, Volume 710, Issue 1, pp 173–187 | Cite as

Contrasting roles of water chemistry, lake morphology, land-use, climate and spatial processes in driving phytoplankton richness in the Danish landscape

  • Korhan ÖzkanEmail author
  • Erik Jeppesen
  • Martin Søndergaard
  • Torben L. Lauridsen
  • Lone Liboriussen
  • Jens-Christian Svenning


Understanding of the forces driving the structure of biotic communities has long been an important focus for ecology, with implications for applied and conservation science. To elucidate the factors driving phytoplankton genus richness in the Danish landscape, we analyzed data derived from late-summer samplings in 195 Danish lakes and ponds in a spatially-explicit framework. To account for the uneven sampling of lakes in the monitoring data, we performed 1,000 permutations. A random set of 131 lakes was assembled and a single sample was selected randomly for each lake at each draw and all the analyses were performed on permuted data 1,000 times. The local environment was described by lake water chemistry, lake morphology, land-use in lake catchments, and climate. Analysis of the effects of four groups of environmental factors on the richness of the main groups of phytoplankton revealed contrasting patterns. Lake water chemistry was the strongest predictor of phytoplankton richness for all groups, while lake morphology also had a strong influence on Bacillariophyceae, Cyanobacteria, Dinophyceae, and Euglenophyceae richness. Climate and land-use in catchments contributed only little to the explained variation in phytoplankton richness, although both factors had a significant effect on Bacillariophyceae richness. Notably, total nitrogen played a more important role for phytoplankton richness than total phosphorus. Overall, models accounted for ca. 30% of the variation in genus richness for all phytoplankton combined as well as the main groups separately. Local spatial structure (<30 km) in phytoplankton richness suggested that connectivity among lakes and catchment-scale processes might also influence phytoplankton richness in Danish lakes.


Freshwater algae Metacommunity structure Nitrogen concentration Shallow lakes Spatial structure 



We greatly acknowledge the great work of a large number of experts who participated in the counting of samples and fieldwork during 20 years of monitoring. We thank Anders Nielsen for his help with landscape data; Thomas Davidson, Liselotte Sander Johansson, and Rikke Bjerring Hansen for helpful discussions and Anne Mette Poulsen for linguistic corrections. This project was supported by the Danish Agency for Science Technology and Innovation, the EU projects WISER and REFRESH, CLEAR (a Villum Kann Rasmussen Centre of Excellence Project), the STF project CRES and the Greenland Climate Research Centre.


  1. Abrams, P. A., 1995. Monotonic or unimodal diversity productivity gradients – what does competition theory predict. Ecology 76: 2019–2027.CrossRefGoogle Scholar
  2. Andersson, G. & G. Cronberg, 1984. Aphanizomenon flosaqua and Daphnia: an interesting plankton association in hypertrophic waters. In Bösheim, S. & M. Nicholls (eds), Interactions Between Different Trophic Levels in Freshwater. Norsk Limnologförening, Oslo: 63–76. (in Norwegian).Google Scholar
  3. Anselin, L., 1988. Spatial Econometrics: Methods and Models. Kluwer, Dordrecht.CrossRefGoogle Scholar
  4. Beisner, B. E., P. R. Peres, E. S. Lindstrom, A. Barnett & M. L. Longhi, 2006. The role of environmental and spatial processes in structuring lake communities from bacteria to fish. Ecology 87: 2985–2991.PubMedCrossRefGoogle Scholar
  5. Bivand, R., 2009. spdep: spatial dependence: weighting schemes, statistics and models. R package version 0.4-56.Google Scholar
