Dedmer Van de Waal

Prof. dr. ir. Dedmer Van de Waal

Senior Researcher


Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands



My aim is to mechanistically understand the cellular processes that underlie population and community dynamics


Dedmer B. Van de Waal received his PhD at the University of Amsterdam in 2010, after which he worked at the Alfred Wegener Institute for Polar and Marine Research in Bremerhaven, Germany, as a post-doctoral fellow until 2013 when he started a tenure-track at the Netherlands Institute of Ecology (NIOO-KNAW). He became tenured as senior scientist in 2018 and is ad-interim Head of Department since 2019. In 2022 he became Professor by special appointment of Aquatic Functional Ecology at the University of Amsterdam. With his group, he studies the impacts of global change on harmful algal and cyanobacterial blooms. Specifically, he is interested in how physiological responses at the cellular level can explain ecological processes at a population and community level. He applies ecological stoichiometry and trait-based approaches to understand the physiology of toxic phytoplankton species, and their interaction with competitors and diseases. He is recipient of the ISSHA 2016 Patrick Gentien Young Scientist Award and the ASLO 2020 Yentsch-Schindler Early Career Award. In 2022 he received a prestigious ERC Consolidator Grant to study global change impacts on cyanobacteiral blooms toxicity. He is member of the editorial boards of the Journal of Ecology and Aquatic Sciences, and of the editorial advisory board of Harmful Algae. Dedmer is furthermore chair of the Dutch Cyanobacteria Working group, connecting scientists and stakeholders in water management.



  • 2021–Present
    Senior Researcher, department of Aquatic Ecology
  • 2019–2021
    Acting Head of Department, department of Aquatic Ecology, NIOO-KNAW
  • 2013–2019
    Senior Researcher, department of Aquatic Ecology, NIOO-KNAW (tenure-track)
  • 2009–2013
    Post-doc, Alfed Wegener Institute, Bremerhaven, Germany
  • 2022–Present
    Professor by special appointment, University of Amsterdam


  • 2005–2009
    PhD Aquatic Microbial Ecology, University of Amsterdam
  • 2003–2005
    MSc Hydrology & Water Quality Management/Aquatic Ecology, Wageningen University
  • 1999–2003
    B.Hons Environmental Sciences/Water Management, Van Hall Institute Leeuwarden


  • 2022
    ERC Consolidator Grant
    Budget: €1,997,454
  • 2022
    NWO L.INT Lectorship (co-applicant)
    Budget: €200,000
    HAS Hogeschool
  • 2021
    RVO Innovation Budget Digital Government (co-applicant)
    Budget: €72,000
    KNMI, Deltares
  • 2018
    NWO Open Programme
    Budget: €279,755
  • 2018
    OBN Knoweldedge Network (co-applicant)
    Budget: €15,653
    Stichting Bargerveen, Vlinderstichting, B-WARE

Editorial board memberships

  • 2020–Present
    Journal of Ecology
  • 2018–Present
    Aquatic Sciences
  • 2019–Present
    Harmful Algae (Editorial Advisory Board)
  • 2015–2020
    Ecology Letters
  • 2016–2018
    Frontiers in Microbiology (Guest Associate Editor of Frontiers Research Fopic)

PhD students

  • 2018–Present
    Douwe de Bruijn
    University of Twente
    Promotors en Copromotors: Albert van den Berg, Wouter Olthuis, Dedmer Van de Waal
  • 2017–2021
    Hui Jin
    NIOO-KNAW/Wageningen University
    Promotors en Copromotors: Liesbeth Bakker, Casper van Leeuwen, Dedmer Van de Waal
  • 2015–2019
    Karen Brandenburg
    NIOO-KNAW/Utrecht University
    Promotors en Copromotors: Dedmer Van de Waal, Ellen van Donk
  • 2014–2018
    Thijs Frenken
    NIOO-KNAW/Utrecht University
    Promotors en Copromotors: Dedmer Van de Waal, Alena Gsell, Ellen van Donk
  • 2013–2017
    Mandy Velthuis
    NIOO-KNAW/Utrecht University
    Promotors en Copromotors: Dedmer Van de Waal, Liesbeth Bakker, Ellen van Donk
  • 2011–2015
    Tim Eberlein
    Alfred Wegener Institute/University of Bremen
    Promotors en Copromotors: Bjoern Rost, Dedmer van de Waal
  • 2010–2015
    Mirja Hoins
    Utrecht University/Alfred Wegener Institut
    Promotors en Copromotors: Appy Sluijs, Bjoern Rost, Dedmer van de Waal, Gert-Jan Reichart

Invited talks and keynote addresses on symposia and conferences

  • 2022
    International Conference on Toxic Cyanobacteria
  • 2022
    Joint Aquatic Sciences Meeting 2022 (award talk)
  • 2021
    Eurotox Congress 2021
  • 2019
    Wadden Academy Symposium
  • 2019
    Department of Biology Seminar
  • 2018
    International Conference on Harmful Algae (invited session talk)



Peer-reviewed publicaties

  • Harmful Algae

    Risk assessment of toxic cyanobacterial blooms in recreational waters

    Quirijn Schürmann, Petra M Visser, Susan Sollie, W.E.A. Kardinaal, Els Faassen, Ridouan Lokmani, Ron van der Oost, Dedmer Van de Waal

    Toxic cyanobacterial blooms impose a health risk to recreational users, and monitoring of cyanobacteria and associated toxins is required to assess this risk. Traditionally, monitoring for risk assessment is based on cyanobacterial biomass, which assumes that all cyanobacteria potentially produce toxins. While these methods may be cost effective, relatively fast, and more widely accessible, they often lead to an overestimation of the health risk induced by cyanotoxins. Monitoring methods that more directly target toxins, or toxin producing genes, may provide a better risk assessment, yet these methods may be more costly, usually take longer, or are not widely accessible. In this study, we compared six monitoring methods (fluorometry, microscopy, qPCR of 16S and mcyE, ELISA assays, and LC-MS/MS), of which the last three focussed on the most abundant cyanotoxin microcystins, across 11 lakes in the Netherlands during the bathing water season (May-October) of 2019. Results of all monitoring methods significantly correlated with LC-MS/MS obtained microcystin levels (the assumed ‘golden standard’), with stronger correlations for methods targeting microcystins (ELISA) and microcystin genes (mcyE). The estimated risk levels differed substantially between methods, with 78 % and 56 % of alert level exceedances in the total number of collected samples for fluorometry and microscopy-based methods, respectively, while this was only 16 % and 6 % when the risk assessment was based on ELISA and LC-MS/MS obtained toxin concentrations, respectively. Integrating our results with earlier findings confirmed a strong association between microcystin concentration and the biovolume of potential microcystin-producing genera. Moreover, using an extended database consisting of 4265 observations from 461 locations across the Netherlands in the bathing water seasons of 2015 – 2019, we showed a strong association between fluorescence and the biovolume of potentially toxin-producing genera. Our results indicate that a two-tiered approach may be an effective risk assessment strategy, with first a biomass-based method (fluorometry, biovolume) until the first alert level is exceeded, after which the risk level can be confirmed or adjusted based on follow-up toxin or toxin gene analyses.
  • Water Research

    Hot summers raise public awareness of toxic cyanobacterial blooms

    Dedmer Van de Waal, Alena Gsell, Ted D. Harris, Hans W. Paerl, Lisette de Senerpont Domis, Jef Huisman
    Water quality of eutrophic lakes is threatened by harmful cyanobacterial blooms, which are favored by summer heatwaves and expected to intensify with global warming. Societal demands on surface water for drinking, irrigation and recreation are also highest in summer, especially during dry and warm conditions. Here, we analyzed trends in online searches to investigate how public awareness of cyanobacterial blooms is impacted by temperature in nine different countries over almost twenty years. Our findings reveal large seasonal and interannual variation, with more online searches for harmful cyanobacteria in temperate regions during hot summers. Online searches and media attention increased even more steeply with temperature than the incidence of cyanobacterial blooms, presumably because lakes attract more people during warm weather. Overall, our study indicates that warmer summers not only increase cyanobacterial bloom incidence, but also lead to a pronounced increase of the public awareness of toxic cyanobacterial blooms.
  • Harmful Algae

    The combined effect of pH and dissolved inorganic carbon concentrations on the physiology of plastidic ciliate Mesodinium rubrum and its cryptophyte prey

    Christine Schultz Yde Eriksen, Melanie Desmaret Walli, Dedmer Van de Waal, Nico Helmsing, Emma Ove Dahl, Helle Sørensen, Per Juel Hansen

    Ocean acidification is caused by rising atmospheric partial pressure of CO2 (pCO2) and involves a lowering of pH combined with increased concentrations of CO2 and dissolved in organic carbon in ocean waters. Many studies investigated the consequences of these combined changes on marine phytoplankton, yet only few attempted to separate the effects of decreased pH and increased pCO2. Moreover, studies typically target photoautotrophic phytoplankton, while little is known of plastidic protists that depend on the ingestion of plastids from their prey. Therefore, we studied the separate and interactive effects of pH and DIC levels on the plastidic ciliate Mesodinium rubrum, which is known to form red tides in coastal waters worldwide. Also, we tested the effects on their prey, which typically are cryptophytes belonging to the Teleaulax/Plagioslemis/Geminigera species complex. These cryptophytes not only serve as food for the ciliate, but also as a supplier of chloroplasts and prey nuclei. We exposed M. rubrum and the two cryptophyte species, T. acuta, T. amphioxeia to different pH (6.8 - 8) and DIC levels (∼ 6.5 - 26 mg C L-1) and assessed their growth and photosynthetic rates, and cellular chlorophyll a and elemental contents. Our findings did not show consistent significant effects across the ranges in pH and/or DIC, except for M. rubrum, for which growth was negatively affected only by the lowest pH of 6.8 combined with lower DIC concentrations. It thus seems that M. rubrum is largely resilient to changes in pH and DIC, and its blooms may not be strongly impacted by the changes in ocean carbonate chemistry projected for the end of the 21st century.
  • Ecology

    Reconciling contrasting effects of nitrogen on host immunity and pathogen transmission using stoichiometric models

    Dedmer Van de Waal, Lauren A. White, Rebecca A. Everett, Lale Asik, Elizabeth T. Borer, Thijs Frenken, Angélica L. González, Rachel Paseka, Eric W. Seabloom, Alexander T. Strauss, Angela Peace

    Hosts rely on the availability of nutrients for growth, and for defense against pathogens. At the same time, changes in host nutrition can alter the dynamics of pathogens that rely on their host for reproduction. For primary producer hosts, enhanced nutrient loads may increase host biomass or pathogen reproduction, promoting faster density-dependent pathogen transmission. However, the effect of elevated nutrients may be reduced if hosts allocate a growth-limiting nutrient to pathogen defense. In canonical disease models, transmission is not a function of nutrient availability. Yet, including nutrient availability is necessary to mechanistically understand the response of infection to changes in the environment. Here, we explore the implications of nutrient-mediated pathogen infectivity and host immunity on infection outcomes. We developed a stoichiometric disease model that explicitly integrates the contrasting dependencies of pathogen infectivity and host immunity on nitrogen (N) and parameterized it for an algal-host system. Our findings reveal dynamic shifts in host biomass build-up, pathogen prevalence, and the force of infection along N supply gradients with N-mediated host infectivity and immunity, compared with a model in which the transmission rate was fixed. We show contrasting responses in pathogen performance with increasing N supply between N-mediated infectivity and N-mediated immunity, revealing an optimum for pathogen transmission at intermediate N supply. This was caused by N limitation of the pathogen at a low N supply and by pathogen suppression via enhanced host immunity at a high N supply. By integrating both nutrient-mediated pathogen infectivity and host immunity into a stoichiometric model, we provide a theoretical framework that is a first step in reconciling the contrasting role nutrients can have on host–pathogen dynamics.
  • Limnology and Oceanography

    Long‐term nutrient load reductions and increasing lake TN

    Thijs Frenken, Karen M. Brandenburg, Dedmer Van de Waal
    Nutrient loading of freshwater and marine habitats has increased during the last century as a result of anthropogenic activities. From the 1980s onwards, following implementation of new policy targeting eutrophication, total phosphorus (TP) and total nitrogen (TN) loads were reduced in many European waters. Often, however, decreases in TP were stronger as compared to TN, leading to increased TN : TP ratios. Our analysis shows that the large and shallow lake IJsselmeer (the Netherlands) experienced a similar trend, whereas TN was reduced by 50%, TP was reduced by 89% between 1975 and 2018. Most of this nutrient load reduction was achieved before the year 2000, changes in nutrient concentrations in the lake became smaller afterwards, especially for TN, leading to a further increase in stoichiometric imbalance up to a yearly averaged TN : TP (molar) of 296 in 2018. The observed changes in nutrients were accompanied by a decline in total phytoplankton biomass, and slight declines in phytoplankton genus evenness and diversity. Although biomass decreases likely resulted from the overall decrease in nutrient availabilities, the reduced diversity may have resulted from the shift toward very high TN : TP ratios that indicate relatively low TP levels and enhanced competition for phosphorus. Overall, our findings demonstrate long-term trends with decreased phytoplankton biomass and diversity following reduced nutrient concentrations and enhanced stoichiometric imbalance. Ultimately, such changes at the food web base may alter the structure and functioning of the entire aquatic food- web in lake IJsselmeer.
  • Biological Reviews

    Towards a mechanistic understanding of the impacts of nitrogen deposition on producer–consumer interactions

    Joost J. Vogels, Dedmer Van de Waal, Michiel F. WallisDeVries, A.B. Van den Burg, Marijn Nijssen, Roland Bobbink, Matty P. Berg, Harry Olde Venterink, Henk Siepel
    Nitrogen (N) deposition has increased substantially since the second half of the 20th century due to human activities. This increase of reactive N into the biosphere has major implications for ecosystem functioning, including primary production, soil and water chemistry and producer community structure and diversity. Increased N deposition is also linked to the decline of insects observed over recent decades. However, we currently lack a mechanistic understanding of the effects of high N deposition on individual fitness, species richness and community structure of both invertebrate and vertebrate consumers. Here, we review the effects of N deposition on producer–consumer interactions, focusing on five existing ecological frameworks: C:N:P ecological stoichiometry, trace element ecological stoichiometry, nutritional geometry, essential micronutrients and allelochemicals. We link reported N deposition-mediated changes in producer quality to life-history strategies and traits of consumers, to gain a mechanistic understanding of the direction of response in consumers. We conclude that high N deposition influences producer quality via eutrophication and acidification pathways. This makes oligotrophic poorly buffered ecosystems most vulnerable to significant changes in producer quality. Changes in producer quality between the reviewed frameworks are often interlinked, complicating predictions of the effects of high N deposition on producer quality. The degree and direction of fitness responses of consumers to changes in producer quality varies among species but can be explained by differences in life-history traits and strategies, particularly those affecting species nutrient intake regulation, mobility, relative growth rate, host-plant specialisation, ontogeny and physiology. To increase our understanding of the effects of N deposition on these complex mechanisms, the inclusion of life-history traits of consumer species in future study designs is pivotal. Based on the reviewed literature, we formulate five hypotheses on the mechanisms underlying the effects of high N deposition on consumers, by linking effects of nutritional ecological frameworks to life-history strategies. Importantly, we expect that N-deposition-mediated changes in producer quality will result in a net decrease in consumer community as well as functional diversity. Moreover, we anticipate an increased risk of outbreak events of a small subset of generalist species, with concomitant declines in a multitude of specialist species. Overall, linking ecological frameworks with consumer life-history strategies provides a mechanistic understanding of the impacts of high N deposition on producer–consumer interactions, which can inform management towards more effective mitigation strategies.
  • Oikos

    Dead or alive

    Eric W. Seabloom, Angela Peace, Lale Asik, Rebecca A. Everett, Thijs Frenken, Angélica L. González, Alexander T. Strauss, Dedmer Van de Waal, Lauren A. White, Elizabeth T. Borer

    Death is a common outcome of infection, but most disease models do not track hosts after death. Instead, these hosts disappear into a void. This assumption lacks critical realism, because dead hosts can alter host–pathogen dynamics. Here, we develop a theoretical framework of carbon-based models combining disease and ecosystem perspectives to investigate the consequences of feedbacks between living and dead hosts on disease dynamics and carbon cycling. Because autotrophs (i.e. plants and phytoplankton) are critical regulators of carbon cycling, we developed general model structures and parameter combinations to broadly reflect disease of autotrophic hosts across ecosystems. Analytical model solutions highlight the importance of disease–ecosystem coupling. For example, decomposition rates of dead hosts mediate pathogen spread, and carbon flux between live and dead biomass pools are sensitive to pathogen effects on host growth and death rates. Variation in dynamics arising from biologically realistic parameter combinations largely fell along a single gradient from slow to fast carbon turnover rates, and models predicted higher disease impacts in fast turnover systems (e.g. lakes and oceans) than slow turnover systems (e.g. boreal forests). Our results demonstrate that a unified framework, including the effects of pathogens on carbon cycling, provides novel hypotheses and insights at the nexus of disease and ecosystem ecology.
  • Water Research

    Restoring gradual land-water transitions in a shallow lake improved phytoplankton quantity and quality with cascading effects on zooplankton production

