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2. 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

3. Data Descriptor: A European Multi Lake Survey dataset of environmental variables, phytoplankton pigments and cyanotoxins

Author

Tunca, Hatice, Mantzouki, E, Campbell, J, van Loon, E, Visser, P, Konstantinou, I, Antoniou, M, Giuliani, G, Machado-Vieira, D, de Oliveira, AG, Maronic, DS, Stevic, F, Pfeiffer, TZ, Vucelic, IB, Zutinic, P, Udovic, MG, Plenkovic-Moraj, A, Tsiarta, N, Blaha, L, Geris, R, Frankova, M, Christoffersen, KS, Warming, TP, Feldmann, T, Laas, A, Panksep, K, Tuvikene, L, Kangro, K, Haggqvist, K, Salmi, P, Arvola, L, Fastner, J, Straile, D, Rothhaupt, KO, Fonvielle, J, Grossart, HP, Avagianos, C, Kaloudis, T, Triantis, T, Zervou, SK, Hiskia, A, Gkelis, S, Panou, M, McCarthy, V, Perello, VC, Obertegger, U, Boscaini, A, Flaim, G, Salmaso, N, Cerasino, L, Koreiviene, J, Karosiene, J, Kasperoviciene, J, Savadova, K, Vitonyte, I, Haande, S, Skjelbred, B, Grabowska, M, Karpowicz, M, Chmura, D, Nawrocka, L, Kobos, J, Mazur-Marzec, H, Alcaraz-Parraga, P, Wilk-Wozniak, E, Krzton, W, Walusiak, E, Gagala, I, Mankiewicz-Boczek, J, Toporowska, M, Pawlik-Skowronska, B, Niedzwiecki, M, Peczula, W, Napiorkowska-Krzebietke, A, Dunalska, J, Sienska, J, Szymanski, D, Kruk, M, 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, Madrecka, B, Kostrzewska-Szlakowska, I, Frak, M, Bankowska-Sobczak, A, Wasilewicz, M, Ochocka, A, Pasztaleniec, A, Jasser, I, Antao-Geraldes, AM, Leira, M, Hernandez, A, Vasconcelos, V, Morais, J, Vale, M, Raposeiro, PM, Goncalves, V, Aleksovski, B, Krstic, S, Nemova, H, Drastichova, I, Chomova, L, Remec-Rekar, S, Elersek, T, Delgado-Martin, J, Garcia, D, Cereijo, JL, Goma, J, Trapote, MC, Vegas-Vilarrubia, T, Obrador, B, Garcia-Murcia, A, Real, M, Romans, E, Noguero-Ribes, J, Duque, DP, Fernandez-Moran, E, Ubeda, B, Galvez, JA, Marce, R, Catalan, N, Perez-Martinez, C, Ramos-Rodriguez, E, Cillero-Castro, C, 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, Hansson, LA, Urrutia-Cordero, P, Ozen, A, Bravo, AG, Buck, M, Colom-Montero, W, Mustonen, K, Pierson, D, Yang, Y, Verspagen, JMH, Domis, LND, Seelen, L, Teurlincx, S, Verstijnen, Y, Lurling, M, Maliaka, V, Faassen, EJ, Latour, D, Carey, CC, Paerl, HW, Torokne, A, Karan, T, Demir, N, Beklioglu, M, Filiz, N, Levi, EE, Iskin, U, Bezirci, G, Tavsanoglu, UN, Celik, K, Ozhan, K, Karakaya, N, Kocer, MAT, Yilmaz, M, Maraslioglu, F, Fakioglu, O, Soylu, EN, Yagci, MA, Cinar, S, Capkin, K, Yagci, A, Cesur, M, Bilgin, F, Bulut, C, Uysal, R, Koker, L, Akcaalan, R, Albay, M, Alp, MT, Ozkan, K, Sevindik, TO, Tunca, H, Onem, B, Richardson, J, Edwards, C, Bergkemper, V, O'Leary, S, Beirne, E, Cromie, H, Ibelings, BW, Sakarya Üniversitesi/Fen-Edebiyat Fakültesi/Biyoloji Bölümü, and Tunca, Hatice

Subjects
Science & Technology - Other Topics
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.

Published
2018

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