  6. Bjornstad, O. N., 2009. ncf: spatial nonparametric covariance functions. R package version 1.1-3.Google Scholar
  7. Declerck, S., J. Vandekerkhove, L. Johansson, K. Muylaert, J. M. Conde-Porcuna, K. Vd. Gucht, C. Pérez-Martínez, T. Lauridsen, K. Schwenk, G. Zwart, W. Rommens, J. López-Ramos, E. Jeppesen, W. Vyverman, L. Brendonck & L. D. Meester, 2005. Multi-group biodiversity in shallow lakes along gradients of phosphorus and water plant cover. Ecology 86: 1905–1915.CrossRefGoogle Scholar
  8. Declerck, S., M. Vanderstukken, A. Pals, K. Muylaert & L. de Meester, 2007. Plankton biodiversity along a gradient of productivity and its mediation by macrophytes. Ecology 88: 2199–2210.PubMedCrossRefGoogle Scholar
  9. Elser, J. J., M. E. S. Bracken, E. E. Cleland, D. S. Gruner, W. S. Harpole, H. Hillebrand, J. T. Ngai, E. W. Seabloom, J. B. Shurin & J. E. Smith, 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10: 1135–1142.PubMedCrossRefGoogle Scholar
  10. ESRI, 2008. ArcView GIS. v. 9.3. Redlands, CA, USAGoogle Scholar
  11. Finlay, B. J., 2002. Global dispersal of free-living microbial eukaryote species. Science 296: 1061–1063.PubMedCrossRefGoogle Scholar
  12. Fott, J., L. Pechar & M. Prazakova, 1980. Fish as a factor controlling water quality in ponds. In Barica, J. & L. R. Mur (eds), Hypertrophic Ecosystems. Developments in Hydrobiology. Junk, The Hague: 255–261.CrossRefGoogle Scholar
  13. Gallego, I., T. A. Davidson, E. Jeppesen, C. Pérez-Martínez, P. Sánchez, M. Juan, F. Fuentes, D. León, P. Peñalver, J. Toja & J. J. Casas, 2012. Taxonomic or ecological approaches? Searching for phytoplankton surrogates in the determination of richness and assemblage composition in ponds. Ecological Indicators (in press).Google Scholar
  14. Gonzalez Sagrario, M. A., E. Jeppesen, J. Gomá, M. Søndergaard, J. P. Jensen, T. Lauridsen & F. Landkildehus, 2005. Does high nitrogen loading prevent clear-water conditions in shallow lakes at moderately high phosphorus concentrations? Freshwater Biology 50: 27–41.CrossRefGoogle Scholar
  15. Harrell, F. E., 2001. Regression Modeling Strategies: With Applications to Linear Models, Logisitic Regression, and Survival Analysis. Springer, New York.Google Scholar
  16. Hillebrand, H., F. Watermann, R. Karez & U. G. Berninger, 2001. Differences in species richness patterns between unicellular and multicellular organisms. Oecologia 126: 114–124.CrossRefGoogle Scholar
  17. Hooper, D. U., F. S. Chapin, J. J. Ewel, A. Hector, P. Inchausti, S. Lavorel, J. H. Lawton, D. M. Lodge, M. Loreau, S. Naeem, B. Schmid, H. Setala, A. J. Symstad, J. Vandermeer & D. A. Wardle, 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75: 3–35.CrossRefGoogle Scholar
  18. Huisman, J., H. C. P. Matthijs & P. M. Visser, 2005. Harmful Cyanobacteria. Springer, Dordrecht.CrossRefGoogle Scholar
  19. Huston, M. A., 1994. Biological Diversity: The Coexistence of Species on Changing Landscapes. Cambridge University Press, Cambridge/New York, NY, USA.Google Scholar
  20. Ibelings, B. W., A. S. Gsell, W. M. Mooij, E. van Donk, S. van den Wyngaert & L. N. D. Domis, 2011. Chytrid infections and diatom spring blooms: paradoxical effects of climate warming on fungal epidemics in lakes. Freshwater Biology 56: 754–766.CrossRefGoogle Scholar
  21. James, W. J., W. D. Taylor & J. W. Barko, 1992. Production and vertical migration of Ceratium hirundinella in relation to phosphorus availability in Eau Galle reservoir, Wisconsin. Canadian Journal of Fisheries and Aquatic Sciences 49: 694–700.CrossRefGoogle Scholar
  22. James, C., J. Fisher, V. Russell, S. Collings & B. Moss, 2005. Nitrate availability and hydrophyte species richness in shallow lakes. Freshwater Biology 50: 1049–1063.CrossRefGoogle Scholar