    Land-water transition areas play a significant role in the functioning of aquatic ecosystems. However, anthropogenic pressures are posing severe threats on land-water transition areas, which leads to degradation of the ecological integrity of many lakes worldwide. Enhancing habitat complexity and heterogeneity by restoring land-water transition areas in lake systems is deemed a suitable method to restore lakes bottom-up by stimulating lower trophic levels. Stimulating productivity of lower trophic levels (phytoplankton, zooplankton) generates important food sources for declining higher trophic levels (fish, birds). Here, we study ecosystem restoration project Marker Wadden in Lake Markermeer, The Netherlands. This project involved the construction of a 700-ha archipelago of five islands in a degrading shallow lake, aiming to create additional sheltered land-water transition areas to stimulate food web development from its base by improving phytoplankton quantity and quality. We found that phytoplankton quantity (chlorophyll-a concentration) and quality (inversed carbon:nutrient ratio) in the shallow waters inside the Marker Wadden archipelago were significantly improved, likely due to higher nutrient availabilities, while light availability remained sufficient, compared to the surrounding lake. Higher phytoplankton quantity and quality was positively correlated with zooplankton biomass, which was higher inside the archipelago than in the surrounding lake due to improved trophic transfer efficiency between phytoplankton and zooplankton. We conclude that creating new land-water transition areas can be used to increase light and nutrient availabilities and thereby enhancing primary productivity, which in turn can stimulate higher trophic levels in degrading aquatic ecosystems.
  • Ecology

    Environmental refuges from disease in host‐parasite interactions under global change

    Alena Gsell, Arjen Biere, Wietse de Boer, Irene de Bruijn, Götz Eichhorn, Thijs Frenken, Stefan Geisen, Henk P. van der Jeugd, Kyle Mason-Jones, Annelein Meisner, Maddy Thakur, Ellen Van Donk, Mark Zwart, Dedmer Van de Waal
    The physiological performance of organisms depends on their environmental context, resulting in performance–response curves along environmental gradients. Parasite performance–response curves are generally expected to be broader than those of their hosts due to shorter generation times and hence faster adaptation. However, certain environmental conditions may limit parasite performance more than that of the host, thereby providing an environmental refuge from disease. Thermal disease refuges have been extensively studied in response to climate warming, but other environmental factors may also provide environmental disease refuges which, in turn, respond to global change. Here, we (1) showcase laboratory and natural examples of refuges from parasites along various environmental gradients, and (2) provide hypotheses on how global environmental change may affect these refuges. We strive to synthesize knowledge on potential environmental disease refuges along different environmental gradients including salinity and nutrients, in both natural and food-production systems. Although scaling up from single host–parasite relationships along one environmental gradient to their interaction outcome in the full complexity of natural environments remains difficult, integrating host and parasite performance–response can serve to formulate testable hypotheses about the variability in parasitism outcomes and the occurrence of environmental disease refuges under current and future environmental conditions.
  • Ecology Letters

    Elemental and biochemical nutrient limitation of zooplankton

    Patrick K. Thomas, Charlotte Kunze, Dedmer Van de Waal, Helmut Hillebrand, Maren Striebel
    Primary consumers in aquatic ecosystems are frequently limited by the quality of their food, often expressed as phytoplankton elemental and biochemical composition. However, the effects of these food quality indicators vary across studies, and we lack an integrated understanding of how elemental (e.g. nitrogen, phosphorus) and biochemical (e.g. fatty acid, sterol) limitations interactively influence aquatic food webs. Here, we present the results of a meta-analysis using >100 experimental studies, confirming that limitation by N, P, fatty acids, and sterols all have significant negative effects on zooplankton performance. However, effects varied by grazer response (growth vs. reproduction), specific manipulation, and across taxa. While P limitation had greater effects on zooplankton growth than fatty acids overall, P and fatty acid limitation had equal effects on reproduction. Furthermore, we show that: nutrient co-limitation in zooplankton is strong; effects of essential fatty acid limitation depend on P availability; indirect effects induced by P limitation exceed direct effects of mineral P limitation; and effects of nutrient amendments using laboratory phytoplankton isolates exceed those using natural field communities. Our meta-analysis reconciles contrasting views about the role of various food quality indicators, and their interactions, for zooplankton performance, and provides a mechanistic understanding of trophic transfer in aquatic environments.
  • Biogeosciences

    Physiological control on carbon isotope fractionation in marine phytoplankton

    Karen M. Brandenburg, Björn Rost, Dedmer Van de Waal, Mirja Hoins, Appy Sluijs

    One of the great challenges in biogeochemical research over the past half a century has been to quantify and understand the mechanisms underlying stable carbon isotope fractionation (ϵp) in phytoplankton in response to changing CO2 concentrations. This interest is partly grounded in the use of fossil photosynthetic organism remains as a proxy for past atmospheric CO2 levels. Phytoplankton organic carbon is depleted in 13C compared to its source because of kinetic fractionation by the enzyme RubisCO during photosynthetic carbon fixation, as well as through physiological pathways upstream of RubisCO. Moreover, other factors such as nutrient limitation, variations in light regime as well as phytoplankton culturing systems and inorganic carbon manipulation approaches may confound the influence of aquatic CO2 concentrations [CO2] on ϵp. Here, based on experimental data compiled from the literature, we assess which underlying physiological processes cause the observed differences in ϵp for various phytoplankton groups in response to C-demand/C-supply, i.e., particulate organic carbon (POC) production / [CO2]) and test potential confounding factors. Culturing approaches and methods of carbonate chemistry manipulation were found to best explain the differences in ϵp between studies, although day length was an important predictor for ϵp in haptophytes. Extrapolating results from culturing experiments to natural environments and for proxy applications therefore require caution, and it should be carefully considered whether culture methods and experimental conditions are representative of natural environments.
  • Oecologia

    Impacts of inorganic nutrients on the physiology of a mixoplanktonic ciliate and its cryptophyte prey

    Maira Maselli, Dedmer Van de Waal, Per Juel Hansen

    Many marine planktonic ciliates retain functional chloroplasts from their photosynthetic prey and use them to incorporate inorganic carbon via photosynthesis. While this strategy provides the ciliates with carbon, little is known about their ability to incorporate major dissolved inorganic nutrients, such as nitrogen and phosphorus. Here, we studied how ciliates respond to different concentrations of dissolved inorganic nitrogen and phosphorus. Specifically, we tested the direct and indirect effects of nutrient availability on the ciliate Strombidium cf. basimorphum fed the cryptophyte prey Teleaulax amphioxeia. We assessed responses in the rates of growth, ingestion, photosynthesis, inorganic nutrient uptake, and excretion. Our results show that the prey changed its carbon content depending on the nutrient concentrations. Low inorganic nutrient concentrations increased S. cf. basimorphum growth and prey ingestion. The higher carbon content of the prey under these low nutrient conditions likely supported the growth of the ciliate, while the higher carbon:nutrient stoichiometry of the prey led to the higher ingestion rates. The low carbon content of the prey at high nutrient concentrations resulted in reduced growth of S. cf. basimorphum, which indicates that carbon acquired via photosynthesis in the ciliate cannot compensate for the ingestion of prey with low carbon content. In conclusion, our findings show S. cf. basimorphum is not able to utilize dissolved inorganic nitrogen and phosphorus for growth, and this species seems to be well adapted to exploit its prey when grown at low nutrient conditions.
  • Harmful Algae

    The coupling between irradiance, growth, photosynthesis and prymnesin cell quota and production in two strains of the bloom-forming haptophyte, Prymnesium parvum

    Nikola Medic, Elisabeth Varga, Dedmer Van de Waal, Thomas Ostenfeld Larsen, Per Juel Hansen
    Prymnesium parvum causes harmful algal blooms worldwide that are often associated with massive fish-kills and subsequent economic losses. Most of our knowledge of the toxicity of P. parvum derives from bioassays since methods for the identification and quantification of their toxins have been lacking. Recently, a quantitation method was developed for the causative lytic toxins, the prymnesins. Here, we for the first time present data on the influence of irradiance on cellular content and production of prymnesins under nutrient replete conditions in two P. parvum strains, which both produce B-type prymnesins. Large differences were observed between the two strains with regard to the influence of irradiance on prymnesin cell quota and production rates. At the highest irradiance level (550 µmol photons m−2 s−1), the cellular prymnesin quota was thirty times higher in strain K-0081 strain than in K-0374. The cellular prymnesin quota and production rates were closely linked to rates of growth and photosynthesis in strain K-0081, while this was not the case for K-0374. Yet, growth rate did explain the differences in prymnesin quota in the two strains. Consequently, the maximum prymnesin production rate (414 attomol cell−1 d−1) was only about three times higher in strain K-0081 than in K-0374, and revealed an optimum at the same irradiance of 200 µmol photons m−2 s−1 in both strains. At low irradiance levels, the difference in production rates between both strains became smaller, with 41 and 49 attomol cell−1 d−1 for K-0081 and K-0374, respectively. The carbon content of prymnesins made up for ∼3% and
  • 2022

    Phytoplankton Growth and Nutrients

    S.C. Maberly, Dedmer Van de Waal, J. Raven
    Aims: We describe the different nutrients that phytoplankton require, their variation among phytoplankton groups and their different nutritional modes and acquisition mechanisms. We furthermore describe the consequences of nutrient scarcity and excess on competition among phytoplankton and the effects of anthropogenic nutrient enrichment on phytoplankton community composition, productivity, and ecosystem functioning.

    Main concepts: Nutrient requirements and stoichiometry. Nutrient acquisition mechanisms. Competition for nutrients among taxa. Role of nutrients in controlling productivity. Ecological consequences of varying nutrient availability.

    Main methods: Cell nutrient analysis, growth rate measurements, physiological, biochemical and molecular genetic analysis of acquisition mechanisms. Competition experiments, theoretical modeling of species interactions. Measurements of the physical structure, nutrient chemistry and composition, and abundance of biota in inland waters.

    Conclusions: The concentration of nutrients are low in many inland waters and therefore are a major controlling factor on phytoplankton abundance and productivity. Moreover, because phytoplankton exploit inorganic, dissolved organic and particulate nutrients to satisfy their nutrient requirements, nutrients may become limiting even in nutrient-rich systems. Differential element requirements, uptake rates and storage capacities among taxa, along with other environmental conditions, control phytoplankton community composition. Anthropogenic increases in nutrient loads to inland waters, particularly of phosphorus and nitrogen, has led to widespread eutrophication of inland waters leading to increased productivity. The changed conditions alter phytoplankton species composition, lead to the reduction or loss of freshwater plants and cause oxygen depletion, especially at depth when lakes or reservoirs are stratified. This alters the ecological distribution of species reliant on oxygen, can cause fish kills and produces a positive feedback by increasing the internal load of nutrients stored in the sediment to the overlying water. Future research should investigate the ecological significance of organic nutrients, explore the uptake characteristics of a wider range of taxa and exploit the burgeoning information available from genome sequences.
  • Science of the Total Environment

    Impacts of sediment resuspension on phytoplankton biomass production and trophic transfer: Implications for shallow lake restoration

    Wind-induced sediment resuspension in shallow lakes may enhance nutrient availability while reducing light availability for phytoplankton growth, thereby affecting the entire food-web. Lake restoration projects that reduce wind-induced resuspension are expected to enhance trophic transfer efficiencies, thereby improving food-web structure and functioning. Yet, reduced resuspension may also lead to lower nutrient concentrations in the water column, promote benthic algae development, reduce phytoplankton biomass production and thereby reduce secondary production by zooplankton. Lake Markermeer is a shallow delta lake in The Netherlands subject to wind-induced sediment resuspension. Restoration project Marker Wadden consists of newly built islands aiming to reduce sediment resuspension and promote higher trophic levels. Here, we tested the effects of reduced sediment resuspension on phytoplankton biomass build-up, benthic algae development, and zooplankton abundances at different temperatures in a 14-day indoor microcosm experiment. We used Marker Wadden sediment with three resuspension intensities combined with three temperatures, to also test effects of higher temperatures in shallow sheltered waters. Reduced sediment resuspension decreased nutrient concentrations and phytoplankton biomass build-up, while increasing light availability and enhancing benthic algae biomass development. Reduced sediment resuspension furthermore increased zooplankton biomass. Enhanced sediment resuspension and higher temperatures synergistically interacted, maintaining a high level of inorganic suspended solids. Our experimental results are in line with long-term seasonal observations from Lake Markermeer. Our findings demonstrate that for shallow lakes suffering from wind effects, measures such as Marker Wadden aimed at reducing sediment resuspension can be effective in restoring secondary production and supporting higher trophic levels.
  • Ecological Monographs

    Disease-mediated nutrient dynamics

    Elizabeth T. Borer, Rachel Paseka, Angela Peace, Lale Asik, Rebecca A. Everett, Thijs Frenken, Angélica L. González, Alexander T. Strauss, Dedmer Van de Waal, Lauren A. White, Eric W. Seabloom
    Autotrophs play an essential role in the cycling of carbon and nutrients, yet disease-ecosystem relationships are often overlooked in these dynamics. Importantly, the availability of elemental nutrients like nitrogen and phosphorus impacts infectious disease in autotrophs, and disease can induce reciprocal effects on ecosystem nutrient dynamics. Relationships linking infectious disease with ecosystem nutrient dynamics are bidirectional, though the interdependence of these processes has received little attention. We introduce disease-mediated nutrient dynamics (DND) as a framework to describe the multiple, concurrent pathways linking elemental cycles with infectious disease. We illustrate the impact of disease–ecosystem feedback loops on both disease and ecosystem nutrient dynamics using a simple mathematical model, combining approaches from classical ecological (logistic and Droop growth) and epidemiological (susceptible and infected compartments) theory. Our model incorporates the effects of nutrient availability on the growth rates of susceptible and infected autotroph hosts and tracks the return of nutrients to the environment following host death. While focused on autotroph hosts here, the DND framework is generalizable to higher trophic levels. Our results illustrate the surprisingly complex dynamics of host populations, infection patterns, and ecosystem nutrient cycling that can arise from even a relatively simple feedback between disease and nutrients. Feedback loops in disease-mediated nutrient dynamics arise via effects of infection and nutrient supply on host stoichiometry and population size. Our model illustrates how host growth rate, defense, and tissue chemistry can impact the dynamics of disease–ecosystem relationships. We use the model to motivate a review of empirical examples from autotroph–pathogen systems in aquatic and terrestrial environments, demonstrating the key role of nutrient–disease and disease–nutrient relationships in real systems. By assessing existing evidence and uncovering data gaps and apparent mismatches between model predictions and the dynamics of empirical systems, we highlight priorities for future research intended to narrow the persistent disciplinary gap between disease and ecosystem ecology. Future empirical and theoretical work explicitly examining the dynamic linkages between disease and ecosystem ecology will inform fundamental understanding for each discipline and will better position the field of ecology to predict the dynamics of disease and elemental cycles in the context of global change.
  • Global Challenges

    Microfluidic Impedance Cytometry for Single‐Cell Particulate Inorganic Carbon: Particulate Organic Carbon Measurements of Calcifying Algae

    Douwe S. de Bruijn, Dedmer Van de Waal, Nico Helmsing, Wouter Olthuis, Albert van den Berg
    Calcifying algae, like coccolithophores, greatly contribute to the oceanic carbon cycle and are therefore of particular interest for ocean carbon models. They play a key role in two processes that are important for the effective CO2 flux: The organic carbon pump (photosynthesis) and the inorganic carbon pump (calcification). The relative contribution of calcification and photosynthesis can be measured in algae by the amount of particulate inorganic carbon (PIC) and particulate organic carbon (POC). A microfluidic impedance cytometer is presented, enabling non-invasive and high-throughput assessment of the calcification state of single coccolithophore cells. Gradual modification of the exoskeleton by acidification results in a strong linear fit (R2 = 0.98) between the average electrical phase and the PIC:POC ratio of the coccolithophore Emiliania huxleyi 920/9. The effect of different CO2 treatments on the PIC:POC ratio, however, is inconclusive, indicating that there is no strong effect observed for this particular strain. Lower PIC:POC ratios in cultures that grew to higher cell densities are found, which are also recorded with the impedance-based PIC:POC sensor. The development of this new quantification tool for small volumes paves the way for high-throughput analysis while applying multi-variable environmental stressors to support projections of the future marine carbon cycle.
  • Ecosphere

    Phytoplankton functional composition determines limitation by nutrients and grazers across a lake productivity gradient

    M. Schulhof, Dedmer Van de Waal, Steven A.J. Declerck, J.B. Shurin
    Functional trade-offs among ecologically important traits govern the diversity of communities and changes in species composition along environmental gradients. A trade-off between predator defense and resource competitive ability has been invoked as a mechanism that may maintain diversity in lake phytoplankton. Trade-offs may promote diversity in communities where grazing- and resource-limited taxa coexist, which determines the extent to which communities are resource- or consumer-controlled. In addition, changes in temperature may alter nutrient demands and grazing pressure, changing the balance between the two regulating factors. Our study aims to understand whether a trade-off between grazer vulnerability and nutrient limitation promotes coexistence of phytoplankton functional groups in communities that differ in trophic status, and how this trade-off may shift with warming. We conducted multifactorial experiments manipulating grazing, nutrients, and temperature in phytoplankton communities from three Dutch lakes varying in trophic status, and used a trait-based approach to classify functional groups based on grazing susceptibility. We found no associations between susceptibility to grazing and response to nutrient additions in any of the communities or temperature regimes, indicating that a competition–defense trade-off is unlikely to explain diversity within the tested communities. Instead, we observed a tendency toward both a higher grazing resistance and weaker nutrient limitation along with a shift in the functional composition of phytoplankton in communities across a gradient from low to high productivity.
  • Water Research

