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Applying low concentrations of hydrogen peroxide (H2O2) to lakes is an emerging method to mitigate harmful cyanobacterial blooms. While cyanobacteria are very sensitive to H2O2, little is known about the impacts of these H2O2 treatments on other members of the microbial community. In this study, we investigated changes in microbial community composition during two lake treatments with low H2O2 concentrations (target: 2.5 mg L−1) and in two series of controlled lake incubations. The results show that the H2O2 treatments effectively suppressed the dominant cyanobacteria Aphanizomenon klebahnii, Dolichospermum sp. and, to a lesser extent, Planktothrix agardhii. Microbial community analysis revealed that several Proteobacteria (e.g., Alteromonadales, Pseudomonadales, Rhodobacterales) profited from the treatments, whereas some bacterial taxa declined (e.g., Verrucomicrobia). In particular, the taxa known to be resistant to oxidative stress (e.g., Rheinheimera) strongly increased in relative abundance during the first 24 h after H2O2 addition, but subsequently declined again. Alpha and beta diversity showed a temporary decline but recovered within a few days, demonstrating resilience of the microbial community. The predicted functionality of the microbial community revealed a temporary increase of anti-ROS defenses and glycoside hydrolases but otherwise remained stable throughout the treatments. We conclude that the use of low concentrations of H2O2 to suppress cyanobacterial blooms provides a short-term pulse disturbance but is not detrimental to lake microbial communities and their ecosystem functioning.
Tim Piel; Giovanni Sandrini; Gerard Muyzer; Corina Brussaard; Pieter Slot; Maria van Herk; Jef Huisman; Petra Visser. Resilience of Microbial Communities after Hydrogen Peroxide Treatment of a Eutrophic Lake to Suppress Harmful Cyanobacterial Blooms. Microorganisms 2021, 9, 1495 .
AMA StyleTim Piel, Giovanni Sandrini, Gerard Muyzer, Corina Brussaard, Pieter Slot, Maria van Herk, Jef Huisman, Petra Visser. Resilience of Microbial Communities after Hydrogen Peroxide Treatment of a Eutrophic Lake to Suppress Harmful Cyanobacterial Blooms. Microorganisms. 2021; 9 (7):1495.
Chicago/Turabian StyleTim Piel; Giovanni Sandrini; Gerard Muyzer; Corina Brussaard; Pieter Slot; Maria van Herk; Jef Huisman; Petra Visser. 2021. "Resilience of Microbial Communities after Hydrogen Peroxide Treatment of a Eutrophic Lake to Suppress Harmful Cyanobacterial Blooms." Microorganisms 9, no. 7: 1495.
Benthic cyanobacterial mats (BCMs) are becoming increasingly common on coral reefs. In Fiji, blooms generally occur in nearshore areas during warm months but some are starting to prevail through cold months. Many fundamental knowledge gaps about BCM proliferation remain, including their composition and how they influence reef processes. This study examined a seasonal BCM bloom occurring in a 17-year-old no-take inshore reef area in Fiji. Surveys quantified the coverage of various BCM-types and estimated the biomass of key herbivorous fish functional groups. Using remote video observations, we compared fish herbivory (bite rates) on substrate covered primarily by BCMs (> 50%) to substrate lacking BCMs (< 10%) and looked for indications of fish (opportunistically) consuming BCMs. Samples of different BCM-types were analysed by microscopy and next-generation amplicon sequencing (16S rRNA). In total, BCMs covered 51 ± 4% (mean ± s.e.m) of the benthos. Herbivorous fish biomass was relatively high (212 ± 36 kg/ha) with good representation across functional groups. Bite rates were significantly reduced on BCM-dominated substratum, and no fish were unambiguously observed consuming BCMs. Seven different BCM-types were identified, with most containing a complex consortium of cyanobacteria. These results provide insight into BCM composition and impacts on inshore Pacific reefs.
Amanda K. Ford; Petra M. Visser; Maria J. van Herk; Evelien Jongepier; Victor Bonito. First insights into the impacts of benthic cyanobacterial mats on fish herbivory functions on a nearshore coral reef. Scientific Reports 2021, 11, 1 -14.
AMA StyleAmanda K. Ford, Petra M. Visser, Maria J. van Herk, Evelien Jongepier, Victor Bonito. First insights into the impacts of benthic cyanobacterial mats on fish herbivory functions on a nearshore coral reef. Scientific Reports. 2021; 11 (1):1-14.
