Skip to main content

Advertisement

Log in

Drought-induced water-level reduction favors cyanobacteria blooms in tropical shallow lakes

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

Abstract

Many arid and semiarid regions are likely to become warmer and drier by the end of this century, due to human-induced climate change. We hypothesize that a reduction in water level caused by droughts will aggravate eutrophication, leading to higher cyanobacteria biomass and dominance in tropical regions. To test this hypothesis, we analyzed physical and chemical variables and plankton communities of 40 man-made lakes in warm semiarid northeastern Brazil at the end of the wet and dry seasons. We also constructed a predictive model of cyanobacteria biovolume in these lakes. The lakes had significantly lower water volume, transparency, and CO2 concentrations but higher water temperature, water column stability, electrical conductivity, pH, suspended solids, ammonium, total nitrogen concentrations, bacteria biomass, phytoplankton biomass, and cyanobacteria biomass and dominance in the dry than in the wet season. Our regression model suggested that cyanobacteria biovolume was positively related to water column stability, pH, and total nitrogen and negatively related to water transparency and concentrations of inorganic suspended solids. These results suggest that the projected warmer and drier climate in the future will reduce water quantity and quality of man-made lakes in the region, increasing the risks of salinization, anoxia, eutrophication, and cyanobacteria blooms.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Akaike, H., 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716–723.

    Article  Google Scholar 

  • Anderson, D. R., 2008. Model Based Inference in the Life Sciences: A Primer on Evidence. Springer, New York.

    Book  Google Scholar 

  • Allende, L., G. Tell, H. Zagarese, A. Torremorell, G. Pérez, J. Bustingorry, R. Escaray & I. Izaguirre, 2009. Phytoplankton and primary production in clear-vegetated, inorganic-turbid, and algal-turbid shallow lakes from the pampa plain (Argentina). Hydrobiologia 624: 45–60.

    Article  CAS  Google Scholar 

  • Antenucci, J. P., A. Ghadouani, M. A. Burford & J. R. Romero, 2005. The long-term effect of artificial destratification on phytoplankton species composition in a subtropical reservoir. Freshw Biology 50: 1081–1093.

    Article  CAS  Google Scholar 

  • APHA, 1998. Standard Methods for the Examination of Water and Wastewater. American Public Health Association, Washington DC.

    Google Scholar 

  • Beklioglu, M., S. Romo, I. Kagalou, X. Quintana & E. Bécares, 2007. State of the art in the functioning of shallow Mediterranean lakes: workshop conclusions. Hydrobiologia 584: 317–326.

    Article  Google Scholar 

  • Bottrell, H. H., A. Duncan, Z. M. Gliwicz, E. Grygierek, A. Herzing, H. A. Ilkowska, P. Larsson & T. Weglenska, 1976. A review of some problems in zooplankton production studies. Norwegian Journal of Zoology 24: 419–456.

    Google Scholar 

  • Bouvy, M., R. Molica, S. De Oliveira, M. Marinho & B. Beker, 1999. Dynamics of a toxic cyanobacterial bloom (Cylindrospermopsis raciborskii) in a shallow reservoir in the semi-arid region of northeast Brazil. Aquatic Microbial Ecology 20: 285–297.

    Article  Google Scholar 

  • Bouvy, M., D. Falcão, M. Marinho, M. Pagano & A. Moura, 2000. Occurrence of Cylindrospermopsis (Cyanobacteria) in 39 Brazilian tropical reservoirs during 1998 drought. Aquatic Microbial Ecology 23: 13–27.

    Article  Google Scholar 

  • Branco, C. W. C. & P. A. C. Senna, 1994. Factors influencing the development of Cylindrospermopsis raciborskii and Microcystis aeruginosa in Paranoá Reservoir, Brasília, Brazil. Algological Studies 75: 85–96.

    Google Scholar 

  • Caraco, N. & R. Miller, 1998. Direct and indirect effects of CO2 on competition between a cyanobacteria and eukaryotic phytoplankton. Canadian Journal of Fisheries and Aquatic Sciences 55: 54–62.

    Article  Google Scholar 

  • Conley, D. J., H. W. Paerl, R. W. Howarth, D. F. Boesch, S. P. Seitzinger, K. E. Havens, C. Lancelot & G. E. Likens, 2009. Ecology controlling eutrophication: nitrogen and phosphorus. Science 323: 1014–1015.

    Article  CAS  PubMed  Google Scholar 

  • Cuker, B. E., P. T. Gama & J. M. Burkholder, 1990. Type of suspended clay influences lake productivity and phytoplankton community and response to phosphorus loading. Limnology and Oceanography 35: 830–839.