    Temperature response of aquatic greenhouse gas emissions differs between dominant plant types

    Ralf C. Aben, Mandy Velthuis, Garabet Kazanjian, Thijs Frenken, Edwin T.H.M. Peeters, Dedmer Van de Waal, Sabine Hilt, Lisette de Senerpont Domis, Leon P. M. Lamers, Sarian Kosten
    Greenhouse gas (GHG) emissions from small inland waters are disproportionately large. Climate warming is expected to favor dominance of algae and free-floating plants at the expense of submerged plants. Through different routes these functional plant types may have far-reaching impacts on freshwater GHG emissions in future warmer waters, which are yet unknown. We conducted a 1,000 L mesocosm experiment testing the effects of plant type and warming on GHG emissions from temperate inland waters dominated by either algae, free-floating or submerged plants in controls and warmed (+4 °C) treatments for one year each. Our results show that the effect of experimental warming on GHG fluxes differs between dominance of different functional plant types, mainly by modulating methane ebullition, an often-dominant GHG emission pathway. Specifically, we demonstrate that the response to experimental warming was strongest for free-floating and lowest for submerged plant-dominated systems. Importantly, our results suggest that anticipated shifts in plant type from submerged plants to a dominance of algae or free-floating plants with warming may increase total GHG emissions from shallow waters. This, together with a warming-induced emission response, represents a so far overlooked positive climate feedback. Management strategies aimed at favouring submerged plant dominance may thus substantially mitigate GHG emissions.
  • Science

    Comment on “Models predict planned phosphorus load reduction will make Lake Erie more toxic”

    Jef Huisman, Elke Dittmann, Jutta Fastner, Merijn Schuurmans, J. Thad Scott, Dedmer Van de Waal, Petra M Visser, Martin Welker, Ingrid Chorus

    Hellweger et al. (Reports, 27 May 2022, pp. 1001) predict that phosphorus limitation will increase concentrations of cyanobacterial toxins in lakes. However, several molecular, physiological, and ecological mechanisms assumed in their models are poorly supported or contradicted by other studies. We conclude that their take-home message that phosphorus load reduction will make Lake Erie more toxic is seriously flawed.
  • Limnology and Oceanography

    Differential effects of elevated pCO2 and warming on marine phytoplankton stoichiometry

    Mandy Velthuis, Joost Keuskamp, (Liesbeth) E.S. Bakker, Maarten Boersma, U. Sommer, Ellen Van Donk, Dedmer Van de Waal
    Phytoplankton stand at the base of the marine food-web, and play a major role in global carbon cycling. Rising CO2 levels and temperatures are expected to enhance growth and alter carbon:nutrient stoichiometry of marine phytoplankton, with possible consequences for the functioning of marine food-webs and the oceanic carbon pump. To date, however, the consistency of phytoplankton stoichiometric responses remains unclear. We therefore performed a meta-analysis on data from experimental studies on stoichiometric responses of marine phytoplankton to elevated pCO2 and 3–5° warming under nutrient replete and limited conditions. Our results demonstrate that elevated pCO2 increased overall phytoplankton C:N (by 4%) and C:P (by 9%) molar ratios under nutrient replete conditions, as well as phytoplankton growth rates (by 6%). Nutrient limitation amplified the CO2 effect on C:N and C:P ratios, with increases to 27% and 17%, respectively. In contrast to elevated pCO2, warming did not consistently alter phytoplankton elemental composition. This could be attributed to species- and study-specific increases and decreases in stoichiometry in response to warming. While our observed moderate CO2-driven changes in stoichiometry are not likely to drive marked changes in food web functioning, they are in the same order of magnitude as current and projected estimations of oceanic carbon export. Therefore, our results may indicate a stoichiometric compensation mechanism for reduced oceanic carbon export due to declining primary production in the near future.
  • Biosensors and Bioelectronics

    Coccolithophore calcification studied by single-cell impedance cytometry: Towards single-cell PIC:POC measurements

    Douwe S. de Bruijn, Paul M. ter Braak, Dedmer Van de Waal, Wouter Olthuis, Albert van den Berg
    Since the industrial revolution 30% of the anthropogenic CO2 is absorbed by oceans, resulting in ocean acidification, which is a threat to calcifying algae. As a result, there has been profound interest in the study of calcifying algae, because of their important role in the global carbon cycle. The species studied, coccolithophore Emiliania huxleyi, is considered to be globally the single most dominant calcifying algae, which creates a unique exoskeleton from inorganic calcium carbonate platelets. The PIC (particulate inorganic carbon): POC (particulate organic carbon) ratio describes the relative amount of inorganic carbon in the algae and is a critical parameter in the ocean carbon cycle. In this research we explore the use of microfluidic single-cell impedance spectroscopy in the field of calcifying algae. Microfluidic impedance spectroscopy enables us to characterize single-cell electrical properties in a non-invasive and label-free way. We use the ratio of the impedance at high frequency vs. low frequency, known as opacity, to discriminate between calcified coccolithophores and coccolithophores with a calcite exoskeleton dissolved by acidification (decalcified). We have demonstrated that using opacity we can discriminate between calcified and decalcified coccolithophores with an accuracy of 94.1%. We have observed a correlation between the measured opacity and the cell height in the channel, which is supported by FEM simulations. The difference in cell density between calcified and decalcified cells can explain the difference in cell height and therefore the measured opacity.
  • Harmful Algae

    Intraspecific variation in multiple trait responses of Alexandrium ostenfeldii towards elevated pCO2

    Karen M. Brandenburg, Bernd Krock, Helena C.L. Klip, Appy Sluijs, Paolina Garbeva, Dedmer Van de Waal

    Dissolved oceanic CO2 concentrations are rising as result of increasing atmospheric partial pressure of CO2 (pCO2), which has large consequences for phytoplankton. To test how higher CO2 availability affects different traits of the toxic dinoflagellate Alexandrium ostenfeldii, we exposed three strains of the same population to 400 and 1,000 µatm CO2, and measured traits including growth rate, cell volume, elemental composition, 13C fractionation, toxin content, and volatile organic compounds (VOCs). Strains largely increased their growth rates and particulate organic carbon and nitrogen production with higher pCO2 and showed significant changes in their VOC profile. One strain showed a significant decrease in both PSP and cyclic imine content and thereby in cellular toxicity. Fractionation against 13C increased in response to elevated pCO2, which may point towards enhanced CO2 acquisition and/or a downscaling of the carbon concentrating mechanisms. Besides consistent responses in some traits, other traits showed large variation in both direction and strength of responses towards elevated pCO2. The observed intraspecific variation in phenotypic plasticity of important functional traits within the same population may help A. ostenfeldii to negate the effects of immediate environmental fluctuations and allow populations to adapt more quickly to changing environments.
  • Quaternary Science Reviews

    Drivers of phytoplankton community structure change with ecosystem ontogeny during the Quaternary

    Aleksandra Cvetkoska, Elena Jovanovska, Torsten Hauffe, Timme H. Donders, Zlatko Levkov, Dedmer Van de Waal, Jane M. Reed, Alexander Francke, Hendrik Vogel, Thomas Wilke, Bernd Wagner, Friederike Wagner-Cremer
    Freshwater species are particularly sensitive to climate fluctuations, but little is known of their response to the large-scale environmental change that took place during the Quaternary. This is partly due to the scarcity of continuously preserved freshwater sedimentary records with orbital chronology. We use a 1.363 Ma high-resolution fossil record of planktonic diatoms from ancient Lake Ohrid to evaluate the role of global and regional versus local-scale environmental change in driving temporal community dynamics. By using a Bayesian joint species distribution model, we found that communities were mostly driven by the local-scale environment. Its effects decreased over time, becoming less important than global and regional environment at the onset of the penultimate glacial, 0.183 Ma. Global and regional control over the environment became important with successive deepening of the lake at around 1.0 Ma, and its influence remained persistent until the present. Our high-resolution data demonstrate the critical role of lake depth and its thermal dynamics in determining phytoplankton response to environmental change by influencing lake mixing, nutrient and light availability. With this study we demonstrate the relative impact of various environmental factors and their scale-dependant effect on the phytoplankton communities during the Quaternary, emphasizing the importance of not only considering climate fluctuations in driving their structure and temporal dynamics but also the local environment.
  • Ecology Letters

    Elements of disease in a changing world

    Elizabeth T. Borer, Lale Asik, Rebecca A. Everett, Thijs Frenken, A.L. Gonzalez, Rachel Paseka, Angela Peace, Eric W. Seabloom, Alexander T. Strauss, Dedmer Van de Waal, Lauren A. White
    An overlooked effect of ecosystem eutrophication is the potential to alter disease dynamics in primary producers, inducing disease‐mediated feedbacks that alter net primary productivity and elemental recycling. Models in disease ecology rarely track organisms past death, yet death from infection can alter important ecosystem processes including elemental recycling rates and nutrient supply to living hosts. In contrast, models in ecosystem ecology rarely track disease dynamics, yet elemental nutrient pools (e.g. nitrogen, phosphorus) can regulate important disease processes including pathogen reproduction and transmission. Thus, both disease and ecosystem ecology stand to grow as fields by exploring questions that arise at their intersection. However, we currently lack a framework explicitly linking these disciplines. We developed a stoichiometric model using elemental currencies to track primary producer biomass (carbon) in vegetation and soil pools, and to track prevalence and the basic reproduction number (R0) of a directly transmitted pathogen. This model, parameterised for a deciduous forest, demonstrates that anthropogenic nutrient supply can interact with disease to qualitatively alter both ecosystem and disease dynamics. Using this element‐focused approach, we identify knowledge gaps and generate predictions about the impact of anthropogenic nutrient supply rates on infectious disease and feedbacks to ecosystem carbon and nutrient cycling.
  • Aquaculture Nutrition

    In situ fatty acid production supports shrimp yields in diets lacking fish oil and fishmeal

    D. Hermsen, Dedmer Van de Waal, Steven A.J. Declerck, J. A. J. Verreth, M. C.J. Verdegem

    Using capture fishery-derived fish oil and fishmeal in aquafeeds is unsustainable. This study mimicked semi-intensive shrimp ponds, including primary producers, in mesocosm tanks. Fatty acid mass balances were computed to distinguish between diet-based and primary production-based LC-PUFA contributions to shrimp (Litopenaeus vannamei) production and meat quality. Performance and body fatty acid composition were compared of shrimp fed a commercial diet containing fish oil and fishmeal (control), with a fishmeal- and fish oil-free diet (low LC-PUFA diet: LOW). Six mesocosms were each stocked with 60 juvenile shrimp and randomly assigned to the two diets. After an 8-week grow-out period, biomass production, survival and proximate body composition were similar between diets. Control shrimp contained twice as much LC-PUFA and omega-3 fatty acids than LOW shrimp. Large quantitative losses (85%) were found in both treatments of the LC-PUFA-precursors alpha-linolenic acid (ALA) and linoleic acid (LA) that were being used as energy source by the shrimp instead for LC-PUFA synthesis. Whereas losses were also observed for eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) in the control group, there was a gain for these components in the LOW tanks. LOW shrimp sourced at least 32% of their total EPA gain and 15% of their total DHA gain from the algal-based food web. This quantitative analysis of the fate of major dietary fatty acids strongly suggests that the pond's primary production can provide shrimp additional LC-PUFA. Finding a balance between LC-PUFA contribution through formulated feed and natural production seems possible and deserves further research.
  • Limnology and Oceanography

    Ecological stoichiometry of functional traits in a colonial harmful cyanobacterium

    Zhipeng Duan, Xiao Tan, Hans W. Paerl, Dedmer Van de Waal
    Trait-based approaches provide a mechanistic framework crossing scales from cellular traits to community dynamics, while ecological stoichiometry applies first principles to understand how the balance of energy and elements shape ecological interactions. However, few studies have explicitly linked both frameworks. In this study, we tested the stoichiometric regulation of a number of carbon (C) based (e.g., extracellular polysaccharides and colony formation) and nitrogen (N) containing traits (i.e., chlorophyll a, phycocyanin, and gas vesicle content) in cyanobacteria in laboratory experiments and in the field. We exposed the cosmopolitan colony forming freshwater cyanobacterium Microcystis sp. in batch experiments to light, N and phosphorus (P) limitation, and enhanced CO2 levels, and assessed the regulation of these traits. Cyanobacterial traits followed stoichiometrically predictable patterns, where N containing traits increased with cellular N content, and decreased with increasing C : N ratios. C-based traits increased with cellular C content and C : N ratios under nutrient, particularly N, limitation. The pattern of colony formation was confirmed with field data from Lake Taihu (China), showing an increase in colony size when N was limiting and N : P ratios were low. These findings demonstrate how an explicit coupling of trait-based approaches to ecological stoichiometry can support our mechanistic understanding of responses of cyanobacteria toward shifts in resource availability.
  • Freshwater Biology

    Shifting states, shifting services: Linking regime shifts to changes in ecosystem services of shallow lakes

    Annette B.G. Janssen, Sabine Hilt, Sarian Kosten, J. de Klein, Hans W. Paerl, Dedmer Van de Waal
    Shallow lakes can shift between stable states as a result of anthropogenic or natural drivers. Four common stable states differ in dominant groups of primary producers: submerged, floating, or emergent macrophytes or phytoplankton. Shifts in primary producer dominance affect key supporting, provisioning, regulating, and cultural ecosystem services supplied by lakes. However, links between states and services are often neglected or unknown in lake management, resulting in conflicts and additional costs.
    Here, we identify major shallow lake ecosystem services and their links to Sustainable Development Goals (SDGs), compare service provisioning among the four ecosystem states and discuss potential trade‐offs.
    We identified 39 ecosystem services potentially provided by shallow lakes. Submerged macrophytes facilitate most of the supporting (86%) and cultural (63%) services, emergent macrophytes facilitate most regulating services (60%), and both emergent and floating macrophytes facilitate most provisioning services (63%). Phytoplankton dominance supports fewer ecosystem services, and contributes most to provisioning services (42%).
    The shallow lake ecosystem services we identified could be linked to 10 different SDGs, notably zero hunger (SDG 2), clean water and sanitation (SDG 6), sustainable cities and communities (SDG 11), and climate action (SDG13).
    We highlighted several trade‐offs (1) among ecosystem services, (2) within ecosystem services, and (3) between ecosystem services across ecosystems. These trade‐offs can have significant ecological and economic consequences that may be prevented by early identification in water quality management.
    In conclusion, common stable states in shallow lakes provide a different and diverse set of ecosystem services with numerous links to the majority of SDGs. Conserving and restoring ecosystem states should account for potential trade‐offs between ecosystem services and preserving the natural value of shallow lakes.
  • 2021

    HABs under global change: Experimental conditions and approaches

    Dedmer Van de Waal, Lennart T. Bach, E. Berdalet, Karen M. Brandenburg, Sanna Suikkanen, Sylke Wohlrab, Per Juel Hansen, Anke Kremp
  • Oikos

    Changing elemental cycles, stoichiometric mismatches, and consequences for pathogens of primary producers

    Thijs Frenken, Rachel Paseka, Angélica L. González, Lale Asik, Eric W. Seabloom, Lauren A. White, Elizabeth T. Borer, Alexander T. Strauss, Angela Peace, Dedmer Van de Waal
    Human-induced changes in biogeochemical cycles alter the availability of carbon (C), nitrogen (N) and phosphorus (P) in the environment, leading to changes in the elemental stoichiometry of primary producers. These changes in elemental ratios may, in turn, alter the degree of stoichiometric mismatch between primary producer hosts and their pathogens. Here, we outline how ecological stoichiometry could be used as a framework to predict the effects of changing nutrient supply on stoichiometric mismatches in autotroph–pathogen interactions. We discuss empirical evidence linking pathogen performance to stoichiometric mismatches arising from shifts in elemental availability. Our synthesis indicates that fungi may be particularly sensitive to changes in N supply and viruses generally respond strongly to changes in the supply of either of these elements, but it also highlighted the need for additional data, especially for bacteria. Consequently, fungal pathogens may respond more strongly to changes in host C:N stoichiometry, whereas viruses may be highly sensitive to both changes in C:N and C:P of hosts. Additionally, our synthesis suggests that viruses may be more homeostatic than fungi, and therefore respond more strongly to changing elemental supplies. Revealing stoichiometric mismatches may greatly support our understanding of how host–pathogen interactions in primary producers will respond to changes in global biogeochemical cycles, controlling disease incidence in primary producers under scenarios of global change.
  • Harmful Algae

    Ocean acidification increases domoic acid contents during a spring to summer succession of coastal phytoplankton

