Toxicology and Mutagenesis, lcsh:Medicine, environmental parameters, 010501 environmental sciences, medicine.disease_cause, nitrogen, chemistry.chemical_compound, sea surface temperature, environmental factor, ddc:550, Canvi climàtic, phosphorus, PRIRODNE ZNANOSTI. Biologija, limit of detection, Ecology, Cyanobacteria Toxins, biology, Temperature, levinneisyys, Nodularin, tropane derivative, Europe, DAPHNIA-MAGNA, İndirect Effects, Direct effects, microbial community, Environmental Monitoring, high performance liquid chromatography, Microcystins, Climate Change, Bacterial Toxins, Microcystin, välittömät oikeusvaikutukset, cyanobacterium, ddc:570, geographic distribution, medicine, bacterial toxin, controlled study, ddc:610, Institut für Biochemie und Biologie, 0105 earth and related environmental sciences, nonhuman, WIMEK, Toxin, longitude, PHYTOPLANKTON ASSEMBLAGES, Aquatic Ecology, NITROGEN AVAILABILITY, anatoxin a, Aquatische Ecologie en Waterkwaliteitsbeheer, biology.organism_classification, Climatic change, CLIMATE, 13. Climate action, response variable, Canvis climàtics
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. © 2018 by the authors. Licensee MDPI, Basel, Switzerland., The authors acknowledge COST Action ES 1105 “CYANOCOST—Cyanobacterial blooms and toxins in water resources: Occurrence impacts and management” and COST Action ES 1201 “NETLAKE—Networking Lake Observatories in Europe” for contributing to this study through networking and knowledge sharing with European experts in the field. Evanthia Mantzouki was supported by a grant from the Swiss State Secretariat for Education, Research and Innovation (SERI) to Bas Ibelings and by supplementary funding from the University of Geneva. We thank Clare Ahnlund, Ena Suarez and Irene Gallego for helping out with the Swiss survey. We thank Wendy Beekman and Els J. Faassen for the nutrient and toxin analysis.