Chicago/Turabian StyleAmanda K. Ford; Petra M. Visser; Maria J. van Herk; Evelien Jongepier; Victor Bonito. 2021. "First insights into the impacts of benthic cyanobacterial mats on fish herbivory functions on a nearshore coral reef." Scientific Reports 11, no. 1: 1-14.
In the past decades, the intensity and duration of cyanobacterial blooms are increasing due to anthropogenic factors. These phenomena worry drinking water companies and water managers because cyanobacteria produce a diverse range of cyanotoxins, which can cause liver, digestive and neurological diseases. The main exposure routes for humans are the consumption of drinking water that has not been effectively treated and the recreational use of polluted waters. For risk assessment and to conduct studies on large-scale occurrence, the development of reliable but simple, sensitive and cost-effective analytical approaches able to cover a wide range of cyanotoxins is essential. Additionally, the determination of intracellular and extracellular toxins separately is advantageous for risk management. To the best of our knowledge, this is the first time that a method for the multi-class determination of cyanotoxins in fresh water, which is able to separately report intra- and extracellular toxins, meet the criteria of simplicity (not requiring multiple sample preparation procedures or time-consuming steps) and it is based on highly specific high resolution mass spectrometry (potential for wide screening and retrospective analysis). Matrix effects, trueness and precision met general validation criteria for a group of nine cyanotoxins, including anatoxins, cylindrospermopsin and microcystins. Considering a 50 mL sample, the method quantification limits were within the range of 8–45 ng L−1 and 25–129 ng L−1 for intra- and extracellular cyanotoxins, respectively. Anatoxin-a, cylindrospermopsin and some microcystins were found in three out of four Dutch lakes included in the study, at concentrations up to 52 μg L−1.
Encarnación Romera-García; Rick Helmus; Ana Ballesteros-Gómez; Petra M. Visser. Multi-class determination of intracellular and extracellular cyanotoxins in freshwater samples by ultra-high performance liquid chromatography coupled to high resolution mass spectrometry. Chemosphere 2021, 274, 129770 .
AMA StyleEncarnación Romera-García, Rick Helmus, Ana Ballesteros-Gómez, Petra M. Visser. Multi-class determination of intracellular and extracellular cyanotoxins in freshwater samples by ultra-high performance liquid chromatography coupled to high resolution mass spectrometry. Chemosphere. 2021; 274 ():129770.
Chicago/Turabian StyleEncarnación Romera-García; Rick Helmus; Ana Ballesteros-Gómez; Petra M. Visser. 2021. "Multi-class determination of intracellular and extracellular cyanotoxins in freshwater samples by ultra-high performance liquid chromatography coupled to high resolution mass spectrometry." Chemosphere 274, no. : 129770.
Application of low concentrations of hydrogen peroxide (H2O2) is a relatively new and promising method to selectively suppress harmful cyanobacterial blooms, while minimizing effects on eukaryotic organisms. However, it is still unknown how nutrient limitation affects the sensitivity of cyanobacteria to H2O2. In this study, we compare effects of H2O2 on the microcystin-producing cyanobacterium Microcystis PCC 7806 under light-limited but nutrient-replete conditions, nitrogen (N) limitation and phosphorus (P) limitation. Microcystis was first grown in chemostats to acclimate to these different experimental conditions, and subsequently transferred to batch cultures where they were treated with a range of H2O2 concentrations (0-10 mg L−1) while exposed to high light (100 µmol photons m−2 s−1) or low light (15 µmol photons m−2 s−1). Our results show that, at low light, N- and P-limited Microcystis were less sensitive to H2O2 than light-limited but nutrient-replete Microcystis. A significantly higher expression of the genes encoding for anti-oxidative stress enzymes (2-cys-peroxiredoxin, thioredoxin A and type II peroxiredoxin) was observed prior to and after the H2O2 treatment for both N- and P-limited Microcystis, which may explain their increased resistance against H2O2. At high light, Microcystis was more sensitive to H2O2 than at low light, and differences in the decline of the photosynthetic yield between nutrient-replete and nutrient-limited Microcystis exposed to H2O2 were less pronounced. Leakage of microcystin was stronger and faster from nutrient-replete than from N- and P-limited Microcystis. Overall, this study provides insight in the sensitivity of harmful cyanobacteria to H2O2 under various environmental conditions.
