Causes, Consequences and Control of Cyanobacterial Blooms in a Changing World

A special issue of Toxins (ISSN 2072-6651). This special issue belongs to the section "Marine and Freshwater Toxins".

Deadline for manuscript submissions: closed (31 December 2017) | Viewed by 74496

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Guest Editor
Aquatic Ecology & Water Quality Management Group, Department of Environmental Sciences, Wageningen University, P.O. Box 47, 6700 AA Wageningen, The Netherlands
Interests: controlling cyanobacteria blooms; cyanobacteria ecology; cyanobacteria toxins; managing eutrophication; plankton interactions
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Special Issue Information

Dear Colleagues,

Cyanobacteria are common and in evolutionary context the oldest inhabitants of aquatic systems. Massive occurrences or cyanobacterial blooms, due to accumulation of buoyant cells and/or strong proliferation as a consequence of eutrophication, present a serious threat to the environment and health of wildlife, cattle and humans, because several cyanobacteria can produce very potent toxins that constitute one of the most high-risk categories of waterborne toxic substances.

There is broad consensus that the incidence and intensity of cyanobacterial blooms are on the rise worldwide. Eutrophication, climatic changes (precipitation, drought, heat waves), elevated atmospheric carbon dioxide concentration, higher salinity and direct and indirect temperature effects are all expected to further aggravate the frequency, intensity and spreading of cyanobacterial blooms. As these blooms are in direct conflict with the safe and aesthetically acceptable water needed in a modern society, extenuating nuisance is considered a key challenge to water quality managers now and in the upcoming decades. Global changes, however, confront water managers, decision makers and scientists with new unforeseen uncertainties. Insight in mechanisms that influence bloom development, composition and most importantly their toxicity is needed for changing world scenarios –what to expect?– and for the development of promising mitigation tools—how to control?

This Special Issue invites manuscripts on all aspects dealing with cyanobacterial blooms in a changing world: from warming, eutrophication, carbon dioxide, salinity, brownification effects on cyanobacteria and/or their toxins via biotic interactions such as competition, predation, parasitism, and so on, to techniques mitigating cyanobacterial biomass and controlling toxins. Contributions from areas of the planet underrepresented in the scientific literature are particularly welcome.

Prof. Dr. Miquel Lürling
Guest Editor

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Keywords

  • climate change

  • cyanotoxins

  • eutrophication

  • mitigation

  • warming

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Published Papers (8 papers)