Published
2018

4. A European Multi Lake Survey dataset of environmental variables, phytoplankton pigments and cyanotoxins

Author

Moritz Buck, David García, Nur Filiz, Luděk Bláha, Teresa Vegas-Vilarrúbia, Manel Leira, David Parreño Duque, Donald C. Pierson, Pablo Alcaraz-Párraga, Justyna Kobos, Bárbara Úbeda, Triantafyllos Kaloudis, Elif Neyran Soylu, Eloísa Ramos-Rodríguez, Kerstin Häggqvist, Aleksandra Pełechata, Elżbieta Szeląg-Wasielewska, Meral Apaydın Yağcı, Anna Kozak, Edward Walusiak, Meryem Beklioglu, Monserrat Real, Nusret Karakaya, Carlos Rochera, Iwona Jasser, Kristiina Mustonen, José María Blanco, Delphine Latour, Nilsun Demir, Evanthia Mantzouki, Jutta Fastner, Carmen Cillero-Castro, Danielle Machado-Vieira, Tunay Karan, Jeremy Fonvielle, Kemal Celik, Mehmet Ali Turan Koçer, Miquel Lürling, Rafael Marcé, Dietmar Straile, Valerie McCarthy, Petar Žutinić, Korhan Özkan, Özden Fakioglu, Fuat Bilgin, Maria G. Antoniou, Sarah O'Leary, Itana Bokan Vucelić, Kersti Kangro, Trine Perlt Warming, Hatice Tunca, Kirsten Christoffersen, Lidia Nawrocka, Estela Rodríguez-Pérez, Abdulkadir Yağcı, Justyna Sieńska, Jessica Richardson, Elísabeth Fernández-Morán, Beata Madrecka, Barbara Pawlik-Skowrońska, Hans-Peter Grossart, Petra M. Visser, Leonardo Cerasino, Joanna Rosińska, Ülkü Nihan Tavşanoğlu, Elvira Romans, Boris Aleksovski, Agnieszka Bańkowska-Sobczak, Pauliina Salmi, Latife Köker, Cayelan C. Carey, Magdalena Toporowska, Lauri Arvola, Antonio Picazo, Elisabeth J. Faassen, Cafer Bulut, Joana Mankiewicz-Boczek, William Colom-Montero, Gregory Giuliani, Markéta Fránková, Ulrike Obertegger, Spela Remec-Rekar, Rahmi Uysal, Tanja Žuna Pfeiffer, Sigrid Haande, Jose Luis Cereijo, Victoria Bergkemper, Eilish Beirne, Agnieszka Ochocka, Uğur Işkın, Meriç Albay, Karl-Otto Rothhaupt, Nico Salmaso, Lea Tuvikene, Roberto L. Palomino, Bastiaan Willem Ibelings, Gizem Bezirci, Carmen Pérez-Martínez, Tuğba Ongun Sevindik, Dubravka Špoljarić Maronić, Ana Maria Antão-Geraldes, Jūratė Kasperovičienė, Christos Avagianos, João Morais, Daniel Szymański, Vítor Gonçalves, Susana Romo, Jorge Juan Montes-Pérez, Kristel Panksep, J. A. Gálvez, James B. Campbell, Biel Obrador, Mehmet Cesur, Irma Vitonytė, Andrea Törökné, Hannah Cromie, Tõnu Feldmann, Eti E. Levi, Ryszard Gołdyn, Mikołaj Kokociński, Lisette N. de Senerpont Domis, Kinga Kwasizur, Burçin Önem, Michał Wasilewicz, Magdalena Grabowska, Iwona Kostrzewska-Szlakowska, Mete Yilmaz, Reyhan Akçaalan, Koray Ozhan, Jordi Noguero-Ribes, Antonio Camacho, Giovanna Flaim, Nikoletta Tsiarta, Joan Gomà, Jūratė Karosienė, Elżbieta Wilk-Woźniak, Wojciech Pęczuła, Maciej Karpowicz, Michał Niedźwiecki, Vitor Vasconcelos, Spyros Gkelis, Agnieszka Napiórkowska-Krzebietke, Laura Seelen, Juan M. Soria, Iosif Konstantinou, Kadir Çapkın, Birger Skjelbred, Agnieszka Pasztaleniec, Núria Catalán, Şakir Çinar, Anđelka Plenković-Moraj, Lucia Chomova, Mehmet Tahir Alp, Magdalena Frąk, Theodoros M. Triantis, Adriano Boscaini, Carmen Ferriol, Judita Koreivienė, Julita Dunalska, Andrea G. Bravo, Hana Nemova, Ilona Gagala, Ana García-Murcia, Mariusz Pełechaty, Enrique Moreno-Ostos, Yvon Verstijnen, Lars-Anders Hansson, Ksenija Savadova, Jolanda M. H. Verspagen, Svetislav Krstić, Anastasia Hiskia, Valeriano Rodríguez, Wojciech Krztoń, Filip Stević, Hanna Mazur-Marzec, Agnieszka Budzyńska, Faruk Maraşlıoğlu, R. Carballeira, Alo Laas, Valentini Maliaka, Micaela Vale, Piotr Domek, Jordi Delgado-Martín, Marija Gligora Udovič, Manthos Panou, Iveta Drastichova, Tina Elersek, Sven Teurlincx, Damian Chmura, Beata Messyasz, Arda Özen, Pedro M. Raposeiro, E. Emiel van Loon, Natalia Jakubowska-Krepska, Armand Hernández, Anna C. Santamans, Christine Edwards, Yang Yang, Pablo Urrutia-Cordero, Rodan Geriš, Victor C. Perello, Sevasti-Kiriaki Zervou, Hans W. Paerl, Alinne Gurjão de Oliveira, Mari Carmen Trapote, Marek Kruk, Tokat Gaziosmanpaşa Üniversitesi, Theoretical and Computational Ecology (IBED, FNWI), Freshwater and Marine Ecology (IBED, FNWI), Havran Meslek Yüksekokulu, CIIMAR - Centro Interdisciplinar de Investigação Marinha e Ambiental, Antoniou, Maria-Paraskevi, Giuliani, Gregory, Ibelings, Bastiaan Willem, European Cooperation in Science and Technology, Hernández, Armand, School of Biology, Aristotle University of Thessaloniki, Masaryk University [Brno] (MUNI), Lammi Biological Station (LBS), University of Helsinki, German Federal Environmental Agency / Umweltbundesamt (UBA), Limnological Institute, University of Konstanz, Fdn Edmund Mach, IASMA Research and Innovation Centre, Department of Biology, Faculty of Sciences, Instituto de Engenharia de Sistemas e Computadores Investigação e Desenvolvimento em Lisboa (INESC-ID), Instituto Superior Técnico, Universidade Técnica de Lisboa (IST)-Instituto de Engenharia de Sistemas e Computadores (INESC), University of Strathclyde [Glasgow], Instituto Catalán de Investigación del Agua - ICRA (SPAIN) (ICRA), Mälardalen University (MDH), Freiburg Institute for Advanced Studies-LifeNet, Albert-Ludwigs-Universität Freiburg, Department of Computer Science and Engineering [San Diego] (CSE-UCSD), University of California [San Diego] (UC San Diego), University of California-University of California, Department of Environmental Sciences [Wageningen], Wageningen University and Research [Wageningen] (WUR), Environmental Sciences, Laboratoire Microorganismes : Génome et Environnement (LMGE), Université Clermont Auvergne [2017-2020] (UCA [2017-2020])-Centre National de la Recherche Scientifique (CNRS), Universitat de Barcelona, Fen Edebiyat Fakültesi, BAİBÜ, Mühendislik Fakültesi, Çevre Mühendisliği Bölümü, Karakaya, Nusret, Hernández, Armand [0000-0001-7245-9863], Hitit Üniversitesi, Fen Edebiyat Fakültesi, Biyoloji Bölümü, AKWA, Aquatic Ecology (AqE), Helsingin yliopisto = Helsingfors universitet = University of Helsinki, Department of Computer Science and Engineering [Univ California San Diego] (CSE - UC San Diego), and University of California (UC)-University of California (UC)

