Physical, biogeochemical, and meteorological factors responsible for interannual changes in cyanobacterial community composition and biovolume over two decades in a eutrophic lake

Abstract

This study used a 20-year dataset (1995–2014) to identify factors affecting cyanobacterial community composition (CCC) and abundance in a eutrophic lake. We hypothesized that differences in thermal structure, nutrients, and meteorology drive interannual variability in CCC and abundance. Cluster analysis differentiated dominant cyanobacteria into rare, low abundance, or sporadically occurring taxa. The bloom-forming genera were Microcystis and Aphanizomenon, accounting for ~ 70% of total cyanobacterial biovolume (BV) on average, whereas unusually high abundance of Planktothrix, Synechococcus, and Oscillatoria were clear outliers in three of the years. Variability in CCC was significantly correlated (P < 0.05, R > 0.3) with ice duration, Kjeldahl nitrogen (TKN), and spring nitrite + nitrate (NO2+3); ice duration and TKN were associated with the occurrence of primarily non-bloom-forming genera. Pairwise correlations tested linear, exponential, and polynomial correlates of absolute and relative total Cyanophyta, Microcystis, or Aphanizomenon BV. TKN, total nitrogen (TN) and phosphorus (TP), TN:TP ratio, Schmidt stability, and rainfall correlated with total Cyanophyta, Microcystis, and Aphanizomenon BV, whereas ice cover, NO2+3, and TKN correlated with relative Microcystis and Aphanizomenon BV. Despite increasing TN:TP ratio over two decades, cyanobacterial abundance had not changed significantly. These data suggest differing responses of cyanobacterial genera to important environmental factors over two decades.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Adrian, R., N. Walz, T. Hintze, S. Hoeg & R. Rusche, 1999. Effects of ice duration on plankton succession during spring in a shallow polymictic lake. Freshwater Biology 41: 621–634.

    Article  Google Scholar 

  2. Azam, F., T. Fenchel, J. G. Field, J. S. Gray, L. A. Meyer-Reil & F. Thingstad, 1983. The ecological role of water-column microbes in the Sea. Marine Ecology 10: 257–263.

    Article  Google Scholar 

  3. Beversdorf, L. J., T. R. Miller & K. D. McMahon, 2013. The role of nitrogen fixation in cyanobacterial bloom toxicity in a temperate, eutrophic lake. PloS ONE 8: e56103.

    CAS  Article  Google Scholar 

  4. Beversdorf, L. J., T. R. Miller & K. D. McMahon, 2015. Long-term monitoring reveals carbon-nitrogen metabolism key to microcystin production in eutrophic lakes. Frontiers in Microbiology. https://doi.org/10.3389/fmicb.2015.00456.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Blodgett, D. L., N. L. Booth, T. C. Kunicki, J. L. Walker & R. J. Viger, 2011. Description and Testing of the Geo Data Portal: Data Integration Framework and Web Processing Services for Environmental Science Collaboration. U.S. Geological Survey, Reston.

    Google Scholar 

  6. Boussiba, S. & A. E. Richmond, 1980. C-phycocyanin as a storage protein in the blue-green alga Spirulina platensis. Archives of Microbiology 125: 143–147.

    CAS  Article  Google Scholar 

  7. Briand, J.-F., C. Leboulanger, J.-F. Humbert, C. Bernard & P. Dufour, 2004. Cylindrospermopsis Raciborskii (Cyanobacteria) invasion at mid-latitudes: selection, wide physiological tolerance, or global warming? Journal of Phycology 40: 231–238.

    Article  Google Scholar 

  8. Brookes, J. D., G. G. Ganf, D. Green & J. Whittington, 1999. The influence of light and nutrients on buoyancy, filament aggregation and flotation of Anabaena circinalis. Journal of Plankton Research 21: 327–341.

    Article  Google Scholar 

  9. Carpenter, S. R., E. G. Booth, C. J. Kucharik & R. C. Lathrop, 2015. Extreme daily loads: role in annual phosphorus input into a north temperate lake. Aquatic Sciences 77: 71–79.

