, Volume 723, Issue 1, pp 63–75 | Cite as

Biodiversity in eutrophicated shallow lakes: determination of tipping points and tools for monitoring

  • J. RobinEmail author
  • A. Wezel
  • G. Bornette
  • F. Arthaud
  • S. Angélibert
  • V. Rosset
  • B. Oertli


Nutrient-rich freshwater ecosystems are generally considered as having low ecological quality and low associated biodiversity. In such systems we analysed the effects of water quality on biodiversity of several species groups, to determine tipping points and tools for monitoring. We investigated the water quality of 99 eutrophic and hypertrophic shallow lakes with extensive fish culture during a 3-year study, through the measures of physico-chemical parameters, phytoplankton biomass and structure. In a second step, we related the water quality with richness of aquatic plants, macroinvertebrates and dragonflies. With concentrations of chlorophyll-a above 30 or 70 μg l−1, shallow lakes are normally classified, respectively, in a poor or bad ecological state. However, our results show that chlorophyll-a concentrations up to 78 μg l−1 could be found together with relatively high species or family richness of aquatic plants, invertebrates and dragonflies. We identified most tipping points with 50–60 μg l−1 of chlorophyll-a, values above which a significant decrease of species diversity was found. For monitoring of these shallow lakes we propose to use chlorophyll-a concentrations in combination with water transparency during spring. These parameters are easily applicable and cheap and they yield a good forecast of the biodiversity for the species groups studied.


Phytoplankton Aquatic plants Macroinvertebrates Dragonflies Fish ponds Cyanobacteria Water Framework Directive Water quality 



This study was funded by the French Ministry of the Environment and Sustainable Development through the DIVA2 “Biodiversity and Agriculture” programme, the French Water Agency (Agence de l’Eau Rhône-Mediterranée-Corse) and the Rhône-Alpes Region. We are grateful to Sylvie Prestoz, Pauline Chevassu, David Pobel, Mathieu Guerin, Thomas Lhuillery, David Leclerc, Nicola Indermuhle et Michaël Delahaye for their field and laboratory assistance during this study. A special thanks to Vincent Payet for his help for statistical analyses.