    S. Wohlrab, U. John, K. Klemm, Tim Eberlein, A.M. Forsberg Grivogiannis, Bernd Krock, S. Firckenhaus, Lennart T. Bach, B. Rost, U. Riebesell, Dedmer Van de Waal
    Enrichment of the oceans with CO2 may be beneficial for some marine phytoplankton, including harmful algae. Numerous laboratory experiments provided valuable insights into the effects of elevated pCO2 on the growth and physiology of harmful algal species, including the production of phycotoxins. Experiments close to natural conditions are the next step to improve predictions, as they consider the complex interplay between biotic and abiotic factors that can confound the direct effects of ocean acidification. We therefore investigated the effect of ocean acidification on the occurrence and abundance of phycotoxins in bulk plankton samples during a long-term mesocosm experiment in the Gullmar Fjord, Sweden, an area frequently experiencing harmful algal blooms. During the experimental period, a total of seven phycotoxin-producing harmful algal genera were identified in the fjord, and in accordance, six toxin classes were detected. However, within the mesocosms, only domoic acid and the corresponding producer Pseudo-nitzschia spp. was observed. Despite high variation within treatments, significantly higher particulate domoic acid contents were measured in the mesocosms with elevated pCO2. Higher particulate domoic acid contents were additionally associated with macronutrient limitation. The risks associated with potentially higher phycotoxin levels in the future ocean warrants attention and should be considered in prospective monitoring strategies for coastal marine waters.
  • Ecology

    The potential of zooplankton in constraining chytrid epidemics in phytoplankton hosts

    Thijs Frenken, Takeshi Miki, M. Kagami, Dedmer Van de Waal, Ellen Van Donk, Thomas Rohrlack, Alena Gsell
    Abstract Fungal diseases threathen natural and man-made ecosystems. Chytridiomycota (chytrids) infect a wide host range, including phytoplankton species that form the basis of aquatic food webs and produce roughly half of Earth's oxygen. However, blooms of large or toxic phytoplankton form trophic bottlenecks as they are inedible to zooplankton. Chytrids infecting inedible phytoplankton provide a trophic link to zooplankton by producing edible zoospores of high nutritional quality. By grazing chytrid zoospores, zooplankton may induce a trophic cascade as a decreased zoospore density will reduce new infections. Conversely, fewer infections will not produce enough zoospores to sustain long-term zooplankton growth and reproduction. This intricate balance between zoospore density necessary for zooplankton energetic demands (growth/survival), and the loss in new infections (and thus new zoospores) due to grazing was tested empirically. To this end, we exposed a cyanobacterial host (Planktothrix rubescens) infected by a chytrid (Rizophydium megarrhizum) to a grazer density gradient (the rotifer Keratella cf. cochlearis). Rotifers survived and reproduced on a zoospore diet, but the Keratella population growth was limited by the amount of zoospores provided by chytrid infections, resulting in a situation where zooplankton survived but was restricted in their ability to control disease in the cyanobacterial host. We subesequently developed and parameterized a dynamical food-chain model using an allometric relationship for clearance rate to theoretically assess the potential of different-sized zooplankton groups to restrict disease in phytoplankton hosts. Our model suggests that smaller-sized zooplankton may have a high potential to reduce chytrid infections on inedible phytoplankton. Together, our results point out the complexity of tri-way interactions between hosts-parasites-grazers, and highlight that trophic cascades are not always sustainable and may depend on the grazer's energetic demand.
  • Trends in Ecology & Evolution

    Disease-mediated ecosystem services: Pathogens, plants, and people

    Rachel Paseka, Lauren A. White, Dedmer Van de Waal, Alexander T. Strauss, Angélica L. González, Rebecca A. Everett, Angela Peace, Eric W. Seabloom, Thijs Frenken, Elizabeth T. Borer
    Despite the ubiquity of pathogens in ecological systems, their roles in influencing ecosystem services are often overlooked. Pathogens that infect primary producers (i.e., plants, algae, cyanobacteria) can have particularly strong effects because autotrophs are responsible for a wide range of provisioning, regulating, and cultural services. We review the roles of pathogens in mediating ecosystem services provided by autotrophs and outline scenarios in which infection may lead to unexpected outcomes in response to global change. Our synthesis highlights a deficit of information on this topic, and we outline a vision for future research that includes integrative theory and cross-system empirical studies. Ultimately, knowledge about the mediating roles of pathogens on ecosystem services should inform environmental policy and practice.
  • Limnology & Oceanography Letters

    Warming advances virus population dynamics in a temperate freshwater plankton community

    Thijs Frenken, Corina P. D. Brussaard, Mandy Velthuis, Ralf C. Aben, Garabet Kazanjian, Sabine Hilt, Sarian Kosten, Edwin T.H.M. Peeters, Lisette de Senerpont Domis, Susanne Stephan, Ellen Van Donk, Dedmer Van de Waal
    Viruses are important drivers in the cycling of carbon and nutrients in aquatic ecosystems. Since viruses are obligate parasites, their production completely depends on growth and metabolism of hosts and therefore can be affected by climate change. Here, we investigated if warming (+4°C) can change the outcome of viral infections in a natural freshwater virus community over a 5‐month period in a mesocosm experiment. We monitored dynamics of viruses and potential hosts. Results show that warming significantly advanced the early summer peak of the virus community by 24 d, but neither affected viral peak abundances nor time‐integrated number of viruses present. Our results demonstrate that warming advances the timing of viruses in a natural community. Although warming may not necessarily result in a stronger viral control of bacterial and phytoplankton communities, our results suggest it can alter host population dynamics through advanced timing of infections, and thus timing of carbon and nutrient recycling.
  • Oecologia

    Trophic position, elemental ratios and nitrogen transfer in a planktonic host–parasite–consumer food chain including a fungal parasite

    Virginia Sánchez Barranco, M.T.J. Van der Meer, M. Kagami, Silke van den Wyngaert, Dedmer Van de Waal, Ellen Van Donk, Alena Gsell
    Parasitism is arguably the most commonly occurring consumer strategy. However, only a few food web studies assess how well stable isotopes reflect the trophic position of parasitic consumers and results are variable. Even fewer studies have measured the nutrient transfer by parasitic consumers, hindering an assessment of their role in nutrient transfer through food webs. Here we used a food chain consisting of a diatom as host, a chytrid as its parasitic consumer and a rotifer as the predatory consumer of the chytrid, to assess the trophic position of all three food-chain components using their natural 13C and 15N isotope signatures, and to measure the nitrogen transfer from the host via the chytrid to the rotifer by tracing 15N of a labelled host up the food chain. Additionally, we measured the carbon to nitrogen (C:N) ratios of all food-chain components. Natural isotope abundance results showed no clear 15N enrichment in the chytrid or rotifer relative to the primary producer. However, estimates of nitrogen transfer indicated that about 14% of host nitrogen was transferred per day from host to chytrid during infection epidemics and that some of this nitrogen was also transferred onward to the rotifer. Moreover, C:N ratios decreased with trophic level, suggesting that the chytrid provided a high-quality food source to the rotifer. In conclusion, our results support the “mycoloop”. The mycooloop proposes that chytrid infections allow the transfer of nutrients bound in large, inedible phytoplankton to zooplankton through the production of edible transmission spores, thereby rerouting nutrients back into the food web.
  • Frontiers in Microbiology

    Cyanophage Propagation in the Freshwater Cyanobacterium Phormidium Is Constrained by Phosphorus Limitation and Enhanced by Elevated pCO2

    Kai Cheng, Thijs Frenken, C.P.D. Brussaard, Dedmer Van de Waal
    Intensification of human activities has led to changes in the availabilities of CO2 and nutrients in freshwater ecosystems, which may greatly alter the physiological status of phytoplankton. Viruses require hosts for their reproduction and shifts in phytoplankton host physiology through global environmental change may thus affect viral infections as well. Various studies have investigated the impacts of single environmental factors on phytoplankton virus propagation, yet little is known about the impacts of multiple factors, particularly in freshwater systems. We therefore tested the combined effects of phosphorus limitation and elevated pCO2 on the propagation of a cyanophage infecting a freshwater cyanobacterium. To this end, we cultured Phormidium in P-limited chemostats under ambient (400 μatm) and elevated (800 μatm) pCO2 at growth rates of 0.6, 0.3, and 0.05 d-1. Host C:P ratios generally increased with strengthened P-limitation and with elevated pCO2. Upon host steady state conditions, virus growth characteristics were obtained in separate infection assays where hosts were infected by the double-stranded DNA cyanophage PP. Severe P-limitation (host growth 0.05 d-1) led to a 85% decrease in cyanophage production rate and a 73% decrease in burst size compared to the 0.6 d-1 grown P-limited cultures. Elevated pCO2 induced a 96% increase in cyanophage production rate and a 57% increase in burst size, as well as an 85% shorter latent period as compared to ambient pCO2 at the different host growth rates. In addition, elevated pCO2 caused a decrease in the plaquing efficiency and an increase in the abortion percentage for the 0.05 d-1 P-limited treatment, while the plaquing efficiency increased for the 0.6 d-1 P-limited cultures. Together, our results demonstrate interactive effects of elevated pCO2 and P-limitation on cyanophage propagation, and show that viral propagation is generally constrained by P-limitation but enhanced with elevated pCO2. Our findings indicate that global change will likely have a severe impact on virus growth characteristics and thereby on the control of cyanobacterial hosts in freshwater ecosystems.
  • Bioresource Technology

    Enhancement of co-production of nutritional protein and carotenoids in Dunaliella salina using a two-phase cultivation assisted by nitrogen level and light intensity

    Yixing Sui, Maarten Muys, Dedmer Van de Waal, Sarah D'Adamo, Pieter Vermeir, Tania Vasconcelos Fernandes, Siegfried E. Vlaeminck
    Microalga Dunaliella salina is known for its carotenogenesis. At the same time, it can also produce high-quality protein. The optimal conditions for D. salina to co-produce intracellular pools of both compounds, however, are yet unknown. This study investigated a two-phase cultivation strategy to optimize combined high-quality protein and carotenoid production of D. salina. In phase-one, a gradient of nitrogen concentrations was tested. In phase-two, effects of nitrogen pulse and high illumination were tested. Results reveal optimized protein quantity, quality (expressed as essential amino acid index EAAI) and carotenoids content in a two-phase cultivation, where short nitrogen starvation in phase-one was followed by high illumination during phase-two. Adopting this strategy, productivities of protein, EAA and carotenoids reached 22, 7 and 3 mg/L/d, respectively, with an EAAI of 1.1. The quality of this biomass surpasses FAO/WHO standard for human nutrition, and the observed level of β-carotene presents high antioxidant pro-vitamin A activity.
  • Global Change Biology

    Phytoplankton growth and stoichiometric responses to warming, nutrient addition and grazing depend on lake productivity and cell size

    M. Schulhof, Jonathan B. Shurin, Steven A.J. Declerck, Dedmer Van de Waal
    Abstract Global change involves shifts in multiple environmental factors that act in concert to shape ecological systems in ways that depend on local biotic and abiotic conditions. Little is known about the effects of combined global change stressors on phytoplankton communities, and particularly how these are mediated by distinct community properties such as productivity, grazing pressure and size distribution. Here, we tested for the effects of warming and eutrophication on phytoplankton net growth rate and C:N:P stoichiometry in two phytoplankton cell size fractions (30?m) in the presence and absence of grazing in microcosm experiments. Because effects may also depend on lake productivity, we used phytoplankton communities from three Dutch lakes spanning a trophic gradient. We measured the response of each community to multifactorial combinations of temperature, nutrient, and grazing treatments and found that nutrients elevated net growth rates and reduced carbon:nutrient ratios of all three phytoplankton communities. Warming effects on growth and stoichiometry depended on nutrient supply and lake productivity, with enhanced growth in the most productive community dominated by cyanobacteria, and strongest stoichiometric responses in the most oligotrophic community at ambient nutrient levels. Grazing effects were also most evident in the most oligotrophic community, with reduced net growth rates and phytoplankton C:P stoichiometry that suggests consumer-driven nutrient recycling. Our experiments indicate that stoichiometric responses to warming and interactions with nutrient addition and grazing are not universal but depend on lake productivity and cell size distribution. This article is protected by copyright. All rights reserved.
  • Limnology & Oceanography Letters

    Highest plasticity of carbon-concentrating mechanisms in earliest evolved phytoplankton

    Dedmer Van de Waal, Karen M. Brandenburg, Joost Keuskamp, S. Trimborn, S. Rokitta, S.A. Kranz, B. Rost
    Phytoplankton photosynthesis strongly relies on the operation of carbon‐concentrating mechanisms (CCMs) to accumulate CO2 around their carboxylating enzyme ribulose‐1,5‐bisphosphate carboxylase/oxygenase (RuBisCO). Earlier evolved phytoplankton groups were shown to exhibit higher CCM activities to compensate for their RuBisCO with low CO2 specificities. Here, we tested whether earlier evolved phytoplankton groups also exhibit a higher CCM plasticity. To this end, we collected data from literature and applied a Bayesian linear meta‐analytic model. Our results show that with elevated pCO2, photosynthetic CO2 affinities decreased strongest and most consistent for the earlier evolved groups, i.e., cyanobacteria and dinoflagellates, while CO2‐dependent changes in affinities for haptophytes and diatoms were smaller and less consistent. In addition, responses of maximum photosynthetic rates toward elevated pCO2 were generally small and inconsistent across species. Our results demonstrate that phytoplankton groups with an earlier origin possess a high CCM plasticity, whereas more recently evolved groups do not, which likely results from evolved differences in the CO2 specificity of RuBisCO.
  • Global Change Biology

    Meta-analysis reveals enhanced growth of marine harmful algae from temperate regions with warming and elevated CO2 levels

    Karen M. Brandenburg, Mandy Velthuis, Dedmer Van de Waal
    Abstract Elevated pCO2 and warming may promote algal growth and toxin production, and thereby possibly support the proliferation and toxicity of HABs. Here, we tested whether empirical data supports this hypothesis using a meta-analytic approach and investigated the responses of growth rate and toxin content or toxicity of numerous marine and estuarine HAB species to elevated pCO2 and warming. Most of the available data on HAB responses towards the two tested climate change variables concerns dinoflagellates, as many members of this phytoplankton group are known to cause HAB outbreaks. Toxin content and toxicity did not reveal a consistent response towards both tested climate change variables, while growth rate increased consistently with elevated pCO2. Warming also led to higher growth rates, but only for species isolated at higher latitudes. The observed gradient in temperature growth responses shows the potential for enhanced development of HABs at higher latitudes. Increases in growth rates with more CO2 may present an additional competitive advantage for HAB species, particularly as CO2 was not shown to enhance growth rate of other non-HAB phytoplankton species. However, this may also be related to the difference in representation of dinoflagellate and diatom species in the respective HAB and non-HAB phytoplankton groups. Since the proliferation of HAB species may strongly depend on their growth rates, our results warn for a greater potential of dinoflagellate HAB development in future coastal waters, particularly in temperate regions. This article is protected by copyright. All rights reserved.
  • Frontiers in Microbiology

    Editorial: Progress in Ecological Stoichiometry

    Dedmer Van de Waal, J.J. Elser, A.C. Martiny, Robert Werner Sterner, James B. Cotner
  • Scientific Reports

    Impacts of warming on top-down and bottom-up controls of periphyton production

    Garabet Kazanjian, Mandy Velthuis, Ralf C. Aben, Susanne Stephan, Edwin T.H.M. Peeters, Thijs Frenken, Jell Touwen, Fei Xue, Sarian Kosten, Dedmer Van de Waal, Lisette de Senerpont Domis, Ellen Van Donk, Sabine Hilt
    Global warming profoundly impacts the functioning of aquatic ecosystems. Nonetheless, the effect of warming on primary producers is poorly understood, especially periphyton production, which is affected both directly and indirectly by temperature-sensitive top-down and bottom-up controls. Here, we study the impact of warming on gross primary production in experimental ecosystems with near-realistic foodwebs during spring and early summer. We used indoor mesocosms following a temperate temperature regime (control) and a warmed (+4 °C) treatment to measure biomass and production of phytoplankton and periphyton. The mesocosms’ primary production was dominated by periphyton (>82%) during the studied period (April-June). Until May, periphyton production and biomass were significantly higher in the warm treatment (up to 98% greater biomass compared to the control) due to direct temperature effects on growth and indirect effects resulting from higher sediment phosphorus release. Subsequently, enhanced grazer abundances seem to have counteracted the positive temperature effect causing a decline in periphyton biomass and production in June. We thus show, within our studied period, seasonally distinct effects of warming on periphyton, which can significantly affect overall ecosystem primary production and functioning.
  • Algal Research

    Biological stoichiometry of oleaginous microalgal lipid synthesis: The role of N:P supply ratios and growth rate on microalgal elemental and biochemical composition

    Baoyan Gao, Jing Liu, Chengwu Zhang, Dedmer Van de Waal
    Abstract Biological Stoichiometry is an ecological framework connecting the balance of elements to the functioning of organisms. Here, we applied this framework to study the relationships between carbon:nitrogen:phosphorus (C:N:P) ratios and synthesis of industrial high value biochemicals in the highly oleaginous alga Tetradesmus bernardii. We expected an increase in protein content with increasing cellular N content and decreasing C:N stoichiometry, and an increase in lipid content with increasing C:N and C:P stoichiometry. We tested these hypotheses by exposing T. bernardii to N and P limitation at a range of N:P supply ratios in chemostats set at low and high dilution rates. Following expectations, the cellular protein content increased with the N content, and decreased with cellular C:N ratios across all treatments. Carbohydrates and lipids largely followed the relative availability of C and increased under both N and P limitation, with higher C:N and C:P ratios. Specifically, lipid content increased by 100–125% upon N and P limitation, with a shift towards more neutral lipids at the cost of glycolipids and phospholipids. Generally, we observed a re-allocation of cellular C from protein to carbohydrates upon modest N limitation, and towards lipids under P and severe N limitation. Our results demonstrate stoichiometrically predictable patterns of industrially valuable compounds in an oleaginous microalga.
  • Harmful Algae