    CAS  Article  Google Scholar 

  10. Dantas, Ê. W., A. N. Moura & M. D. C. Bittencourt-Oliveira, 2011. Cyanobacterial blooms in stratified and destratified eutrophic reservoirs in semi-arid region of Brazil. Annals of the Brazilian Academy of Sciences 83: 1327–1338.

    CAS  Article  Google Scholar 

  11. Dillon, P. J. & F. H. Rigler, 1974. The phosphorus-chlorophyll relationship in lakes. Limnology and Oceanography 19: 767–773.

    CAS  Article  Google Scholar 

  12. Dixon, P., 2009. VEGAN, a package of R functions for community ecology. Journal of Vegetation Science 14: 927–930.

    Article  Google Scholar 

  13. Dodds, W. K., W. W. Bouska, J. L. Eitzmann, T. J. Pilger, K. L. Pitts, A. J. Riley, J. T. Schloesser & D. J. Thornbrugh, 2009. Eutrophication of U.S. freshwaters: analysis of potential economic damages. Environmental Science & Technology 43: 12–19.

    CAS  Article  Google Scholar 

  14. Dolman, A. M., J. Rucker, F. R. Pick, J. Fastner, T. Rohrlack, U. Mischke & C. Wiedner, 2012. Cyanobacteria and cyanotoxins: the influence of nitrogen versus phosphorus. PloS ONE 7: e38757.

    CAS  Article  Google Scholar 

  15. Downing, J. A., S. B. Watson & E. McCauley, 2001. Predicting Cyanobacteria dominance in lakes. Canadian Journal of Fisheries and Aquatic Sciences 58: 1905–1908.

    Article  Google Scholar 

  16. Dugan, H. A., S. L. Bartlett, S. M. Burke, J. P. Doubek, F. E. Krivak-Tetley, N. K. Skaff, J. C. Summers, K. J. Farrell, I. M. McCullough, A. M. Morales-Williams, D. C. Roberts, Z. Ouyang, F. Scordo, P. C. Hanson & K. C. Weathers, 2017. Salting our freshwater lakes. Proceedings of the National Academy of Science of the United States of America. https://doi.org/10.1073/pnas.1620211114.

    Article  Google Scholar 

  17. Dupuis, A. P. & B. J. Hann, 2009. Warm spring and summer water temperatures in small eutrophic lakes of the Canadian prairies: potential implications for phytoplankton and zooplankton. Journal of Plankton Research 31: 489–502.

    CAS  Article  Google Scholar 

  18. Elliott, J. A., 2012. Is the future blue-green? A review of the current model predictions of how climate change could affect pelagic freshwater cyanobacteria. Water Research 46: 1364–1371.

    CAS  Article  Google Scholar 

  19. Elliott, J. A., S. J. Thackeray, C. Hungtinford & R. G. Jones, 2005. Combining a regional climate model with a phytoplankton community model to predict future changes in phytoplankton in lakes. Freshwater Biology 50: 1404–1411.

    Article  Google Scholar 

  20. Elliott, J. A., J. D. Jones & S. J. Thackeray, 2006. Testing the sensitivity of phytoplankton communities to changes in water temperature and nutrient load, in a temperate lake. Hydrobiologia 559: 401–411.

    CAS  Article  Google Scholar 

  21. Ganf, G. G. & R. L. Oliver, 1982. Vertical separation of light and available nutrients as a factor causing replacement of green algae by blue-green algae in the plankton of a stratified lake. Journal of Ecology 70: 829–844.

    Article  Google Scholar 

  22. Gehringer, M. M. & N. Wannicke, 2014. Climate change and regulation of hepatotoxin production in Cyanobacteria. FEMS Microbiology Ecology 88: 1–25.

    CAS  Article  Google Scholar 

  23. Giordanino, M. V., S. M. Strauch, V. E. Villafañe & E. W. Helbling, 2011. Influence of temperature and UVR on photosynthesis and morphology of four species of cyanobacteria. Journal of Photochemistry and Photobiology B 103: 68–77.

