Modelling the plankton groups of the deep, peri-alpine Lake Bourget

Predicting phytoplankton succession and variability in natural systems remains to be a grand challenge in aquatic ecosystems research. In this study, we identified six major plankton groups in Lake Bourget (France), based on cell size, taxonomic properties, food-web interactions and occurrence patterns: cyanobacterium Planktothrix rubescens, small and large phytoplankton, mixotrophs, herbivorous and carnivorous zooplankton. We then developed a deterministic dynamic model that describes the dynamics of these groups in terms of carbon and phosphorus fluxes, as well as of particulate organic phosphorus and dissolved inorganic phosphorus. The modular and generic model scheme, implemented as a set of modules under Framework for Aquatic Biogeochemical Models (FABM) enables run-time coupling of the plankton module an arbitrary number of times, each time with a prescribed position across the autotrophy/heterotrophy continuum. Parameters of the plankton groups were mainly determined conjointly by the taxonomic and allometric relationships, based on the species composition and average cellular volume of each group. The biogeochemical model was coupled to the one-dimensional General Ocean Turbulence Model (GOTM) and forced with local meteorological conditions. The coupled model system shows very high skill in predicting the spatiotemporal distributions of water temperature and dissolved inorganic phosphorus for five simulated years within the period 2004 to 2010, and intermediate skill in predicting the plankton succession. We performed a scenario analysis to gain insight into the factors driving the sudden disappearance of P. rubescens in 2010. Our results provide evidence for the hypothesis that the abundance of this species before the onset of stratification is critical for its success later in the growing season, pointing thereby to a priority effect.

[1]  David Hamilton,et al.  Coupling high-resolution measurements to a three-dimensional lake model to assess the spatial and temporal dynamics of the cyanobacterium Planktothrix rubescens in a medium-sized lake , 2012, Hydrobiologia.

[2]  R. Payne,et al.  Albedo of the Sea Surface , 1972 .

[3]  A. Walsby,et al.  The daily integral of growth by Planktothrix rubescens calculated from growth rate in culture and irradiance in Lake Zürich. , 2000, The New phytologist.

[4]  J. Steele,et al.  The role of predation in plankton models , 1992 .

[5]  M. R. Droop,et al.  Vitamin B12 and Marine Ecology. IV. The Kinetics of Uptake, Growth and Inhibition in Monochrysis Lutheri , 1968, Journal of the Marine Biological Association of the United Kingdom.

[6]  P. J. Hansen,et al.  Modeling succession of key resource-harvesting traits of mixotrophic plankton , 2016, The ISME Journal.

[7]  Per Juel Hansen,et al.  Zooplankton grazing and growth: Scaling within the 2–2,000‐µm body size range , 2000 .

[8]  C. Avois-Jacquet,et al.  Variations in the Microcystin Production of Planktothrix rubescens (Cyanobacteria) Assessed from a Four-Year Survey of Lac du Bourget (France) and from Laboratory Experiments , 2005, Microbial Ecology.

[9]  H. Ducklow,et al.  A nitrogen-based model of plankton dynamics in the oceanic mixed layer , 1990 .

[10]  Marcel Babin,et al.  Bio‐optical and biogeochemical properties of different trophic regimes in oceanic waters , 2005 .

[11]  Stephanie Dutkiewicz,et al.  A size‐structured food‐web model for the global ocean , 2012 .

[12]  Jacco C. Kromkamp,et al.  A computer model of buoyancy and vertical migration in cyanobacteria , 1990 .

[13]  O. Anneville,et al.  The need for ecological monitoring of freshwaters in a changing world: a case study of Lakes Annecy, Bourget, and Geneva , 2014, Environmental Monitoring and Assessment.

[14]  Nicholas R. Bates,et al.  Pelagic functional group modeling: Progress, challenges and prospects , 2006 .

[15]  Thomas R. Anderson,et al.  Plankton functional type modelling : running before we can walk? , 2005 .

