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.
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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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Dillon, P. J. & F. H. Rigler, 1974. The phosphorus-chlorophyll relationship in lakes. Limnology and Oceanography 19: 767–773.
Dixon, P., 2009. VEGAN, a package of R functions for community ecology. Journal of Vegetation Science 14: 927–930.
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.
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.
Downing, J. A., S. B. Watson & E. McCauley, 2001. Predicting Cyanobacteria dominance in lakes. Canadian Journal of Fisheries and Aquatic Sciences 58: 1905–1908.
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.
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.
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.
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.
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.
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.
Gehringer, M. M. & N. Wannicke, 2014. Climate change and regulation of hepatotoxin production in Cyanobacteria. FEMS Microbiology Ecology 88: 1–25.
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.
Hill, M. O., J. Gauch & G. Hugh, 1980. Detrended correspondence analysis: an improved ordination technique. Vegetatio 42: 47–58.
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.
Johnston, B. R. & J. M. Jacoby, 2003. Cyanobacterial toxicity and migration in a mesotrophic lake in western Washington, USA. Hydrobiologia 495: 79–91.
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.
Kebede, E. & A. Belay, 1994. Species composition and phytoplankton biomass in a tropical African Lake (Lake Awassa, Ethiopia). Hydrobiologia 288: 13–32.
Kendall, M. G., 1976. Chapter 3 Rank Correlation Methods, Vol. 4th. Edition, Griffin.
Konopka, A. & T. D. Brock, 1978. Effect of temperature on blue-green algae (Cyanobacteria) in Lake Mendota. Applied and Environmental Microbiology 36: 572–576.
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.
Lathrop, R. C., 2007. Perspectives on the eutrophication of the Yahara lakes. Lake and Reservoir Management 23: 345–365.
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.
Litchman, E. & C. A. Klausmeier, 2008. Trait-based community ecology of phytoplankton. Annual Review of Ecology, Evolution, and Systematics 39: 615–639.
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.
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.
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.
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.
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.
Murtagh, F. & P. Legendre, 2014. Ward’s hierarchical agglomerative clustering method: which algorithms implement ward’s criterion? Journal of Classification 31: 274–295.
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.
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.
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.
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.
Paerl, H. W. & J. Huisman, 2009. Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environmental Microbiology Reports 1: 27–37.
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.
Paerl, H. W. & V. J. Paul, 2012. Climate change: links to global expansion of harmful cyanobacteria. Water Research 46: 1349–1363.
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.
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.
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.
R Development Core Team, 2013. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
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.
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.
Reed, T. & S. R. Carpenter, 2002. Comparisons of P-yield, riparian buffer strips, and Land cover in six agricultural watersheds. Ecosystems 5: 568–577.
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.
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.
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.
Simon, R. D., 1973. Measurement of the Cyanophycin granule polypeptide contained in the blue-green alga Anabaena cylindrica. Journal of Bacteriology 114: 1213–1216.
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.
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.
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.
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.
Sterner, R. W., 2008. On the phosphorus limitation paradigm for lakes. International Review of Hydrobiology 93: 433–445.
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.
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.
Tonk, L., K. Bosch, P. M. Visser & J. Huisman, 2007. Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa. Aquatic Microbial Ecology 46: 117–123.
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.
Torrey, M. S. & G. F. Lee, 1976. Nitrogen fixation in Lake Mendota, Madison, Wisconsin. Limnology and Oceanography 21: 365–378.
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.
Wagner, C. & R. Adrian, 2009. Cyanobacteria dominance: quantifying the effects of climate change. Limnology and Oceanography 54: 2460–2468.
Wallace, B. B. & D. P. Hamilton, 2000. Simulation of water-bloom formation in the cyanobacterium Microcystis aeruginosa. Journal of PLankton Research 22: 1127–1138.
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.
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.
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.
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.
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.
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.
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.
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.
Handling editor: David Philip Hamilton
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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
- Community composition
- Lake Mendota
- Harmful algal blooms
- Climate change