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Research

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24 pages, 16409 KiB  
Article
Temperature Effects Explain Continental Scale Distribution of Cyanobacterial Toxins
by 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. Ibelingsadd Show full author list remove Hide full author list
Toxins 2018, 10(4), 156; https://doi.org/10.3390/toxins10040156 - 13 Apr 2018
Cited by 159 | Viewed by 25024
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 [...] Read more.
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. Full article
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16 pages, 6010 KiB  
Article
The Impact of Warming and Nutrients on Algae Production and Microcystins in Seston from the Iconic Lake Lesser Prespa, Greece
by Valentini Maliaka, Elisabeth J. Faassen, Alfons J.P. Smolders and Miquel Lürling
Toxins 2018, 10(4), 144; https://doi.org/10.3390/toxins10040144 - 2 Apr 2018
Cited by 9 | Viewed by 5864
Abstract
Lake Lesser Prespa and its adjacent pond, Vromolimni in Greece, is a shallow freshwater system and a highly protected area hosting an exceptional biodiversity. The occurrence of microcystins (MCs) producing cyanobacterial blooms in these waters during recent years can be harmful to the [...] Read more.
Lake Lesser Prespa and its adjacent pond, Vromolimni in Greece, is a shallow freshwater system and a highly protected area hosting an exceptional biodiversity. The occurrence of microcystins (MCs) producing cyanobacterial blooms in these waters during recent years can be harmful to the wildlife. We tested the hypothesis that both cyanobacterial biomass and MCs are strongly influenced by nutrients (eutrophication) and warming (climate change). Lake and pond water was collected from two sites in each water body in 2013 and incubated at three temperatures (20 °C, 25 °C, 30 °C) with or without additional nutrients (nitrogen +N, phosphorus +P and both +N and +P). Based on both biovolume and chlorophyll-a concentrations, cyanobacteria in water from Lesser Prespa were promoted primarily by combined N and P additions and to a lesser extent by N alone. Warming seemed to yield more cyanobacteria biomass in these treatments. In water from Vromolimni, both N alone and N+P additions increased cyanobacteria and a warming effect was hardly discernible. MC concentrations were strongly increased by N and N+P additions in water from all four sites, which also promoted the more toxic variant MC-LR. Hence, both water bodies seem particularly vulnerable to further N-loading enhancing MC related risks. Full article
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21 pages, 5453 KiB  
Article
Warming Affects Growth Rates and Microcystin Production in Tropical Bloom-Forming Microcystis Strains
by Trung Bui, Thanh-Son Dao, Truong-Giang Vo and Miquel Lürling
Toxins 2018, 10(3), 123; https://doi.org/10.3390/toxins10030123 - 14 Mar 2018
Cited by 36 | Viewed by 6786
Abstract
Warming climate is predicted to promote cyanobacterial blooms but the toxicity of cyanobacteria under global warming is less well studied. We tested the hypothesis that raising temperature may lead to increased growth rates but to decreased microcystin (MC) production in tropical Microcystis strains. [...] Read more.
Warming climate is predicted to promote cyanobacterial blooms but the toxicity of cyanobacteria under global warming is less well studied. We tested the hypothesis that raising temperature may lead to increased growth rates but to decreased microcystin (MC) production in tropical Microcystis strains. To this end, six Microcystis strains were isolated from different water bodies in Southern Vietnam. They were grown in triplicate at 27 °C (low), 31 °C (medium), 35 °C (high) and 37 °C (extreme). Chlorophyll-a-, particle- and MC concentrations as well as dry-weights were determined. All strains yielded higher biomass in terms of chlorophyll-a concentration and dry-weight at 31 °C compared to 27 °C and then either stabilised, slightly increased or declined with higher temperature. Five strains easily grew at 37 °C but one could not survive at 37 °C. When temperature was increased from 27 °C to 37 °C total MC concentration decreased by 35% in strains with MC-LR as the dominant variant and by 94% in strains with MC-RR. MC quota expressed per particle, per unit chlorophyll-a and per unit dry-weight significantly declined with higher temperatures. This study shows that warming can prompt the growth of some tropical Microcystis strains but that these strains become less toxic. Full article
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11 pages, 1368 KiB  
Article
Fatal Neurotoxicosis in Dogs Associated with Tychoplanktic, Anatoxin-a Producing Tychonema sp. in Mesotrophic Lake Tegel, Berlin
by Jutta Fastner, Camilla Beulker, Britta Geiser, Anja Hoffmann, Roswitha Kröger, Kinga Teske, Judith Hoppe, Lars Mundhenk, Hartmud Neurath, Daniel Sagebiel and Ingrid Chorus
Toxins 2018, 10(2), 60; https://doi.org/10.3390/toxins10020060 - 31 Jan 2018
Cited by 59 | Viewed by 9013
Abstract
In May 2017, at least 12 dogs showed signs of acute neurotoxicosis after swimming in or drinking from Lake Tegel, a mesotrophic lake in Berlin, Germany, and several of the affected dogs died shortly afterwards despite intensive veterinary treatment. Cyanobacterial blooms were not [...] Read more.
