, Volume 693, Issue 1, pp 13–28 | Cite as

Phytoplankton biomass is mainly controlled by hydrology and phosphorus concentrations in tropical hydroelectric reservoirs

  • Luciana M. Rangel
  • Lúcia H. S. Silva
  • Priscila Rosa
  • Fábio Roland
  • Vera L. M. Huszar
Primary Research Paper


Phytoplankton is widely recognized as being regulated mainly by resources (nutrients and light) and predation by higher trophic levels. In reservoirs, these controls also can be modulated by hydrology, for example through the influence of flow pulses generated by the operation of the dam. In this study, we tested the influence of light, nutrients, and zooplankton grazing pressure, and also hydrology (as water residence time) on the phytoplankton biomass in eight tropical hydroelectric reservoirs, which differ in size, morphometry, location, trophic state, and water residence time. Our hypothesis was that, as these reservoirs are used for hydroelectric purposes, the control that would otherwise be exerted on phytoplankton biomass primarily by resource availability and grazing will also be modulated by hydrology. Low phytoplankton biomass (range of system medians = 12–299 μg C l−1) occurred in most systems, except for one highly eutrophic reservoir (median = 1331 μg C l−1). Our data showed that phosphorus was more often likely to be the limiting nutrient in these systems, as assessed through nutrient limitation indexes (nitrogen and phosphorus), based on concentrations and ratios. For most reservoirs, excluding the eutrophic system with high cyanobacteria biomass, seasonal water residence time was the variable that best explained phytoplankton variation among the several environmental variables analyzed in this study (P < 0.0001; adjusted r 2 = 0.38). Hydrology was an important and additional factor modulating phytoplankton in these tropical reservoirs, directly removing phytoplankton populations and their potential zooplankton grazers by washout, and also affecting nutrient availability.


Cyanobacteria Nitrogen-fixing Nutrients Phytoplankton limitation Water residence time Zooplankton grazing 



The authors are grateful to FURNAS Centrais Elétricas S.A, CAPES (Foundation for the Coordination of Higher Education and Graduate Training) and CNPQ (Brazilian National Research Council) for financial support. We also thank Dr. Janet W. Reid (JWR Associates) for the revision of the English text, and two anonymous reviewers for their valuable contributions.


  1. Abell, J. M., D. Özkundakci & D. P. Hamilton, 2010. Nitrogen and phosphorus limitation of phytoplankton growth in New Zealand lakes: implications for eutrophication control. Ecosystems 13: 966–977.CrossRefGoogle Scholar
  2. Abril, G., F. Guérin, S. Richard, R. Delmas, C. Galy-Lacaux, P. Gosse, A. Tremblay, L. Varfalvy, M. A. Dos Santos & B. Matvienko, 2005. Carbon dioxide and methane emissions and the carbon budget of a 10-year old tropical reservoir (Petit Saut, French Guiana). Global Biogeochemical Cycles 19: GB4007.CrossRefGoogle Scholar
  3. Baranyi, C., T. Hein, C. Holarek, S. Keckeis & F. Schiemer, 2002. Zooplankton biomass and community structure in a Danube River floodplain system: effects of hydrology. Freshwater Biology 47: 473–482.CrossRefGoogle Scholar
  4. Barros, N. O., J. J. Cole, L. Tranvik, Y. T. Prairie, D. Bastviken, V. L. M. Huszar, P. del Giorgio & F. Roland, 2011. Carbon emission from hydroelectric reservoirs linked to reservoir age and latitude. Nature Geosciences 4: 593–596.CrossRefGoogle Scholar
