Harmful filamentous cyanobacteria favoured by reduced water turnover with lake warming

Abstract

Anthropogenic-induced changes in nutrient ratios have increased the susceptibility of large temperate lakes to several effects of rising air temperatures and the resulting heating of water bodies1. First, warming leads to stronger thermal stratification, thus impeding natural complete water turnover (holomixis), which compensates for oxygen deficits in the deep zones2,3. Second, increased water temperatures and nutrient concentrations can directly favour the growth of harmful algae4,5,6. Thus, lake-restoration programmes have focused on reducing nutrients to limit toxic algal blooms7. Here we present evidence that the ubiquitous8,9,10 harmful cyanobacterium Planktothrix rubescens has become the dominant species in a large lake during the past four decades, although the phosphorus content of the ecosystem decreased fivefold. However, the nitrogen input was not diminished concomitantly, favouring this non-N2-fixing cyanobacterium owing to increased N:P ratios10. P. rubescens contains gas vesicles that allow for buoyancy to accumulate within the depth of optimal irradiance11. As the toxic cyanobacterium has low consumption by predators12, water turnover represents the main mechanism of seasonal population control. Thus, unidirectional lake-restoration measures13 in parallel with recurrent absence of holomixis owing to lake warming may lead to similar undesired effects that have formerly emerged from fertilization.

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Figure 1: Trends in whole-lake content of nutrients and phytoplankton in Lake Zurich.
Figure 2: Seasonality of P. rubescens and its spatial distribution.
Figure 3: Context of rising air temperatures with thermal stratification, total-lake O2 content and biomass of P. rubescens.
Figure 4: Relationship between mixing depth, lake warming and growth of P. rubescens.

References

  1. 1

    Shimoda, Y. et al. Our current understanding of lake ecosystem response to climate change: What have we really learned from the north temperate deep lakes? J. Great Lakes Res. 37, 173–193 (2011).

    CAS  Article  Google Scholar 

  2. 2

    Foley, B., Jones, I. D., Maberly, S. C. & Rippey, B. Long-term changes in oxygen depletion in a small temperate lake: Effects of climate change and eutrophication. Freshwat. Biol. 57, 278–289 (2012).

    CAS  Article  Google Scholar 

  3. 3

    Straile, D., Jöhnk, K. & Rossknecht, H. Complex effects of winter warming on the physicochemical characteristics of a deep lake. Limnol. Oceanogr. 48, 1432–1438 (2003).

    CAS  Article  Google Scholar 

  4. 4

    O’Neil, J. M., Davis, T. W., Burford, M. A. & Gobler, C. J. The rise of harmful cyanobacteria blooms: The potential roles of eutrophication and climate change. Harmful Algae 14, 313–334 (2012).

    Article  Google Scholar 

  5. 5

    Paerl, H. W. & Huisman, J. Climate change: A catalyst for global expansion of harmful cyanobacterial blooms. Environ. Microbiol. Rep. 1, 27–37 (2009).

    CAS  Article  Google Scholar 

  6. 6

    Jöhnk, K. D. et al. Summer heatwaves promote blooms of harmful cyanobacteria. Glob. Change Biol. 14, 495–512 (2008).

    Article  Google Scholar 

  7. 7

    Paerl, H. W., Hall, N. S. & Calandrino, E. S. Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Sci. Tot. Environ. 409, 1739–1745 (2011).

    CAS  Article  Google Scholar 

  8. 8

    Ernst, B., Hoeger, S. J., O’Brien, E. & Dietrich, D. R. Abundance and toxicity of Planktothrix rubescens in the pre-alpine Lake Ammersee, Germany. Harmful Algae 8, 329–342 (2009).

    CAS  Article  Google Scholar 

  9. 9

    Kurmayer, R., Schober, E., Tonk, L., Visser, P. M. & Christiansen, G. Spatial divergence in the proportions of genes encoding toxic peptide synthesis among populations of the cyanobacterium Planktothrix in European lakes. FEMS Microbiol. Lett. 317, 127–137 (2011).

    CAS  Article  Google Scholar 

  10. 10

    Jacquet, S. et al. The proliferation of the toxic cyanobacterium Planktothrix rubescens following restoration of the largest natural french lake (Lac du Bourget). Harmful Algae 4, 651–672 (2005).

    Article  Google Scholar 

  11. 11

    Walsby, A. E., Ng, G., Dunn, C. & Davis, A. P. Comparison of the depth where Planktothrix rubescens stratifies and the depth where the daily insolation supports its neutral buoyancy. New Phytol. 162, 133–145 (2004).

    Article  Google Scholar 

  12. 12

    Kurmayer, R. & Jüttner, F. Strategies for the co-existence of zooplankton with the toxic cyanobacterium Planktothrix rubescens in Lake Zürich. J. Plankt. Res. 21, 659–683 (1999).

    Article  Google Scholar 

  13. 13

    Lewis, W. M., Wurtsbaugh, W. A. & Paerl, H. W. Rationale for control of anthropogenic nitrogen and phosphorus to reduce eutrophication of inland waters. Environ. Sci. Technol. 45, 10300–10305 (2011).