  23. Jensen, J. P., E. Jeppesen, K. Olrik & P. Kristensen, 1994. Impact of nutrients and physical factors on the shift from cyanobacterial to chlorophyte dominance in shallow Danish lakes. Canadian Journal of Fisheries and Aquatic Sciences 51: 1692–1699.CrossRefGoogle Scholar
  24. Jeppesen, E., M. Søndergaard, M. Søndergaard & K. Christoffersen, 1997. The Structuring Role of Submerged Water Plants in Lakes. Springer-Verlag, New York, USA.Google Scholar
  25. Jeppesen, E., M. Søndergaard, J. P. Jensen, E. Mortensen, A. M. Hansen & T. Jorgensen, 1998. Cascading trophic interactions from fish to bacteria and nutrients after reduced sewage loading: an 18-year study of a shallow hypertrophic lake. Ecosystems 1: 250–267.CrossRefGoogle Scholar
  26. Jeppesen, E., M. Søndergaard, B. Kronvang, J. P. Jensen, L. M. Svendsen & T. L. Lauridsen, 1999. Lake and catchment management in Denmark. Hydrobiologia 396: 419–432.CrossRefGoogle Scholar
  27. 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
  28. Jeppesen, E., B. Kronvang, M. Meerhoff, M. Søndergaard, K. M. Hansen, H. E. Andersen, T. L. Lauridsen, L. Liboriussen, M. Beklioglu, A. Özen & J. E. Olesen, 2009. Climate change effects on runoff, catchment phosphorus loading and lake ecological state, and potential adaptations. Journal of Environmental Quality 38: 1930–1941.PubMedCrossRefGoogle Scholar
  29. Jeppesen, E., B. Kronvang, J. E. Olesen, J. Audet, M. Søndergaard, C. C. Hoffmann, H. E. Andersen, T. L. Lauridsen, L. Liboriussen, S. E. Larsen, M. Beklioglu, M. Meerhoff, A. Özen & K. Özkan, 2011. Climate change effects on nitrogen loading from cultivated catchments in Europe: implications for nitrogen retention, ecological state of lakes and adaptation. Hydrobiologia 663: 1–21.CrossRefGoogle Scholar
  30. Kennedy, W. J. J. & J. E. Gentle, 1980. Statistical Computing. Marcel Dekker, New York.Google Scholar
  31. Kissling, W. D. & G. Carl, 2008. Spatial autocorrelation and the selection of simultaneous autoregressive models. Global Ecology and Biogeography 17: 59–71.CrossRefGoogle Scholar
  32. Kronvang, B., G. Ærtebjerg, R. Grant, P. Kristensen, M. Hovmand & J. Kirkegaard, 1993. Nationwide monitoring of nutrients and their ecological effects state of the Danish aquatic environment. Ambio 22: 176–187.Google Scholar
  33. Kronvang, B., E. Jeppesen, D. J. Conley, M. Søndergaard, S. E. Larsen, N. B. Ovesen & J. Carstensen, 2005. Nutrient pressures and ecological responses to nutrient loading reductions in Danish streams, lakes and coastal waters. Journal of Hydrology 304: 274–288.CrossRefGoogle Scholar
  34. Kruk, C., L. Rodriguez-Gallego, M. Meerhoff, F. Quintans, G. Lacerot, N. Mazzeo, F. Scasso, J. C. Paggi, E. T. H. M. Peeters & S. Marten, 2009. Determinants of biodiversity in subtropical shallow lakes (Atlantic coast, Uruguay). Freshwater Biology 54: 2628–2641.CrossRefGoogle Scholar
  35. Legendre, P. & L. Legendre, 1998. Numerical Ecology. Elsevier, Amsterdam.Google Scholar
  36. Leibold, M. A., M. Holyoak, N. Mouquet, P. Amarasekare, J. M. Chase, M. F. Hoopes, R. D. Holt, J. B. Shurin, R. Law, D. Tilman, M. Loreau & A. Gonzalez, 2004. The metacommunity concept: a framework for multi-scale community ecology. Ecological Letters 7: 601–613.CrossRefGoogle Scholar
  37. Longhi, M. L. & B. E. Beisner, 2010. Patterns in taxonomic and functional diversity of lake phytoplankton. Freshwater Biology 55: 1349–1366.CrossRefGoogle Scholar
  38. Loreau, M., N. Mouquet & R. D. Holt, 2003. Meta-ecosystems: a theoretical framework for a spatial ecosystem ecology. Ecological Letters 6: 673–679.CrossRefGoogle Scholar
