Advertisement

Hydrobiologia

, Volume 776, Issue 1, pp 125–138 | Cite as

Prolongation, deepening and warming of the metalimnion change habitat conditions of the harmful filamentous cyanobacterium Planktothrix rubescens in a prealpine lake

  • Yana Yankova
  • Jörg Villiger
  • Jakob Pernthaler
  • Ferdinand Schanz
  • Thomas Posch
Primary Research Paper

Abstract

The most prominent responses of Lake Zurich to climate warming include the increase of surface water temperatures, a reduced depth of spring mixing, and the persistent thriving of the harmful cyanobacterium Planktothrix rubescens, a low-light adapted species concentrating in the metalimnion during summer. To study changes of its habitat, we assessed the spatio-temporal metalimnetic boundaries by applying low-pass filtering and binary thresholding to temperature profiles of long-term data (1978–2013, weekly measurements). Due to increasing temperatures over the last 3.5 decades, the onset and duration of metalimnion formation changed significantly (stratification increased by 33 days). Moreover, the upper metalimnetic boundary has undergone a significant drawdown of 2.3 m, accounting for an overall decrease in metalimnion thickness. Being the most abundant species in this zone, P. rubescens was not negatively affected by altered temporal or spatial stratification patterns during its phase of net growth (July–September), as the zone of its optimal light-dependent buoyancy was still located within the metalimnion. The biomass of P. rubescens in August was even significantly related to increasing temperatures. Nevertheless, a further depression of the metalimnetic top boundary may eventually restrict P. rubescens by forcing it into layers of unfavourable light conditions or into the turbulent epilimnetic zone.

Keywords

Lake warming Lake Zurich Long-term data Metalimnion Neutral buoyancy Planktothrix rubescens 

Notes

Acknowledgments

We would like to thank Eugen Loher and everyone who helped sampling over the years. The Water Supply Zurich is also acknowledged for providing long-term data on P. rubescens. We thank two anonymous reviewers for their constructive comments. This study is funded by the University Research Priority Program (URPP) ‘Global Change and Biodiversity’ of the University of Zurich and by the Swiss National Fund (SNF 310030E-160603).

Compliance with ethical standards

Conflicts of interest

All authors have declared no conflicts of interest.

Supplementary material

10750_2016_2745_MOESM1_ESM.pdf (866 kb)
Supplementary material 1 (PDF 866 kb)

