Skip to main content

Advertisement

SpringerLink
Log in

Effects of temperature fluctuation on the development of cyanobacterial dominance in spring: implication of future climate change

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

Abstract

Global warming is predicted to increase the intensity and frequency of short-term temperature fluctuation. However, the effect of temperature fluctuation on phytoplankton is rarely considered. We analyzed the effect of fluctuating temperature on cyanobacterial dominance and blooms in spring (March–May) with long-term data analyses, laboratory simulation, and field observation. Our results showed that the magnitude of air temperature fluctuation in spring has increased in Lake Taihu over the past 58 years (1956–2013) and was negatively correlated with cyanobacterial blooms onset time (1987–2013). Air temperature fluctuation was one of the predictors of the best model for the variability in the bloom size in spring (2000–2011). The results from the field observation (2009–2013) also indicated that there was a positive correlation between diel air temperature difference and the ratio of cyanobacteria to total algae. Laboratory experiments suggested that water temperature fluctuation slowed the growth rates of Chlorella pyrenoidosa and Cyclotella meneghiniana but not Microcystis aeruginosa, which confirmed our findings of field observation and long-term data analysis. Therefore, the increased temperature fluctuation under global warming may promote cyanobacterial dominance. Our findings provide further understanding of inter-annual difference of cyanobacterial blooms onset time in the warming world.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abalde, J., L. Betancourt, E. Torres, A. Cid & C. Barwell, 1998. Purification and characterization of phycocyanin from the marine cyanobacterium Synechococcus sp. IO9201. Plant Science 136: 109–120.

    Article  CAS  Google Scholar 

  • Amano, Y., Y. Sakai, T. Sekiya, K. Takeya, K. Taki & M. Machida, 2010. Effect of phosphorus fluctuation caused by river water dilution in eutrophic lake on competition between blue-green alga Microcystis aeruginosa and diatom Cyclotella sp. Journal of Environmental Sciences 22: 1666–1673.

    Article  CAS  Google Scholar 

  • APHA, 1985. Standard Methods for the Examination of Water and Wastewater. APHA-AWWA-WPCF, Washington, U. S. A.

  • Bäuerle, E., D. Ollinger & J. Ilmberger, 1998. Some meteorological hydrological and hydrodynamical aspects of upper Lake Constance. Archiv für Hydrobiologie Special Issues Advanced Limnology 53: 31–83.

    Google Scholar 

  • Benincà, E., V. Dakos, E. H. Van Nes, J. Huisman & M. Scheffer, 2011. Resonance of plankton communities with temperature fluctuations. The American Naturalist 178: E85–E95.

    Article  PubMed  Google Scholar 

  • Cao, H., Y. Tao, F. Kong & Z. Yang, 2008. Relationship between temperature and cyanobacterial recruitment from sediments in laboratory and field studies. Journal of Freshwater Ecology 23: 405–412.

    Article  CAS  Google Scholar 

  • Carpenter, S. R., S. G. Fisher, N. B. Grimm & J. F. Kitchell, 1992. Global change and freshwater ecosystems. Annual Review of Ecology and Systematics 23: 119–139.

    Article  Google Scholar 

  • Chen, Y. W., B. Q. Qin, K. Teubner & M. T. Dokulil, 2003. Long-term dynamics of phytoplankton assemblages: Microcystis-domination in Lake Taihu, a large shallow lake in China. Journal of Plankton Research 25: 445–453.

    Article  Google Scholar 

  • Deng, J., B. Qin, H. W. Paerl, Y. Zhang, J. Ma & Y. Chen, 2014a. Earlier and warmer springs increase cyanobacterial (Microcystis spp.) blooms in subtropical Lake Taihu, China. Freshwater Biology 59: 1076–1085.

    Article  Google Scholar 

  • Deng, J., B. Qin, H. W. Paerl, Y. Zhang, P. Wu, J. Ma & Y. Chen, 2014b. Effects of nutrients, temperature and their interactions on spring phytoplankton community succession in Lake Taihu, China. PLoS One 9: e113960. doi:10.1371/journal.pone.0113960.

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Duan, H., R. Ma, X. Xu, F. Kong, S. Zhang, W. Kong, J. Hao & L. Shang, 2009. Two-decade reconstruction of algal blooms in China’s Lake Taihu. Environmental Science & Technology 43: 3522–3528.

    Article  CAS  Google Scholar 

  • Elliott, J. A. & L. May, 2008. The sensitivity of phytoplankton in Loch Leven (UK) to changes in nutrient load and water temperature. Freshwater Biology 53: 32–41.

    CAS  Google Scholar 

  • Falkowski, P. G. & J. A. Raven, 1997. Aquatic Photosynthesis. Blackwell Science, Malden, MA.

    Google Scholar 

  • Fotheringham, A. S., C. Brunsdon & M. Charlton, 2002. Geographically Weighted Regression: the Analysis of Spatially Varying Relationships. Wiley, Chichester.