  39. MacArthur, R. H. & E. O. Wilson, 1967. The Theory of Island Biogeography. Princeton University Press, Princeton, NJ.Google Scholar
  40. McCann, K. S., 2000. The diversity–stability debate. Nature 405: 228–233.PubMedCrossRefGoogle Scholar
  41. McCauley, E. & W. W. Murdoch, 1987. Cyclic and stable populations: plankton as paradigm. American Naturalist 129: 97–121.CrossRefGoogle Scholar
  42. Meerhoff, M., J. M. Clemente, F. Teixeira de Mello, C. Iglesias, A. R. Pedersen & E. Jeppesen, 2007. Can warm climate-related structure of littoral predator assemblies weaken the clear water state in shallow lakes? Global Change Biology 13: 1888–1897.CrossRefGoogle Scholar
  43. Mittelbach, G. G., C. F. Steiner, S. M. Scheiner, K. L. Gross, H. L. Reynolds, R. B. Waide, M. R. Willig, S. I. Dodson & L. Gough, 2001. What is the observed relationship between species richness and productivity? Ecology 82: 2381–2396.CrossRefGoogle Scholar
  44. Moss, B., E. Jeppesen, M. Søndergaard, T. L. Lauridsen & Z. W. Liu, 2012. Nitrogen, macrophytes, shallow lakes and nutrient limitation – resolution of a current controversy? Hydrobiologia.Google Scholar
  45. Muylaert, K., C. Perez-Martinez, P. Sanchez-Castillo, T. L. Lauridsen, M. Vanderstukken, S. A. J. Declerck, K. Van der Gucht, J. M. Conde-Porcuna, E. Jeppesen, L. De Meester & W. Vyverman, 2010. Influence of nutrients, submerged macrophytes and zooplankton grazing on phytoplankton biomass and diversity along a latitudinal gradient in Europe. Hydrobiologia 653: 79–90.CrossRefGoogle Scholar
  46. Nielsen, A., D. Trolle, M. Søndergaard, T. L. Lauridsen, R. Bjerring, J. E. Olesen & E. Jeppesen, 2012. Watershed land use effects on lake water quality – role of depth, alkalinity, season and distance to water bodies (conditionally accepted).Google Scholar
  47. Oksanen, L., S. D. Fretwell, J. Arruda & P. Niemela, 1981. Exploitation ecosystems in gradients of primary productivity. American Naturalist 118: 240–261.CrossRefGoogle Scholar
  48. Özkan, K., E. Jeppesen, L. S. Johansson & M. Beklioglu, 2010. The response of periphyton and submerged macrophytes to nitrogen and phosphorus loading in shallow warm lakes: a mesocosm experiment. Freshwater Biology 55: 463–475.CrossRefGoogle Scholar
  49. Pádisak, J., 1993. The influence of different disturbance frequencies on the species richness, diversity and equitability of phytoplankton in shallow lakes. Hydrobiologia 249: 135–156.CrossRefGoogle Scholar
  50. Pádisak, J., L. O. Crossetti & L. Naselli-Flores, 2009. Use and misuse in the application of the phytoplankton functional classification: a critical review with updates. Hydrobiologia 621: 1–19.CrossRefGoogle Scholar
  51. Ptacnik, R., A. G. Solimini, T. Andersen, T. Tamminen, P. Brettum, L. Lepisto, E. Willen & S. Rekolainen, 2008. Diversity predicts stability and resource use efficiency in natural phytoplankton communities. Proceedings of the National Academy of Sciences of the United States of America 105: 5134–5138.PubMedCrossRefGoogle Scholar
  52. Ptacnik, R., T. Andersen, P. Brettum, L. Lepisto & E. Willen, 2010. Regional species pools control community saturation in lake phytoplankton. Proceedings of the Royal Society B-Biological Sciences 277: 3755–3764.CrossRefGoogle Scholar
  53. R Development Core Team, 2008. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
  54. Reynolds, C. S., 1984. The Ecology of Freshwater Phytoplankton. Cambridge University Press, Cambridge.Google Scholar
  55. Reynolds, C. S., V. Huszar, C. Kruk, L. Naselli-Flores & S. Melo, 2002. Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research 24: 417–428.CrossRefGoogle Scholar
  56. Rørslett, B., 1991. Principal determinants of aquatic water plant richness in northern European lakes. Aquatic Botany 39: 173–193.CrossRefGoogle Scholar