References

  1. Austin, J. A. & S. M. Colman, 2007. Lake Superior summer water temperatures are increasing more rapidly than regional air temperatures: a positive ice-albedo feedback. Geophysical Research Letters 34: L06604.CrossRefGoogle Scholar
  2. Bleiker, W. & F. Schanz, 1997. Light climate as the key factor controlling the spring dynamics of phytoplankton in Lake Zurich. Aquatic Sciences 59: 135–157.CrossRefGoogle Scholar
  3. Blenckner, T., R. Adrian, D. M. Livingstone, E. Jennings, G. A. Weyhenmeyer, D. G. George, T. Jankowski, M. Jarvinen, C. N. Aonghusa, T. Nõges, D. Straile & K. Teubner, 2007. Large-scale climatic signatures in lakes across Europe: a meta-analysis. Global Change Biology 13: 1314–1326.CrossRefGoogle Scholar
  4. Blom, J. F., H. I. Baumann, G. A. Codd & F. Jüttner, 2006. Sensitivity and adaptation of aquatic organisms to oscillapeptin J and D-Asp(3),(E)-Dhb(7) microcystin-RR. Archiv Für Hydrobiologie 167: 547–559.CrossRefGoogle Scholar
  5. Bossard, P., S. Gammeter, C. Lehmann, F. Schanz, R. Bachofen, H. R. Bürgi, D. Steiner & U. Zimmermann, 2001. Limnological description of the Lakes Zurich, Lucerne, and Cadagno. Aquatic Sciences 63: 225–249.CrossRefGoogle Scholar
  6. Davis, P. A. & A. E. Walsby, 2002. Comparison of measured growth rates with those calculated from rates of photosynthesis in Planktothrix spp. isolated from Blelham Tarn, English Lake District. New Phytologist 156: 225–239.CrossRefGoogle Scholar
  7. Dokulil, M. T., 2014. Impact of climate warming on European inland waters. Inland Waters 4: 27–40.CrossRefGoogle Scholar
  8. Dokulil, M. T. & K. Teubner, 2012. Deep living Planktothrix rubescens modulated by environmental constraints and climate forcing. Hydrobiologia 698: 29–46.CrossRefGoogle Scholar
  9. Dokulil, M. T., A. Jagsch, G. D. George, O. Anneville, T. Jankowski, B. Wahl, B. Lenhart, T. Blenckner & K. Teubner, 2006. Twenty years of spatially coherent deepwater warming in lakes across Europe related to the North Atlantic Oscillation. Limnology and Oceanography 51: 2787–2793.CrossRefGoogle Scholar
  10. Dokulil, M. T., K. Teubner, A. Jagsch, U. Nickus, R. Adrian, D. Straile, T. Jankowski, A. Herzig & J. Padisak, 2010. The impact of climate change on lakes in Central Europe. In George, G. (ed.), Impact of Climate Change on European Lakes. Aquatic Ecology Series, Springer, Dordrecht: 387–409.Google Scholar
  11. Ernst, B., B. Hitzfeld & D. Dietrich, 2001. Presence of Planktothrix sp. and cyanobacterial toxins in Lake Ammersee, Germany and their impact on whitefish (Coregonus lavaretus L.). Environmental Toxicology 16: 483–488.CrossRefPubMedGoogle Scholar
  12. Gammeter, S. & U. Zimmermann, 2001. Changes in phytoplankton productivity and composition during reoligotrophication in two Swiss lakes. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 27: 2190–2193.Google Scholar
  13. Garneau, M.-È., T. Posch, G. Hitz, F. Pomerleau, C. Pradalier, R. Siegwart & J. Pernthaler, 2013. Short-term displacement of Planktothrix rubescens (cyanobacteria) in a pre-alpine lake observed using an autonomous sampling platform. Limnology and Oceanography 58: 1892–1906.CrossRefGoogle Scholar
  14. Gauthier, J., Y. T. Prairie & B. E. Beisner, 2014. Thermocline deepening and mixing alter zooplankton phenology, biomass and body size in a whole-lake experiment. Freshwater Biology 59: 998–1011.CrossRefGoogle Scholar
  15. Guilizzoni, P., S. N. Levine, M. Manca, A. Marchetto, A. Lami, W. Ambrosetti, A. Brauer, S. Gerli, E. A. Carrara, A. Rolla, L. Guzzella & D. A. L. Vignati, 2012. Ecological effects of multiple stressors on a deep lake (Lago Maggiore, Italy) integrating neo and palaeolimnological approaches. Journal of Limnology 71: 1–22.CrossRefGoogle Scholar