  1. AFNOR, 2006. Qualité de l’eau – Norme guide pour le dénombrement du phytoplancton par microscopie inversée (méthode Utermöhl): 39 pp.Google Scholar
  2. Arst, H. & A. Reinart, 2009. Application of optical classifications to North European lakes. Aquatic Ecology 43: 789–801.CrossRefGoogle Scholar
  3. Arthaud, F., M. Mousset, D. Vallod, J. Robin, A. Wezel & G. Bornette, 2012. Effect of light stress from phytoplankton on the relationship between aquatic vegetation and the propagule bank in shallow lakes. Freshwater Biology 57: 666–675.CrossRefGoogle Scholar
  4. Arthaud, F., D. Vallod, J. Robin, A. Wezel & G. Bornette, 2013. Short-term succession of aquatic plant species richness along ecosystem productivity and dispersal gradients in shallow lakes. Journal of Vegetation Science 24: 148–156.CrossRefGoogle Scholar
  5. Barbe, J., M. Lafont, J. Mouthon & M. Philippe, 2003. Protocole actualisé de la diagnose rapide des plans d’eau. Rapport CEMAGREF: 30 pp.Google Scholar
  6. Blindow, I., A. Hargeby & G. Andersson, 1998. Alternative stable states in shallow lakes: what causes a shift? In Jeppesen, E., M. Søndergaard, M. Søndergaard & K. Christoffersen (eds), The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York: 353–360.CrossRefGoogle Scholar
  7. Bornette, G. & S. Puijalon, 2011. Response of aquatic plants to abiotic factors: a review. Aquatic Sciences 73: 1–14.CrossRefGoogle Scholar
  8. Brönmark, C. & L. A. Hansson, 2005. The Biology of Lakes and Ponds. Oxford University Press, Oxford: 300 pp.Google Scholar
  9. Carpenter, S. R., N. F. Caracao, D. L. Correll, R. W. Howarth, A. N. Sharpley & V. H. Smith, 1998. Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecological applications 8: 559–568.CrossRefGoogle Scholar
  10. Céréghino, R., J. Biggs, B. Oertli, S. Declerck & S. Declerck, 2008. The ecology of European ponds: defining the characteristics of a neglected freshwater habitat. Hydrobiologia 597: 1–6.CrossRefGoogle Scholar
  11. Chovannec, A., J. Waringer, M. Straif, W. Graf, W. Reckendorfer, W. Waringer-Löschenkohl, A. Waidbacher & H. Schultz, 2005. The Floodplain Index – a new approach for assessing the ecological status of river/floodplain-systems according to the EU Water Framework Directive. Archiv Fur Hydrobiologie Supplement 155: 169–185.Google Scholar
  12. Codd, G. A., J. Lindsay, F. M. Young, L. F. Morrison & J. S. Metcalf, 2005. Harmful cyanobacteria. In Huisman, J., H. C. P. Matthijs & P. M. Visser (eds), Harmful Cyanobacteria. Springer, Dordrecht: 1–23.CrossRefGoogle Scholar
  13. De Nie, H. W., 1987. The decrease in aquatic vegetation in Europe and its consequences for fish populations. EIFAC/CECPI. Occasional Paper 19: 52 pp.Google Scholar
  14. Declerck, S., J. Vandekerkhove, L. Johansson, K. Muylaert, J. M. Conde-Porcuna, K. Van der Gucht, C. Perez-Martinez, T. Lauridsen, K. Schwenk, G. Zwart, W. Rommens, J. Lopez-Ramos, E. Jeppesen, W. Vyverman, L. Brendonck & L. De Meester, 2005. Multigroup biodiversity in shallow lakes along gradients of phosphorus and water plant cover. Ecology 86: 1905–1915.CrossRefGoogle Scholar
  15. Dokulil, M. & K. Teubner, 2003. Eutrophication and restoration of shallow lakes – the concept of stable equilibria revisited. Hydrobiologia 506: 29–35.CrossRefGoogle Scholar
  16. Egertson, C. J., J. A. Kopaska & J. A. Downing, 2004. A century of change in macrophyte abundance and composition in response to agricultural eutrophication. Hydrobiologia 524: 145–156.CrossRefGoogle Scholar
  17. Elliott, J. A., C. S. Reynolds & A. E. Irisch, 2001. An investigation of dominance in phytoplankton using the PROTECH model. Freshwater Biology 46: 99–108.CrossRefGoogle Scholar
  18. Fairchild, G. W., J. N. Anderson & D. J. Velinsky, 2005. The trophic sate chain of relationships in ponds. Does size matter? Hydrobiologia 539: 35–46.CrossRefGoogle Scholar
  19. Hakanson, L., 2005. The importance of lake morphometry for the structure and function of lakes. International Review of Hydrobiology 90: 433–461.CrossRefGoogle Scholar