[16]  N. Swenson,et al.  Eco‐evolutionary differences in light utilization traits and distributions of freshwater phytoplankton , 2011 .

[17]  Bruno Tassin,et al.  Long-term temperature evolution in a deep sub-alpine lake, Lake Bourget, France: how a one-dimensional model improves its trend assessment , 2014, Hydrobiologia.

[18]  Barbara J. Robson,et al.  When do aquatic systems models provide useful predictions, what is changing, and what is next? , 2014, Environ. Model. Softw..

[19]  J. Burkholder,et al.  Misuse of the phytoplankton-zooplankton dichotomy : the need to assign organisms as mixotrophs within plankton functional types , 2013 .

[20]  Alessandro Oggioni,et al.  A biogeochemical model of Lake Pusiano (North Italy) and its use in the predictability of phytoplankton blooms: first preliminary results , 2006 .

[21]  O. Anneville,et al.  The proliferation of the toxic cyanobacterium Planktothrix rubescens following restoration of the largest natural French lake (Lac du Bourget) , 2005 .

[22]  K. Flynn,et al.  Building the “perfect beast”: modelling mixotrophic plankton , 2009 .

[23]  D. Dietrich,et al.  Abundance and toxicity of Planktothrix rubescens in the pre-alpine Lake Ammersee, Germany , 2009 .

[24]  Dietmar Straile,et al.  Seasonal, inter‐annual and long term variation in top–down versus bottom–up regulation of primary production , 2013 .

[25]  J. Grover,et al.  Coexistence of mixotrophs, autotrophs, and heterotrophs in planktonic microbial communities. , 2010, Journal of theoretical biology.

[26]  S. Jacquet,et al.  Predicting future effects from nutrient abatement and climate change on phosphorus concentrations in Lake Bourget, France , 2010 .

[27]  J. Kindle,et al.  Summary diagrams for coupled hydrodynamic-ecosystem model skill assessment , 2009 .

[28]  Henri J. Dumont,et al.  The dry weight estimate of biomass in a selection of Cladocera, Copepoda and Rotifera from the plankton, periphyton and benthos of continental waters , 1975, Oecologia.

[29]  B. Riemann,et al.  On the Strategy of "Eating Your Competitor": A Mathematical Analysis of Algal Mixotrophy , 1996 .

[30]  J. Elser,et al.  Ecological stoichiometry: An elementary approach using basic principles , 2013 .

[31]  D. Straile Gross growth efficiencies of protozoan and metazoan zooplankton and their dependence on food concentration, predator‐prey weight ratio, and taxonomic group , 1997 .

[32]  Mridul K. Thomas,et al.  Allometric scaling and taxonomic variation in nutrient utilization traits and maximum growth rate of phytoplankton , 2012 .

[33]  O. Kerimoglu,et al.  Autotrophic Stoichiometry Emerging from Optimality and Variable Co-limitation , 2016, Front. Ecol. Evol..

[34]  Karsten Bolding,et al.  A general framework for aquatic biogeochemical models , 2014, Environ. Model. Softw..

[35]  Tom Andersen,et al.  Carbon, nitrogen, and phosphorus content of freshwater zooplankton , 1991 .

[36]  P. Reichert,et al.  Biogeochemical model of Lake Zurich: model equations and results , 2001 .

[37]  L. Krienitz,et al.  Rarity, ecological memory, rate of floral change in phytoplankton—and the mystery of the Red Cock , 2010, Hydrobiologia.

[38]  R. Armstrong,et al.  Grazing limitation and nutrient limitation in marine ecosystems: Steady state solutions of an ecosystem model with multiple food chains , 1994 .

[39]  K. Wirtz Mechanistic origins of variability in phytoplankton dynamics: Part I: niche formation revealed by a size-based model , 2013 .

[40]  Martin Beniston,et al.  Mountain Weather and Climate: A General Overview and a Focus on Climatic Change in the Alps , 2006, Hydrobiologia.