  5. Bernhardt, J., J. A. Elliott & I. D. Jones, 2008. Modelling the effects on phytoplankton communities of changing mixed depth and background extinction coefficient on three contrasting lakes in the English Lake District. Freshwater Biology 53: 2573–2586.CrossRefGoogle Scholar
  6. Blomqvist, P., A. Pettersson & P. Hyenstrand, 1994. Ammonium-nitrogen: a key regulatory factor causing dominance of non-nitrogen-fixing cyanobacteria in aquatic systems. Archiv für Hydrobiologie 132: 141–164.Google Scholar
  7. Brett, M. T. & M. M. Benjamin, 2008. A reassessment of lake phosphorus residence and the nutrient loading concept in limnology. Freshwater Biology 53: 194–211.Google Scholar
  8. Carpenter, S. R., 2008. Phosphorus control is critical to mitigating eutrophication. Proceedings of the National Academy of Sciences 105: 11039–11040.CrossRefGoogle Scholar
  9. Carpenter, S. R., J. F. Kitchell, K. L. Cottingham, D. E. Schindler, D. L. Christense, D. M. Post & N. Voichick, 1996. Chlorophyll variability, nutrient input and grazing: evidence from whole-lake experiments. Ecology 77: 725–735.CrossRefGoogle Scholar
  10. Cole, G. A., 1994. Textbook of Limnology. Waveland Press Inc, Prospect Heights, IL.Google Scholar
  11. Cole, J. F. & C. Jones, 2000. Effect of temperature on photosynthesis-light response and growth of four phytoplankton species isolated from a tidal freshwater river. Journal of Phycology 36: 7–16.CrossRefGoogle Scholar
  12. Dillon, P. J. & F. H. Rigler, 1974. A test of a simple nutrient budget model, predicting the phosphorus concentration in lake water. Journal of the Fisheries Research Board of Canada 31: 1771–1778.CrossRefGoogle Scholar
  13. Downing, J. A., M. McClain, R. Twilley, J. M. Melack, J. Elser, N. N. Rabalais, W. M. Lewis Jr, R. E. Turner, J. Corredor, D. Soto, A. Yanez-Arancibia, J. A. Kopaska & R. W. Howarth, 1999. The impact of accelerating land-use change on the N-Cycle of tropical aquatic ecosystems: Current conditions and projected changes. Biogeochemistry 46: 109–148.Google Scholar
  14. Downing, J. A., Y. T. Prairie, J. J. Cole, C. M. Duarte, L. J. Tranvik, R. G. Striegl, W. H. McDowell, P. Kortelainen, N. F. Caraco, J. M. Melack & J. Middelburg, 2006. The global abundance and size distribution of lakes, ponds, and impoundments. Limnology and Oceanography 51: 2388–2397.CrossRefGoogle Scholar
  15. Elser, J. J., E. R. Marzolf & C. R. Goldman, 1990. Phosphorus and nitrogen limitation of phytoplankton growth in the freshwaters of North America: a review and critique of experimental enrichments. Canadian Journal of Fisheries and Aquatic Sciences 47: 1468–1477.CrossRefGoogle Scholar
  16. Elser, J. J., M. E. S. Bracken, E. E. Cleland, D. S. Gruner, W. S. Harpole, H. Hillebrand, J. T. Ngai, E. W. Seabloom, J. B. Shurin & J. E. Smith, 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10: 1135–1142.PubMedCrossRefGoogle Scholar
  17. Fisher, T. R., J. M. Melack, J. U. Grobbelaar & R. W. Howarth, 1995. Nutrient limitation of phytoplankton and eutrophication of inland, estuarine, and marine waters. In Tiessen, H. (ed.), Phosphorus in the Global Environment: Transfers, Cycles and Management. Wiley, New York: 301–322.Google Scholar
  18. Havens, K. E., A. C. Elia, M. I. Taticchi & R. S. Fulton III, 2009. Zooplankton–phytoplankton relationships in shallow subtropical versus temperate lakes Apopka (Florida, USA) and Trasimeno (Umbria, Italy). Hydrobiologia 628: 165–175.CrossRefGoogle Scholar