In May 2017, at least 12 dogs showed signs of acute neurotoxicosis after swimming in or drinking from Lake Tegel, a mesotrophic lake in Berlin, Germany, and several of the affected dogs died shortly afterwards despite intensive veterinary treatment. Cyanobacterial blooms were not visible at the water surface or the shorelines. However, detached and floating water moss (Fontinalis antipyretica) with high amounts of Tychonema sp., a potential anatoxin-a (ATX) producing cyanobacterium, was found near the beaches where the dogs had been swimming and playing. Necropsies of two of the dogs revealed no specific lesions beside the anamnestic neurotoxicosis. ATX was detected in concentrations up to 8700 µg L−1 in the stomach contents, while other (neuro)toxic substances were not found. In the aqueous fraction of Fontinalis/Tychonema clumps sampled after the casualties, ATX was found in concentrations up to 1870 µg L−1. This is the first report of a dense population of Tychonema sp. in stands of Fontinalis resulting in high ATX contents. This case emphasizes the need for further investigation of potentially toxic, non-bloom forming cyanobacteria in less eutrophic water bodies and underlines the novel challenge of developing appropriate surveillance schemes for respective bathing sites. Full article
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1361 KiB  
Article
Responses of Microcystis Colonies of Different Sizes to Hydrogen Peroxide Stress
by Mixue Liu, Xiaoli Shi, Chao Chen, Li Yu and Chuang Sun
Toxins 2017, 9(10), 306; https://doi.org/10.3390/toxins9100306 - 27 Sep 2017
Cited by 44 | Viewed by 4988
Abstract
Microcystis blooms have become a ubiquitous phenomenon in freshwater ecosystems, and the size of Microcystis colonies varies widely throughout the year. In the present study, hydrogen peroxide (H2O2) was applied to test the effect of this algaecide on Microcystis [...] Read more.
Microcystis blooms have become a ubiquitous phenomenon in freshwater ecosystems, and the size of Microcystis colonies varies widely throughout the year. In the present study, hydrogen peroxide (H2O2) was applied to test the effect of this algaecide on Microcystis colonies of different sizes and to evaluate the colonies' antioxidant strategy. The results showed that Microcystis populations collapsed under treatment with 5 mg/L H2O2 at colony sizes smaller than 25 μm. A dosage of 20 mg/L H2O2 was necessary to efficiently control Microcystis colonies larger than 25 μm. The enzymatic and non-enzymatic antioxidant systems of different colonies exhibited various strategies to mitigate oxidative stress. In small colonies, superoxide dismutase (SOD) activity was readily stimulated and operated with catalase (CAT) activity to eliminate reactive oxygen species (ROS). In colonies larger than 25 μm, the antioxidant enzyme CAT and antioxidant substance glutathione (GSH) played major roles in mitigating oxidative stress at H2O2 concentrations below 20 mg/L. In addition, application of the algaecide led to the release of intracellular-microcystins (MCs), and oxidatively-driven MCs reached high concentrations when colony size was larger than 100 μm. Algaecide control measures should be implemented before the formation of large colonies to limit the algaecide dosage and MC release. Full article
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2274 KiB  
Article
Benthic Archives Reveal Recurrence and Dominance of Toxigenic Cyanobacteria in a Eutrophic Lake over the Last 220 Years
by Benjamin Legrand, Amélie Lamarque, Marion Sabart and Delphine Latour
Toxins 2017, 9(9), 271; https://doi.org/10.3390/toxins9090271 - 4 Sep 2017
Cited by 10 | Viewed by 4410
Abstract
Akinetes are resistant cells which have the ability to persist in sediment for several decades. We have investigated the temporal distribution of akinetes of two species, Dolichospermum macrosporum and Dolichospermum flos-aquae, in a sediment core sampled in Lake Aydat (France), which covers [...] Read more.
Akinetes are resistant cells which have the ability to persist in sediment for several decades. We have investigated the temporal distribution of akinetes of two species, Dolichospermum macrosporum and Dolichospermum flos-aquae, in a sediment core sampled in Lake Aydat (France), which covers 220 years. The upper part, from 1907 to 2016, the number of akinetes fluctuated but stayed at high concentrations, especially for D. macrosporum in surface sediment (with the maximal value close to 6.105 akinetes g DW−1 of sediment), suggesting a recurrence of blooms of this species which was probably closely related to anthropic eutrophication since the 1960s. Before 1907, the abundance of akinetes of both species was very low, suggesting only a modest presence of these cyanobacteria. In addition, the percentage of intact akinetes was different for each species, suggesting different ecological processes in the water column. This percentage also decreased with depth, revealing a reduction in germination potential over time. In addition, biosynthetic genes of anatoxin-a (anaC) and microcystin (mcyA) were detected. First results show a high occurrence of mcyA all down the core. In contrast, anaC gene was mostly detected in the surface sediment (since the 1980s), revealing a potentially more recent occurrence of this cyanotoxin in Lake Aydat which may be associated with the recurrence of blooms of D. macrosporum and thus with anthropic activities. Full article
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Review