    CAS  Article  Google Scholar 

  24. Hill, M. O., J. Gauch & G. Hugh, 1980. Detrended correspondence analysis: an improved ordination technique. Vegetatio 42: 47–58.

    Article  Google Scholar 

  25. Hubbard, L., D. W. Kolpin, S. J. Kalkhoff & D. M. Robertson, 2011. Nutrient and sediment concentrations and corresponding loads during the historic June 2008 flooding in Eastern Iowa. Journal of Environmental Quality 40: 166–175.

    CAS  Article  Google Scholar 

  26. Johnston, B. R. & J. M. Jacoby, 2003. Cyanobacterial toxicity and migration in a mesotrophic lake in western Washington, USA. Hydrobiologia 495: 79–91.

    CAS  Article  Google Scholar 

  27. Jones, G. J. & W. Poplawski, 1998. Understanding and management of cyanobacterial blooms in sub-tropical reservoirs of Queensland, Australia. Water Science and Technology 37: 161–168.

    CAS  Article  Google Scholar 

  28. Kebede, E. & A. Belay, 1994. Species composition and phytoplankton biomass in a tropical African Lake (Lake Awassa, Ethiopia). Hydrobiologia 288: 13–32.

    CAS  Article  Google Scholar 

  29. Kendall, M. G., 1976. Chapter 3 Rank Correlation Methods, Vol. 4th. Edition, Griffin.

    Google Scholar 

  30. Konopka, A. & T. D. Brock, 1978. Effect of temperature on blue-green algae (Cyanobacteria) in Lake Mendota. Applied and Environmental Microbiology 36: 572–576.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Kosten, S., V. L. M. Huszar, E. Bécares, L. S. Costa, E. Donk, L.-A. Hansson, E. Jeppesen, C. Kruk, G. Lacerot, N. Mazzeo, L. Meester, B. Moss, M. Lürling, T. Nõges, S. Romo & M. Scheffer, 2012. Warmer climates boost cyanobacterial dominance in shallow lakes. Global Change Biology 18: 118–126.

    Article  Google Scholar 

  32. Lathrop, R. C., 2007. Perspectives on the eutrophication of the Yahara lakes. Lake and Reservoir Management 23: 345–365.

    Article  Google Scholar 

  33. Lathrop, R. C., S. R. Carpenter & D. M. Robertson, 1999. Summer water clarity responses to phosphorus, Daphnia grazing and internal mixing in Lake Mendota. Limnology and Oceanography 44: 137–146.

    Article  Google Scholar 

  34. Litchman, E. & C. A. Klausmeier, 2008. Trait-based community ecology of phytoplankton. Annual Review of Ecology, Evolution, and Systematics 39: 615–639.

    Article  Google Scholar 

  35. Magnuson, J. J., D. M. Robertson, B. J. Benson, R. H. Wynne, D. M. Livingstone, T. Arai, R. C. Assel, R. G. Barry, V. Card, E. Kuusisto, N. G. Granin, T. D. Prowse, K. M. Stewart & V. S. Vuglinski, 2000. Historical trends in lake and river ice cover in the Northern Hemisphere. Science 289: 1743–1746.

    CAS  Article  Google Scholar 

  36. McDonald, K. E. & J. T. Lehman, 2013. Dynamics of Aphanizomenon and Microcystis (cyanobacteria) during experimental manipulation of an urban impoundment. Lake and Reservoir Management 29: 103–115.

    CAS  Article  Google Scholar 

  37. McLeod, A. I., 2011. Kendall rank correlation and Mann-Kendall trend test. 2.2 edn, Computes the Kendall rank correlation and Mann-Kendall trend test. See documentation for use of block bootstrap when there is autocorrelation.