  19. Hense, I. & A. Beckmann, 2006. Towards a model of cyanobacteria life cycle-effects of growing and resting stages on bloom formation of N2-fixing species. Ecological Modelling 195: 205–218.CrossRefGoogle Scholar
  20. Hillebrand, H., C.-D. Dürselen, D. Kirschtel, U. Pollingher & T. Zohary, 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35: 403–424.CrossRefGoogle Scholar
  21. Huszar, V. L. M., N. F. Caraco, F. Roland & J. Cole, 2006. Nutrient–chlorophyll relationships in tropical–subtropical lakes: Do temperate models fit? Biogeochemistry 79: 239–250.CrossRefGoogle Scholar
  22. Jackson, L. J., M. Søndergaard, T. L. Lauridsen & E. Jeppesen, 2007. Patterns, processes, and contrast of macrophyte-dominated and turbid Danish and Canadian shallow lakes, and implications of climate change. Freshwater Biology 52: 1782–1792.CrossRefGoogle Scholar
  23. Jensen, P., E. Jeppesen, K. Olrik & P. Kristensen, 1994. Impact of nutrients and physical factors on the shift from cyanobacterial to chlorophyte dominance in shallow Danish lakes. Canadian Journal of Fisheries and Aquatic Sciences 51: 1692–1699.CrossRefGoogle Scholar
  24. Jeppesen, E., M. Søndergaard, E. Kanstrup, B. Petersen, R. B. Henriksen, M. Hammershøj, E. Mortensen, J. P. Jensen & A. Have, 1994. Does the impact of nutrients on the biological structure and function of brackish and freshwater lakes differ? Hydrobiologia 275(276): 15–30.CrossRefGoogle Scholar
  25. Jeppesen, E., J. P. Jensen, M. Søndergaard, T. Lauridsen, L. J. Pedersen & L. Jensen, 1997. Top-down control in freshwater lakes: the role of nutrient state, submerged macrophytes and water depth. Hydrobiologia 342(343): 151–164.CrossRefGoogle Scholar
  26. Jeppesen, E., J. P. Jensen, C. Jensen, B. Faafeng, D. O. Hessen, M. Søndergaard, T. Lauridsen, P. Brettum & K. Christoffersen, 2003. The impact of nutrient state and lake depth on top-down control in the pelagic zone of lakes: a study of 466 lakes from the temperate zone to the Arctic. Ecosystems 6: 313–325.CrossRefGoogle Scholar
  27. Jeppesen, E., M. Meerhoff, B. A. Jacobsen, R. S. Hansen, M. Søndergaard, J. P. Jensen, T. L. Lauridsen, N. Mazzeo & C. W. 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.CrossRefGoogle Scholar
  28. Kalff, J., 2002. Limnology: Inland Water Ecosystems. Prentice-Hall, Upper Saddle River, New Jersey.Google Scholar
  29. Kennedy, R. H. & W. W. Walker, 1990. Reservoir nutrient dynamics. In Thornton, B., K. W. Kimmel & F. E. Payne (eds), Reservoir Limnology: Ecological Perspectives. John Wiley and Sons, Inc, New York: 109–131.Google Scholar
  30. Köppen, W., 1936. Das geographische System der Klimate—Handbuch der Klimatologie. Gebrüder Bornträger Verlag, Berlin.Google Scholar
  31. Kosten, S., V. L. M. Huszar, N. Mazzeo, M. Scheffer, L. da S. Sternberg & E. Jeppesen, 2009. Lake and watershed characteristics rather than climate influence nutrient limitation in shallow lakes. Ecological Applications 19: 1791–1804.PubMedCrossRefGoogle Scholar
  32. Kosten, S., V. L. M. Huszar, E. Bécares, L. S. Costa, E. Van Donk, L. A. Hansson, E. Jeppesen, C. Kruk, G. Lacerot, N. Mazzeo, L. De 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.CrossRefGoogle Scholar
  33. Latja, R. & K. Salonen, 1978. Carbon analysis for the determination of individual biomass of planktonic animals. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 20: 2556–2560.Google Scholar