  16. Hirsch, R. M. & J. R. Slack, 1984. A nonparametric trend test for seasonal data with serial dependence. Water Resources Research 20: 727–732.CrossRefGoogle Scholar
  17. Idso, S. B., 1973. Concept of lake stability. Limnology and Oceanography 18: 681–683.CrossRefGoogle Scholar
  18. Imboden, D. M. & A. Wüest, 1995. Mixing mechanisms in lakes. In Lerman, A., D. M. Imboden & J. R. Gat (eds), Physics and Chemistry of Lakes, 2nd ed. Springer, New York: 83–138.CrossRefGoogle Scholar
  19. Jacquet, S., O. Kerimoglu, F. Rimet, G. Paolini & O. Anneville, 2014. Cyanobacterial bloom termination: the disappearance of Planktothrix rubescens from Lake Bourget (France) after restoration. Freshwater Biology 59: 2472–2487.CrossRefGoogle Scholar
  20. Johnk, K. D., J. Huisman, J. Sharples, B. Sommeijer, P. M. Visser & J. M. Stroom, 2008. Summer heatwaves promote blooms of harmful cyanobacteria. Global Change Biology 14: 495–512.CrossRefGoogle Scholar
  21. Livingstone, D. M., 2003. Impact of secular climate change on the thermal structure of a large temperate central European lake. Climatic Change 57: 205–225.CrossRefGoogle Scholar
  22. North, R. P., R. L. North, D. M. Livingstone, O. Köster & R. Kipfer, 2014. Long-term changes in hypoxia and soluble reactive phosphorus in the hypolimnion of a large temperate lake: consequences of a climate regime shift. Global Change Biology 20: 811–823.CrossRefPubMedGoogle Scholar
  23. O’Neil, J. M., T. W. Davis, M. A. Burford & C. J. Gobler, 2012. The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14: 313–334.CrossRefGoogle Scholar
  24. Oberhaus, L., J. F. Briand, C. Leboulanger, S. Jacquet & J. F. Humbert, 2007. Comparative effects of the quality and quantity of light and temperature on the growth of Planktothrix agardhii and P. rubescens. Journal of Phycology 43: 1191–1199.CrossRefGoogle Scholar
  25. Paerl, H. W. & J. Huisman, 2008. Climate – blooms like it hot. Science 320: 57–58.CrossRefPubMedGoogle Scholar
  26. Paerl, H. W., N. S. Hall & E. S. Calandrino, 2011. Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Science of the Total Environment 409: 1739–1745.CrossRefPubMedGoogle Scholar
  27. Peeters, F., D. M. Livingstone, G. H. Goudsmit, R. Kipfer & R. Forster, 2002. Modeling 50 years of historical temperature profiles in a large central European lake. Limnology and Oceanography 47: 186–197.CrossRefGoogle Scholar
  28. Peeters, F., D. Straile, A. Lorke & D. M. Livingstone, 2007. Earlier onset of the spring phytoplankton bloom in lakes of the temperate zone in a warmer climate. Global Change Biology 13: 1898–1909.CrossRefGoogle Scholar
  29. Posch, T., O. Köster, M. M. Salcher & J. Pernthaler, 2012. Harmful filamentous cyanobacteria favoured by reduced water turnover with lake warming. Nature Climate Change 2: 809–813.CrossRefGoogle Scholar
  30. Rempfer, J., D. M. Livingstone, C. Blodau, R. Forster, P. Niederhauser & R. Kipfer, 2010. The effect of the exceptionally mild European winter of 2006–2007 on temperature and oxygen profiles in lakes in Switzerland: a foretaste of the future? Limnology and Oceanography 55: 2170–2180.CrossRefGoogle Scholar
  31. Salmaso, N., 2010. Long-term phytoplankton community changes in a deep subalpine lake: responses to nutrient availability and climatic fluctuations. Freshwater Biology 55: 825–846.CrossRefGoogle Scholar
  32. Salmaso, N., G. Morabito, R. Mosello, L. Garibaldi & M. Simona, 2003. A synoptic study of phytoplankton in the deep lakes south of the Alps (Lakes Garda, Iseo, Como, Lugano and Maggiore). Journal of Limnology 62: 207–227.CrossRefGoogle Scholar
  33. Schmidt, W., 1928. Über die Temperatur- und Stabilitätsverhältnisse von Seen. Geografiska Annaler 10: 145–177.CrossRefGoogle Scholar