Subjects
Ecologia dels llacs, Data Descriptor, Water resources, Aquatic Ecology and Water Quality Management, thermocline, 010504 meteorology & atmospheric sciences, vesien tila, phytoplankton pigments, 010501 environmental sciences, 01 natural sciences, Ecosystem services, ympäristön tila, BU Contaminants & Toxins, Environmental monitoring, Limnology, lakes, ddc:550, Canvi climàtic, Geosciences, Multidisciplinary, Survey, ComputingMilieux_MISCELLANEOUS, ddc:333.7-333.9, Climate-Change, Europe Lakes, Environmental resource management, [Belirlenecek], Climate-change ecology, plankton, Eutrophication, 6. Clean water, Computer Science Applications, Europe, Disparate system, data, international, Bloom, Statistics, Probability and Uncertainty, Europa, Environmental Monitoring, Information Systems, environmental variables, Statistics and Probability, Biological pigments, Fitoplàncton, Climate Change, Cyanotoxins, ta1172, BU Contaminanten & Toxines, Climate change, observation design, Library and Information Sciences, Cyanobacteria, järvet, Education, European Multi Lake, cyanotoxins, ddc:570, Life Science, Ecosystem, 14. Life underwater, database creation objective, syanobakteerit, 0105 earth and related environmental sciences, WIMEK, business.industry, data analysis objective, nutrient, muuttujat, Pigments, Biological, 15. Life on land, Climatic changes, dataset, phytoplankton, pigments, mikrolevät, Aquatische Ecologie en Waterkwaliteitsbeheer, Environmental variables, Phytoplankton pigments, Multidisciplinär geovetenskap, Climatic change, Lakes, 13. Climate action, Nutrient pollution, Phytoplankton, Environmental science, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, business, Lake ecology, Canvis climàtics, Waters
Abstract

Under ongoing climate change and increasing anthropogenic activity, which continuously challenge ecosystem resilience, an in-depth understanding of ecological processes is urgently needed. Lakes, as providers of numerous ecosystem services, face multiple stressors that threaten their functioning. Harmful cyanobacterial blooms are a persistent problem resulting from nutrient pollution and climate-change induced stressors, like poor transparency, increased water temperature and enhanced stratification. Consistency in data collection and analysis methods is necessary to achieve fully comparable datasets and for statistical validity, avoiding issues linked to disparate data sources. The European Multi Lake Survey (EMLS) in summer 2015 was an initiative among scientists from 27 countries to collect and analyse lake physical, chemical and biological variables in a fully standardized manner. This database includes in-situ lake variables along with nutrient, pigment and cyanotoxin data of 369 lakes in Europe, which were centrally analysed in dedicated laboratories. Publishing the EMLS methods and dataset might inspire similar initiatives to study across large geographic areas that will contribute to better understanding lake responses in a changing environment., The authors acknowledge COST Action ES 1105 “CYANOCOST – Cyanobacterial blooms and toxins in water resources: Occurrence impacts and management” and COST Action ES 1201 “NETLAKE – Networking Lake Observatories in Europe” for contributing to this study through networking and knowledge sharing with European experts in the field. Evanthia Mantzouki was supported by a grant from the Swiss State Secretariat for Education, Research and Innovation (SERI) to Bas Ibelings and by supplementary funding from University of Geneva. We thank Wendy Beekman for the nutrient analysis and the University of Wageningen for covering the costs of this analysis from the personal funding of dr. Miquel Lürling. We thank Pieter Slot for assisting with the pigment analysis and the University of Amsterdam for covering the costs of the analysis through funding from the group of Prof. Jef Huisman and dr. Petra Visser (IBED). We would like to thank the Environmental Data Initiative for covering the cost of archiving the EMLS dataset. We would like to thank the Leibniz Institute of Freshwater Ecology and Inland Fisheries, Dept. of Experimental Limnology and the Aquatic Microbial Ecology Group for logistic and technical support of J. Fonvielle and H.-P. Grossart; and the Leibniz Association for financial support. The collection of data for Lough Erne and Lough Neagh were funded by the Department of Agriculture, Environment and Rural Affairs, Northern Ireland.

Published
2018

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