Giovanni Sandrini; Tim Piel; Tianshuo Xu; Emily White; Hongjie Qin; Pieter C. Slot; Jef Huisman; Petra M. Visser. Sensitivity to hydrogen peroxide of the bloom-forming cyanobacterium Microcystis PCC 7806 depends on nutrient availability. Harmful Algae 2020, 99, 101916 .
AMA StyleGiovanni Sandrini, Tim Piel, Tianshuo Xu, Emily White, Hongjie Qin, Pieter C. Slot, Jef Huisman, Petra M. Visser. Sensitivity to hydrogen peroxide of the bloom-forming cyanobacterium Microcystis PCC 7806 depends on nutrient availability. Harmful Algae. 2020; 99 ():101916.
Chicago/Turabian StyleGiovanni Sandrini; Tim Piel; Tianshuo Xu; Emily White; Hongjie Qin; Pieter C. Slot; Jef Huisman; Petra M. Visser. 2020. "Sensitivity to hydrogen peroxide of the bloom-forming cyanobacterium Microcystis PCC 7806 depends on nutrient availability." Harmful Algae 99, no. : 101916.
Hydrogen peroxide (H2O2) can be used as an emergency method to selectively suppress cyanobacterial blooms in lakes and drinking water reservoirs. However, it is largely unknown how environmental parameters alter the effectiveness of H2O2 treatments. In this study, the toxic cyanobacterial strain Microcystis aeruginosa PCC 7806 was treated with a range of H2O2 concentrations (0 to 10 mg/L), while being exposed to different light intensities and light colors. H2O2 treatments caused a stronger decline of the photosynthetic yield in high light than in low light or in the dark, and also a stronger decline in orange than in blue light. Our results are consistent with the hypothesis that H2O2 causes major damage at photosystem II (PSII) and interferes with PSII repair, which makes cells more sensitive to photoinhibition. Furthermore, H2O2 treatments caused a decrease in cell size and an increase in extracellular microcystin concentrations, indicative of leakage from disrupted cells. Our findings imply that even low H2O2 concentrations of 1–2 mg/L can be highly effective, if cyanobacteria are exposed to high light intensities. We therefore recommend performing lake treatments during sunny days, when a low H2O2 dosage is sufficient to suppress cyanobacteria, and may help to minimize impacts on non-target organisms.
Tim Piel; Giovanni Sandrini; Emily White; Tianshuo Xu; J. Merijn Schuurmans; Jef Huisman; Petra M. Visser. Suppressing Cyanobacteria with Hydrogen Peroxide Is More Effective at High Light Intensities. Toxins 2019, 12, 18 .
AMA StyleTim Piel, Giovanni Sandrini, Emily White, Tianshuo Xu, J. Merijn Schuurmans, Jef Huisman, Petra M. Visser. Suppressing Cyanobacteria with Hydrogen Peroxide Is More Effective at High Light Intensities. Toxins. 2019; 12 (1):18.
Chicago/Turabian StyleTim Piel; Giovanni Sandrini; Emily White; Tianshuo Xu; J. Merijn Schuurmans; Jef Huisman; Petra M. Visser. 2019. "Suppressing Cyanobacteria with Hydrogen Peroxide Is More Effective at High Light Intensities." Toxins 12, no. 1: 18.
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.
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 Paerl; Cayelan C. Carey; Bas W. Ibelings. Temperature Effects Explain Continental Scale Distribution of Cyanobacterial Toxins. Toxins 2018, 10, 156 .
AMA StyleEvanthia 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 Paerl, Cayelan C. Carey, Bas W. Ibelings. Temperature Effects Explain Continental Scale Distribution of Cyanobacterial Toxins. Toxins. 2018; 10 (4):156.
Chicago/Turabian StyleEvanthia 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 Paerl; Cayelan C. Carey; Bas W. Ibelings. 2018. "Temperature Effects Explain Continental Scale Distribution of Cyanobacterial Toxins." Toxins 10, no. 4: 156.
To help ban the use of general toxic algicides, research efforts are now directed towards the discovery of compounds that are specifically acting as cyanocides. Here, we review the past and look forward into the future, where the less desirable general algicides like copper sulphate, diuron or endothall may become replaced by compounds that show better specificity for cyanobacteria and are biodegradable or transform into non-toxic products after application. For a range of products, we review the activity, the mode of action, effectiveness, durability, toxicity towards non-target species, plus costs involved, and discuss the experience with and prospects for small water volume interventions up to the mitigation of entire lakes; we arrive at recommendations for a series of natural products and extracted organic compounds or derived synthetic homologues with promising cyanocidal properties, and briefly mention emerging nanoparticle applications. Finally, we detail on the recently introduced application of hydrogen peroxide for the selective killing of cyanobacteria in freshwater lakes.