  34. Lazzaro, X., 1997. Do the trophic cascade hypothesis and classical biomanipulation approaches apply to tropical lakes and reservoirs? Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 26: 719–730.Google Scholar
  35. Legendre, P. & L. Legendre, 1998. Numerical Ecology. Elsevier, Amsterdam.Google Scholar
  36. Lewis, W. M., 2000. Basis for the protection and management of tropical lakes. Lakes and Reservoirs Research and Management 5: 35–48.CrossRefGoogle Scholar
  37. Lund, J. W. G., C. Kipling & E. D. Lecren, 1958. The inverted microscope method of estimating algal number and the statistical basis of estimating by counting. Hydrobiologia 11: 143–170.CrossRefGoogle Scholar
  38. Maberly, S. C., L. King, C. E. Gibson, L. May, R. I. Jones, M. M. Dent & C. Jordan, 2003. Linking nutrient limitation and water chemistry in upland lakes to catchment characteristics. Hydrobiologia 506(509): 83–91.CrossRefGoogle Scholar
  39. MacDonagh, M. E., M. A. Casco & M. C. Claps, 2009. Plankton relationships under small water level fluctuations in a subtropical reservoir. Aquatic Ecology 43: 371–381.CrossRefGoogle Scholar
  40. Manca, M. & P. Comoli, 1999. Studies on zooplankton of Lago Paione Superiore. Journal of Limnology 59: 131–135.Google Scholar
  41. Matsumura-Tundisi, T., J. G. Tundisi, A. Saggio, A. L. Oliveira Neto & E. G. Espíndola, 1991. Limnology of Samuel Reservoir (Brazil, Rondônia) in the filling phase. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 24: 1428–1487.Google Scholar
  42. Mazumder, A., 1994. Phosphorus–chlorophyll relationships under contrasting herbivory and thermal stratification: predictions and patterns. Canadian Journal of Fisheries and Aquatic Sciences 51: 390–400.CrossRefGoogle Scholar
  43. Mazumder, A. & K. E. Havens, 1998. Nutrient-chlorophyll-Secchi relationships under contrasting grazer communities of temperate versus subtropical lakes. Canadian Journal of Fisheries and Aquatic Sciences 55: 1652–1662.CrossRefGoogle Scholar
  44. Morris, D. P. & W. M. Lewis, 1988. Phytoplankton nutrient limitation in Colorado mountain lakes. Freshwater Biology 20: 315–327.CrossRefGoogle Scholar
  45. Niemer, E.,1989. Climatologia do Brasil. IBGE, Rio de Janeiro.Google Scholar
  46. Nürnberg, G. K., 1996. Trophic state of clear and colored, soft- and hard-water lakes with special consideration of nutrients, anoxia, phytoplankton and fish. Journal of Lake and Reservoir Management 12: 432–447.CrossRefGoogle Scholar
  47. Nusch, E. A. & G. Palme, 1975. Biologische Methoden für die Praxis der Gewässeruntersuchung. Gewässer und Abwässer 116: 562–565.Google Scholar
  48. 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.CrossRefGoogle Scholar
  49. Obertegger, U., G. Flaim, M. G. Braioni, R. Sommaruga, F. Corradini & A. Borsato, 2007. Water residence time as a driving force of zooplankton structure and succession. Aquatic Sciences 69: 575–583.CrossRefGoogle Scholar
  50. Pauli, H. R., 1989. A new method to estimate individual dry weights of rotifers. Hydrobiologia 186(187): 355–361.CrossRefGoogle Scholar
  51. Pearl, H. W. & J. Huissman, 2008. Blooms like it hot. Science 320: 57–58.CrossRefGoogle Scholar
  52. Phillips, G., O.-P. Pietiläinen, L. Carvalho, A. Solimini, A. Lyche Solheim & A. C. Cardoso, 2008. Chlorophyll–nutrient relationships of different lake types using a large European dataset. Aquatic Ecology 42: 213–226.CrossRefGoogle Scholar
