Nitrogen Constrains the Growth of Late Summer Cyanobacterial Blooms in Lake Erie

Abstract

Phosphorus (P) is generally considered to be the main limiting nutrient to freshwater phytoplankton productivity. However, recent research is drawing attention to the importance of nitrogen (N) in freshwater eutrophication and N often constrains growth of cyanobacteria in small lakes. In this study we determined phytoplankton nutrient limitation in a large lake, Lake Erie during two growing seasons. During 2010 and 2011, nutrient enrichment bioassays (+P, +N and, +P and N) were conducted monthly from June through September with water collected in Maumee Bay (site MB18) and in the center of the western basin (site WBC). Nutrient concentrations were monitored every other week. At MB18, total P concentration was often >3 mmol/L and nitrate concentration decreased from >250 mmol/L in early summer to <1 mmol/L in late summer. Nitrogen and P levels were about five-fold less at WBC. Bioassays indicated that phytoplankton nutrient limitation varied in summer, spatially, and even among phytoplankton groups. For site MB18, +P increased chlorophyll concentration in one of the eight bioassays, indicating that P did not typically limit production. For site WBC, +P increased chlorophyll concentration in six of the eight bioassays. As a result of very low ambient nitrate concentration (<5 mmol/L) in late summer, +N (without P) increased chlorophyll concentration, suggesting symptoms of N-limitation. The N-fixing cyanobacterium Anabaena became dominant following N-limitation. This study highlights the need to reduce P loading to restore water quality. Furthermore, due to low nitrate concentration, the severity of the cyanobacterial blooms could be worse if not for N-limitation in western Lake Erie.

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J. Chaffin, T. Bridgeman and D. Bade, "Nitrogen Constrains the Growth of Late Summer Cyanobacterial Blooms in Lake Erie," Advances in Microbiology, Vol. 3 No. 6A, 2013, pp. 16-26. doi: 10.4236/aim.2013.36A003.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] V. H. Smith, “Eutrophication of Freshwater and Coastal Marine Ecosystems a Global Problem,” Environmental Science and Pollution Research, Vol. 10, No. 2, 2003, pp. 126-139. http://dx.doi.org/10.1065/espr2002.12.142
[2] J. D. Brookes and C. C. Carey, “Resilience to Blooms,” Science, Vol. 334, No. 6052, 2011, pp. 46-47.
http://dx.doi.org/10.1126/science.1207349
[3] J. Huisman, H. C. P. Matthijs and P. M. Visser, “Harmful Cyanobacteria,” Kluwer Academic Publisher, Norwell, 2005.
[4] W. K. Dodds, W. W. Bouska, J. L. Eitzmann, et al., “Eutrophication of US Freshwaters: Analysis of Potential Economic Damages,” Environmental Science & Technology, Vol. 43, No. 1, 2008, pp. 12-19.
http://dx.doi.org/10.1021/es801217q
[5] D. W. Schindler, “Evolution of Phosphorus Limitation in Lakes,” Science, Vol. 195, No. 4275, 1977, pp. 260-262.
http://dx.doi.org/10.1126/science.195.4275.260
[6] J. A. Downing, S. B. Watson and E. McCauley, “Predicting Cyanobacteria Dominance in Lakes,” Canadian Journal of Fisheries and Aquatic Sciences, Vol. 58, No. 10, 2001, pp. 1905-1908.
http://dx.doi.org/10.1139/f01-143
[7] C. L. Schelske, “Eutrophication: Focus on Phosphorus,” Science, Vol. 324, No. 5928, 2009, p. 722.
http://dx.doi.org/10.1126/science.324_722
[8] D. W. Schindler, “The Dilemma of Controlling Cultural Eutrophication of Lakes,” Proceedings of the Royal Society B: Biological Sciences, 2012, pp. 1-12
[9] W. M. Lewis and W. A. Wurtsbaugh, “Control of Lacustrine Phytoplankton by Nutrients: Erosion of the Phosphorus Paradigm,” International Review of Hydrobiology, Vol. 93, No. 4-5, 2008, pp. 446-465.
http://dx.doi.org/10.1002/iroh.200811065
[10] D. J. Conley, H. W. Paerl, R. W. Howarth, et al., “Controlling Eutrophication: Nitrogen and Phosphorus,” Science, Vol. 323, No. 5917, 2009, pp. 1014-1015.