Hans C. P. Matthijs; Daniel Jančula; Petra M. Visser; Blahoslav Maršálek. Existing and emerging cyanocidal compounds: new perspectives for cyanobacterial bloom mitigation. Aquatic Ecology 2016, 50, 443 -460.
AMA StyleHans C. P. Matthijs, Daniel Jančula, Petra M. Visser, Blahoslav Maršálek. Existing and emerging cyanocidal compounds: new perspectives for cyanobacterial bloom mitigation. Aquatic Ecology. 2016; 50 (3):443-460.
Chicago/Turabian StyleHans C. P. Matthijs; Daniel Jančula; Petra M. Visser; Blahoslav Maršálek. 2016. "Existing and emerging cyanocidal compounds: new perspectives for cyanobacterial bloom mitigation." Aquatic Ecology 50, no. 3: 443-460.
Climate change is likely to stimulate the development of harmful cyanobacterial blooms in eutrophic waters, with negative consequences for water quality of many lakes, reservoirs and brackish ecosystems across the globe. In addition to effects of temperature and eutrophication, recent research has shed new light on the possible implications of rising atmospheric CO2 concentrations. Depletion of dissolved CO2 by dense cyanobacterial blooms creates a concentration gradient across the air-water interface. A steeper gradient at elevated atmospheric CO2 concentrations will lead to a greater influx of CO2, which can be intercepted by surface-dwelling blooms, thus intensifying cyanobacterial blooms in eutrophic waters. Bloom-forming cyanobacteria display an unexpected diversity in CO2 responses, because different strains combine their uptake systems for CO2 and bicarbonate in different ways. The genetic composition of cyanobacterial blooms may therefore shift. In particular, strains with high-flux carbon uptake systems may benefit from the anticipated rise in inorganic carbon availability. Increasing temperatures also stimulate cyanobacterial growth. Many bloom-forming cyanobacteria and also green algae have temperature optima above 25 °C, often exceeding the temperature optima of diatoms and dinoflagellates. Analysis of published data suggests that the temperature dependence of the growth rate of cyanobacteria exceeds that of green algae. Indirect effects of elevated temperature, like an earlier onset and longer duration of thermal stratification, may also shift the competitive balance in favor of buoyant cyanobacteria while eukaryotic algae are impaired by higher sedimentation losses. Furthermore, cyanobacteria differ from eukaryotic algae in that they can fix dinitrogen, and new insights show that the nitrogen-fixation activity of heterocystous cyanobacteria can be strongly stimulated at elevated temperatures. Models and lake studies indicate that the response of cyanobacterial growth to rising CO2 concentrations and elevated temperatures can be suppressed by nutrient limitation. The greatest response of cyanobacterial blooms to climate change is therefore expected to occur in eutrophic and hypertrophic lakes
Petra M. Visser; Jolanda M.H. Verspagen; Giovanni Sandrini; Lucas J. Stal; Hans C.P. Matthijs; Timothy W. Davis; Hans W. Paerl; Jef Huisman. How rising CO2 and global warming may stimulate harmful cyanobacterial blooms. Harmful Algae 2016, 54, 145 -159.
AMA StylePetra M. Visser, Jolanda M.H. Verspagen, Giovanni Sandrini, Lucas J. Stal, Hans C.P. Matthijs, Timothy W. Davis, Hans W. Paerl, Jef Huisman. How rising CO2 and global warming may stimulate harmful cyanobacterial blooms. Harmful Algae. 2016; 54 ():145-159.
Chicago/Turabian StylePetra M. Visser; Jolanda M.H. Verspagen; Giovanni Sandrini; Lucas J. Stal; Hans C.P. Matthijs; Timothy W. Davis; Hans W. Paerl; Jef Huisman. 2016. "How rising CO2 and global warming may stimulate harmful cyanobacterial blooms." Harmful Algae 54, no. : 145-159.