    Molecular detection of harmful cyanobacteria and expression of their toxin genes in Dutch lakes using multi-probe RNA chips

    Dedmer Van de Waal, Delphine Guillebault, Amparo Alfonso, Inés Rodríguez, Luis M. Botana, Ronald Bijkerk, Linda K. Medlin
    Abstract Harmful cyanobacterial blooms are a major threat to water quality and human health. Adequate risk assessment is thus required, which relies strongly on comprehensive monitoring. Here, we tested novel multi-probe RNA chips developed in the European project, μAqua, to determine the abundance of harmful cyanobacterial species and expression of selected toxin genes in six Dutch lakes. All of the targeted cyanobacterial genera, except for Planktothrix, were detected using the microarray, with predominance of Dolichospermum and Microcystis signals, of which the former was found across all sites and detected by the probes for Anabaena where it was formerly placed. These were confirmed by microscopic cell counts at three sites, whereas at the other sites, microscopic cell counts were lower. Probe signals of Microcystis showed larger variation across sites but also matched microscopic counts for three sites. At the other sites, microscopic counts were distinctly higher. We detected anatoxin-a in the water at all sites, but unfortunately no genes for this toxin were on this generation of the toxin array. For microcystins, we found none or low concentrations in the water, despite high population densities of putative microcystin producers (i.e. Microcystis, Dolichospermum). The described method requires further testing with a wider range of cyanobacterial communities and toxin concentrations before implementation into routine cyanobacterial risk assessment. Yet, our results demonstrate a great potential for applying multi-probe RNA chips for species as well as toxins to eutrophic waters with high cyanobacterial densities as a routine monitoring tool and as a predictive tool for toxin potential.
  • Limnology and Oceanography

    Fungal parasites of a toxic inedible cyanobacterium provide food to zooplankton

    Thijs Frenken, Joren Wierenga, Ellen Van Donk, Steven A.J. Declerck, Lisette de Senerpont Domis, Thomas Rohrlack, Dedmer Van de Waal
    During the end of spring and throughout summer, large‐sized phytoplankton taxa often proliferate and form dense blooms in freshwater ecosystems. In many cases, they are inedible to zooplankton and prevent efficient transfer of energy and elements to higher trophic levels. Such a constraint may be alleviated by fungal parasite infections on large‐sized phytoplankton taxa like diatoms and filamentous cyanobacteria, as infections may provide zooplankton with a complementary food source in the form of fungal zoospores. Zoospores have been shown to support somatic growth of large filter feeding zooplankton species. Here, we tested if selectively feeding zooplankton, more specifically rotifers, also can use fungal zoospores as a food source. Our results show that chytrid fungal parasites can indeed support population growth of rotifers (Keratella sp.). Specifically, in cultures of an inedible filamentous cyanobacterium (Planktothrix rubescens), Keratella populations rapidly declined, while in Planktothrix cultures infected with chytrids, Keratella population growth rate equaled the growth observed for populations fed with a more suitable green algal diet (Chlorella sorokiniana). Feeding of Keratella on zoospores was furthermore indicated by a reduced number of zoospores during the last sampling day. These findings not only imply that rotifers may survive on zoospores, but also that the zoospores can support high rotifer population growth rates. We thus show that fungal parasites of inedible cyanobacteria can facilitate grazers by providing them alternative food sources. Together, these results highlight the important role that parasites may play in the aquatic plankton food web.
  • Ecology Letters

    Intraspecific trait variation and trade-offs within and across populations of a toxic dinoflagellate

    Karen M. Brandenburg, Sylke Wohlrab, Uwe John, Anke Kremp, Jacqueline Jerney, Bernd Krock, Dedmer Van de Waal
    Abstract Intraspecific trait diversity can promote the success of a species, as complementarity of functional traits within populations may enhance its competitive success and facilitates resilience to changing environmental conditions. Here, we experimentally determined the variation and relationships between traits in 15 strains of the toxic dinoflagellate Alexandrium ostenfeldii derived from two populations. Measured traits included growth rate, cell size, elemental composition, nitrogen uptake kinetics, toxin production and allelochemical potency. Our results demonstrate substantial variation in all analysed traits both within and across populations, particularly in nitrogen affinity, which was even comparable to interspecific variation across phytoplankton species. We found distinct trade-offs between maximum nitrogen uptake rate and affinity, and between defensive and competitive traits. Furthermore, we identified differences in trait variation between the genetically similar populations. The observed high trait variation may facilitate development and resilience of harmful algal blooms under dynamic environmental conditions.
  • Journal of Applied Ecology

    Biodiversity change is uncoupled from species richness trends: consequences for conservation and monitoring

    Helmut Hillebrand, Bernd Blasius, Elizabeth T. Borer, Jonathan M. Chase, John Downing, Britas Klemens Eriksson, Christopher T. Filstrup, W. Stanley Harpole, Dorothee Hodapp, Stefano Larsen, Aleksandra M. Lewandowska, Eric W. Seabloom, Dedmer Van de Waal, Alexey B. Ryabov
    * Global concern about human impact on biological diversity has triggered an intense research agenda on drivers and consequences of biodiversity change in parallel with international policy seeking to conserve biodiversity and associated ecosystem functions. Quantifying the trends in biodiversity is far from trivial however, as recently documented by meta-analyses, which report little if any net change of local species richness through time. * Here, we summarize several limitations of species richness as a metric of biodiversity change and show that the expectation of directional species richness trends under changing conditions is invalid. Instead, we illustrate how a set of species turnover indices provide more information content regarding temporal trends in biodiversity, as they reflect how dominance and identity shift in communities over time. * We apply these metrics to three monitoring data sets representing different ecosystem types. In all data sets, nearly complete species turnover occurred, but this was disconnected from any species richness trends. Instead, turnover was strongly influenced by changes in species presence (identities) and dominance (abundances). We further show that these metrics can detect phases of strong compositional shifts in monitoring data and thus identify a different aspect of biodiversity change decoupled from species richness. * Synthesis and applications: Temporal trends in species richness are insufficient to capture key changes in biodiversity in changing environments. In fact, reductions in environmental quality can lead to transient increases in species richness if immigration or extinction have different temporal dynamics. Thus, biodiversity monitoring programs need to go beyond analyses of trends in richness in favour of more meaningful assessments of biodiversity change. This article is protected by copyright. All rights reserved.
  • Harmful Algae

    Combined physical, chemical and biological factors shape Alexandrium ostenfeldii blooms in the Netherlands

    Karen M. Brandenburg, Lisette de Senerpont Domis, Sylke Wohlrab, Bernd Krock, Uwe John, Yvonne van Scheppingen, Ellen Van Donk, Dedmer Van de Waal
    Abstract Harmful algal blooms (HABs) are globally expanding, compromising water quality worldwide. HAB dynamics are determined by a complex interplay of abiotic and biotic factors, and their emergence has often been linked to eutrophication, and more recently to climate change. The dinoflagellate Alexandrium is one of the most widespread HAB genera and its success is based on key functional traits like allelopathy, mixotrophy, cyst formation and nutrient retrieval migrations. Since 2012, dense Alexandrium ostenfeldii blooms (up to 4500 cells mL−1) have recurred annually in a creek located in the southwest of the Netherlands, an area characterized by intense agriculture and aquaculture. We investigated how physical, chemical and biological factors influenced A. ostenfeldii bloom dynamics over three consecutive years (2013–2015). Overall, we found a decrease in the magnitude of the bloom over the years that could largely be linked to changing weather conditions during summer. More specifically, low salinities due to excessive rainfall and increased wind speed corresponded to a delayed A. ostenfeldii bloom with reduced population densities in 2015. Within each year, highest population densities generally corresponded to high temperatures, low DIN:DIP ratios and low grazer densities. Together, our results demonstrate an important role of nutrient availability, absence of grazing, and particularly of the physical environment on the magnitude and duration of A. ostenfeldii blooms. Our results suggest that predicted changes in the physical environment may enhance bloom development in future coastal waters and embayments.
  • PLoS One

    Effects of ocean acidification on primary production in a coastal North Sea phytoplankton community

    Tim Eberlein, Sylke Wohlrab, Björn Rost, Uwe John, Lennart T. Bach, U. Riebesell, Dedmer Van de Waal
    We studied the effect of ocean acidification (OA) on a coastal North Sea plankton community in a long-term mesocosm CO2-enrichment experiment (BIOACID II long-term mesocosm study). From March to July 2013, 10 mesocosms of 19 m length with a volume of 47.5 to 55.9 m3 were deployed in the Gullmar Fjord, Sweden. CO2 concentrations were enriched in five mesocosms to reach average CO2 partial pressures (pCO2) of 760 μatm. The remaining five mesocosms were used as control at ambient pCO2 of 380 μatm. Our paper is part of a PLOS collection on this long-term mesocosm experiment. Here, we here tested the effect of OA on total primary production (PPT) by performing 14C-based bottle incubations for 24 h. Furthermore, photoacclimation was assessed by conducting 14C-based photosynthesis-irradiance response (P/I) curves. Changes in chlorophyll a concentrations over time were reflected in the development of PPT, and showed higher phytoplankton biomass build-up under OA. We observed two subsequent phytoplankton blooms in all mesocosms, with peaks in PPT around day 33 and day 56. OA had no significant effect on PPT, except for a marginal increase during the second phytoplankton bloom when inorganic nutrients were already depleted. Maximum light use efficiencies and light saturation indices calculated from the P/I curves changed simultaneously in all mesocosms, and suggest that OA did not alter phytoplankton photoacclimation. Despite large variability in time-integrated productivity estimates among replicates, our overall results indicate that coastal phytoplankton communities can be affected by OA at certain times of the seasonal succession with potential consequences for ecosystem functioning.
  • Ecosphere

    Warming advances top-down control and reduces producer biomass in a freshwater plankton community

    Mandy Velthuis, Lisette de Senerpont Domis, Thijs Frenken, Susanne Stephan, Garabet Kazanjian, Ralf C. Aben, Sabine Hilt, Sarian Kosten, Ellen Van Donk, Dedmer Van de Waal
    Global warming has been shown to affect ecosystems worldwide. Warming may, for instance, disrupt plant herbivore synchrony and bird phenology in terrestrial systems, reduce primary production in oceans, and promote toxic cyanobacterial blooms in freshwater lakes. Responses of communities will not only depend on direct species-specific temperature effects, but also on indirect effects related to bottom-up and top-down processes. Here, we investigated the impact of warming on freshwater phytoplankton community dynamics, and assessed the relative contribution of nutrient availability, fungal parasitism, and grazing therein. For this purpose, we performed an indoor mesocosm experiment following seasonal temperature dynamics of temperate lakes and a warmed (+4°C) scenario from early spring to late summer. We assessed phytoplankton biomass, C:N:P stoichiometry and community composition, dissolved nutrient availabilities, fungal parasite (i.e., chytrid) prevalence, and zooplankton abundance. Warming led to an overall reduction in phytoplankton biomass as well as lower C:P and N:P ratios, while phytoplankton community composition remained largely unaltered. Warming resulted in an earlier termination of the diatom spring bloom, and an epidemic of its fungal parasite ended earlier as well. Furthermore, warming advanced zooplankton phenology, leading to an earlier top-down control on phytoplankton in the period after the spring bloom. Linear model analysis showed that most of the observed variance in phytoplankton biomass was related to seasonal temperature dynamics in combination with zooplankton abundance. Our findings showed that warming advanced grazer phenology and reduced phytoplankton biomass, thereby demonstrating how bottom-up and top-down related processes may shape future phytoplankton dynamics.
  • Frontiers in Microbiology

    Toward an Ecologically Optimized N:P Recovery from Wastewater by Microalgae

    Tania Vasconcelos Fernandes, María Suárez-Muñoz, Lukas M. Trebuch, Paul J. Verbraak, Dedmer Van de Waal
    Global stores of important resources such as phosphorus (P) are being rapidly depleted, while the excessive use of nutrients has led to the enrichment of surface waters worldwide. Ideally, nutrients would be recovered from wastewater, which will not only prevent eutrophication but also provide access to alternative nutrient stores. Current state-of-the-art wastewater treatment technologies are effective in removing these nutrients from wastewater, yet they can only recover P and often in an insufficient way. Microalgae, however, can effectively assimilate P and nitrogen (N), as well as other macro- and micronutrients, allowing these nutrients to be recovered into valuable products that can be used to close nutrient cycles (e.g. fertilizer, bioplastics, colour dyes, bulk chemicals). Here, we show that the green alga Chlorella sorokiniana is able to remove all inorganic N and P present in concentrated toilet wastewater (i.e. black water) with N:P ratios ranging between 15 and 26. However, the N and P uptake by the algae is imbalanced relative to the wastewater N:P stoichiometry, resulting in a rapid removal of P but relatively slower removal of N. Here, we discuss how ecological principles such as ecological stoichiometry and resource-ratio theory may help optimize N:P removal and allow for more effective recovery of N and P from black water.
  • Environmental Microbiology

    Integrating chytrid fungal parasites into plankton ecology: research gaps and needs.

    Thijs Frenken, Elisabet Alacid, Stella A. Berger, Elizabeth C. Bourne, Melanie Gerphagnon, Hans-Peter Grossart, Alena Gsell, Bas Ibelings, M. Kagami, Frithjof C. Küpper, Peter M. Letcher, Adeline Loyau, Takeshi Miki, Jens C. Nejstgaard, Serena Rasconi, Albert Reñé, Thomas Rohrlack, Keilor Rojas-Jimenez, Dirk S. Schmeller, Bettina Scholz, Kensuke Seto, Télesphore Sime-Ngando, A. Sukenik, Dedmer Van de Waal, Silke van den Wyngaert, Ellen Van Donk, J. Wolinska, Christian Wurzbacher, Ramsy Agha
    Chytridiomycota, often referred to as chytrids, can be virulent parasites with the potential to inflict mass mortalities on hosts, causing e.g. changes in phytoplankton size distributions and succession, and the delay or suppression of bloom events. Molecular environmental surveys have revealed an unexpectedly large diversity of chytrids across a wide range of aquatic ecosystems worldwide. As a result, scientific interest towards fungal parasites of phytoplankton has been gaining momentum in the past few years. Yet, we still know little about the ecology of chytrids, their life cycles, phylogeny, host specificity and range. Information on the contribution of chytrids to trophic interactions, as well as co-evolutionary feedbacks of fungal parasitism on host populations is also limited. This paper synthesizes ideas stressing the multifaceted biological relevance of phytoplankton chytridiomycosis, resulting from discussions among an international team of chytrid researchers. It presents our view on the most pressing research needs for promoting the integration of chytrid fungi into aquatic ecology. This article is protected by copyright. All rights reserved.
  • Nature Communications

    Cross continental increase in methane ebullition under climate change

    Ralf C. Aben, Nathan Barros, Ellen Van Donk, Thijs Frenken, Sabine Hilt, Garabet Kazanjian, Leon P. M. Lamers, Edwin T.H.M. Peeters, Jan G. M. Roelofs, Lisette de Senerpont Domis, Susanne Stephan, Mandy Velthuis, Dedmer Van de Waal, Martin Wik, Brett F. Thornton, Jeremy Wilkinson, Tonya DelSontro, Sarian Kosten
    Methane (CH4) strongly contributes to observed global warming. As natural CH4 emissions mainly originate from wet ecosystems, it is important to unravel how climate change may affect these emissions. This is especially true for ebullition (bubble flux from sediments), a pathway that has long been underestimated but generally dominates emissions. Here we show a remarkably strong relationship between CH4 ebullition and temperature across a wide range of freshwater ecosystems on different continents using multi-seasonal CH4 ebullition data from the literature. As these temperature–ebullition relationships may have been affected by seasonal variation in organic matter availability, we also conducted a controlled year-round mesocosm experiment. Here 4 °C warming led to 51% higher total annual CH4 ebullition, while diffusion was not affected. Our combined findings suggest that global warming will strongly enhance freshwater CH4 emissions through a disproportional increase in ebullition (6–20% per 1 °C increase), contributing to global warming.
  • Frontiers in Microbiology

    Changes in N:P Supply Ratios affect the Ecological Stoichiometry of a Toxic Cyanobacterium and its Fungal Parasite