    Google Scholar 

  • Gao, Y., J. C. Cornwell, D. K. Stoecker & M. S. Owens, 2012. Effects of cyanobacterial-driven pH increases on sediment nutrient fluxes and coupled nitrification-denitrification in a shallow fresh water estuary. Biogeosciences 9: 2697–2710.

    Article  CAS  Google Scholar 

  • Geller, W., R. Berberovic, U. Gaedke, H. Muller & H. R. Pauli, 1991. Relations among the components of autotrophic and heterotrophic plankton during the seasonal cycle 1987 in Lake Constance. Verhandlungen des Internationalen Verein Limnologie 24: 831–836.

    Google Scholar 

  • Houghton, J., 2005. Global warming. Reports on Progress in Physics 68: 1343–1403.

    Article  Google Scholar 

  • Hu, C. M., Z. Lee, R. H. Ma, K. Yu, D. Li & S. L. Shang, 2010. Moderate resolution imaging spectroradiometer (MODIS) observations of cyanobacteria blooms in Taihu Lake, China. Journal of Geophysical Research 115: C04002.

  • Huber, V., C. Wagner, D. Gerten & R. Adrian, 2012. To bloom or not to bloom: contrasting responses of cyanobacteria to recent heat waves explained by critical thresholds of abiotic drivers. Oecologia 169: 245–256.

    Article  PubMed  Google Scholar 

  • Jeppesen, E., M. Meerhoff, B. Jacobsen, R. Hansen, M. Søndergaard, J. Jensen, T. Lauridsen, N. Mazzeo & C. Branco, 2007. Restoration of shallow lakes by nutrient control and biomanipulation – the successful strategy varies with lake size and climate. Hydrobiologia 581: 269–285.

    Article  CAS  Google Scholar 

  • Jöhnk, 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 

  • Ke, Z. X., P. Xie & L. G. Guo, 2008. Controlling factors of spring–summer phytoplankton succession in Lake Taihu (Meiliang Bay, China). Hydrobiologia 607: 41–49.

    Article  CAS  Google Scholar 

  • Latour, D., O. Sabido, M. J. Salencon & H. Giraudet, 2004. Dynamics and metabolic activity of the benthic cyanobacterium Microcystis aeruginosa in the Grangent reservoir (France). Journal of Plankton Research 26: 719–726.

    Article  CAS  Google Scholar 

  • Lürling, M., 2006. Effects of a surfactant (FFD-6) on Scenedesmus morphology and growth under different nutrient conditions. Chemosphere 62: 1351–1358.

    Article  PubMed  Google Scholar 

  • Lürling, M., F. Eshetu, E. J. Faassen, S. Kosten & V. L. M. Huszar, 2012. Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshwater Biology 58: 552–559.

    Article  Google Scholar 

  • McKee, D., D. Atkinson, S. E. Collings, J. W. Eaton, A. Gill, I. Harvey, K. Hatton, T. Heyes, D. Wilson & B. Moss, 2003. Response of freshwater microcosm communities to nutrients, fish, and elevated temperature during winter and summer. Limnology and Oceanography 48: 707–722.

    Article  Google Scholar 

  • McQueen, D. J. & D. R. S. Lean, 1987. Influence of water temperature and nitrogen to phosphorus ratios on the dominance of blue-green algae in Lake St. George, Ontario. Canadian Journal of Fisheries and Aquatic Sciences 44: 598–604.

    Article  CAS  Google Scholar 

  • Meis, S., S. J. Thackeray & I. D. Jones, 2009. Effects of recent climate change on phytoplankton phenology in a temperate lake. Freshwater Biology 54: 1888–1898.

    Article  CAS  Google Scholar 

  • Montagnes, D. & T. Weisse, 2000. Fluctuating temperatures affect growth and production rates of planktonic ciliates. Aquatic Microbial Ecology 21: 97–102.

    Article  Google Scholar 

  • Mooij, W., S. Hülsmann, L. De Senerpont Domis, B. Nolet, P. Bodelier, P. Boers, L. Pires, H. Gons, B. Ibelings, R. Noordhuis, R. Portielje, K. Wolfstein & E. Lammens, 2005. The impact of climate change on lakes in the Netherlands: a review. Aquatic Ecology 39: 381–400.

    Article  CAS  Google Scholar 

  • Myers, R. H., 1990. Classical and Modern Regression with Applications. PWS and Kent Publishing Company, Boston.

    Google Scholar 

  • Norusis, M., 2008. SPSS 16.0 Statistical Procedures Companion. Prentice Hall Press.

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

    Article  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. & J. Huisman, 2009. Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environmental Microbiology Reports 1: 27–37.