Artificial mixing has been used as a measure to prevent the growth of cyanobacteria in eutrophic lakes and reservoirs for many years. In this paper, we give an overview of studies that report on the results of this remedy. Generally, artificial mixing causes an increase in the oxygen content of the water, an increase in the temperature in the deep layers but a decrease in the upper layers, while the standing crop of phytoplankton (i.e. the chlorophyll content per m2) often increases partly due to an increase in nutrients entrained from the hypolimnion or resuspended from the sediments. A change in composition from cyanobacterial dominance to green algae and diatoms can be observed if the imposed mixing is strong enough to keep the cyanobacteria entrained in the turbulent flow, the mixing is deep enough to limit light availability and the mixing devices are well distributed horizontally over the lake. Both models and experimental studies show that if phytoplankton is entrained in the turbulent flow and redistributed vertically over the entire depth, green algae and diatoms win the competition over (colonial) cyanobacteria due to a higher growth rate and reduced sedimentation losses. The advantage of buoyant cyanobacteria to float up to the illuminated upper layers is eradicated in a well-mixed system.
Petra M. Visser; Bastiaan Willem Ibelings; Myriam Bormans; Jef Huisman. Artificial mixing to control cyanobacterial blooms: a review. Aquatic Ecology 2015, 50, 423 -441.
AMA StylePetra M. Visser, Bastiaan Willem Ibelings, Myriam Bormans, Jef Huisman. Artificial mixing to control cyanobacterial blooms: a review. Aquatic Ecology. 2015; 50 (3):423-441.
Chicago/Turabian StylePetra M. Visser; Bastiaan Willem Ibelings; Myriam Bormans; Jef Huisman. 2015. "Artificial mixing to control cyanobacterial blooms: a review." Aquatic Ecology 50, no. 3: 423-441.
Experiments with different phytoplankton densities in lake samples showed that a high biomass increases the rate of HP degradation and decreases the effectiveness of hydrogen peroxide (HP) in the selective suppression of dominant cyanobacteria. Selective application of HP requires usage of low doses only, accordingly this defines the limits for use in lake mitigation. To acquire insight into the impact of HP on other phytoplankton species, we have followed the succession of three phytoplankton groups in lake samples that were treated with different concentrations of HP using a taxa-specific fluorescence emission test. This fast assay reports relatively well on coarse changes in the phytoplankton community, the measured data and the counts from microscopical analysis of the phytoplankton match quite well. The test was used to pursuit HP application in a Planktothrix agardhii-dominated lake sample and displayed a promising shift in the phytoplankton community in only a few weeks. From a low diversity community, a change to a status with a significantly higher diversity and increased abundance of eukaryotic phytoplankton species was established. Re-inoculation experiments of treated samples with original P. agardhii-rich lake water demonstrated prolonged absence of cyanobacteria, and displayed a remarkable stability of the newly developed post-HP treatment state of the phytoplankton community.
Erik F. J. Weenink; Veerle M. Luimstra; Jasper Merijn Schuurmans; Maria J. Van Herk; Petra M. Visser; Hans C. P. Matthijs. Combatting cyanobacteria with hydrogen peroxide: a laboratory study on the consequences for phytoplankton community and diversity. Frontiers in Microbiology 2015, 6, 714 .
AMA StyleErik F. J. Weenink, Veerle M. Luimstra, Jasper Merijn Schuurmans, Maria J. Van Herk, Petra M. Visser, Hans C. P. Matthijs. Combatting cyanobacteria with hydrogen peroxide: a laboratory study on the consequences for phytoplankton community and diversity. Frontiers in Microbiology. 2015; 6 ():714.
Chicago/Turabian StyleErik F. J. Weenink; Veerle M. Luimstra; Jasper Merijn Schuurmans; Maria J. Van Herk; Petra M. Visser; Hans C. P. Matthijs. 2015. "Combatting cyanobacteria with hydrogen peroxide: a laboratory study on the consequences for phytoplankton community and diversity." Frontiers in Microbiology 6, no. : 714.