http://dx.doi.org/10.1126/science.1167755
[11] H. W. Paerl, H. Xu, M. J. McCarthy, et al., “Controlling Harmful Cyanobacterial Blooms in a Hyper-Eutrophic Lake (Lake Taihu, China): The Need for a Dual Nutrient (N & P) Management Strategy,” Water Research, Vol. 45, No. 5, 2011, pp. 1973-1983.
http://dx.doi.org/10.1016/j.watres.2010.09.018
[12] J. A. Downing and E. McCauley, “The Nitrogen: Phosphorus Relationship in Lakes,” Limnology and Oceanography, Vol. 37, No. 5, 1992, pp. 936-945.
http://dx.doi.org/10.4319/lo.1992.37.5.0936
[13] S. J. Guildford and R. E. Hecky, “Total Nitrogen, Total Phosphorus, and Nutrient Limitation in Lakes and Oceans: Is There a Common Relationship?” Limnography and Oceanography, Vol. 45, No. 6, 2000, pp. 1213-1223.
http://dx.doi.org/10.4319/lo.2000.45.6.1213
[14] R. P. Stumpf, T. T. Wynne, D. B. Baker and G. L. Fahnenstiel, “Interannual Variability of Cyanobacterial Blooms in Lake Erie,” PloS One, Vol. 7, No. 8, 2012, Article ID: e42444. http://dx.doi.org/10.1371/journal.pone.0042444
[15] T. B. Bridgeman, J. D. Chaffin and J. E. Filbrun, “A Novel Method for Tracking Western Lake Erie Microcystis Blooms, 2002-2011,” Journal of Great Lakes Research, Vol. 39, No. 1, 2013, pp. 83-89.
http://dx.doi.org/10.1016/j.jglr.2012.11.004
[16] C. E. Herdendorf, “Large Lakes of the World,” Journal of Great Lakes Research, Vol. 8, No. 3, 1982, pp. 379-412.
http://dx.doi.org/10.1016/S0380-1330(82)71982-3
[17] S. J. Bolsenga and C. E. Herdendorf, “Lake Erie and Lake Saint Clair handbook,” Wayne State University Press, 1993.
[18] A. M. Michalak, E. J. Anderson, D. Beletsky, et al., “Re-cordsetting Algal Bloom in Lake Erie Caused by Agricultural and Meteorological Trends Consistent with Expected Future Conditions,” Proceedings of the National Academy of Sciences, 2013, Vol. 110, No. 16, pp. 6448-6452. http://dx.doi.org/10.1073/pnas.1216006110
[19] D. B. Baker and R. P. Richards, “Phosphorus Budgets and Riverine Phosphorus Export in Northwestern Ohio Watersheds,” Journal of Environmental Quality, Vol. 31, No. 1, 2002, pp. 96-108.
http://dx.doi.org/10.2134/jeq2002.0096
[20] H. Han, N. Bosch and J. D. Allan, “Spatial and Temporal Variation in Phosphorus Budgets for 24 Watersheds in the Lake Erie and Lake Michigan Basins,” Biogeochemistry, Vol. 102, 2011, pp. 45-58.
http://dx.doi.org/10.1007/s10533-010-9420-y
[21] J. D. Chaffin, T. B. Bridgeman, S. A. Heckathorn and S. Mishra, “Assessment of Microcystis Growth Rate Potential and Nutrient Status Across a Trophic Gradient in Western Lake Erie,” Journal of Great Lakes Research, Vol. 37, No. 1, 2011, pp. 92-100.
http://dx.doi.org/10.1016/j.jglr.2010.11.016
[22] W. M. Lewis, W. A. Wurtsbaugh and H. W. Paerl, “Rationale for Control of Anthropogenic Nitrogen and Phosphorus to Reduce Eutrophication of Inland Waters,” Environmental Science & Technology, Vol. 45, No. 24, 2011, pp. 10300-10305. http://dx.doi.org/10.1021/es202401p
[23] T. B. Bridgeman, J. D. Chaffin, D. D. Kane, J. D. Conroy, S. E. Panek and P. M. Armenio, “From River to Lake: Phosphorus Partitioning and Algal Community Compositional Changes in Western Lake Erie,” Journal of Great Lakes Research, Vol. 38, No. 1, 2012, pp. 90-97.