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16 pages, 10171 KiB  
Review
Mitigating Toxic Planktonic Cyanobacterial Blooms in Aquatic Ecosystems Facing Increasing Anthropogenic and Climatic Pressures
by Hans W. Paerl
Toxins 2018, 10(2), 76; https://doi.org/10.3390/toxins10020076 - 8 Feb 2018
Cited by 130 | Viewed by 10024
Abstract
Toxic planktonic cyanobacterial blooms are a pressing environmental and human health problem. Blooms are expanding globally and threatening sustainability of our aquatic resources. Anthropogenic nutrient enrichment and hydrological modifications, including water diversions and reservoir construction, are major drivers of bloom expansion. Climatic change, [...] Read more.
Toxic planktonic cyanobacterial blooms are a pressing environmental and human health problem. Blooms are expanding globally and threatening sustainability of our aquatic resources. Anthropogenic nutrient enrichment and hydrological modifications, including water diversions and reservoir construction, are major drivers of bloom expansion. Climatic change, i.e., warming, more extreme rainfall events, and droughts, act synergistically with human drivers to exacerbate the problem. Bloom mitigation steps, which are the focus of this review, must consider these dynamic interactive factors in order to be successful in the short- and long-term. Furthermore, these steps must be applicable along the freshwater to marine continuum connecting streams, lakes, rivers, estuarine, and coastal waters. There is an array of physical, chemical, and biological approaches, including flushing, mixing, dredging, application of algaecides, precipitating phosphorus, and selective grazing, that may arrest and reduce bloom intensities in the short-term. However, to ensure long term, sustainable success, targeting reductions of both nitrogen and phosphorus inputs should accompany these approaches along the continuum. Lastly, these strategies should accommodate climatic variability and change, which will likely modulate and alter nutrient-bloom thresholds. Full article
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20 pages, 2164 KiB  
Review
Allelopathic and Bloom-Forming Picocyanobacteria in a Changing World
by Sylwia Śliwińska-Wilczewska, Jakub Maculewicz, Aldo Barreiro Felpeto and Adam Latała
Toxins 2018, 10(1), 48; https://doi.org/10.3390/toxins10010048 - 20 Jan 2018
Cited by 50 | Viewed by 7286
Abstract
Picocyanobacteria are extremely important organisms in the world’s oceans and freshwater ecosystems. They play an essential role in primary production and their domination in phytoplankton biomass is common in both oligotrophic and eutrophic waters. Their role is expected to become even more relevant [...] Read more.
Picocyanobacteria are extremely important organisms in the world’s oceans and freshwater ecosystems. They play an essential role in primary production and their domination in phytoplankton biomass is common in both oligotrophic and eutrophic waters. Their role is expected to become even more relevant with the effect of climate change. However, this group of photoautotrophic organisms still remains insufficiently recognized. Only a few works have focused in detail on the occurrence of massive blooms of picocyanobacteria, their toxicity and allelopathic activity. Filling the gap in our knowledge about the mechanisms involved in the proliferation of these organisms could provide a better understanding of aquatic environments. In this review, we gathered and described recent information about allelopathic activity of picocyanobacteria and occurrence of their massive blooms in many aquatic ecosystems. We also examined the relationships between climate change and representative picocyanobacterial genera from freshwater, brackish and marine ecosystems. This work emphasizes the importance of studying the smallest picoplanktonic fractions of cyanobacteria. Full article
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