Skip to main content
Log in

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

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

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.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Dokulil, M. T., 2014. Impact of climate warming on European inland waters. Inland Waters 4: 27–40.

    Article  Google Scholar 

  • Dokulil, M. T. & K. Teubner, 2012. Deep living Planktothrix rubescens modulated by environmental constraints and climate forcing. Hydrobiologia 698: 29–46.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hirsch, R. M. & J. R. Slack, 1984. A nonparametric trend test for seasonal data with serial dependence. Water Resources Research 20: 727–732.

    Article  Google Scholar 

  • Idso, S. B., 1973. Concept of lake stability. Limnology and Oceanography 18: 681–683.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Paerl, H. W. & J. Huisman, 2008. Climate – blooms like it hot. Science 320: 57–58.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Schmidt, W., 1928. Über die Temperatur- und Stabilitätsverhältnisse von Seen. Geografiska Annaler 10: 145–177.

    Article  Google Scholar 

  • Sen, P. R., 1968. Estimates of the regression coefficient based on Kendall’s tau. Journal of the American Statistical Association 63: 1379–1389.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Winder, M. & D. E. Schindler, 2004. Climatic effects on the phenology of lake processes. Global Change Biology 10: 1844–1856.

    Article  Google Scholar 

  • Winder, M. & U. Sommer, 2012. Phytoplankton response to a changing climate. Hydrobiologia 698: 5–16.

    Article  Google Scholar 

  • Wuest, A. & A. Lorke, 2003. Small-scale hydrodynamics in lakes. Annual Review of Fluid Mechanics 35: 373–412.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas Posch.

Ethics declarations

Conflicts of interest

All authors have declared no conflicts of interest.

Additional information

Handling editor: Diego Fontaneto

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 866 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yankova, Y., Villiger, J., Pernthaler, J. et al. Prolongation, deepening and warming of the metalimnion change habitat conditions of the harmful filamentous cyanobacterium Planktothrix rubescens in a prealpine lake. Hydrobiologia 776, 125–138 (2016). https://doi.org/10.1007/s10750-016-2745-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-016-2745-3

Keywords

Navigation