    CAS  Article  Google Scholar 

  14. 14

    Rippey, B. & McSorley, C. Oxygen depletion in lake hypolimnia. Limnol. Oceanogr. 54, 905–916 (2009).

    CAS  Article  Google Scholar 

  15. 15

    Wagner, C. & Adrian, R. Cyanobacteria dominance: Quantifying the effects of climate change. Limnol. Oceanogr. 54, 2460–2468 (2009).

    Article  Google Scholar 

  16. 16

    Winder, M., Reuter, E. R. & Schladow, S. W. Lake warming favours small-sized planktonic diatom species. Proc. R. Soc. B 276, 427–435 (2009).

    Article  Google Scholar 

  17. 17

    Bálint, M. et al. Cryptic biodiversity loss linked to global climate change. Nature Clim. Change 1, 313–318 (2011).

    Article  Google Scholar 

  18. 18

    Dokulil, M. T. & Teubner, K. Cyanobacterial dominance in lakes. Hydrobiologia 438, 1–12 (2000).

    CAS  Article  Google Scholar 

  19. 19

    Walsby, A. E. & Jüttner, F. The uptake of amino acids by the cyanobacterium Planktothrix rubescens is stimulated by light at low irradiances. Microb. Ecol. 58, 14–22 (2006).

    CAS  Article  Google Scholar 

  20. 20

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

    CAS  Article  Google Scholar 

  21. 21

    Salcher, M. M., Pernthaler, J., Frater, N. & Posch, T. Vertical and longitudinal distribution patterns of different bacterioplankton populations in a canyon-shaped, deep prealpine lake. Limnol. Oceanogr. 56, 2027–2039 (2011).

    CAS  Article  Google Scholar 

  22. 22

    Campos, A. & Vasconcelos, V. Molecular mechanisms of microcystin toxicity in animal cells. Int. J. Mol. Sci. 11, 268–287 (2010).

    CAS  Article  Google Scholar 

  23. 23

    Hoeger, S. J., Schmid, D., Blom, J. F., Ernst, B. & Dietrich, D. R. Analytical and functional characterization of microcystins [Asp3]MC-RR and [Asp3,Dhb7]MC-RR: Consequences for risk assessment? Environ. Sci. Technol. 41, 2609–2616 (2007).

    CAS  Article  Google Scholar 

  24. 24

    Walsby, A. E. & Schanz, F. 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 (2002).

    Article  Google Scholar 

  25. 25

    Holland, D. P. & Walsby, A. E. Viability of the cyanobacterium Planktothrix rubescens in the cold and dark, related to over-winter survival and summer recruitment in Lake Zurich. Eur. J. Phycol. 43, 179–184 (2008).

    Article  Google Scholar 

  26. 26

    Zotina, T., Köster, O. & Jüttner, F. Photoheterotrophy and light-dependent uptake of organic and organic nitrogenous compounds by Planktothrix rubescens under low irradiance. Freshwat. Biol. 48, 1859–1872 (2003).

    CAS  Article  Google Scholar 

  27. 27

    Bright, D. I. & Walsby, A. E. The relationship between critical pressure and width of gas vesicles in isolates of Planktothrix rubescens from Lake Zürich. Microbiol. 145, 2769–2775 (1999).

    CAS  Article  Google Scholar 

  28. 28

    Walsby, A. E., Avery, A. & Schanz, F. The critical pressure of gas vesicles in Planktothrix rubescens in relation to the depth of winter mixing in Lake Zürich, Switzerland. J. Plankt. Res. 20, 1357–1375 (1998).

    Article  Google Scholar 

  29. 29

    Bossard, P. et al. Limnological description of the lakes Zürich, Lucerne, and Cadagno. Aquat. Sci. 63, 225–249 (2001).

    CAS  Article  Google Scholar 

  30. 30

    Begert, M., Schlegel, T. & Kirchhofer, W. Homogeneous temperature and precipitation series of Switzerland from 1864 to 2000. Int. J. Climatol. 25, 65–80 (2005).

    Article  Google Scholar 

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Acknowledgements

The long-term monitoring was financially supported by the WVZ and the Amt für Abfall, Wasser, Energie und Luft. Meteorological data were obtained from the Federal Office of Meteorology and Climatology (MeteoSwiss). The evaluation of the data set was financially supported by projects of the Swiss National Fund (31003A_138473; CR22I2_130023/1). We thank M. E. Garneau and R. Psenner for comments on the manuscript.

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Interpolation of depth profiles and calculations of whole-lake contents were carried out by T.P. The long-term data set was provided by O.K., as representative of the WVZ. Statistical analyses were carried out by M.M.S. All authors discussed the results and created the design of the figures. T.P. and J.P. prepared the manuscript, which was edited by M.M.S. and O.K.

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Correspondence to Thomas Posch.

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Posch, T., Köster, O., Salcher, M. et al. Harmful filamentous cyanobacteria favoured by reduced water turnover with lake warming. Nature Clim Change 2, 809–813 (2012). https://doi.org/10.1038/nclimate1581

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