Skip to main content
SpringerLink
Log in

High-frequency monitoring of phytoplankton dynamics within the European water framework directive: application to metalimnetic cyanobacteria

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

Large, sub-alpine, stratified lakes are directly within the scope of the European Water Framework Directive (WFD) and need adapted monitoring systems. Moreover, anthropogenic eutrophication was frequently the main cause of their water quality degradation in the 20th century. This paper is primarily aimed at demonstrating how in situ sensor-equipped buoys could be the base of monitoring designs to support the WFD objectives. The core of this paper, mainly methodological, focuses on single-depth, high frequency (4 per hour) fluorescence measurements. It shows that the internal wave pattern provides additional information to the single-depth time series to assess phytoplankton dynamics in a stratified water column displaying strong, vertical biomass heterogeneity. The paper deals with the following three aspects: (1) definition of an indicator to determine whether or not the sensor actually detects the metalimnetic fluorescence peak, (2) vertical representation of chlorophyll distribution from single-depth series; (3) time evolution of the fluorescence peak (maximum value, depth and associated temperature, peak width).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Notes

  1. The ®MAREL buoy (Mesures Automatisées en Réseau pour l’Environnement et le Littoral) is an automatic measurement system developed by IFREMER (French Research Institute for Exploitation of the Sea) for operational monitoring of coastal water quality.

  2. The PROLIPHYC project is conducted by a joint team of public research laboratories (LEESU, INRA, LGE, MNHN), the INSU-CNRS technical department (DT-INSU), an environmental engineering company (Sogreah), a water instrumentation company (nke) and a local authority (CISALB).

References

  • AFNOR (2006) Water quality—Guidance standard on the enumeration of phytoplankton using inverted microscopy (Utermöhl technique). In: NF EN 15204

  • Alford MH, Gregg MC, Merrifield MA (2006) Structure, propagation, and mixing of energetic baroclinic tides in Mamala Bay, Oahu, Hawaii. J Phys Oceanogr 36:997–1018

    Article  Google Scholar 

  • Allan I, Vrana B, Greenwood R, Mills G, Roig B, Gonzalez C (2006) A “toolbox” for biological and chemical monitoring requirements for the European Union’s Water Framework Directive. Talanta 1st Swift-WFD workshop on validation of Robustness of sensors and bioassays for Screening Pollutants—1st SWIFT-WFD 2004 69:302–322

  • Anneville O, Gammeter S, Straile D (2005) Phosphorus decrease and climate variability: mediators of synchrony in phytoplankton changes among European peri-alpine lakes. Freshw Biol 50:1731–1746

    Article  Google Scholar 

  • Arneborg L, Liljebladh B (2001) The internal seiches in Gullmar Fjord. Part I: Dynamics. J Phys Oceanogr 31:2549–2566

    Article  Google Scholar 

  • Bensoussan N, Calzas M, Degres Y, Drezen C, Escoffier N, Freissinet C, Humbert J, Jezequel D, Le Vu B, Paolini G, Prévot F, Quiblier C, Sarazin G, Tassin B, Vinçon-Leite B, Viollier E, Groleau A. (2008) From in Situ Time Series to Mean Image: new Tools for Monitoring Harmful Algal Blooms. In: AGU fall meeting Geophysical research abstracts. San Francisco, USA

  • Bensoussan N, Calzas M, Degres Y, Drezen C, Escoffier N, Freissinet C, Guillerm O, Humbert J, Jezequel D, Le Vu B, Paolini G, Prévot F, Quiblier C, Sarazin G, Tassin B, Vinçon-Leite B, Viollier E, Groleau A (2009) Observing and integrating deep chlorophyll maximum of the metalimnetic cyanobacteria P. rubescens from single point measurements. In: ASLO Aquatic Science Meeting Abstracts. Nice, France. p 22

  • Bergondo DL, Kester DR, Stoffel HE, Woods WL (2005) Time-series observations during the low sub-surface oxygen events in Narragansett Bay during summer 2001. Marine Chemistry Special Issue in honor of Dana R. Kester 97:90–103

    Google Scholar 

  • Beutler M, Wiltshire K, Meyer B, Moldaenke C, Lüring C, Meyerhöfer M, Hansen U-P, Dau H (2002) A fluorometric method for the differentiation of algal populations in vivo and in situ. Photosynth Res 72:39–53