  57. Scheffer, M., S. Rinaldi, A. Gragnani, L. R. Mur & E. H. vanNes, 1997. On the dominance of filamentous cyanobacteria in shallow, turbid lakes. Ecology 78: 272–282.CrossRefGoogle Scholar
  58. Schindler, D. W., 1977. Evolution of phosphorus limitation in lakes. Science 195: 260–262.PubMedCrossRefGoogle Scholar
  59. Schnitzer, S. A., J. N. Klironomos, J. HilleRisLambers, L. L. Kinkel, P. B. Reich, K. Xiao, M. C. Rillig, B. A. Sikes, R. M. Callaway, S. A. Mangan, E. H. van Nes & M. Scheffer, 2011. Soil microbes drive the classic plant diversity–productivity pattern. Ecology 92: 296–303.PubMedCrossRefGoogle Scholar
  60. Shapiro, J., 1984. Blue-green dominance in lakes: the role and management significance of pH and CO2. Internationale Revue der Gesamten Hydrobiologie 69: 765–780.CrossRefGoogle Scholar
  61. Shurin, J. B., K. Cottenie & H. Hillebrand, 2009. Spatial autocorrelation and dispersal limitation in freshwater organisms. Oikos 159: 151–159.Google Scholar
  62. Soininen, J., M. Kokocinski, S. Estlander & J. Kotanen, 2007. Neutrality, niches, and determinants of plankton metacommunity structure across boreal wetland ponds. Ecoscience 14: 146–154.CrossRefGoogle Scholar
  63. Sommer, U., J. Pádisak, C. S. Reynolds & P. Juhasznagy, 1993. Hutchinson heritage – the diversity–disturbance relationship in phytoplankton. Hydrobiologia 249: 1–7.CrossRefGoogle Scholar
  64. Søndergaard, M. & B. Moss, 1998. Impact of submerged macrophytes on phytoplankton in shallow freshwater lakes. In Jeppesen, E., M. Søndergaard & K. Christoffersen (eds), The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York: 115–132.CrossRefGoogle Scholar
  65. Søndergaard, M., E. Jeppesen, J. P. Jensen & S. L. Amsinck, 2005. Water framework directive: ecological classification of Danish lakes. Journal of Applied Ecology 42: 616–629.CrossRefGoogle Scholar
  66. Søndergaard, M., L. Liboriussen, A. R. Pedersen & E. Jeppesen, 2008. Lake restoration by fish removal: short- and long-term effects in 36 Danish lakes. Ecosystems 11: 1291–1305.Google Scholar
  67. Sterner, R. W. & J. J. Elser, 2002. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. Princeton University Press, Princeton, NJ.Google Scholar
  68. Tilman, D., 1982. Resource Competition and Community Structure. Princeton University Press, Princeton, NJ.Google Scholar
  69. Tilman, D., 1993. Species richness of experimental productivity gradients – how important is colonization limitation. Ecology 74: 2179–2191.CrossRefGoogle Scholar
  70. Tilman, D., D. Wedin & J. Knops, 1996. Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379: 718–720.CrossRefGoogle Scholar
  71. Vanormelingen, P., K. Cottenie, E. Michels, K. Muylaert, W. Vyverman & L. De Meester, 2008. The relative importance of dispersal and local processes in structuring phytoplankton communities in a set of highly interconnected ponds. Freshwater Biology 53: 2170–2183.Google Scholar
  72. Venables, W. N. & B. D. Ripley, 2000. Modern Applied Statistics with S-Plus. Springer, New York.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Korhan Özkan
    • 1
    • 2
    Email author
  • Erik Jeppesen
    • 1
    • 3
    • 4
  • Martin Søndergaard
    • 1
  • Torben L. Lauridsen
    • 1
  • Lone Liboriussen
    • 1
  • Jens-Christian Svenning
    • 2
  1. 1.Freshwater Ecology Group, Department of BioscienceAarhus UniversitySilkeborgDenmark
  2. 2.Ecoinformatics and Biodiversity Group, Department of BioscienceAarhus UniversityAarhusDenmark
  3. 3.Greenland Climate Research CentreGreenland Institute of Natural ResourcesNuukGreenland
  4. 4.Sino-Danish Centre for Education and Research (SDC)BeijingChina

Personalised recommendations