  53. Rangel, L. M., L. H. S. Silva, M. S. Arcifa & A. Perticarrari, 2009. Driving forces of the diel distribution of phytoplankton functional groups in a shallow tropical lake (Lake Monte Alegre, Southeast Brazil). Brazilian Journal of Biology 69: 631–637.CrossRefGoogle Scholar
  54. Reynolds, C. S., 1984. The Ecology of Freshwater Phytoplankton. Cambridge University Press, London.Google Scholar
  55. Reynolds, C. S., 1992a. Dynamics, selection and composition of phytoplankton in relation to vertical structure in lakes. Archiv für Hydrobiologie, Beiheft Ergebnisse der Limnologie 35: 13–31.Google Scholar
  56. Reynolds, C. S., 1992b. Eutrophication and the management of planktonic algae: what Vollenweider couldn’t tell us. In: Sutcliffe, D. W. & J. G. Jones (eds), Eutrophication: Research and Application to Water Supply. Freshwater Biological Association, Ambleside: 4–29.Google Scholar
  57. Reynolds, C. S., 1994. The long, the short and the stalled: on the attributes of phytoplankton selected by physical mixing in lakes and rivers. Hydrobiologia 289: 9–21.CrossRefGoogle Scholar
  58. Reynolds, C. S., 1997. Vegetation Processes in the Pelagic: A Model for Ecosystem Theory. Ecology Institute, Oldendorf/Luhe.Google Scholar
  59. Reynolds, C. S., 1999a. Phytoplankton assemblages in reservoirs. In Tundisi, J. G. & M. Straškraba (eds), Theoretical Reservoir Ecology and Its Applications. International Institute of Ecology, Brazilian Academy of Sciences and Backhuys, São Carlos: 439–456.Google Scholar
  60. Reynolds, C. S., 1999b. Non-determinism to probability, or N:P in the community ecology of phytoplankton. Archiv für Hydrobiologie 146: 23–35.Google Scholar
  61. Reynolds, C. S., 2006. The Ecology of Phytoplankton (Ecology, Biodiversity and Conservation). Cambridge University Press, Cambridge.Google Scholar
  62. Reynolds, C. S. & S. C. Maberly, 2002. A simple method for approximating the supportive capacities and metabolic constraints in lakes and reservoirs. Freshwater Biology 47: 1183–1188.CrossRefGoogle Scholar
  63. Rocha, O. & A. Duncan, 1985. The relationship between cell carbon and cell volume in freshwater algal species used in zooplanktonic studies. Journal of Plankton Research 7: 279–294.CrossRefGoogle Scholar
  64. Roland, F., L. O. Vidal, F. S. Pacheco, N. O. Barros, A. Assireu, J. P. H. B. Ometto, A. C. P. Cimbleris & J. J. Cole, 2010. Variability of carbon dioxide flux from tropical (Cerrado) hydroelectric reservoirs. Aquatic Sciences 72: 283–293.CrossRefGoogle Scholar
  65. Ruttner-Kolisko, A., 1977. Suggestions of biomass calculation of plankton rotifers. Archiv für Hydrobiologie, Beiheft Ergebnisse der Limnologie 8: 71–76.Google Scholar
  66. Sakamoto, M., 1966. Primary production by phytoplankton community in some Japanese lakes and its dependence on lake depth. Archiv für Hydrobiologie 62: 1–28.Google Scholar
  67. Sarnelle, O., S. D. Cooper, S. Weisman & K. Mavuti, 1998. The relationship between nutrients and trophic-level biomass in turbid tropical ponds. Freshwater Biology 40: 65–75.CrossRefGoogle Scholar
  68. Sas, H., 1989. Lake Restoration by Reduction of Nutrient Loading: Expectations, Experiences, Extrapolations. Academia Verlag Richarz, St. Augustin.Google Scholar
  69. Schindler, D. W., 2006. Recent advances in the understanding and management of eutrophication. Limnology and Oceanography 51: 356–363.CrossRefGoogle Scholar
  70. Schindler, D. W., R. E. Hecky, D. L. Findlay, M. P. Stainton, B. R. Parker, M. J. Paterson, K. G. Beaty, M. Lyng & S. E. M. Kasian, 2008. 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 USA 105: 11254–11258.CrossRefGoogle Scholar