  38. Miller, T. R., L. Beversdorf, S. D. Chaston & K. D. McMahon, 2013. Spatiotemporal molecular analysis of cyanobacteria blooms reveals microcystis-aphanizomenon interactions. PloS ONE. https://doi.org/10.1371/journal.pone.0074933.g001.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Mitchell, K. E., D. Lohmann, P. R. Houser, E. F. Wood, J. C. Schaake, A. Robock, B. A. Cosgrove, J. Sheffield, Q. Duan, L. Luo, R. W. Higgins, R. T. Pinker, J. D. Tarpley, D. P. Lettenmaier, C. H. Marshall, J. K. Entin, M. Pan, W. Shi, V. Koren, J. Meng, B. H. Ramsay & A. A. Bailey, 2004. The multi-institution North American Land Data Assimilation System (NLDAS): Utilizing multiple GCIP products and partners in a continental distributed hydrological modeling system. Journal of Geophysical Research. https://doi.org/10.1029/2003JD003823.

    Article  Google Scholar 

  40. Murtagh, F. & P. Legendre, 2014. Ward’s hierarchical agglomerative clustering method: which algorithms implement ward’s criterion? Journal of Classification 31: 274–295.

    Article  Google Scholar 

  41. O’Reilly, C. M., S. Sharma, D. K. Gray, S. E. Hampton, J. S. Read, R. J. Rowley, P. Schneider, J. D. Lenters, P. B. McIntyre, B. M. Kraemer, G. A. Weyhenmeyer, D. Straile, B. Dong, R. Adrian, M. G. Allan, O. Anneville, L. Arvola, J. Austin, J. L. Bailey, J. S. Baron, J. D. Brookes, E. de Eyto, M. T. Dokulil, D. P. Hamilton, K. Havens, A. L. Hetherington, S. N. Higgins, S. Hook, L. R. Izmest’eva, K. D. Joehnk, K. Kangur, P. Kasprzak, M. Kumagi, E. Kuusisto, G. Leshkevich, D. M. Livingstone, S. MacIntyre, L. May, J. M. Melack, D. C. Mueller-Navarra, M. Naumenko, P. Noges, T. Noges, R. P. North, P.-D. Plisnier, A. Rigosi, A. Rimmer, D. E. Schindler, S. G. Schladow, M. Schmid, S. R. Schmidt, E. Silow, M. E. Soylu, K. Teubner, P. Verburg, A. Voutilainen, A. Watkinson, C. E. Williamson & G. Zhang, 2015. Rapid and highly variable warming of lake surface waters around the globe. Geophysical Research Letters 42: 10773–10781.

    Article  Google Scholar 

  42. 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 

  43. Oksanen, J., F. G. Blanchet, M. Friendly, R. Kindt, P. Legendre, D. McGlinn, P. R. Minchin, R. B. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, E. Szoecs & H. Wagner, 2016. Community Ecology Package. 2.4-1 edn, Ordination methods, diversity analysis and other functions for community and vegetation ecologists.

  44. Örnólfsdóttir, E. B., S. E. Lumsden & J. L. Pinckney, 2004. Phytoplankton community growth-rate response to nutrient pulses in a shallow turbid estuary, Galveston Bay, Texas. Journal of Plankton Research 26: 325–339.

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  46. Paerl, H. W. & T. G. Otten, 2016. Duelling ‘CyanoHABs’: unravelling the environmental drivers controlling dominance and succession among diazotrophic and non-N2-fixing harmful cyanobacteria. Environmental Microbiology 18: 316–324.

    CAS  Article  Google Scholar 

  47. Paerl, H. W. & V. J. Paul, 2012. Climate change: links to global expansion of harmful cyanobacteria. Water Research 46: 1349–1363.

    CAS  Article  Google Scholar 

  48. 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 

  49. Poole, H. H. & W. R. G. Atkins, 1929. Photo-electric Measurements of Submarine Illumination throughout the Year. Journal of the Marine Biological Association of the United Kingdom 16: 297–324.