  20. Jeffries, M., 2005. Small ponds and big landscapes: the challenge of invertebrate spatial and temporal dynamics for European pond conservation. Aquatic Conservation: Marine and Freshwater Ecosystems 15: 541–547.CrossRefGoogle Scholar
  21. Jeppesen, E., J. P. Jensen, M. Søndergaard, T. Lauridsen & F. Landkildehus, 2000. Trophic structure, species richness and biodiversity in Danish lakes: changes along a phosphorus gradient. Freshwater Biology 45: 201–218.CrossRefGoogle Scholar
  22. Jeppesen, E., J. P. Jensen, M. Sondergaard, K. S. Hansen, P. H. Moller, H. U. Rasmussen, V. Norby & S. E. Larsen, 2003. Does resuspension prevent a shift to a clear state in shallow lakes during reoligotrophication? Limnology and Oceanography 48: 1913–1919.CrossRefGoogle Scholar
  23. Joniak, T., B. Nagengast & N. Kuczynska-Kippen, 2009. Can popular systems of trophic classification be used for small water bodies? Oceanological and Hydrobiological Studies 38: 145–151.CrossRefGoogle Scholar
  24. Kuiper-Goodman, T., J. Falconer & J. Fitzgerald, 1999. Human health aspects. In Chorus, I. & J. Bartram (eds), Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management. London, E & FN Spon: 125–160.Google Scholar
  25. Laplace-Treyture, C., C. Chauvin, M. Menay & A. Dutartre, 2010. Protocole standardisé d’échantillonnage et de conservation du phytoplancton en grands cours d’eau applicable aux réseaux de mesure DCE. Rapport CEMAGREF: 19 pp.Google Scholar
  26. Le Vu, B., B. Vinçon-Leite, B. J. Lemaire, N. Bensoussan, M. Calzas, C. Drezen, J. F. Deroubaix, N. Escoffier, Y. Dégrés, C. Freissinet, A. Groleau, J. F. Humbert, G. Paolini, F. Prévot, C. Quiblier, E. Rioust & B. Tassin, 2011. High-frequency monitoring of phytoplankton dynamics within the European water framework directive: application to metalimnetic cyanobacteria. Biogeochemistry 106: 229–242.CrossRefGoogle Scholar
  27. Leboulanger, C., U. Dorigo, S. Jacquet, B. Le Berre, G. Paolini & J.-F. Humbert, 2002. Application of a submersible spectrofluorometer for rapid monitoring of freshwater cyanobacterial blooms: a case study. Aquatic Microbial Ecology 30: 83–89.CrossRefGoogle Scholar
  28. Leclerc, D., S. Angélibert, V. Rosset & B. Oertli, 2010. Les Libellules (Odonata) des étangs piscicoles de la Dombes. Martinia 26(3–4): 98–108.Google Scholar
  29. MEEDAD, 2009. Evaluation de l’état des eaux douces de surface de métropole. Guide technique. Report of the French Ministry of Ecology: 72 pp.Google Scholar
  30. Melzer, A., 1999. Aquatic macrophytes as tool for lake management. Hydrobiologia 395(396): 181–190.CrossRefGoogle Scholar
  31. Murphy, K. J., 2002. Plant communities and plant diversity in softwater lakes of northern Europe. Aquatic Botany 73: 287–324.CrossRefGoogle Scholar
  32. Naumann, E., 1927. Aims and main problems of regional limnology. Botaniska Notiser: 81–103.Google Scholar
  33. OECD, 1982. Eutrophication of waters: monitoring, assessment and control. OCDE, Paris, France: 154 pp.Google Scholar
  34. Oertli, B., D. Auderset Joye, E. Castella, R. Juge, D. Cambin & J. B. Lachavanne, 2002. Does size matter? The relationship between pond area and biodiversity. Biological Conservation 104: 59–70.CrossRefGoogle Scholar
  35. Oertli, B., D. Auderset Joye, E. Castella, R. Juge, A. Lehmann & J. B. Lachavanne, 2005. PLOCH: a standardized method for sampling and assessing the biodiversity in ponds. Aquatic Conservation: Marine and Freshwater Ecosystems 15: 665–679.CrossRefGoogle Scholar
  36. Oertli, B., N. Indermuehle, S. Angélibert, H. Hinden & A. Stoll, 2008. Macroinvertebrate assemblages in 25 high alpine ponds of the Swiss National Park (Cirque of Macun) and relation to environmental variables. Hydrobiologia 597: 29–41.CrossRefGoogle Scholar
  37. Parsons, T. R. & J. D. H. Strickland, 1963. Discussion of spectrophotometric determination of marine-plant pigments with revised equations for ascertaining chlorophylls and carotenoïds. Journal of Marine Research 21: 155–163.Google Scholar