  71. Shiklomanov, I. A. & J. C. Rodda, 2003. World Water Resources at the Beginning of the Twenty-first Century. Cambridge University Press, Cambridge.Google Scholar
  72. Smith, V. H. & D. W. Schindler, 2009. Eutrophication science: where do we go from here? Trends in Ecology and Evolution 24: 201–207.PubMedCrossRefGoogle Scholar
  73. Soares, M. C. S., M. M. Marinho, S. M. F. O. Azevedo, C. W. C. Branco & V. L. M. Huszar, 2008. The effects of water retention time and watershed features on the limnology of two tropical reservoirs in Brazil. Lakes & Reservoirs: Research and Management 13: 257–269.CrossRefGoogle Scholar
  74. Soares, M. C. S., M. I. A. Rocha, M. M. Marinho, S. M. F. O. Azevedo, C. W. C. Branco & V. L. M. 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.CrossRefGoogle Scholar
  75. Soares, M. C. S., M. M. Marinho, S. M. F. O. Azevedo, C. W. C. Branco & V. L. M. Huszar, 2012. Eutrophication and retention time affecting spatial heterogeneity in a tropical reservoir. Limnologica. doi: 10.1016/j.limno.2011.11.002.
  76. Søndergaard, M., J. P. Jensen & E. Jeppesen, 2003. Role of sediment and internal loading of phosphorus in shallow lakes. Hydrobiologia 506: 135–145.CrossRefGoogle Scholar
  77. Søndergaard, M., S. E. Larsen, T. B. Jørgensen & E. Jeppesen, 2011. Using chlorophyll a and cyanobacteria in the ecological classification of lakes. Ecological Indicators 11: 1403–1412.CrossRefGoogle Scholar
  78. Sterner, R. W., 2008. On the phosphorus limitation paradigm for lakes. International Review of Hydrobiology 93: 433–445.CrossRefGoogle Scholar
  79. Straškraba, M., 1999. Residence time as a key variable of reservoir limnology. In Tundisi, T. G. & M. Straškraba (eds), Theoretical Reservoir Ecology and Its Applications, International Institute of Ecology. Brazilian Academy of Sciences and Backhuys Publishers, São Carlos: 385–410.Google Scholar
  80. Thornton, K. W., 1990. Perspectives on reservoir limnology. In Thornton, K. W., B. L. Kimmel & F. E. Payne (eds), Reservoir Limnology: Ecological Perspectives. John Wiley and Sons, New York: 1–14.Google Scholar
  81. Uehlinger, V., 1964. Étude statistique des méthodes de dénombrement planctonique. Archives des Sciences, Société de Physique et d’Histoire Naturelle de Genève 17: 121–123.Google Scholar
  82. Unrein, F., I. O’Farrell, I. Izaguirre, R. Sinistro, M. S. Afonso & G. Tell, 2010. Phytoplankton response to pH rise in a N-limited floodplain lake: relevance of N2-fixing heterocystous cyanobacteria. Aquatic Sciences 72: 179–190.CrossRefGoogle Scholar
  83. Utermöhl, H., 1958. Zur Vervollkommung der quantitativen Phytoplankton - Methodik. Mitteilungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 9: 1–38.Google Scholar
  84. Vollenweider, R. A., 1976. Advances in defining critical loading levels for phosphorus in lake eutrophication. Memorie dell’Istituto Italiano di Idrobiologia 33: 53–83.Google Scholar
  85. Wetzel, R. G. & G. E. Likens, 1990. Limnological Analyses. Springer-Verlag, New York.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Luciana M. Rangel
    • 1
  • Lúcia H. S. Silva
    • 1
  • Priscila Rosa
    • 2
  • Fábio Roland
    • 2
  • Vera L. M. Huszar
    • 1
  1. 1.Laboratório de Ficologia, Museu NacionalUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Laboratório de Ecologia AquáticaUniversidade Federal de Juiz de ForaJuiz de ForaBrazil

Personalised recommendations