[41]  Luigi Naselli-Flores,et al.  Toxic cyanobacterial blooms in reservoirs under a semiarid mediterranean climate: The magnification of a problem , 2007, Environmental toxicology.

[42]  Miquel Lürling,et al.  Beyond the Plankton Ecology Group (PEG) Model : Mechanisms Driving Plankton Succession , 2012 .

[43]  C. Klausmeier,et al.  Contrasting size evolution in marine and freshwater diatoms , 2009, Proceedings of the National Academy of Sciences.

[44]  Phillip A. Davis,et al.  Comparison of the depth where Planktothrix rubescens stratifies and the depth where the daily insolation supports its neutral buoyancy , 2004 .

[45]  Brigitte Vinçon-Leite,et al.  High-frequency monitoring of phytoplankton dynamics within the European water framework directive: application to metalimnetic cyanobacteria , 2011 .

[46]  M. Pahlow,et al.  Optimality-based model of phytoplankton growth and diazotrophy , 2013 .

[47]  J. Humbert,et al.  Grazing of two toxic Planktothrix species by Daphnia pulicaria: potential for bloom control and transfer of microcystins , 2007 .

[48]  K. Miyakoda,et al.  A General Circulation Model for Upper Ocean Simulation , 1988 .

[49]  Francesco Bignami,et al.  Longwave radiation budget in the Mediterranean Sea , 1995 .

[50]  Frédéric Rimet,et al.  Blue-Green Algae in a “Greenhouse Century”? New Insights from Field Data on Climate Change Impacts on Cyanobacteria Abundance , 2015, Ecosystems.

[51]  Mridul K. Thomas,et al.  Linking traits to species diversity and community structure in phytoplankton , 2010, Hydrobiologia.

[52]  B. Edvardsen,et al.  Seasonal dynamics and depth distribution of Planktothrix spp. in Lake Steinsfjorden (Norway) related to environmental factors , 2007 .

[53]  T. Kiørboe How zooplankton feed: mechanisms, traits and trade‐offs , 2011, Biological reviews of the Cambridge Philosophical Society.

[54]  James P Grover,et al.  Stoichiometry, herbivory and competition for nutrients: simple models based on planktonic ecosystems. , 2002, Journal of theoretical biology.

[55]  O. Kerimoglu,et al.  Cyanobacterial bloom termination: the disappearance of Planktothrix rubescens from Lake Bourget (France) after restoration , 2014 .

[56]  Hongbin Liu,et al.  Relationships between phytoplankton growth and cell size in surface oceans: Interactive effects of temperature, nutrients, and grazing , 2010 .

[57]  U. Sommer,et al.  Climate change and the phytoplankton spring bloom: warming and overwintering zooplankton have similar effects on phytoplankton , 2011 .

[58]  Deep living Planktothrix rubescens modulated by environmental constraints and climate forcing , 2012, Hydrobiologia.

[59]  O. Anneville,et al.  Seasonal and inter-annual scales of variability in phytoplankton assemblages: comparison of phytoplankton dynamics in three peri-alpine lakes over a period of 28 years , 2004 .

[60]  A. Walsby,et al.  Light-dependent growth rate determines changes in the population of Planktothrix rubescens over the annual cycle in Lake Zürich, Switzerland. , 2002, The New phytologist.

[61]  C. Lancelot,et al.  Trait‐based representation of diatom functional diversity in a plankton functional type model of the eutrophied southern North Sea , 2014 .

[62]  J. Kondo,et al.  Air-sea bulk transfer coefficients in diabatic conditions , 1975 .

[63]  P. K. Bjørnsen,et al.  Zooplankton grazing and growth: Scaling within the 2‐2,‐μm body size range , 1997 .

[64]  O. Anneville,et al.  Occurrence and mass development of Mougeotia spp. (Zygnemataceae) in large, deep lakes , 2015, Hydrobiologia.

[65]  F. Jüttner,et al.  Strategies for the co-existence of zooplankton with the toxic cyanobacterium Planktothrix rubescens in Lake Zürich , 1999 .