    Article  CAS  PubMed  Google Scholar 

  • Paul, V. J., 2008. Global warming and cyanobacterial harmful algal blooms. In Hudnell, H. K. (ed) Cyanobacterial Harmful Algal Blooms: State of the Science and Research Needs, Vol. 619. Advances in Experimental Medicine and Biology. Springer, New York: 239–257.

  • Qin, B. Q., W. P. Hu & W. M. Chen, 2004. Process and Mechanism of Environmental Changes of the Taihu Lake. Science Press, Beijing (In Chinese).

  • Qin, B., P. Xu, Q. Wu, L. Luo & Y. Zhang, 2007. Environmental issues of Lake Taihu, China. In Qin, B., Z. Liu & K. Havens (eds) Eutrophication of Shallow Lakes with Special Reference to Lake Taihu, China. Developments in Hydrobiology, Vol. 194. Springer, Dordrecht: 3–14.

  • Rangel, T. F., J. A. F. Diniz-Filho & L. M. Bini, 2010. SAM: a comprehensive application for Spatial Analysis in Macroecology. Ecography 33: 46–50.

    Article  Google Scholar 

  • Recknagel, F., J. Bobbin, P. Whigham & H. Wilson, 2002. Comparative application of artificial neural networks and genetic algorithms for multivariate time-series modelling of algal blooms in freshwater lakes. Journal of Hydroinformatics 4: 125–133.

    Google Scholar 

  • Reynolds, C. S., 1984. Phytoplankton periodicity: the interactions of form, function and environmental variability. Freshwater Biology 14: 111–142.

    Article  Google Scholar 

  • Reynolds, C. S., 2006. Ecology of Phytoplankton (Ecology, Biodiversity and Conservation). Cambridge University Press, Cambridge.

    Google Scholar 

  • Rippka, R., J. Deruelles, J. B. Waterbury, M. Herdman & R. Y. Stanier, 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Journal of General Microbiology 111: 1–61.

    Article  Google Scholar 

  • Robarts, R. D. & T. Zohary, 1987. Temperature effects on photosynthetic capacity, respiration, and growth rates of bloom-forming cyanobacteria. New Zealand Journal of Marine and Freshwater Research 21: 391–399.

    Article  CAS  Google Scholar 

  • Stanier, R., R. Kunisawa, M. Mandel & G. Cohen-Bazire, 1971. Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriological Reviews 35: 171.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Valderrama, J., 1981. The simultaneous analysis of total nitrogen and total phosphorus in natural waters. Marine Chemistry 10: 109–122.

    Article  CAS  Google Scholar 

  • Wagner, C. & R. Adrian, 2009. Cyanobacteria dominance: quantifying the effects of climate change. Limnology and Oceanography 54: 2460–2468.

    Article  Google Scholar 

  • Yan, R., F. Kong & X. Han, 2004. Analysis of the recruitment of the winter survival algae on the sediments of Lake Taihu by fluorometry. Journal of Lake Science 16: 163–168. (In Chinese).

    Article  CAS  Google Scholar 

  • Zhang, M., X. Shi, Y. Yu & F. Kong, 2011. The acclimative changes in photochemistry after colony formation of the cyanobacterial Microcystis aeruginosa. Journal of Phycology 47: 524–532.

    Article  Google Scholar 

  • Zhang, M., H. Duan, X. Shi, Y. Yu & F. Kong, 2012a. Contributions of meteorology to the phenology of cyanobacterial blooms: implications for future climate change. Water Research 46: 442–452.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, M., Y. Yu, Z. Yang & F. Kong, 2012b. Photochemical responses of phytoplankton to rapid increasing-temperature process. Phycological Research 60: 199–207.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Hongtao Duan for the assistance in achieving the data sets of cyanobacterial blooms onset time and area. This work was supported by grants from the National Natural Science Foundation of China (31200353, 31470520, 31200296, 310702420), the project of water pollution control and treatment in Lake Taihu (JSZC-G2013-257), and the frontier project of Nanjing Institute of Geography and Limnology, CAS (NIGLAS2012135010). We also thank the two anonymous reviewers for their useful comments and constructive suggestions.

Author information

Authors and Affiliations

  1. State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 73 East Beijing Road, Nanjing, 210008, China

    Min Zhang, Yang Yu, Zhen Yang, Xiaoli Shi & Fanxiang Kong

  2. Jiangsu Province Key Laboratory for Biodiversity and Biotechnology, School of Biological Sciences, Nanjing Normal University, Wenyuan Road, Nanjing, 210046, China

    Baoli Qin

Authors
  1. Min Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Baoli Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yang Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhen Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaoli Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fanxiang Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Min Zhang or Fanxiang Kong.

Additional information

Handling editor: Zhengwen Liu

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, M., Qin, B., Yu, Y. et al. Effects of temperature fluctuation on the development of cyanobacterial dominance in spring: implication of future climate change. Hydrobiologia 763, 135–146 (2016). https://doi.org/10.1007/s10750-015-2368-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-015-2368-0

Keywords

Search

Navigation