Algal turf communities are ubiquitous on coral reefs in the Caribbean and are often dominated by N2-fixing cyanobacteria. However, it is largely unknown (1) how much N2 is actually fixed by turf communities and (2) which factors affect their N2 fixation rates. Therefore, we compared N2 fixation activity by turf communities at different depths and during day and night-time on a degraded versus a less degraded coral reef site on the island of Curaçao. N2 fixation rates measured with the acetylene reduction assay were slightly higher in shallow (5-10-m depth) than in deep turf communities (30-m depth), and N2 fixation rates during the daytime significantly exceeded those during the night. N2 fixation rates by the turf communities did not differ between the degraded and less degraded reef. Both our study and a literature survey of earlier studies indicated that turf communities tend to have lower N2 fixation rates than cyanobacterial mats. However, at least in our study area, turf communities were more abundant than cyanobacterial mats. Our results therefore suggest that turf communities play an important role in the nitrogen cycle of coral reefs. N2 fixation by turfs may contribute to an undesirable positive feedback that promotes the proliferation of algal turf communities while accelerating coral reef degradation
Joost Den Haan; Petra M. Visser; Anjani E. Ganase; Elfi E. Gooren; Lucas J. Stal; Fleur C. Van Duyl; Mark Vermeij; Jef Huisman. Nitrogen fixation rates in algal turf communities of a degraded versus less degraded coral reef. Coral Reefs 2014, 33, 1003 -1015.
AMA StyleJoost Den Haan, Petra M. Visser, Anjani E. Ganase, Elfi E. Gooren, Lucas J. Stal, Fleur C. Van Duyl, Mark Vermeij, Jef Huisman. Nitrogen fixation rates in algal turf communities of a degraded versus less degraded coral reef. Coral Reefs. 2014; 33 (4):1003-1015.
Chicago/Turabian StyleJoost Den Haan; Petra M. Visser; Anjani E. Ganase; Elfi E. Gooren; Lucas J. Stal; Fleur C. Van Duyl; Mark Vermeij; Jef Huisman. 2014. "Nitrogen fixation rates in algal turf communities of a degraded versus less degraded coral reef." Coral Reefs 33, no. 4: 1003-1015.
The dinoflagellate Alexandrium ostenfeldii is a well-known harmful algal species that can potentially cause paralytic shellfish poisoning (PSP). Usually A. ostenfeldii occurs in low background concentrations only, but in August of 2012 an exceptionally dense bloom of more than 1millioncellsL occurred in the brackish Ouwerkerkse Kreek in The Netherlands. The A. ostenfeldii bloom produced both saxitoxins and spirolides, and is held responsible for the death of a dog with a high saxitoxin stomach content. The Ouwerkerkse Kreek routinely discharges its water into the adjacent Oosterschelde estuary, and an immediate reduction of the bloom was required to avoid contamination of extensive shellfish grounds. Previously, treatment of infected waters with hydrogen peroxide (HO) successfully suppressed cyanobacterial blooms in lakes. Therefore, we adapted this treatment to eradicate the Alexandrium bloom using a three-step approach. First, we investigated the required HO dosage in laboratory experiments with A. ostenfeldii. Second, we tested the method in a small, isolated canal adjacent to the Ouwerkerkse Kreek. Finally, we brought 50mgL of HO into the entire creek system with a special device, called a water harrow, for optimal dispersal of the added HO. Concentrations of both vegetative cells and pellicle cysts declined by 99.8% within 48h, and PSP toxin concentrations in the water were reduced below local regulatory levels of 15μgL. Zooplankton were strongly affected by the HO treatment, but impacts on macroinvertebrates and fish were minimal. A key advantage of this method is that the added HO decays to water and oxygen within a few days, which enables rapid recovery of the system after the treatment. This is the first successful field application of HO to suppress a marine harmful algal bloom, although Alexandrium spp. reoccurred at lower concentrations in the following year. The results show that HO treatment provides an effective emergency management option to mitigate toxic Alexandrium blooms, especially when immediate action is required.
Amanda Burson; Hans C.P. Matthijs; Wilco de Bruijne; Renee Talens; Ron Hoogenboom; Arjen Gerssen; Petra M. Visser; Maayke Stomp; Kees Steur; Yvonne van Scheppingen; Jef Huisman. Termination of a toxic Alexandrium bloom with hydrogen peroxide. Harmful Algae 2014, 31, 125 -135.
AMA StyleAmanda Burson, Hans C.P. Matthijs, Wilco de Bruijne, Renee Talens, Ron Hoogenboom, Arjen Gerssen, Petra M. Visser, Maayke Stomp, Kees Steur, Yvonne van Scheppingen, Jef Huisman. Termination of a toxic Alexandrium bloom with hydrogen peroxide. Harmful Algae. 2014; 31 ():125-135.
Chicago/Turabian StyleAmanda Burson; Hans C.P. Matthijs; Wilco de Bruijne; Renee Talens; Ron Hoogenboom; Arjen Gerssen; Petra M. Visser; Maayke Stomp; Kees Steur; Yvonne van Scheppingen; Jef Huisman. 2014. "Termination of a toxic Alexandrium bloom with hydrogen peroxide." Harmful Algae 31, no. : 125-135.