    Thijs Frenken, Joren Wierenga, Alena Gsell, Ellen Van Donk, Thomas Rohrlack, Dedmer Van de Waal
    Human activities have dramatically altered nutrient fluxes from the landscape into receiving waters. As a result, not only the concentration of nutrients in surface waters has increased, but also their elemental ratios have changed. Such shifts in resource supply ratios will alter autotroph stoichiometry, which may in turn have consequences for higher trophic levels, including parasites. Here, we hypothesize that parasite elemental composition will follow changes in the stoichiometry of its host, and that its reproductive success will decrease with host nutrient limitation. We tested this hypothesis by following the response of a host-parasite system to changes in nitrogen (N) and phosphorus (P) supply in a controlled laboratory experiment. To this end, we exposed a fungal parasite (the chytrid Rhizophydium megarrhizum) to its host (the freshwater cyanobacterium Planktothrix rubescens) under control, low N:P and high N:P conditions. Host N:P followed treatment conditions, with a decreased N:P ratio under low N:P supply, and an increased N:P ratio under high N:P supply, as compared to the control. Shifts in host N:P stoichiometry were reflected in the parasite stoichiometry. Furthermore, at low N:P supply, host intracellular microcystin concentration was lowered as compared to high N:P supply. In contrast to our hypothesis, zoospore production decreased at low N:P and increased at high N:P ratio as compared to the control. These findings suggest that fungal parasites have a relatively high N, but low P requirement. Furthermore, zoospore elemental content, and thereby presumably their size, decreased at high N:P ratios. From these results we hypothesize that fungal parasites may exhibit a trade-off between zoospore size and production. Since zooplankton can graze on chytrid zoospores, changes in parasite production, stoichiometry and cell size may have implications for aquatic food web dynamics.
  • Frontiers in Environmental Science

    From elements to function: toward unifying ecological stoichiometry and trait-based ecology

    Cédric L. Meunier, Maarten Broersma, Rana El-Sabaawi, Halvor Halvorson, Emily M. Herstoff, Dedmer Van de Waal, Richard J. Vogt, Elena Litchman
    The theories developed in ecological stoichiometry (ES) are fundamentally based on traits. Traits directly linked to cell/body stoichiometry, such as nutrient uptake and storage, as well as the associated trade-offs, have the potential to shape ecological interactions such as competition and predation within ecosystems. Further, traits that indirectly influence and are influenced by nutritional requirements, such as cell/body size and growth rate, are tightly linked to organismal stoichiometry. Despite their physiological and ecological relevance, traits are rarely explicitly integrated in the framework of ES and, currently, the major challenge is to more closely inter-connect ES with trait-based ecology (TBE). Here, we highlight four interconnected nutrient trait groups, i.e., acquisition, body stoichiometry, storage, and excretion, which alter interspecific competition in autotrophs and heterotrophs. We also identify key differences between producer-consumer interactions in aquatic and terrestrial ecosystems. For instance, our synthesis shows that, in contrast to aquatic ecosystems, traits directly influencing herbivore stoichiometry in forested ecosystems should play only a minor role in the cycling of nutrients. We furthermore describe how linking ES and TBE can help predict the ecosystem consequences of global change. The concepts we highlight here allow us to predict that increasing N:P ratios in ecosystems should shift trait dominances in communities toward species with higher optimal N:P ratios and higher P uptake affinity, while decreasing N retention and increasing P storage
  • Ecology Letters

    Species sorting and stoichiometric plasticity control community C:P ratio of first-order aquatic consumers

    Sven Teurlincx, Mandy Velthuis, D. Seroka, Lynn Govaert, Ellen Van Donk, Dedmer Van de Waal, Steven A.J. Declerck
    Ecological stoichiometry has proven to be invaluable for understanding consumer response to changes in resource quality. Although interactions between trophic levels occur at the community level, most studies focus on single consumer species. In contrast to individual species, communities may deal with trophic mismatch not only through elemental plasticity but also through changes in species composition. Here, we show that a community of first-order consumers (e.g. zooplankton) is able to adjust its stoichiometry (C:P) in response to experimentally induced changes in resource quality, but only to a limited extent. Furthermore, using the Price equation framework we show the importance of both elemental plasticity and species sorting. These results illustrate the need for a community perspective in ecological stoichiometry, requiring consideration of species-specific elemental composition, intraspecific elemental plasticity and species turnover.
  • Frontiers in Microbiology

    Combined Effects of Elevated pCO2 and Warming Facilitate Cyanophage Infections

    Kai Cheng, Dedmer Van de Waal, X.Y. Niu, Y.J. Zhao
    Elevated pCO2 and warming are generally expected to influence cyanobacterial growth, and may promote the formation of blooms. Yet, both climate change factors may also influence cyanobacterial mortality by favoring pathogens, such as viruses, which will depend on the ability of the host to adapt. To test this hypothesis, we grew Plectonema boryanum IU597 under two temperature (25 and 29°C) and two pCO2 (400 and 800 μatm) conditions for 1 year, after which all treatments were re-exposed to control conditions for a period of 3 weeks. At several time points during the 1 year period, and upon re-exposure, we measured various infection characteristics of it associated cyanophage PP, including the burst size, latent period, lytic cycle and the efficiency of plaquing (EOP). As expected, elevated pCO2 promoted growth of P. boryanum equally over the 1 year period, but warming did not. Burst size increased in the warm treatment, but decreased in both the elevated pCO2 and combined treatment. The latent period and lytic cycle both became shorter in the elevated pCO2 and higher temperature treatment, and were further reduced by the combined effect of both factors. Efficiency of plaquing (EOP) decreased in the elevated pCO2 treatment, increased in the warm treatment, and increased even stronger in the combined treatment. These findings indicate that elevated pCO2 enhanced the effect of warming, thereby further promoting the virus infection rate. The re-exposure experiments demonstrate adaptation of the host leading to higher biomass build-up with elevated pCO2 over the experimental period, and lower performance upon re-exposure to control conditions. Similarly, virus burst size and EOP increased when given warm adapted host, but were lower as compared to the control when the host was re-exposed to control conditions. Our results demonstrate that adaptation but particularly physiological acclimation to climate change conditions favored viral infections, while limited host plasticity and slow adaptation after re-exposure to control conditions impeded host biomass build-up and viral infections.
  • Journal of Experimental Marine Biology and Ecology

    CO2-dependent carbon isotope fractionation in dinoflagellates relates to their inorganic carbon fluxes

    Mirja Hoins, Tim Eberlein, Dedmer Van de Waal, Appy Sluijs, Gert-Jan Reichart, Björn Rost
    Carbon isotope fractionation (εp) between the inorganic carbon source and organic matter has been proposed to be a function of pCO2. To understand the CO2-dependency of εp and species-specific differences therein, inorganic carbon fluxes in the four dinoflagellate species Alexandrium fundyense, Scrippsiella trochoidea, Gonyaulax spinifera and Protoceratium reticulatum have been measured by means of membrane-inlet mass spectrometry. In-vivo assays were carried out at different CO2 concentrations, representing a range of pCO2 from 180 to 1200 μatm. The relative bicarbonate contribution (i.e. the ratio of bicarbonate uptake to total inorganic carbon uptake) and leakage (i.e. the ratio of CO2 efflux to total inorganic carbon uptake) varied from 0.2 to 0.5 and 0.4 to 0.7, respectively, and differed significantly between species. These ratios were fed into a single-compartment model, and εp values were calculated and compared to carbon isotope fractionation measured under the same conditions. For all investigated species, modeled and measured εp values were comparable (A. fundyense, S. trochoidea, P. reticulatum) and/or showed similar trends with pCO2 (A. fundyense, G. spinifera, P. reticulatum). Offsets are attributed to biases in inorganic flux measurements, an overestimated fractionation factor for the CO2-fixing enzyme RubisCO, or the fact that intracellular inorganic carbon fluxes were not taken into account in the model. This study demonstrates that CO2-dependency in εp can largely be explained by the inorganic carbon fluxes of the individual dinoflagellates.
  • Harmful Algae

    The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms

    C.J. Gobler, J. Burkholder, T.W. Davis, M.J. Harke, T. Johengen, C.A. Stow, Dedmer Van de Waal
    Historically, phosphorus (P) has been considered the primary limiting nutrient for phytoplankton assemblages in freshwater ecosystems. This review, supported by new findings from Lake Erie, highlights recent molecular, laboratory, and field evidence that the growth and toxicity of some non-diazotrophic blooms of cyanobacteria can be controlled by nitrogen (N). Cyanobacteria such as Microcystis possess physiological adaptations that allow them to dominate low-P surface waters, and in temperate lakes, cyanobacterial densities can be controlled by N availability. Beyond total cyanobacterial biomass, N loading has been shown to selectively promote the abundance of Microcystis and Planktothrix strains capable of synthesizing microcystins over strains that do not possess this ability. Among strains of cyanobacteria capable of synthesizing the N-rich microcystins, cellular toxin quotas have been found to depend upon exogenous N supplies. Herein, multi-year observations from western Lake Erie are presented demonstrating that microcystin concentrations peak in parallel with inorganic N, but not orthophosphate, concentrations and are significantly lower (p < 0.01) during years of reduced inorganic nitrogen loading and concentrations. Collectively, this information underscores the importance of N as well as P in controlling toxic cyanobacteria blooms. Furthermore, it supports the premise that management actions to reduce P in the absence of concurrent restrictions on N loading may not effectively control the growth and/or toxicity of non-diazotrophic toxic cyanobacteria such as the cosmopolitan, toxin-producing genus, Microcystis.
  • PLoS One

    Combined Effects of Ocean Acidification and Light or Nitrogen Availabilities on 13C Fractionation in Marine Dinoflagellates

    Mirja Hoins, Tim Eberlein, Christian H. Groβmann, Karen M. Brandenburg, Gert-Jan Reichart, Björn Rost, Appy Sluijs, Dedmer Van de Waal

    Along with increasing oceanic CO2 concentrations, enhanced stratification constrains phytoplankton to shallower upper mixed layers with altered light regimes and nutrient concentrations. Here, we investigate the effects of elevated pCO2 in combination with light or nitrogen-limitation on 13C fractionation (εp) in four dinoflagellate species. We cultured Gonyaulax spinifera and Protoceratium reticulatum in dilute batches under low-light (‘LL’) and high-light (‘HL’) conditions, and grew Alexandrium fundyense and Scrippsiella trochoidea in nitrogen-limited continuous cultures (‘LN’) and nitrogen-replete batches (‘HN’). The observed CO2-dependency of εp remained unaffected by the availability of light for both G. spinifera and P. reticulatum, though at HL εp was consistently lower by about 2.7‰ over the tested CO2 range for P. reticulatum. This may reflect increased uptake of (13C-enriched) bicarbonate fueled by increased ATP production under HL conditions. The observed CO2-dependency of εp disappeared under LN conditions in both A. fundyense and S. trochoidea. The generally higher εp under LN may be associated with lower organic carbon production rates and/or higher ATP:NADPH ratios. CO2-dependent εp under non-limiting conditions has been observed in several dinoflagellate species, showing potential for a new CO2-proxy. Our results however demonstrate that light- and nitrogen-limitation also affect εp, thereby illustrating the need to carefully consider prevailing environmental conditions.
  • Philosophical Transactions of the Royal Society B: Biological Sciences

    The influence of balanced and imbalanced resource supply on biodiversity–functioning relationship across ecosystems

    Aleksandra M. Lewandowska, Antje Biermann, Elizabeth T. Borer, Miguel A. Cebrián-Piqueras, Steven A.J. Declerck, Luc De Meester, Ellen Van Donk, Lars Gamfeldt, Daniel S. Gruner, Nicole Hagenah, W. Stanley Harpole, Kevin P. Kirkman, Christopher A. Klausmeier, Michael Kleyer, Johannes M. H. Knops, Pieter Lemmens, Eric M. Lind, Elena Litchman, Jasmin Mantilla-Contreras, Koen Martens, Sandra Meier, Vanessa Minden, Joslin L. Moore, Harry Olde Venterink, Eric W. Seabloom, Ulrich Sommer, Maren Striebel, Anastasia Trenkamp, Juliane Trinogga, Jotaro Urabe, Wim Vyverman, Dedmer Van de Waal, Claire E. Widdicombe, Helmut Hillebrand
    Numerous studies show that increasing species richness leads to higher ecosystem productivity. This effect is often attributed to more efficient portioning of multiple resources in communities with higher numbers of competing species, indicating the role of resource supply and stoichiometry for biodiversity–ecosystem functioning relationships. Here, we merged theory on ecological stoichiometry with a framework of biodiversity–ecosystem functioning to understand how resource use transfers into primary production. We applied a structural equation model to define patterns of diversity–productivity relationships with respect to available resources. Meta-analysis was used to summarize the findings across ecosystem types ranging from aquatic ecosystems to grasslands and forests. As hypothesized, resource supply increased realized productivity and richness, but we found significant differences between ecosystems and study types. Increased richness was associated with increased productivity, although this effect was not seen in experiments. More even communities had lower productivity, indicating that biomass production is often maintained by a few dominant species, and reduced dominance generally reduced ecosystem productivity. This synthesis, which integrates observational and experimental studies in a variety of ecosystems and geographical regions, exposes common patterns and differences in biodiversity–functioning relationships, and increases the mechanistic understanding of changes in ecosystems productivity.
  • FEMS Microbiology Ecology

    Elevated pCO2 causes a shift towards more toxic microcystin variants in nitrogen limited Microcystis aeruginosa.

    Jing Liu, Elmer van Oosterhout, Els Faassen, Miquel Lürling, Nico Helmsing, Dedmer Van de Waal
    Elevated pCO2 may promote phytoplankton growth, and potentially alleviate carbon limitation during dense blooms. Under nitrogen-limited conditions, elevated pCO2 may furthermore alter the phytoplankton carbon: nitrogen (C:N) balance and thereby the synthesis of secondary metabolites, such as cyanobacterial toxins. A common group of these toxins are microcystins, with variants that not only differ in C:N stoichiometry, but also in toxicity. Here, we hypothesized that elevated pCO2 will increase the cellular C:N ratios of cyanobacteria, thereby promoting the more toxic microcystin variants with higher C:N ratios. To test this hypothesis, we performed chemostat experiments under nitrogen-limited conditions, exposing three Microcystis aeruginosa strains to two pCO2 treatments: 400 and 1200 μatm. Biomass, cellular C:N ratios and total microcystin contents at steady state remained largely unaltered in all three strains. Across strains and treatments, however, cellular microcystin content decreased with increasing cellular C:N ratios, suggesting a general stoichiometric regulation. Furthermore, as predicted, microcystin variants with higher C:N ratios generally increased with elevated pCO2, while the variant with a low C:N ratio decreased. Thus, elevated pCO2 under nitrogen-limited conditions may shift the cellular microcystin composition towards the more toxic variants. Such CO2 driven changes may have consequences for the toxicity of Microcystis blooms.
  • Journal of Plankton Research

    Salinity effects on growth and toxin production in an Alexandrium ostenfeldii (Dinophyceae) isolate from The Netherlands

    Helge Martens, Dedmer Van de Waal, Karen M. Brandenburg, Bernd Krock, U. Tillmann
    Alexandrium ostenfeldii is among the most intensely studied marine planktonic dinophytes and in the last few years blooms have become a recurrent phenomenon mainly in brackish coastal waters. Since 2012, A. ostenfeldii recurs annually in the Ouwerkerkse Kreek, a Dutch brackish water creek discharging into an estuary with large stocks of mussels, oysters and cockles. The creek is characterized by highly dynamic abiotic conditions, notably salinity. Here, we investigated the impacts of salinities ranging from 3 to 34 on growth and toxin content of an A. ostenfeldii isolate from the creek. Our results demonstrate a broad salinity tolerance of the Dutch A. ostenfeldii population, with growth rates from 0.13 to 0.2 d−1 over a salinity range from 6 to 34. Highest paralytic shellfish toxin and cyclic imine toxin cell quotas were observed for the lowest and highest salinities, and were associated with increases in cell size. Lytic activity was highest at the lowest salinity, and was 5-fold higher in the cell-free supernatants compared to cell extracts. Together our results demonstrate a tight coupling between salinity and A. ostenfeldii growth rate, cell size and toxin synthesis, which may have consequences for the seasonal dynamics of bloom toxicity.
  • Marine Ecology Progress Series

    Interactive effects of ocean acidification and nitrogen limitation on two bloom-forming dinoflagellate species

    T. Eberlein, Dedmer Van de Waal, Karen M. Brandenburg, U. John, M. Voss, E.P. Achterberg, B. Rost
    Global climate change involves an increase in oceanic CO2 concentrations as well as thermal stratification of the water column, thereby reducing nutrient supply from deep to surface waters. Changes in inorganic carbon (C) or nitrogen (N) availability have been shown to affect marine primary production, yet little is known about their interactive effects. To test for these effects, we conducted continuous culture experiments under N limitation and exposed the bloom-forming dinoflagellate species Scrippsiella trochoidea and Alexandrium fundyense (formerly A. tamarense) to CO2 partial pressures (pCO2) ranging between 250 and 1000 µatm. Ratios of particulate organic carbon (POC) to organic nitrogen (PON) were elevated under N limitation, but also showed a decreasing trend with increasing pCO2. PON production rates were highest and affinities for dissolved inorganic N were lowest under elevated pCO2, and our data thus demonstrate a CO2-dependent trade-off in N assimilation. In A. fundyense, quota of paralytic shellfish poisoning toxins were moreover lowered under N limitation, but the offset to those obtained under N-replete conditions became smaller with increasing pCO2. Consequently, cellular toxicity under N limitation was highest under elevated pCO2. All in all, our observations imply reduced N stress under elevated pCO2, which we attribute to a reallocation of energy from C to N assimilation as a consequence of lowered costs in C acquisition. Such interactive effects of ocean acidification and nutrient limitation may favor species with adjustable carbon concentrating mechanisms and have consequences for their competitive success in a future ocean.
  • Global Change Biology

    Warming accelerates termination of a phytoplankton spring bloom by fungal parasites

    Thijs Frenken, Mandy Velthuis, Lisette de Senerpont Domis, Susanne Stephan, Ralf C. Aben, Sarian Kosten, Ellen Van Donk, Dedmer Van de Waal
    Climate change is expected to favour infectious diseases across ecosystems worldwide. In freshwater and marine
    environments, parasites play a crucial role in controlling plankton population dynamics. Infection of phytoplankton
    populations will cause a transfer of carbon and nutrients into parasites, which may change the type of food available
    for higher trophic levels. Some phytoplankton species are inedible to zooplankton, and the termination of their population
    by parasites may liberate otherwise unavailable carbon and nutrients. Phytoplankton spring blooms often consist
    of large diatoms inedible for zooplankton, but the zoospores of their fungal parasites may serve as a food source
    for this higher trophic level. Here, we investigated the impact of warming on the fungal infection of a natural phytoplankton
    spring bloom and followed the response of a zooplankton community. Experiments were performed in ca.
    1000 L indoor mesocosms exposed to a controlled seasonal temperature cycle and a warm (+4 °C) treatment in the
    period from March to June 2014. The spring bloom was dominated by the diatom Synedra. At the peak of infection
    over 40% of the Synedra population was infected by a fungal parasite (i.e. a chytrid) in both treatments. Warming did
    not affect the onset of the Synedra bloom, but accelerated its termination. Peak population density of Synedra tended
    to be lower in the warm treatments. Furthermore, Synedra carbon: phosphorus stoichiometry increased during the
    bloom, particularly in the control treatments. This indicates enhanced phosphorus limitation in the control treatments,
    which may have constrained chytrid development. Timing of the rotifer Keratella advanced in the warm
    treatments and closely followed chytrid infections. The chytrids’ zoospores may thus have served as an alternative
    food source to Keratella. Our study thus emphasizes the importance of incorporating not only nutrient limitation and
    grazing, but also parasitism in understanding the response of plankton communities towards global warming.
  • Inland Waters

    Combined effects of nitrogen to phosphorus ratios and nitrogen speciation on cyanobacterial metabolite concentrations in eutrophic Midwestern USA reservoirs.