    Article  Google Scholar 

  50. Porat, R., B. Teltsch, A. Perelman & Z. Dubinsky, 2001. Diel buoyancy changes by the Cyanobacterium Aphanizomenon ovalisporum from a Shallow Reservoir. Journal of Plankton Research 23: 753–763.

    Article  Google Scholar 

  51. R Development Core Team, 2013. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

    Google Scholar 

  52. Read, J. S., D. P. Hamilton, I. D. Jones, K. Muraoka, L. A. Winslow, R. Kroiss, C. H. Wu & E. Gaiser, 2011. Derivation of lake mixing and stratification indices from high-resolution lake buoy data. Environmental Modelling & Software 26: 1325–1336.

    Article  Google Scholar 

  53. Read, J. S., J. I. Walker, A. P. Appling, D. L. Blodgett, E. K. Read & L. A. Winslow, 2016. geoknife: reproducible web-processing of large gridded datasets. Ecography 39: 354–360.

    Article  Google Scholar 

  54. Reed, T. & S. R. Carpenter, 2002. Comparisons of P-yield, riparian buffer strips, and Land cover in six agricultural watersheds. Ecosystems 5: 568–577.

    CAS  Article  Google Scholar 

  55. Reichwaldt, E. S. & A. Ghadouani, 2012. Effects of rainfall patterns on toxic cyanobacterial blooms in a changing climate: between simplistic scenarios and complex dynamics. Water Research 46: 1372–1393.

    CAS  Article  Google Scholar 

  56. Robertson, D. M. & J. Imberger, 1994. Lake number, a quantitative indicator of mixing used to estimate changes in dissolved oxygen. Internationale Revue Der Gesamten Hydrobiologie 79: 159–176.

    CAS  Article  Google Scholar 

  57. Robertson, D. M., J. Imberger & K. Boland, 1990. Lake number: a quantitative indicator of mixing to be used in water quality management. Water: Journal of the Australian Water and Wastewater Association. https://doi.org/10.1002/iroh.19940790202.

    Article  Google Scholar 

  58. Simon, R. D., 1973. Measurement of the Cyanophycin granule polypeptide contained in the blue-green alga Anabaena cylindrica. Journal of Bacteriology 114: 1213–1216.

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Smeltzer, E., A. D. Shambaugh & P. Stangel, 2012. Environmental change in Lake Champlain revealed by long-term monitoring. Journal of Great Lakes Research 38: 6–18.

    CAS  Article  Google Scholar 

  60. Soares, M. C., M. I. Rocha, M. M. Marinho, S. M. Azevedo, C. W. Branco & V. L. Huszar, 2009. Changes in species composition during annual cyanobacterial dominance in a tropical reservoir: physical factors, nutrients and grazing effects. Aquatic Microbial Ecology 57: 137–149.

    Article  Google Scholar 

  61. Soranno, P. A., 1997. Factors affecting the timing of surface scums and epilimnetic blooms of blue-green algae in a eutrophic lake. Canadian Journal of Fisheries and Aquatic Sciences 54: 1965–1975.

    Google Scholar 

  62. Soranno, P. A., S. R. Carpenter & R. C. Lathrop, 1997. Internal phosphorus loading in Lake Mendota: response to external loads and weather. Canadian Journal of Fisheries and Aquatic Sciences 54: 1883–1893.

    CAS  Article  Google Scholar 

  63. Sterner, R. W., 2008. On the phosphorus limitation paradigm for lakes. International Review of Hydrobiology 93: 433–445.

    CAS  Article  Google Scholar 

  64. Stow, C. A., S. R. Carpenter & R. C. Lathrop, 1997. A Bayesian observation error model to predict cyanobacterial biovolume from spring total phosphorus in Lake Mendota, Wisconsin. Canadian Journal of Fisheries and Aquatic Sciences 54: 464–473.

    Article  Google Scholar 

  65. ter Braak, C. J. F., 1985. Correspondence analysis of incidence and abundance data: properties in terms of a unimodal response model. Biometrics 41: 859–873.