  38. Peeters, E. T. H. M., R. J. M. Franken, E. Jeppesen, B. Moss, E. Bécares, L. A. Hansson, S. Romo, T. Kairesalo, E. M. Gross, E. Van Donk, T. Noges, K. Irvine, R. Kornijow & M. Scheffer, 2009. Assessing ecological quality of shallow lakes: does knowledge of transparency suffice? Basic and Applied Ecology 10: 89–96.CrossRefGoogle Scholar
  39. Pobel, D., J. Robin & J. F. Humbert, 2011. Influence of sampling strategies on the monitoring of cyanobacteria in shallow lakes: lessons from a case study in France. Water Research 45: 1005–1014.PubMedCrossRefGoogle Scholar
  40. Remsburg, A. J. & M. G. Turner, 2009. Aquatic and terrestrial drivers of dragonfly (Odonata) assemblages within and among north-temperate lakes. Journal of the North American Benthological Society 28: 44–56.CrossRefGoogle Scholar
  41. Reynolds, C. S., 1984. Phytoplankton periodicity: the interactions of form, function and environmental variability. Freshwater Biology 14: 111–142.CrossRefGoogle Scholar
  42. Scheffer, M., S. H. Hospera, M. L. Meijera, B. Moss & E. Jeppesen, 1993. Alternative equilibria in shallow lakes. Trends in Ecology and Evolution 8: 275–279.PubMedCrossRefGoogle Scholar
  43. Schindler, M., C. Fesl & A. Chovanec, 2003. Dragonfly associations (Insecta: Odonata) in relation to habitat variables: a multivariate approach. Hydrobiologia 497: 169–180.CrossRefGoogle Scholar
  44. Sommer, U., Z. M. Gliwicz, W. Lampert & A. Duncan, 1986. The PEG-model of seasonal succession of planktonic events in fresh waters. Archiv für Hydrobiologie 106: 433–471.Google Scholar
  45. Sondergaard, M., E. Jeppesen & J. P. Jensen, 2005. Ponds or lake: does it make any difference? Archiv fur Hydrobiologie 162: 143–165.CrossRefGoogle Scholar
  46. Watson, S. B., E. McCauley & J. A. Downing, 1997. Patterns in phytoplankton taxonomic composition across temperate lakes of differing nutrient status. Limnology and Oceanography 42: 486–495.CrossRefGoogle Scholar
  47. Wezel, A., F. Arthaud, C. Dufloux, F. Renoud, D. Vallod, J. Robin & B. Sarrazin, 2013a. Varied impact of land use on water and sediment parameters on fish ponds of the Dombes agroecosystem, France. Hydrological Sciences Journal 58(4): 1–18.CrossRefGoogle Scholar
  48. Wezel, A., M. Guerin, J. Robin, F. Arthaud & D. Vallod, 2013b. Management effects on water quality, sediments and fish production in extensive fish ponds in the Dombes region, France. Limnologica 43(3): 210–218.CrossRefGoogle Scholar
  49. White, J. & K. Irvine, 2003. The use of littoral mesohabitats and their macroinvertebrate assemblages in the ecological assessment of lakes. Aquatic Conservation: Marine and Freshwater Ecosystems 13: 331–351.CrossRefGoogle Scholar
  50. Wilcox, G. R. & J. DeCosta, 1990. The effects of Anabaena flos-aquae inoculation, pH elevation and N/P manipulation on the algal biomass and species composition of an acid lake. Hydrobiologia 202: 85–104.Google Scholar
  51. Zhu, W., L. Wan & L. Zhao, 2010. Effect of nutrient level on phytoplankton community structure in different water bodies. Journal of Environmental Sciences 22: 32–39.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • J. Robin
    • 1
    • 2
    Email author
  • A. Wezel
    • 2
  • G. Bornette
    • 1
  • F. Arthaud
    • 3
  • S. Angélibert
    • 4
  • V. Rosset
    • 4
  • B. Oertli
    • 4
  1. 1.Laboratory Ecology of Fluvial Hydrosystems, UMR 5023 LEHNACNRS University of Lyon, ENTPE, ISARALyonFrance
  2. 2.Department of Agroecology and Environment, Research Group Ecosystems and Aquatic ResourcesISARA LyonLyon Cedex 07France
  3. 3.UMR INRA 042 CARRTELUniversity of SavoieLe Bourget-du-Lac CedexFrance
  4. 4.Hepia Geneva Technology, Architecture and Landscape, Department of Nature ManagementUniversity of Applied Sciences Western SwitzerlandJussy-GenevaSwitzerland

Personalised recommendations