http://dx.doi.org/10.1016/j.jglr.2011.09.010
[24] S. J. Guildford, R. E. Hecky, R. E. H. Smith, et al., “Phytoplankton Nutrient Status in Lake Erie in 1997,” Journal of Great Lakes Research, Vol. 31, Suppl. 2, 2005, pp. 72-88.
http://dx.doi.org/10.1016/S0380-1330(05)70306-3
[25] R. P. Richards, D. B. Baker, J. P. Crumrine and A. M. Stearns, “Unusually Large Loads in 2007 from the Maumee and Sandusky Rivers, Tributaries to Lake Erie,” Journal of Soil and Water Conservation, Vol. 65, No. 6, 2010, pp. 450-462.
http://dx.doi.org/10.2489/jswc.65.6.450
[26] R. G. Wetzel and G. E. Likens, “Limnological Analyses,” Springer Verlag, 2000.
[27] T. W. Davis, F. Koch, M. A. Marcoval, et al., “Mesozooplankton and Microzooplankton Grazing during Cyanobacterial Blooms in the Western Basin of Lake Erie,” Harmful Algae, Vol. 15, 2012, pp. 26-35.
http://dx.doi.org/10.1016/j.hal.2011.11.002
[28] C. L. Schelske, “In Situ and Natural Phytoplankton Assemblage Bioassays,” In: L. E. Shubert, Ed., Algae as Ecolgocial Indicators, Academic Press, Cambridge, 1984, pp. 15-47.
[29] J. B. Moon and H. J. Carrick, “Seasonal Variation of Phytoplankton Nutrient Limitation in Lake Erie,” Aquatic Microbial Ecology, Vol. 48, No. 1, 2007, pp. 61-71.
http://dx.doi.org/10.3354/ame048061
[30] M. Beutler, K. H. Wiltshire, B. Meyer, et al., “A Fluorometric Method for the Differentiation of Algal Populations In Vivo and in Situ,” Photosynthesis Research, Vol. 72, No. 1, 2002, pp. 39-53.
http://dx.doi.org/10.1023/A:1016026607048
[31] M. R. Twiss, C. Ulrich, S. A. Kring, et al., “Plankton Dynamics along a 180 km Reach of the Saint Lawrence River from Its Headwaters in Lake Ontario,” Hydrobiologia, Vol. 647, No. 1, 2010, pp. 7-20.
http://dx.doi.org/10.1007/s10750-010-0115-0
[32] J. D. Chaffin, T. B. Bridgeman, S. A. Heckathorn and A. E. Krause, “Role of Suspended Sediments and Mixing in Reducing Photoinhibition in the Bloom-Forming Cyanobacterium Microcystis,” Journal of Water Resource and Protection, Vol. 04, No. 12, 2012, pp. 1029-1041.
http://dx.doi.org/10.4236/jwarp.2012.412119
[33] H. S. Kim, S. J. Hwang, J. K. Shin, et al., “Effects of Limiting Nutrients and N: P Ratios on the Phytoplankton Growth in a Shallow Hypertrophic Reservoir,” Hydrobiologia, Vol. 581, No. 1, 2007, pp. 255-267.
http://dx.doi.org/10.1007/s10750-006-0501-9
[34] H. Xu, H. W. Paerl, B. Qin, et al., “Nitrogen and Phosphorus Inputs Control Phytoplankton Growth in Eutrophic Lake Taihu, China,” Limnology and Oceanography, Vol. 55, No. 1, 2010, pp. 420-432.
http://dx.doi.org/10.4319/lo.2010.55.1.0420
[35] C. L. Schelske, E. F. Stoermer, G. L. Fahnenstiel and M. Haibach, “Phosphorus Enrichment, Silica Utilization, and Biogeochemical Silica Depletion in the Great Lakes,” Canadian Journal of Fisheries and Aquatic Sciences, Vol. 43, No. 2, 1986, pp. 407-415.
http://dx.doi.org/10.1139/f86-051
[36] S. F. Baldia, A. D. Evangelista, E. V. Aralar and A. E. Santiago, “Nitrogen and Phosphorus Utilization in the Cyanobacterium microcystis aeruginosa Isolated from Laguna de Bay, Philippines,” Journal of Applied Phycology, Vol. 19, No. 6, 2007, pp. 607-613.
http://dx.doi.org/10.1007/s10811-007-9209-0
[37] P. M. Vitousek, J. D. Aber, R. W. Howarth, G. E. Likens, P. A. Matson, D. W. Schindler, W. H. Schlesinger and D. G. Tilman, “Human Alteration of the Global Nitrogen Cycle: Sources and Consequences,” Ecological Applications, Vol. 7, No. 3, 1997, pp. 737-750.