[66]  J. Humbert,et al.  Impact of internal waves on the spatial distribution of Planktothrix rubescens (cyanobacteria) in an alpine lake , 2011, The ISME Journal.

[67]  Zoe V. Finkel,et al.  Phytoplankton in a changing world: cell size and elemental stoichiometry , 2010 .

[68]  B. Blasius,et al.  Vertical distribution and composition of phytoplankton under the influence of an upper mixed layer. , 2010, Journal of theoretical biology.

[69]  J. Huisman,et al.  Summer heatwaves promote blooms of harmful cyanobacteria , 2008 .

[70]  W. Richard,et al.  TEMPERATURE AND PHYTOPLANKTON GROWTH IN THE SEA , 1972 .

[71]  Effects of nutrient availability and temperature on phytoplankton development: a case study from large lakes south of the Alps , 2012, Aquatic Sciences.

[72]  W. Arthur,et al.  Effects of Temporal Priority on Interspecific Interactions and Community Development , 1996 .

[73]  Nico Salmaso,et al.  Long‐term phytoplankton community changes in a deep subalpine lake: responses to nutrient availability and climatic fluctuations , 2010 .

[74]  A. Konopka Buoyancy regulation and vertical migration by Oscillatoria rubescens in Crooked Lake, Indiana , 1982 .

[75]  C. Paulson,et al.  Irradiance Measurements in the Upper Ocean , 1977 .

[76]  Martin Beniston,et al.  Estimating future cyanobacterial occurrence and importance in lakes: a case study with Planktothrix rubescens in Lake Geneva , 2017, Aquatic Sciences.

[77]  Susanne Menden-Deuer,et al.  Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton , 2000 .

[78]  J. Burkholder,et al.  The role of mixotrophic protists in the biological carbon pump , 2013 .

[79]  K. Rinke,et al.  A simulation study of the feedback of phytoplankton on thermal structure via light extinction , 2010 .

[80]  Oliver Köster,et al.  Harmful filamentous cyanobacteria favoured by reduced water turnover with lake warming , 2012 .

[81]  S. Heaney,et al.  Diversity in the influence of temperature on the growth rates of freshwater algae, and its ecological relevance , 2004 .

[82]  Andreas Meister,et al.  Description of a flexible and extendable physical–biogeochemical model system for the water column , 2006 .

[83]  N. Kamjunke,et al.  Phosphorus gain by bacterivory promotes the mixotrophic flagellate Dinobryon spp. during re-oligotrophication , 2006 .

[84]  F. Morel,et al.  KINETICS OF NUTRIENT UPTAKE AND GROWTH IN PHYTOPLANKTON 1 , 1987 .

[85]  James W. Murray,et al.  Functional responses for zooplankton feeding on multiple resources: a review of assumptions and biological dynamics , 2003 .

[86]  George B. Arhonditsis,et al.  Phytoplankton functional type modelling: Running before we can walk? A critical evaluation of the current state of knowledge , 2016 .

[87]  A. Walsby,et al.  The critical pressures of gas vesicles in Planktorhrix rubescens in relation tothe depth of winter mixing in Lake Zürich, Switzerland , 1998 .

[88]  Elena Litchman,et al.  The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. , 2007, Ecology letters.

[89]  P. Reichert,et al.  Modelling functional groups of phytoplankton in three lakes of different trophic state , 2008 .

[90]  Matthew R. Hipsey,et al.  Implementation of ecological modeling as an effective management and investigation tool: Lake Kinneret as a case study , 2009 .

[91]  Ben A. Ward,et al.  Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux , 2016, Proceedings of the National Academy of Sciences.

[92]  O. Kerimoglu,et al.  Role of phytoplankton cell size on the competition for nutrients and light in incompletely mixed systems. , 2012, Journal of theoretical biology.

[93]  James P. Grover,et al.  Resource Competition in a Variable Environment: Phytoplankton Growing According to the Variable-Internal-Stores Model , 1991, The American Naturalist.