    Ted D. Harris, V.H. Smith, J.L. Graham, Dedmer Van de Waal, L.P. Tedesco, N. Clercin
    Recent studies have shown that the total nitrogen to total phosphorus (TN:TP) ratio and nitrogen oxidation state may have substantial effects on secondary metabolite (e.g., microcystins) production in cyanobacteria. We investigated the relationship between the water column TN:TP ratio and the cyanobacterial secondary metabolites geosmin, 2-methylisoborneol (MIB), and microcystin using multiple years of data from 4 reservoirs located in the Midwestern United States. We also examined the relationship between water column concentrations of chemically oxidized (NO3) and reduced (NH3) nitrogen, the NO3:NH3 ratio, cyanobacterial biovolume, and associated secondary metabolites. We found that the cyanobacterial secondary metabolites geosmin, MIB, and microcystin primarily occurred when the TN:TP ratio was <30:1 (by mass), likely due to higher cyanobacterial biovolumes at lower TN:TP ratios. We also found that relative cyanobacterial biovolume was inversely related to the NO3:NH3 ratio. Both N2- and non-N2-fixing cyanobacteria appeared to produce secondary metabolites and had higher concentrations per unit biovolume when NO3:NH3 ratios were relatively low. Our data thus are consistent with the hypothesis that lower TN:TP ratios favor cyanobacterial dominance, and also suggest that relatively low NO3:NH3 ratios provide conditions that may favor the production of cyanobacterial secondary metabolites. Our data further suggest that increases in the absolute concentrations of TP or NH3 (or both), causing decreases in TN:TP and NO3:NH3 ratios, respectively, may stimulate cyanobacteria having the metabolic ability to produce geosmin, MIB or microcystins. Future studies should address how the NO3:NH3 ratio affects phytoplankton community structure and occurrence and production of cyanobacterial secondary metabolites.
  • Harmful Algae

    Characterization of multiple isolates from an Alexandrium ostenfeldii bloom in The Netherlands

    Dedmer Van de Waal, Urban Tillmann, Helge Martens, Bernd Krock, Yvonne van Scheppingen, Uwe John
    Alexandrium ostenfeldii is an emerging harmful algal bloom species forming a global threat to coastal marine ecosystems, with consequences for fisheries and shellfish production. The Oosterschelde estuary is a shallow, macrotidal and mesotrophic estuary in the southwest of The Netherlands with large stocks of mussels, oysters, and cockles. These shellfish stocks were threatened by a recent A. ostenfeldii bloom in the Ouwerkerkse Kreek, which is a brackish water creek discharging water into the Oosterschelde. Little is yet known about the characteristics of the A. ostenfeldii population in this creek. We therefore isolated 20 clones during an A. ostenfeldii bloom in 2013, and characterized these clones on their growth and toxin profile in their exponential growth phase. The cyclic imines were identified by comparison of A. ostenfeldii extracts with the retention time and CID spectra of standard solutions, or with published CID spectra. We furthermore assessed the allelochemical potency and phylogeny of a selection of 10–12 clones. Morphology and molecular phylogeny showed that all clones belong to Group 1 of A. ostenfeldii. All clones showed comparable growth rates of on average 0.22 ± 0.03 d−1. During exponential growth, they all produced a unique combination of paralytic shellfish poisoning toxins, spirolides and gymnodimines, of which particularly the latter showed a high intra-specific variability, with a 25-fold difference between clones with the lowest and highest cell quota. Furthermore, the selected 12 clones showed high allelopathic potencies with EC50 values based on lysis assays against the cryptophyte Rhodomonas salina between 212 and 525 A. ostenfeldii cells mL−1. Lytic activities were lower for cell extracts, indicating an important extracellular role of these compounds. A high intra-specific variability may add to the success of genotypically diverse A. ostenfeldii blooms, and make populations resilient to changes in environmental and climatic conditions.
  • Geochimica et Cosmochimica Acta

    Stable carbon isotope fractionation of organic cyst-forming dinoflagellates: evaluating the potential for a CO2 proxy

    Mirja Hoins, Dedmer Van de Waal, Tim Eberlein, Gert-Jan Reichart, Björn Rost, Appy Sluijs
    Over the past decades, significant progress has been made regarding the quantification and mechanistic understanding of stable carbon isotope fractionation (13C fractionation) in photosynthetic unicellular organisms in response to changes in the partial pressure of atmospheric CO2 (pCO2). However, hardly any data is available for organic cyst-forming dinoflagellates while this is an ecologically important group with a unique fossil record. We performed dilute batch experiments with four harmful dinoflagellate species known for their ability to form organic cysts: Alexandrium tamarense, Scrippsiella trochoidea, Gonyaulax spinifera and Protoceratium reticulatum. Cells were grown at a range of dissolved CO2 concentrations characterizing past, modern and projected future values (∼5–50 μmol L-1), representing atmospheric pCO2 of 180, 380, 800 and 1200 μatm. In all tested species, 13C fractionation depends on CO2 with a slope of up to 0.17‰ (μmol L)-1. Even more consistent correlations were found between 13C fractionation and the combined effects of particulate organic carbon quota (POC quota; pg C cell-1) and CO2. Carbon isotope fractionation as well as its response to CO2 is species-specific. These results may be interpreted as a first step towards a proxy for past pCO2 based on carbon isotope ratios of fossil organic dinoflagellate cysts. However, additional culture experiments focusing on environmental variables other than pCO2, physiological underpinning of the recorded response, testing for possible offsets in 13C values between cells and cysts, as well as field calibration studies are required to establish a reliable proxy.
  • Proceedings of the Royal Society B-Biological Sciences

    Intraspecific facilitation by allelochemical mediated grazing protection within a toxigenic dinoflagellate population

    U. John, U. Tillmann, Jennifer Hülskötter, Tilman J. Alpermann, S. Wohlrab, Dedmer Van de Waal
    Dinoflagellates are a major cause of harmful algal blooms, with consequences for coastal marine ecosystem functioning and services. Alexandrium tamarense is one of the most abundant and widespread toxigenic species in the temperate northern and southern hemisphere, and produces paralytic shellfish poisoning toxins as well as lytic allelochemical substances. These bioactive compounds may support the success of A. tamarense and its ability to form blooms. Here we investigate the impact of grazing on monoclonal and mixed set-ups of highly (Alex2) and moderately (Alex4) allelochemically active A. tamarense strains and on a non-allelochemically active conspecific (Alex5) by the heterotrophic dinoflagellate Polykrikos kofoidii. While Alex4 and particularly Alex5 were strongly grazed by P. kofoidii when offered alone, both strains grew well in the mixed assemblages (Alex4+Alex5 and Alex2+Alex5). Hence, the allelochemical active strains facilitated growth of the non-active strain by protecting the population as a whole against grazing. Based on our results, we argue that facilitation among clonal lineages within a species may partly explain the high genotypic and phenotypic diversity of Alexandrium populations. Populations of Alexandrium may comprise multiple cooperative traits that act in concert with intraspecific facilitation, and hence promote the success of this notorious harmful algal bloom species.
  • Basic and Applied Ecology

    Think ratio! A stoichiometric view on biodiversity-ecosystem functioning research

    H. Hillebrand, J.M. Cowles, A. Lewandowska, Dedmer Van de Waal, C. Plum
    Ecological stoichiometry (ES) has become one of the most pervasive theoretical frameworks in environmental sciences and biology in the last two decades. ES allows predicting processes on all organizational levels from subcellular structures to ecosystems by relating the elemental composition and demand of organisms to the relative availability of resources. However, ES has been rarely used to understand and predict the relationship between biodiversity and ecosystem functioning (BEF), although ES would be ideally suited as it makes predictions on both population processes underlying biodiversity as well as on matter transformations underlying ecosystem processes. Here, we propose to link the two fields of research on ES and BEF relationships and highlight a number of potential avenues for further research. First, we cast a stoichiometric view on drivers of biodiversity change. Second, we address the stoichiometric underpinning of biodiversity-productivity relationships. Third, we discuss potential interactions between stoichiometry and diversity in a food web context.
  • Ecology

    Community stoichiometry in a changing world: combined effects of warming and eutrophication on phytoplankton dynamics

    The current changes in our climate will likely have far reaching consequences for aquatic ecosystems. These changes in the climate, however, do not act alone and are often accompanied by additional stressors such as eutrophication. Both global warming and eutrophication have been shown to affect the timing and magnitude of phytoplankton blooms. Little is known about the combined effects of rising temperatures and eutrophication on the stoichiometry of entire phytoplankton communities. We exposed a natural phytoplankton spring community to different warming and phosphorus loading scenarios using a full-factorial design. Our results demonstrate that rising temperatures promote the growth rate of an entire phytoplankton community. Furthermore, both rising temperatures and phosphorus loading stimulated the maximum biomass built up by the phytoplankton community. Rising temperatures led to higher carbon:nutrient stoichiometry of the phytoplankton community under phosphorus limited conditions. Such a shift towards higher carbon:nutrient ratios, in combination with a higher biomass build-up, suggests a temperature-driven increase in nutrient use efficiency of the phytoplankton community. Importantly, higher carbon:nutrient stoichiometry of phytoplankton is generally of poorer nutritional value for zooplankton. Thus, although warming may result in higher phytoplankton biomass, this may be accompanied by a stoichiometric mismatch between phytoplankton and their grazers, with possible consequences for the entire aquatic food web. Read More:
  • Physiologia Plantarum

    Differential effects of ocean acidification on carbon acquisition in two bloom-forming dinoflagellate species

    T. Eberlein, Dedmer Van de Waal, B. Rost
    Dinoflagellates represent a cosmopolitan group of phytoplankton with the ability to form harmful algal blooms. Featuring a Ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) with very low CO2-affinities, photosynthesis of this group may be particularly prone to carbon limitation and thus benefit from rising atmospheric CO2 partial pressure (pCO2) under ocean acidification (OA). Here, we investigated the consequences of OA on two bloom-forming dinoflagellate species, the calcareous Scrippsiella trochoidea and the toxic Alexandrium tamarense. Using dilute batch incubations, we assessed growth characteristics over a range of pCO2 (i.e. 180–1200 µatm). To understand the underlying physiology, several aspects of inorganic carbon acquisition were investigated by membrane-inlet mass spectrometry. Our results show that both species kept growth rates constant over the tested pCO2 range, but we observed a number of species-specific responses. For instance, biomass production and cell size decreased in S. trochoidea, while A. tamarense was not responsive to OA in these measures. In terms of oxygen fluxes, rates of photosynthesis and respiration remained unaltered in S. trochoidea whereas respiration increased in A. tamarense under OA. Both species featured efficient carbon concentrating mechanisms (CCMs) with a CO2-dependent contribution of HCO3– uptake. In S. trochoidea, the CCM was further facilitated by exceptionally high and CO2-independent carbonic anhydrase activity. Comparing both species, a general trade-off between maximum rates of photosynthesis and respective affinities is indicated. In conclusion, our results demonstrate effective CCMs in both species, yet very different strategies to adjust their carbon acquisition. This regulation in CCMs enables both species to maintain growth over a wide range of ecologically relevant pCO2.
  • Ecology Letters

    Contrasting effects of rising CO2 on primary production and ecological stoichiometry at different nutrient levels

    Jolanda Verspagen, Dedmer Van de Waal, J.F Finke, P.M. Visser, J. Huisman
    Although rising CO2 concentrations are thought to promote the growth and alter the carbon : nutrient stoichiometry of primary producers, several studies have reported conflicting results. To reconcile these contrasting results, we tested the following hypotheses: rising CO2 levels (1) will increase phytoplankton biomass more at high nutrient loads than at low nutrient loads, but (2) will increase their carbon : nutrient stoichiometry more at low than at high nutrient loads. We formulated a mathematical model to predict dynamic changes in phytoplankton population density, elemental stoichiometry and inorganic carbon chemistry in response to rising CO2. The model was tested in chemostat experiments with the freshwater cyanobacterium Microcystis aeruginosa. The model predictions and experimental results confirmed the hypotheses. Our findings provide a novel theoretical framework to understand and predict effects of rising CO2 concentrations on primary producers and their nutritional quality as food for herbivores under different nutrient conditions
  • FEMS Microbiology Ecology

    Nitrogen fixation and respiratory electron transport in the cyanobacterium Cyanothece under different light:dark cycles

    S.A.M. Rabouille, Dedmer Van de Waal, Hans C. P. Matthijs, J. Huisman
    Incompatibility of nitrogen fixation and oxygen production compels unicellular diazotrophic cyanobacteria to perform photosynthesis during daytime and restrict nitrogen fixation to nighttime. The marine diazotroph Cyanothece BG 043511 was grown in continuous culture under three light/dark regimes (16L : 8D, 12L : 12D, and 8L : 16D h); we monitored nitrogen fixation and potential photosynthetic efficiency simultaneously online to reveal how their temporal separation is affected by different LD regimes. An increase in nitrogen fixation rate at night coincided with a rise in pulse-amplitude modulated fluorescence, indicating that the enhanced respiratory electron transport to fuel diazotrophy affects the oxidation state of the plastoquinone pool. This may offer an alternative approach to assess instantaneous nitrogen fixation activity. Regardless of photoperiod, the maximum rate of nitrogen fixation was conserved at about 20 h after the onset of the light. Consequently, nitrogen fixation rates peaked at different moments in the dark: relatively early in the 16L : 8D cycle, at midnight in 12L : 12D, and relatively late in 8L : 16D. Under 16L : 8D, nitrogen fixation extended into the light, demonstrating the functional plasticity of nitrogen fixation in Cyanothece. Highest daily amounts of nitrogen fixed were obtained in 12L : 12D, which is consistent with the natural LD cycle of subtropical latitudes in which Cyanothece thrives.
  • Journal of Plankton Research

    Shake it easy: a gently mixed continuous culture system for dinoflagellates

    Dedmer Van de Waal, T. Eberlein, Y. Bublitz, U. John, B. Rost
    An important requirement for continuous cultures is a homogeneous distribution of resources and microorganisms, often achieved by rigorous mixing. Many dinoflagellate species are known to be vulnerable to turbulence. Here, we present a newly developed continuous culture system based on gentle mixing in which the two dinoflagellate species Scrippsiella trochoidea and Alexandrium tamarense, with different turbulence sensitivities, grew well under steady state conditions. We also show that the continuous culture system can be applied at low nutrient conditions and low population densities.
  • PLoS One

    Rising CO2 levels will intensify phytoplankton blooms in eutrophic and hypertrophic lakes