    Article  Google Scholar 

  66. Tonk, L., K. Bosch, P. M. Visser & J. Huisman, 2007. Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa. Aquatic Microbial Ecology 46: 117–123.

    Article  Google Scholar 

  67. Toporowska, M., B. Pawlik-Skowronska & R. Kalinowska, 2016. Mass development of Diazotrophic Cyanobacteria (Nostocales) and production of neurotoxic anatoxin-a in a planktothrix (Oscillatoriales) dominated temperate lake. Water, Air, & Soil Pollution 227(9): 321.

    Article  Google Scholar 

  68. Torrey, M. S. & G. F. Lee, 1976. Nitrogen fixation in Lake Mendota, Madison, Wisconsin. Limnology and Oceanography 21: 365–378.

    CAS  Article  Google Scholar 

  69. Vautard, R., J. Cattiaux, P. Yiou, J.-N. Thépaut & P. Ciais, 2010. Northern Hemisphere atmospheric stilling partly attributed to an increase in surface roughness. Nature Geoscience Letters 3: 756–761.

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  71. Wallace, B. B. & D. P. Hamilton, 2000. Simulation of water-bloom formation in the cyanobacterium Microcystis aeruginosa. Journal of PLankton Research 22: 1127–1138.

    Article  Google Scholar 

  72. Weyhenmeyer, G. A., 2001. Warmer winters: are planktonic algal populations in sweden’s largest lakes affected? AMBIO: A Journal of the Human Environment 30: 565–571.

    CAS  Article  Google Scholar 

  73. Winslow, L. A., J. S. Read, G. J. A. Hansen, K. C. Rose & D. M. Robertson, 2017. Seasonality of change: summer warming rates do not fully represent effects of climate change on lake temperatures. Limnology and Oceanography 62: 2168–2178.

    Article  Google Scholar 

  74. Wisconsin State Climatology Office, 2014. History of Freezing and Thawing of Lake Mendota, 1852–1853 to 2014–2015. In. http://www.aos.wisc.edu/~sco/lakes/Mendota-ice.html Accessed December 30 2014.

  75. Woolway, R. I., M. T. Dokulil, W. Marszelewski, M. Schmid, D. Bouffard & C. J. Merchant, 2017. Warming of Central European lakes and their response to the 1980 climate regime shift. Climatic Change 142(3–4): 505–520.

    Article  Google Scholar 

  76. Wu, X. & F. Kong, 2009. Effects of light and wind speed on the vertical distribution of Microcystis aeruginosa colonies of different sizes during a summer bloom. International Review of Hydrobiology 94: 258–266.

    Article  Google Scholar 

  77. Wu, Y., L. Li, L. Zheng, G. Dai, H. Ma, K. Shan, H. Wu, Q. Zhou & L. Song, 2016. Patterns of succession between bloom-forming cyanobacteria Aphanizomenon flos-aquae and Microcystis and related environmental factors in large, shallow Dianchi Lake, China. Hydrobiologia 765: 1–13.

    Article  Google Scholar 

  78. Xiao, M., M. Li & C. S. Reynolds, 2018. Colony formation in the cyanobacterium Microcystis. Biological Reviews of the Cambridge Philosophical Society. https://doi.org/10.1111/brv.12401.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was funded by a grant from the National Institutes of Environmental Health Sciences, Oceans and Human Health program (R01 ES022075-01). The authors would like to thank USGS and anonymous reviewers for their helpful comments that have greatly improved this manuscript. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Todd R. Miller.

Additional information

Handling editor: David Philip Hamilton

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Weirich, C.A., Robertson, D.M. & Miller, T.R. Physical, biogeochemical, and meteorological factors responsible for interannual changes in cyanobacterial community composition and biovolume over two decades in a eutrophic lake. Hydrobiologia 828, 165–182 (2019). https://doi.org/10.1007/s10750-018-3810-x

Download citation

Keywords

  • Cyanobacteria
  • Community composition
  • Lake Mendota
  • Harmful algal blooms
  • Climate change