    Article  Google Scholar 

  • Blain S, Guillou J, Treguer P, Woerther P, Delauney L, Follenfant E, Gontier O, Hamon M, Leilde B, Masson A, Tartu C, Vuillemin R (2004) High frequency monitoring of the coastal marine environment using the MAREL buoy. J Environ Monit 6:569–575

    Article  Google Scholar 

  • Bournet PE, Dartus D, Tassin B, Vinçon Leite B (1996) Ondes internes du lac du Bourget: analyse des observations par des modèles linéaires. Revue des Sciences de l’Eau 9:247–266

    Google Scholar 

  • Briand J-F, Jacquet S, Flinois C, Avois-Jacquet C, Maisonnette C, Leberre B, Humbert J-F (2005) Variations in the microcystin production of Planktothrix rubescens (Cyanobacteria) assessed from a four-year survey of Lac du Bourget (France) and from laboratory experiments. Microb Ecol 50:418–428

    Article  Google Scholar 

  • Bricker SB, Ferreira JG, Simas T (2003) An integrated methodology for assessment of estuarine trophic status. Ecol Model 169:39–60

    Article  Google Scholar 

  • Carstensen J (2007) Statistical principles for ecological status classification of Water Framework Directive monitoring data. Mar Pollut Bull 55:3–15

    Article  Google Scholar 

  • Chorus I, Bartram J (eds) (1999) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. World Health Organization, Geneva

    Google Scholar 

  • Cuypers Y, Vinçon-Leite B, Poulin M, Tassin B (2006) Non linear internal seiches degeneration in a in a deep sub-alpine. In: Proceedings of the 10th european workshop on physical processes in natural waters. Granada, Spain

  • Davies AM, Xing JX, Willmott AJ (2009) Influence of open boundary conditions and sill height upon seiche motion in a gulf. Ocean Dyn 59:863–879

    Article  Google Scholar 

  • Dokulil MT, Teubner K (2000) Cyanobacterial dominance in lakes. Hydrobiologia 438:1–12

    Article  Google Scholar 

  • Dokulil MT, Teubner K (2005) Do phytoplankton communities correctly track trophic changes? An assessment using directly measured and palaeolimnological data. Freshw Biol 50:1594–1604

    Article  Google Scholar 

  • Dorigo U, Fontvieille D, Humbert JF (2006) Spatial variability in the abundance and composition of the free-living bacterioplankton community in the pelagic zone of Lake Bourget (France). Fems Microbiol Ecol 58:109–119

    Article  Google Scholar 

  • Dur G, Schmitt F, Souissi S (2007) Analysis of high frequency temperature time series in the Seine estuary from the Marel autonomous monitoring buoy. Hydrobiologia 588:59–68

    Article  Google Scholar 

  • Dworak T, Gonzalez C, Laaser C, Interwies E (2005) The need for new monitoring tools to implement the WFD. Environmental Science and Policy Research and Technology Integration in Support of the European Union Water Framework Directive 8:301–306

    Google Scholar 

  • Environmental Protection Agency (2006) Water Framework Directive Monitoring Programme. Ireland

  • Ernst B, Hoeger SJ, O’Brien E, Dietrich DR (2006) Oral toxicity of the microcystin-containing cyanobacterium Planktothrix rubescens in European whitefish (Coregonus lavaretus). Aquat Toxicol 79:31–40

    Article  Google Scholar 

  • Ernst B, Hoeger SJ, O’Brien E, Dietrich DR (2009) Abundance and toxicity of Planktothrix rubescens in the pre-alpine Lake Ammersee, Germany. Harmful Algae 8:329–342

    Article  Google Scholar 

  • European Parliament and Council (2000) Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for Community action in the field of water policy

  • Ferreira J, Vale C, Soares C, Salas F, Stacey P, Bricker S, Silva M, Marques J (2007) Monitoring of coastal and transitional waters under the E.U. Water Framework Directive. Environ Monit Assess 135:195–216

    Article  Google Scholar 

  • Feuillade J, Orand A (1994) Studies on Lake Nantua. Lake surroundings and historical background. Studies on Lake Nantua (France). A Eutrophic Lake on the way to rehabilitation. Arch Hydrobiol Beih Ergebn Limnol 42:1–16