Rapid determination of which nutrients limit the primary production of macroalgae and seagrasses is vital for understanding the impacts of eutrophication on marine and freshwater ecosystems. However, current methods to assess nutrient limitation are often cumbersome and time consuming. For phytoplankton, a rapid method has been described based on short-term changes in chlorophyll fluorescence upon nutrient addition, also known as Nutrient-Induced Fluorescence Transients (NIFTs). Thus far, though, the NIFT technique was not well suited for macroalgae and seagrasses. We developed a new experimental setup so that the NIFT technique can be used to assess nutrient limitation of benthic macroalgae and seagrasses. We first tested the applicability of the technique on sea lettuce (Ulva lactuca) cultured in the laboratory on nutrient-enriched medium without either nitrogen or phosphorus. Addition of the limiting nutrient resulted in a characteristic change in the fluorescence signal, whereas addition of non-limiting nutrients did not yield a response. Next, we applied the NIFT technique to field samples of the encrusting fan-leaf alga Lobophora variegata, one of the key algal species often involved in the degradation of coral reef ecosystems. The results pointed at co-limitation of L. variegata by phosphorus and nitrogen, although it responded more strongly to phosphate than to nitrate and ammonium addition. For turtle grass (Thalassia testudinum) we found the opposite result, with a stronger NIFT response to nitrate and ammonium than to phosphate. Our extension of the NIFT technique offers an easy and fast method (30–60 min per sample) to determine nutrient limitation of macroalgae and seagrasses. We successfully applied this technique to macroalgae on coral reef ecosystems and to seagrass in a tropical inner bay, and foresee wider application to other aquatic plants, and to other marine and freshwater ecosystems.
Joost Den Haan; Jef Huisman; Friso Dekker; Jacomina L. Ten Brinke; Amanda Ford; Jan Van Ooijen; Fleur C. Van Duyl; Mark Vermeij; Petra M. Visser. Fast Detection of Nutrient Limitation in Macroalgae and Seagrass with Nutrient-Induced Fluorescence. PLOS ONE 2013, 8, e68834 .
AMA StyleJoost Den Haan, Jef Huisman, Friso Dekker, Jacomina L. Ten Brinke, Amanda Ford, Jan Van Ooijen, Fleur C. Van Duyl, Mark Vermeij, Petra M. Visser. Fast Detection of Nutrient Limitation in Macroalgae and Seagrass with Nutrient-Induced Fluorescence. PLOS ONE. 2013; 8 (7):e68834.
Chicago/Turabian StyleJoost Den Haan; Jef Huisman; Friso Dekker; Jacomina L. Ten Brinke; Amanda Ford; Jan Van Ooijen; Fleur C. Van Duyl; Mark Vermeij; Petra M. Visser. 2013. "Fast Detection of Nutrient Limitation in Macroalgae and Seagrass with Nutrient-Induced Fluorescence." PLOS ONE 8, no. 7: e68834.
Although harmful cyanobacteria form a major threat to water quality, few methods exist for the rapid suppression of cyanobacterial blooms. Since laboratory studies indicated that cyanobacteria are more sensitive to hydrogen peroxide (H2O2) than eukaryotic phytoplankton, we tested the application of H2O2 in natural waters. First, we exposed water samples from a recreational lake dominated by the toxic cyanobacterium Planktothrix agardhii to dilute H2O2. This reduced the photosynthetic vitality by more than 70% within a few hours. Next, we installed experimental enclosures in the lake, which revealed that H2O2 selectively killed the cyanobacteria without major impacts on eukaryotic phytoplankton, zooplankton, or macrofauna. Based on these tests, we introduced 2 mg L−1 (60 μM) of H2O2 homogeneously into the entire water volume of the lake with a special dispersal device, called the water harrow. The cyanobacterial population as well as the microcystin concentration collapsed by 99% within a few days. Eukaryotic phytoplankton (including green algae, cryptophytes, chrysophytes and diatoms), zooplankton and macrofauna remained largely unaffected. Following the treatment, cyanobacterial abundances remained low for 7 weeks. Based on these results, we propose the use of dilute H2O2 for the selective elimination of harmful cyanobacteria from recreational lakes and drinking water reservoirs, especially when immediate action is urgent and/or cyanobacterial control by reduction of eutrophication is currently not feasible. A key advantage of this method is that the added H2O2 degrades to water and oxygen within a few days, and thus leaves no long-term chemical traces in the environment.