    Jolanda Verspagen, Dedmer Van de Waal, J.F Finke, P.M. Visser, Ellen Van Donk, J. Huisman
    Harmful algal blooms threaten the water quality of many eutrophic and hypertrophic lakes and cause severe ecological and economic damage worldwide. Dense blooms often deplete the dissolved CO2 concentration and raise pH. Yet, quantitative prediction of the feedbacks between phytoplankton growth, CO2 drawdown and the inorganic carbon chemistry of aquatic ecosystems has received surprisingly little attention. Here, we develop a mathematical model to predict dynamic changes in dissolved inorganic carbon (DIC), pH and alkalinity during phytoplankton bloom development. We tested the model in chemostat experiments with the freshwater cyanobacterium Microcystis aeruginosa at different CO2 levels. The experiments showed that dense blooms sequestered large amounts of atmospheric CO2, not only by their own biomass production but also by inducing a high pH and alkalinity that enhanced the capacity for DIC storage in the system. We used the model to explore how phytoplankton blooms of eutrophic waters will respond to rising CO2 levels. The model predicts that (1) dense phytoplankton blooms in low- and moderately alkaline waters can deplete the dissolved CO2 concentration to limiting levels and raise the pH over a relatively wide range of atmospheric CO2 conditions, (2) rising atmospheric CO2 levels will enhance phytoplankton blooms in low- and moderately alkaline waters with high nutrient loads, and (3) above some threshold, rising atmospheric CO2 will alleviate phytoplankton blooms from carbon limitation, resulting in less intense CO2 depletion and a lesser increase in pH. Sensitivity analysis indicated that the model predictions were qualitatively robust. Quantitatively, the predictions were sensitive to variation in lake depth, DIC input and CO2 gas transfer across the air-water interface, but relatively robust to variation in the carbon uptake mechanisms of phytoplankton. In total, these findings warn that rising CO2 levels may result in a marked intensification of phytoplankton blooms in eutrophic and hypertrophic waters.
  • Ecology Letters

    Stoichiometric regulation of phytoplankton toxins

    Dedmer Van de Waal, V.H. Smith, Steven A.J. Declerck, E.C.M. Stam, J.J. Elser
    Ecological Stoichiometry theory predicts that the production, elemental structure and cellular content of biomolecules should depend on the relative availability of resources and the elemental composition of their producer organism. We review the extent to which carbon- and nitrogen-rich phytoplankton toxins are regulated by nutrient limitation and cellular stoichiometry. Consistent with theory, we show that nitrogen limitation causes a reduction in the cellular quota of nitrogen-rich toxins, while phosphorus limitation causes an increase in the most nitrogen-rich paralytic shellfish poisoning toxin. In addition, we show that the cellular content of nitrogen-rich toxins increases with increasing cellular N : P ratios. Also consistent with theory, limitation by either nitrogen or phosphorus promotes the C-rich toxin cell quota or toxicity of phytoplankton cells. These observed relationships may assist in predicting and managing toxin-producing phytoplankton blooms. Such a stoichiometric regulation of toxins is likely not restricted to phytoplankton, and may well apply to carbon- and nitrogen-rich secondary metabolites produced by bacteria, fungi and plants.
  • Toxicon

    Impact of elevated pCO2 on paralytic shellfish poisoning toxin content and composition in Alexandrium tamarense

    Dedmer Van de Waal, T. Eberlein, U. John, S. Wohlrab, B. Rost
    Ocean acidification is considered a major threat to marine ecosystems and may particularly affect primary producers. Here we investigated the impact of elevated pCO2 on paralytic shellfish poisoning toxin (PST) content and composition in two strains of Alexandrium tamarense, Alex5 and Alex2. Experiments were carried out as dilute batch to keep carbonate chemistry unaltered over time. We observed only minor changes with respect to growth and elemental composition in response to elevated pCO2. For both strains, the cellular PST content, and in particular the associated cellular toxicity, was lower in the high CO2 treatments. In addition, Alex5 showed a shift in its PST composition from a non-sulfated analogue towards less toxic sulfated analogues with increasing pCO2. Transcriptomic analyses suggest that the ability of A. tamarense to maintain cellular homeostasis is predominantly regulated on the post-translational level rather than on the transcriptomic level. Furthermore, genes associated to secondary metabolite and amino acid metabolism in Alex5 were down-regulated in the high CO2 treatment, which may explain the lower PST content. Elevated pCO2 also induced up-regulation of a putative sulfotransferase sxtN homologue and a substantial down-regulation of several sulfatases. Such changes in sulfur metabolism may explain the shift in PST composition towards more sulfated analogues. All in all, our results indicate that elevated pCO2 will have minor consequences for growth and elemental composition, but may potentially reduce the cellular toxicity of A. tamarense.
  • Marine Ecology Progress Series

    Nutrient pulse induces dynamic changes in cellular C:N:P, amino acids, and paralytic shellfish poisoning toxins in Alexandrium tamarense

    Dedmer Van de Waal, U. Tillmann, M. Zhu, B.P. Koch, B. Rost, U. John
    Alexandrium tamarense is a common harmful algal bloom species and can cause high concentrations of paralytic shellfish poisoning toxins (PSTs) in marine coastal waters. PSTs are nitrogen rich alkaloids and their production has been shown to depend on resource conditions as well as on growth rate. We hypothesized that PST content in A. tamarense depends on the nitrogen availability and will increase with cellular N:P ratios and arginine content. To test this hypothesis, we first grew A. tamarense cells under nitrogen starved, phosphorus starved and nutrient replete conditions. Subsequently, we transferred cells into nutrient rich medium and followed dynamic changes in growth, elemental stoichiometry, as well as the amino acid and PST content and composition. Our results illustrate that PST content was lowest under nitrogen starvation, intermediate under nutrient replete conditions, and highest under phosphorus starvation. As expected, PST content correlated well with cellular N:P ratios and arginine content. Upon transfer of cells into nutrient replete medium, PST content varied with growth rate, depending on the growth controlling resource. Specifically, PST content increased with growth when recovering from nitrogen starvation and decreased with growth when recovering from phosphorus starvation. Furthermore, PST composition shifted towards less hydroxylated analogues upon resumption of growth. Our findings also illustrate a high potential for luxury consumption of phosphorus by A. tamarense. The applied comprehensive approach will help to further elucidate the intriguing coupling between carbon, nitrogen and phosphorus assimilation and the synthesis of amino acids and PSTs.
  • PLoS One

    Ocean acidification reduces growth and calcification in a marine dinoflagellate

    Dedmer Van de Waal, U. John, P. Ziveri, G.J. Reichart, M. Hoins, A. Sluijs, B. Rost
    Ocean acidification is considered a major threat to marine ecosystems and may particularly affect calcifying organisms such as corals, foraminifera and coccolithophores. Here we investigate the impact of elevated pCO2 and lowered pH on growth and calcification in the common calcareous dinoflagellate Thoracosphaera heimii. We observe a substantial reduction in growth rate, calcification and cyst stability of T. heimii under elevated pCO2. Furthermore, transcriptomic analyses reveal CO2 sensitive regulation of many genes, particularly those being associated to inorganic carbon acquisition and calcification. Stable carbon isotope fractionation for organic carbon production increased with increasing pCO2 whereas it decreased for calcification, which suggests interdependence between both processes. We also found a strong effect of pCO2 on the stable oxygen isotopic composition of calcite, in line with earlier observations concerning another T. heimii strain. The observed changes in stable oxygen and carbon isotope composition of T. heimii cysts may provide an ideal tool for reconstructing past seawater carbonate chemistry, and ultimately past pCO2. Although the function of calcification in T. heimii remains unresolved, this trait likely plays an important role in the ecological and evolutionary success of this species. Acting on calcification as well as growth, ocean acidification may therefore impose a great threat for T. heimii.
  • ISME Journal

    Reversal in competitive dominance of a toxic versus non-toxic cyanobacterium in response to rising CO2

    Dedmer Van de Waal, Jolanda Verspagen, J.F Finke, V. Vournazou, Anne Immers, W.E.A. Kardinaal, L. Tonk, Sven Becker, Ellen Van Donk, P.M. Visser, J. Huisman
    Climate change scenarios predict a doubling of the atmospheric CO2 concentration by the end of this century. Yet, how rising CO2 will affect the species composition of aquatic microbial communities is still largely an open question. In this study, we develop a resource competition model to investigate competition for dissolved inorganic carbon in dense algal blooms. The model predicts how dynamic changes in carbon chemistry, pH and light conditions during bloom development feed back on competing phytoplankton species. We test the model predictions in chemostat experiments with monocultures and mixtures of a toxic and non-toxic strain of the freshwater cyanobacterium Microcystis aeruginosa. The toxic strain was able to reduce dissolved CO2 to lower concentrations than the non-toxic strain, and became dominant in competition at low CO2 levels. Conversely, the non-toxic strain could grow at lower light levels, and became dominant in competition at high CO2 levels but low light availability. The model captured the observed reversal in competitive dominance, and was quantitatively in good agreement with the results of the competition experiments. To assess whether microcystins might have a role in this reversal of competitive dominance, we performed further competition experiments with the wild-type strain M. aeruginosa PCC 7806 and its mcyB mutant impaired in microcystin production. The microcystin-producing wild type had a strong selective advantage at low CO2 levels but not at high CO2 levels. Our results thus demonstrate both in theory and experiment that rising CO2 levels can alter the community composition and toxicity of harmful algal blooms.
  • Frontiers in Ecology and the Environment

    Climate-driven changes in the ecological stoichiometry of aquatic ecosystems

    Dedmer Van de Waal, Anthony M. Verschoor, Jolanda Verspagen, Ellen Van Donk, J. Huisman
    Advances in ecological stoichiometry, a rapidly expanding research field investigating the elemental composition of organisms and their environment, have shed new light on the impacts of climate change on freshwater and marine ecosystems. Current changes in the Earth's climate alter the availability of carbon and nutrients in lakes and oceans. In particular, atmospheric CO2 concentrations will rise to unprecedented levels by the end of this century, while global warming will enhance stratification of aquatic ecosystems and may thereby diminish the supply of nutrients into the surface layer. These processes enrich phytoplankton with carbon, but suppress nutrient availability. Phytoplankton with a high carbon-to-nutrient content provide poor-quality food for most zooplankton species, which may shift the species composition of zooplankton and higher trophic levels to less nutrient-demanding species. As a consequence, climate-driven changes in plankton stoichiometry may alter the structure and functioning of entire aquatic food webs.
  • FEMS Microbiology Ecology

    Pulsed nitrogen supply induces dynamic changes in the amino acid compositionand microcystin production of the harmful cyanobacterium Planktothrix agardhii

    Dedmer Van de Waal, G. Ferreruela, L. Tonk, Ellen Van Donk, J. Huisman, P.M. Visser, Hans C. P. Matthijs
    Planktothrix agardhii is a widespread harmful cyanobacterium of eutrophic waters, and can produce the hepatotoxins [Asp3]microcystin-LR and [Asp3]microcystin-RR. These two microcystin variants differ in their first variable amino acid position, which is occupied by either leucine (L) or arginine (R). Although microcystins are extensively investigated, little is known about the mechanisms that determine the production of different microcystin variants. We hypothesize that enhanced nitrogen availability will increase the intracellular content of the nitrogen-rich amino acid arginine, and thereby promote the production of the variant [Asp3]microcystin-RR. To test this hypothesis, we transferred P. agardhii strain 126/3 from nitrogen-replete to nitrogen-deficient conditions, and after 2 weeks of growth under nitrogen deficiency, we added a nitrogen pulse. We found a rapid increase in the cellular nitrogen to carbon ratio and the amino acids aspartic acid and arginine, indicative of cyanophycin synthesis. This was followed by a more gradual increase of the total amino acid content connected to balanced growth. As expected, the [Asp3]microcystin-RR variant increased strongly after the nitrogen pulse, while the [Asp3]microcystin-LR increased to a much lesser extent. We conclude that sudden nitrogen enrichment affects the amino acid composition of harmful cyanobacteria, which, in turn, affects the production and composition of their microcystins.
  • Ecology Letters

    The ecological stoichiometry of toxins produced by harmful cyanobacteria: an experimental test of the carbon-nutrient balance hypothesis

    Dedmer Van de Waal, Jolanda Verspagen, Miquel Lürling, Ellen Van Donk, P.M. Visser, J. Huisman
    The elemental composition of primary producers reflects the availability of light, carbon and nutrients in their environment. According to the carbon-nutrient balance hypothesis, this has implications for the production of secondary metabolites. To test this hypothesis, we investigated a family of toxins, known as microcystins, produced by harmful cyanobacteria. The strain Microcystis aeruginosa HUB 5-2-4, which produces several microcystin variants of different N:C stoichiometry, was cultured in chemostats supplied with various combinations of nitrate and CO2. Excess supply of both nitrogen and carbon yielded high cellular N:C ratios accompanied by high cellular contents of total microcystin and the nitrogen-rich variant microcystin-RR. Comparable patterns were found in Microcystis-dominated lakes, where the relative microcystin-RR content increased with the seston N:C ratio. In total, our results are largely consistent with the carbon-nutrient balance hypothesis, and warn that a combination of rising CO2 and nitrogen enrichment will affect the microcystin composition of harmful cyanobacteria.
  • FEMS Microbiology Ecology

    Amino acid availability determines the ratio of microcystin variants in the cyanobacterium Planktothrix agardhii

    L. Tonk, Dedmer Van de Waal, P. Slot, J. Huisman, Hans C. P. Matthijs, P.M. Visser
    Cyanobacteria are capable of producing multiple microcystin variants simultaneously. The mechanisms that determine the composition of microcystin variants in cyanobacteria are still debated. [Asp3]microcystin-RR contains arginine at the position where the more toxic [Asp3]microcystin-LR incorporates leucine. We cultured the filamentous cyanobacterium Planktothrix agardhii strain 126/3 with and without external addition of leucine and arginine. Addition of leucine to the growth medium resulted in a strong increase of the [Asp3]microcystin LR/RR ratio, while addition of arginine resulted in a decrease. This demonstrates that amino acid availability plays a role in the synthesis of different microcystin variants. Environmental changes affecting cell metabolism may cause differences in the intracellular availability of leucine and arginine, which can thus affect the production of microcystin variants. Because leucine contains one nitrogen atom while arginine contains four nitrogen atoms, we hypothesized that low nitrogen availability might shift the amino acid composition in favor of leucine, which might explain seasonal increases in the [Asp3]microcystin LR/RR ratio in natural populations. However, when a continuous culture of P. agardhii was shifted from nitrogen-saturated to a nitrogen-limited mineral medium, leucine and arginine concentrations decreased, but the leucine/arginine ratio did not change. Accordingly, while the total microcystin concentration of the cells decreased, we did not observe changes in the [Asp3]microcystin LR/RR ratio in response to nitrogen limitation.
  • Freshwater Biology

    Estimates of bacterial and phytoplankton mortality caused by viral lysis and microzooplankton grazing in a shallow eutrophic lake

    M. Tijdens, Dedmer Van de Waal, H. Slovackova, H.L. Hoogveld, H.J. Gons
    1. Since viral lysis and zooplankton grazing differ in their impact on the aquatic food web, it is important to assess the relative importance of both mortality factors. In this study, an adapted version of the dilution technique was applied to simultaneously estimate the impact of both viral lysis and zooplankton grazing on the mortality of heterotrophic bacteria, eukaryotic algae, unicellular cyanobacteria, prochlorophytes and especially filamentous cyanobacteria in a shallow eutrophic lake. 2. Four dilution experiments were performed in December 2004, January 2005, and March and April 2006. Viral and heterotrophic bacterial abundances were obtained by epifluorescence microscopy and abundances of different phytoplankton groups by flow cytometry and light microscopy. 3. Viral lysis was identified as the main mortality cause during the December 2004 and January 2005 experiments, apparently removing between 84% and 97% of the potential filamentous cyanobacterial production and up to 101% of the potential heterotrophic bacterial production. Microzooplankton grazing was estimated to remove between 90% and 99% of the potential unicellular cyanobacterial production and up to 46% of the potential heterotrophic bacterial production during the spring 2006 experiments 4. In some cases, no significant impact of viral lysis or zooplankton grazing was detected. Contrary to expectations, the apparent growth rate of filamentous cyanobacteria was even sometimes observed to decrease significantly upon dilution of microzooplankton. 5. The dilution technique can give valuable insight into the impact of zooplankton grazing and viral lysis on the mortality of different plankton groups but require some caveats require special care to be taken when comparing and interpreting results.

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BLOOMTOX: Global change impacts on cyanobacterial bloom toxicity


Think of a hot summer day. Imagine getting a glass of cold water, but no water is coming, or it is brownish with a foul odor. Imagine being a farmer, and your cattle need water but there is only smelly (blue-)green water. Imagine going for a cooling swim, but the lake is closed for recreation. For millions of people, this is not imagination, but a recurring reality caused by toxic cyanobacterial blooms.

Harmful cyanobacterial blooms produce toxins that are a major threat to water quality and human health. Blooms increase with eutrophication and are expected to be amplified by climate change. Yet, we lack a mechanistic understanding on the toxicity of blooms, and their response to the complex interplay of multiple global change factors. Bloom toxicity is determined by a combination of mechanisms acting at different ecological scales, ranging from cyanobacterial biomass accumulation in the ecosystem, to the dominance of toxic species in the community, contribution of toxic genotypes in the population, and the amounts of toxins in cells. 

In this project, we will develop a fundamental understanding of bloom toxicity by revealing the combined effects of nutrients, elevated pCO2 and warming at each scale, and integrate these responses using a unique combination of ecological theory, technological advances, and methodological innovations. Specifically, we will use first principles to scale from cellular traits, like carbon and nutrient acquisition, cellular toxin synthesis and growth rates, to population and community dynamics.