    Google Scholar 

  • Garel E, Nunes S, Neto J, Fernandes R, Neves R, Marques J, Ferreira O (2009) The autonomous Simpatico system for real-time continuous water-quality and current velocity monitoring: examples of application in three Portuguese estuaries. Geo-Mar Lett 29:331–341

    Article  Google Scholar 

  • Gayte X, Vinçon-Leite B, Groleau A, Blanc P, Druart JC, Balvay G, Pelletier J, Paolini G, Fontvieille D, Tassin B (1998) Analyse de l’évolution de la qualité des eaux du lac du Bourget (1995–1996). Chambéry, CISALB

  • Gerdeaux D, Anneville O, Hefti D (2006) Fishery changes during re-oligotrophication in 11 peri-alpine Swiss and French lakes over the past 30 years. Acta Oecologica 30:161–167

    Article  Google Scholar 

  • Groleau A, Sarazin G, Vinçon-Leite B, Tassin B, Quiblier-Lloberas C (2000) Tracing calcite precipitation with specific conductance in a hard water alpine lake (Lake Bourget). Water Res 34:4151–4160

    Article  Google Scholar 

  • Henderson-Sellers B (1984) Engineering limnology. Pitman Advanced Pub. Program, Boston

    Google Scholar 

  • Holland DP, Walsby AE (2008) Viability of the cyanobacterium Planktothrix rubescens in the cold and dark, related to over-winter survival and summer recruitment in Lake Zürich. Eur J Phycol 43:179–184

    Article  Google Scholar 

  • Hudnell HK (2009) The state of U.S. freshwater harmful algal blooms assessments, policy and legislation. Toxicon. doi:10.1016/j.toxicon.2009.07.021

  • Humbert J-F, Paolini G, Leberre B (2000) Monitoring a toxic cyanobacterial bloom in Lake Bourget (France) and its consequences for water quality. In: Hallegraeff G et al. (ed) Proceedings of the 9th International Conference on Harmful Algal Blooms. Hobart, Australia, pp 496–499

  • INSEE (2008) Recensement de la population en France http://www.insee.fr/fr/recensement/page_accueil_rp.htm

  • Jacquet S, Briand J-F, Leboulanger C, Avois-Jacquet C, Oberhaus L, Tassin B, Vinçon-Leite B, Paolini G, Druart J-C, Anneville O, Humbert J-F (2005) The proliferation of the toxic cyanobacterium Planktothrix rubescens following restoration of the largest natural French lake (Lac du Bourget). Harmful Algae 4:651–672

    Article  Google Scholar 

  • Jann-Para G, Schwob I, Feuillade M (2004) Occurrence of toxic Planktothrix rubescens blooms in lake Nantua, France. Toxicon 43:279–285

    Article  Google Scholar 

  • Jeppesen E, Søndergaard M, Jensen JP, Havens KE, Anneville O, Carvalho L, Coveney MF, Deneke R, Dokulil MT, Foy B, Gerdeaux D, Hampton SE, Hilt S, Kangur K, Köhler J, Lammens EHHR, Lauridsen TL, Manca M, Miracle MR, Moss B, Nõges P, Persson G, Phillips G, Portielje R, Romo S, Schelske CL, Straile D, Tatrai I, Willén E, Winder M (2005) Lake responses to reduced nutrient loading—an analysis of contemporary long-term data from 35 case studies. Freshw Biol 50:1747–1771

    Article  Google Scholar 

  • Jones I, Maberly SC (2008) Automatic in-lake monitoring in the English Lake District: the effect of lake size on stratification. International Association of Theoretical and Applied Limnology, Vol 30, Pt 1, Proceedings 30:70–72

  • Kaiblinger C, Anneville O, Tadonléké R, Rimet F, Druart J, Guillard J, Dokulil M (2009) Central European water quality indices applied to long-term data from peri-alpine lakes: test and possible improvements. Hydrobiologia 633:67–74

    Article  Google Scholar 

  • Leboulanger C, Dorigo U, Jacquet S, Berre BL, Paolini G, Humbert J-F (2002) Application of a submersible spectrofluorometer for rapid monitoring of freshwater cyanobacterial blooms: a case study. Aquat Microb Ecol 30:83–89