[38] J. N. Galloway, F. J. Dentener, D. G. Capone, et al., “Nitrogen Cycles: Past, Present, and Future,” Biogeochemistry, Vol. 70, No. 2, 2004, pp. 153-226.
http://dx.doi.org/10.1007/s10533-004-0370-0
[39] M. J. Paterson, D. W. Schindler, R. E. Hecky, et al., “Comment: Lake 227 Shows Clearly That Controlling Inputs of Nitrogen Will Not Reduce or Prevent Eutrophication of Lakes,” Limnology and Oceanography, Vol. 56, No. 4, 2011, pp. 1545-1547.
http://dx.doi.org/10.4319/lo.2011.56.4.1545
[40] D. W. Schindler and R. E. Hecky, “Eutrophication: More Nitrogen Data Needed,” Science, Vol. 324, No. 5928, 2009, pp. 721-722.
http://dx.doi.org/10.1126/science.324_721b
[41] D. W. Schindler, R. E. Hecky, D. L. Findlay, et al., “Eutrophication of Lakes Cannot Be Controlled by Reducing Nitrogen Input: Results of a 37-year Whole-Ecosystem Experiment,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 105, No. 32, 2008, pp. 11254-11258.
http://dx.doi.org/10.1073/pnas.0805108105
[42] J. T. Scott and M. J. McCarthy, “Response to Comment: Nitrogen Fixation Has Not Offset Declines in the Lake 227 Nitrogen Pool and Shows That Nitrogen Control Deserves Consideration in Aquatic Ecosystems,” Limnology and Oceanography, Vol. 56, No. 4, 2011, pp. 1548-1550.
http://dx.doi.org/10.4319/lo.2011.56.4.1548
[43] E. Flores and A. Herrero, “Nitrogen Assimilation and Nitrogen Control in Cyanobacteria,” Biochemical Society Transactions, Vol. 33, No. 1, 2005, pp. 164-167.
http://dx.doi.org/10.1042/BST0330164
[44] R. L. North, S. J. Guildford, R. E. H. Smith, et al., “Evidence for Phosphorus, Nitrogen, and Iron Colimitation of Phytoplankton Communities in Lake Erie,” Limnology and Oceanography, Vol. 52, No. 1, 2007, pp. 315-328.
http://dx.doi.org/10.4319/lo.2007.52.1.0315
[45] S. M. Havens, C. S. Hassler, R. L. North, et al., “Iron Plays a Role in Nitrate Drawdown by Phytoplankton in Lake Erie Surface Waters as Observed in Lake-Wide Assessments,” Canadian Journal of Fisheries and Aquatic Sciences, Vol. 69, No. 2, 2012, pp. 369-381.
http://dx.doi.org/10.1139/f2011-157
[46] J. D. Chaffin and T. B. Bridgeman, “Organic and Inorganic Utilization by Nitrogen-Stressed Cyanobacteria during Bloom Conditions,” Journal of Applied Phycology, accepted. http://dx.doi.org/10.1007/s10811-013-0118-0
[47] J. Huisman, J. Sharples, J. M. Stroom, et al., “Changes in Turbulent Mixing Shift Competition for Light Between Phytoplankton Species,” Ecology, Vol. 85, No. 11, 2004, pp. 2960-2970. http://dx.doi.org/10.1890/03-0763
[48] H. L. MacIntyre, T. M. Kana, T. Anning and R. J. Geider, “Photoacclimation of Photosynthesis Irradiance Response Curves and Photosynthetic Pigments in Microalgae and Cyanobacteria,” Journal of Phycology, Vol. 38, No. 1, 2002, pp. 17-38.
http://dx.doi.org/10.1046/j.1529-8817.2002.00094.x

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