  34. Sen, P. R., 1968. Estimates of the regression coefficient based on Kendall’s tau. Journal of the American Statistical Association 63: 1379–1389.CrossRefGoogle Scholar
  35. Shatwell, T., J. Kohler & A. Nicklisch, 2008. Warming promotes cold-adapted phytoplankton in temperate lakes and opens a loophole for Oscillatoriales in spring. Global Change Biology 14: 2194–2200.CrossRefGoogle Scholar
  36. Straile, D., K. Johnk & H. Rossknecht, 2003. Complex effects of winter warming on the physicochemical characteristics of a deep lake. Limnology and Oceanography 48: 1432–1438.CrossRefGoogle Scholar
  37. Sweers, H. E., 1976. Nomogram to estimate heat-exchange coefficient at air–water-interface as a function of wind speed and temperature – critical survey of some literature. Journal of Hydrology 30: 375–401.CrossRefGoogle Scholar
  38. Teubner, K., M. Tolotti, S. Greisberger, H. Morscheid, M. T. Dokulil & H. Morscheid, 2003. Steady state phytoplankton in a deep pre-alpine lake: species and pigments of epilimnetic versus metalimnetic assemblages. Hydrobiologia 502: 49–64.CrossRefGoogle Scholar
  39. Van den Wyngaert, S., M. M. Salcher, J. Pernthaler, M. Zeder & T. Posch, 2011. Quantitative dominance of seasonally persistent filamentous cyanobacteria (Planktothrix rubescens) in the microbial assemblages of a temperate lake. Limnology and Oceanography 56: 97–109.CrossRefGoogle Scholar
  40. von Storch, V., 1995. Misuses of statistical analysis in climate research. In von Storch, H. & A. Navarra (eds), Analysis of Climate Variability: Applications of Statistical Techniques. Springer, Berlin: 11–26.CrossRefGoogle Scholar
  41. Walsby, A. E. & F. Schanz, 2002. Light-dependent growth rate determines changes in the population of Planktothrix rubescens over the annual cycle in Lake Zurich, Switzerland. New Phytologist 154: 671–687.CrossRefGoogle Scholar
  42. Walsby, A. E., A. Avery & F. Schanz, 1998. The critical pressures of gas vesicles in Planktothrix rubescens in relation to the depth of winter mixing in Lake Zurich, Switzerland. Journal of Plankton Research 20: 1357–1375.CrossRefGoogle Scholar
  43. Walsby, A. E., Z. Dubinsky, J. C. Kromkamp, C. Lehmann & F. Schanz, 2001. The effects of diel changes in photosynthetic coefficients and depth of Planktothrix rubescens on the daily integral of photosynthesis in Lake Zurich. Aquatic Sciences 63: 326–349.CrossRefGoogle Scholar
  44. Walsby, A. E., G. Ng, C. Dunn & P. A. Davis, 2004. Comparison of the depth where Planktothrix rubescens stratifies and the depth where the daily insolation supports its neutral buoyancy. New Phytologist 162: 133–145.CrossRefGoogle Scholar
  45. Weyhenmeyer, G. A., R. Adrian, U. Gaedke, D. M. Livingstone & S. C. Maberly, 2002. Response of phytoplankton in European lakes to a change in the North Atlantic Oscillation. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 28: 1436–1439.Google Scholar
  46. Winder, M. & D. E. Schindler, 2004. Climatic effects on the phenology of lake processes. Global Change Biology 10: 1844–1856.CrossRefGoogle Scholar
  47. Winder, M. & U. Sommer, 2012. Phytoplankton response to a changing climate. Hydrobiologia 698: 5–16.CrossRefGoogle Scholar
  48. Wuest, A. & A. Lorke, 2003. Small-scale hydrodynamics in lakes. Annual Review of Fluid Mechanics 35: 373–412.CrossRefGoogle Scholar
  49. Yue, S., P. Pilon, B. Phinney & G. Cavadias, 2002. The influence of autocorrelation on the ability to detect trend in hydrological series. Hydrological Processes 16: 1807–1829.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Yana Yankova
    • 1
  • Jörg Villiger
    • 1
  • Jakob Pernthaler
    • 1
  • Ferdinand Schanz
    • 1
  • Thomas Posch
    • 1
  1. 1.Limnological Station, Department of Plant and Microbial BiologyUniversity of ZurichKilchbergSwitzerland

Personalised recommendations