    Article  Google Scholar 

  • Lee JHW, Hodgkiss IJ, Wong KTM, Lam IHY (2005) Real time observations of coastal algal blooms by an early warning system. Estuar Coast Shelf Sci 65:172–190

    Article  Google Scholar 

  • Lemmin U, Mortimer CH (1986) Tests of an extension to internal seiches of Defant’s procedure for determination of surface seiche characteristics in real lakes. Limnol Oceanogr 31:1207–1231

    Article  Google Scholar 

  • Madgwick G, Jones ID, Thackeray SJ, Elliott JA, Miller HJ (2006) Phytoplankton communities and antecedent conditions: high resolution sampling in Esthwaite Water. Freshw Biol 51:1798–1810

    Article  Google Scholar 

  • Mills DK, Laane R, Rees JM, van der Loeff MR, Suylen JM, Pearce DJ, Sivyer DB, Heins C, Platt K, Rawlinson M (2003) Smartbuoy: a marine environmental monitoring buoy with a difference. In: Building the European capacity in operational oceanography, Proceedings. pp 311–316

  • Ministère de l’Ecologie et du Développement Durable (2006) Circulaire relative à la constitution et la mise en oeuvre du programme de surveillance pour les eaux douces de surface en application de la directive 2000/60/CE. France

  • Oberhaus L, Groleau A, Quiblier-Lloberas C, Druart J-C, Vinçon-Leite B, Tassin B (2003) Influence of physical factors on Cyanobacteria development in a deep subalpine lake (Lake Bourget). Journal de Recherche Océanographique 28

  • Oberholster PJ, Botha A-M, Cloete TE (2006) Toxic cyanobacterial blooms in a shallow, artificially mixed urban lake in Colorado, USA. Lakes Reserv Res Manage 11:111–123

    Article  Google Scholar 

  • OECD Organisation for Economic Co-operation and Development (1982) Eutrophication of waters: monitoring, assessment and control. Paris, France

  • Painting SJ, Devlin MJ, Rogers SI, Mills DK, Parker ER, Rees HL (2005) Assessing the suitability of OSPAR EcoQOs for eutrophication vs ICES criteria for England and Wales. Mar Pollut Bull 50:1569–1584

    Article  Google Scholar 

  • Palethorpe B, Hayes-Gill B, Crowe J, Sumner M, Crout N, Foster M, Reid T, Benford S, Greenhalgh C, Laybourn-Parry J (2004) Real-time physical data acquisition through a remote sensing platform on a polar lake. Limnol Oceanogr Methods 2:191–201

    Article  Google Scholar 

  • Paolini G (2006) Le suivi de la qualité des eaux du lac du Bourget. In: Colloque “Autour du lac du Bourget”. Chambéry, France

  • Salmaso N (2009) Long-term phytoplankton community changes in a deep subalpine lake: responses to nutrient availability and climatic fluctuations. Freshw Biol. doi:10.1111/j.1365-2427.2009.02325.x

  • Salmaso N, Morabito G, Buzzi F, Garibaldi L, Simona M, Mosello R (2006) Phytoplankton as an Indicator of the Water Quality of the Deep Lakes South of the Alps. Hydrobiologia 563:167–187

    Article  Google Scholar 

  • Sammari C, Koutitonsky VG, Moussa M (2006) Sea level variability and tidal resonance in the Gulf of Gabes, Tunisia. Cont Shelf Res 26:338–350

    Article  Google Scholar 

  • Sarmento H, Descy J-P (2008) Use of marker pigments and functional groups for assessing the status of phytoplankton assemblages in lakes. J Appl Phycol 20:1001–1011

    Article  Google Scholar 

  • Tadonléké RD, Lazzarotto J, Anneville O, Druart JC (2009) Phytoplankton productivity increased in Lake Geneva despite phosphorus loading reduction. J Plankton Res 31:1179–1194

    Article  Google Scholar 

  • Tassin B, Vinçon-Leite B (1998) Forecasting of water quality in lakes: a predictive use of a one-dimensional model. Application to Lake Bourget (Savoie, France). Hydrobiologia 374:47–60

    Article  Google Scholar 

  • Tilzer MM, Gaedke U, Schweizer A, Beese B, Wieser T (1991) Interannual variability of phytoplankton productivity and related parameters in Lake Constance—no response to decreased phosphorus loading. J Plankton Res 13:755–777