Hans C.P. Matthijs; Petra M. Visser; Bart Reeze; Jeroen Meeuse; Pieter C. Slot; Geert Wijn; Renée Talens; Jef Huisman. Selective suppression of harmful cyanobacteria in an entire lake with hydrogen peroxide. Water Research 2012, 46, 1460 -1472.
AMA StyleHans C.P. Matthijs, Petra M. Visser, Bart Reeze, Jeroen Meeuse, Pieter C. Slot, Geert Wijn, Renée Talens, Jef Huisman. Selective suppression of harmful cyanobacteria in an entire lake with hydrogen peroxide. Water Research. 2012; 46 (5):1460-1472.
Chicago/Turabian StyleHans C.P. Matthijs; Petra M. Visser; Bart Reeze; Jeroen Meeuse; Pieter C. Slot; Geert Wijn; Renée Talens; Jef Huisman. 2012. "Selective suppression of harmful cyanobacteria in an entire lake with hydrogen peroxide." Water Research 46, no. 5: 1460-1472.
This study investigated the effects of light intensity, temperature, and phosphorus limitation on the peptide production of the cyanobacteria Microcystis PCC 7806 and Anabaena 90. Microcystis PCC 7806 produced two microcystin variants and three cyanopeptolins, whereas Anabaena 90 produced four microcystin variants, three anabaenopeptins, and two anabaenopeptilides. Microcystin and cyanopeptolin contents varied by a factor 2–3, whereas the anabaenopeptins and anabaenopeptilides of Anabaena varied more strongly. Under phosphorus limitation, peptide production rates increased with the specific growth rate. The response of peptide production to light intensity and temperature was more complex: in many cases peptide production decreased with specific growth rate. We observed compensatory changes of different peptide variants: decreased cyanopeptolin A and C contents were accompanied by increased cyanopeptolin 970 contents, and decreased anabaenopeptin A and C contents were accompanied by increased anabaenopeptilide 90B contents. Compensatory dynamics in peptide production may enable cyanobacteria to sustain stable peptide levels in a variable environment.
Linda Tonk; Martin Welker; Jef Huisman; Petra M. Visser. Production of cyanopeptolins, anabaenopeptins, and microcystins by the harmful cyanobacteria Anabaena 90 and Microcystis PCC 7806. Harmful Algae 2009, 8, 219 -224.
AMA StyleLinda Tonk, Martin Welker, Jef Huisman, Petra M. Visser. Production of cyanopeptolins, anabaenopeptins, and microcystins by the harmful cyanobacteria Anabaena 90 and Microcystis PCC 7806. Harmful Algae. 2009; 8 (2):219-224.
Chicago/Turabian StyleLinda Tonk; Martin Welker; Jef Huisman; Petra M. Visser. 2009. "Production of cyanopeptolins, anabaenopeptins, and microcystins by the harmful cyanobacteria Anabaena 90 and Microcystis PCC 7806." Harmful Algae 8, no. 2: 219-224.
Analyses of boreal zooplankton of Shediac Bay demonstrate the abundance of copepods (81%) and meroplankters (18%). Whether exclusively pelagic or not, 67 species are mentioned for the first time in this Northumberland Strait area, out of 76 recorded within 23 higher taxa. The fluctuations were observed from May to November and pointed out the dominance of such copepods as Acartia tonsa, A. clausi, Oithona similis and Centropages hamatus in relation with temperature, salinity and food distributions.
Petra M. Visser; Bas W. Ibelings; Luuc R. Mur; Georges Citarella. Autunmal sedimentation of Microcystis spp. as result of an increase in carbohydrate ballast at reduced temperature. Journal of Plankton Research 1995, 17, 919 -933.
AMA StylePetra M. Visser, Bas W. Ibelings, Luuc R. Mur, Georges Citarella. Autunmal sedimentation of Microcystis spp. as result of an increase in carbohydrate ballast at reduced temperature. Journal of Plankton Research. 1995; 17 (5):919-933.
Chicago/Turabian StylePetra M. Visser; Bas W. Ibelings; Luuc R. Mur; Georges Citarella. 1995. "Autunmal sedimentation of Microcystis spp. as result of an increase in carbohydrate ballast at reduced temperature." Journal of Plankton Research 17, no. 5: 919-933.