    Article  Google Scholar 

  • Vandenberghe V, Goethals PLM, Van Griensven A, Meirlaen J, De Pauw N, Vanrolleghem P, Bauwens W (2005) Application of automated measurement stations for continuous water quality monitoring of the Dender River in Flanders, Belgium. Environ Monit Assess 108:85–98

    Article  Google Scholar 

  • Vinçon-Leite B, Mouchel JM, Tassin B (1989) Modélisation de l’évolution thermique saisonnière du lac du Bourget (Savoie, France). Revue des Sciences de l’Eau 2:483–510

    Google Scholar 

  • Vinçon-Leite B, Tassin B, Jaquet J-M (1995) Contribution of mathematical modeling to lake ecosystem understanding: Lake Bourget (Savoy, France). Hydrobiologia 300–301:433–442

    Article  Google Scholar 

  • Vinçon-Leite B, Tassin B, Druart J-C (2002) Phytoplankton variability in Lake Bourget: Phytoplankton dynamics and meteorology. Lakes Reserv Res Manage 7:93–102

    Google Scholar 

  • Walsby AE, Schanz F (2002) Light-dependent growth rate determines changes in the population of Planktothrix rubescens over the annual cycle in lake Zürich, Switzerland. New Phytol 154:671–687

    Article  Google Scholar 

  • Walsby AE, Schanz F, Schmid M (2006) The Burgundy-blood phenomenon: a model of buoyancy change explains autumnal waterblooms by Planktothrix rubescens in Lake Zürich. New Phytol 169:109–122

    Article  Google Scholar 

Download references

Acknowledgements

The PROLIPHYC project is funded by the ANR-PRECODD Programme. We wish to acknowledge Pascal Perney (INRA) for the logistic support and Yannis Cuypers (LOCEAN, Université Pierre et Marie Curie) for fruitful discussions. The authors also express their gratitude to Jean Sutcliffe for the revision of the English text. We very much appreciated the valuable comments by two referees.

Author information

Authors and Affiliations

  1. LEESU UMR MA-102 Agro ParisTech, Université Paris-Est Ecole des Ponts ParisTech, 6 Avenue Blaise Pascal, 77455, Marne-la-Vallée, France

    B. Le Vu, Brigitte Vinçon-Leite, B. J. Lemaire, J. F. Deroubaix, E. Rioust & B. Tassin

  2. IPGP UMR 7154, Université Paris Diderot, Paris 7, Laboratoire de Géochimie des Eaux, 75205, Paris Cedex 13, France

    N. Bensoussan, A. Groleau & F. Prévot

  3. CNRS DT-INSU, Bâtiment IPEV, 29280, Plouzané, France

    M. Calzas & C. Drezen

  4. INRA, UMR BIOEMCO, 46 rue d’Ulm, 75005, Paris, France

    N. Escoffier & J. F. Humbert

  5. FRE 3206 CNRS/MNHN MCAM, USM 505 Cyanobactéries, Cyanotoxines et Environnement, Muséum National d’Histoire Naturelle, 75231, Paris, France

    N. Escoffier & C. Quiblier

  6. Université Paris 7 Diderot, 5 rue Thomas Mann, 75013, Paris, France

    C. Quiblier

  7. nke Electronics, ZI de Kerandré, 56700, Hennebont, France

    Y. Dégrés

  8. CISALB, 73000, Chambéry, France

    G. Paolini

  9. Water and Territorial Service Group, SOGREAH Consultants, 38130, Echirolles, France

    C. Freissinet

Authors
  1. B. Le Vu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brigitte Vinçon-Leite
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. B. J. Lemaire
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. Bensoussan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Calzas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. Drezen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. F. Deroubaix
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. N. Escoffier
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Y. Dégrés
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. C. Freissinet
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. A. Groleau
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. J. F. Humbert
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. G. Paolini
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. F. Prévot
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. C. Quiblier
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. E. Rioust
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. B. Tassin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Brigitte Vinçon-Leite.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Le Vu, B., Vinçon-Leite, B., Lemaire, B.J. et al. High-frequency monitoring of phytoplankton dynamics within the European water framework directive: application to metalimnetic cyanobacteria. Biogeochemistry 106, 229–242 (2011). https://doi.org/10.1007/s10533-010-9446-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-010-9446-1

Keywords

Search

Navigation