    Article  Google Scholar 

  • Daley, R. J. & J. E. Hobbie, 1975. Direct counts of aquatic bacteria by a modified epifluorescence technique. Limnology and Oceanography 20: 875–882.

    Article  Google Scholar 

  • de Senerpont Domis, L. N., J. J. Elser, A. S. Gsell, V. L. M. Huszar, B. W. Ibelings, E. Jeppesen, S. Kosten, W. M. Mooij, F. Roland, U. Sommer, E. Van Donk, M. Winder & M. Lürling, 2013a. Plankton dynamics under different climatic conditions in space and time. Freshwater Biology 58: 463–482.

    Article  Google Scholar 

  • de Senerpont Domis, L. N., J. J. Elser, A. S. Gsell, V. L. M. Huszar, B. W. Ibelings, E. Jeppesen, S. Kosten, W. M. Mooij, F. Roland, U. Sommer, E. Van Donk, M. Winder & M. Lürling, 2013b. Plankton dynamics under different climate conditions in tropical freshwater systems (a reply to the comment by Sarmento, Amado and Descy, 2013). Freshwater Biology 58: 2211–2213.

    Article  Google Scholar 

  • Duong, T. T., T. P. Q. Le, T.-S. Dao, S. Pflugmacher, E. Rochelle-Newall, T. K. Hoand, T. N. Vu, C. T. Ho & D. K. Dang, 2013. Seasonal variation of cyanobacteria and microcystins in the Nui Coc Reservoir, Northern Vietnam. Journal of Applied Phycology 25: 1065–1075.

    Article  CAS  Google Scholar 

  • Elliott, J. A., 2012. The seasonal sensitivity of cyanobacteria and other phytoplankton to changes in flushing rate and water temperature. Global Change Biology 16: 864–876.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Figueredo, C. C. & A. Giani, 2009. Phytoplankton community in the tropical lake of Lagoa Santa (Brazil): conditions favoring a persistent bloom of Cylindrospermopsis raciborskii. Limnologica 39: 264–272.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hobbie, J. E., R. J. Daley & S. Jasper, 1977. Use of nuclepore filters for counting bacteria by fluorescence microscopy. Applied and Environmental Microbiology 33: 1225–1228.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holland, D. P., A. Pantorno, P. T. Orr, S. Stojkovic & J. Beardall, 2012. The impacts of a high CO2 environment on a bicarbonate user: the cyanobacterium Cylindrospermopsis raciborskii. Water Research 46: 1430–1437.

    Article  CAS  PubMed  Google Scholar 

  • Huisman, J., J. Sharples, J. M. Stroom, P. M. Visser, W. E. A. Kardinaal, J. M. H. Verspagen & B. Sommeijer, 2004. Changes in turbulent mixing shift competition for light between phytoplankton species. Ecology 85: 2960–2970.

    Article  Google Scholar 

  • Huszar, V. L. M., L. H. S. Silva, M. Marinho, P. Domingos & C. L. S. Anna, 2000. Cyanoprokaryote assemblages in eight productive tropical Brazilian waters. Hydrobiologia 424: 67–77.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Hutchinson, G. E., 1957. A Treatise on Limnology: Vol. I. Geography, Physics and Chemistry. Wiley, New York.

    Google Scholar 

  • IPCC, 2013. Summary for policymakers. In Stocker, T. F., D. Qin, G. K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex & P. M. Midgley (eds), Climate Change 2013: The physical science basis. Contribution of working group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge: 3–29.

  • Isvánovics, V., H. M. Shafik, M. Présing & S. Juhos, 2000. Growth and phosphate uptake kinetics of the cyanobacterium, Cylindrospermopsis raciborskii (Cyanophyceae) in throughflow cultures. Freshwater Biology 43: 257–275.

    Article  Google Scholar 

  • Izaguirre, I., M. L. Sánchez, M. R. Schiaffino, I. O’Farrell, P. Huber, N. Ferrer, J. Zunino, L. Lagomarsino & M. Mancini, 2015. Which environmental factors trigger the dominance of phytoplankton species across a moisture gradient of shallow lakes? Hydrobiologia 752: 47–64.

    Article  Google Scholar 

  • Jeppesen, E., M. Søndergaard, E. Kanstrup & B. Petersen, 1994. Does the impact of nutrients on the biological structure and function of brackish and freshwater lakes differ? Hydrobiologia 276: 15–30.

    Article  Google Scholar 

  • Jeppensen, E., M. Søndergaard, J. P. Jensen, K. E. Havens, O. Anneville, L. Carvalho, M. F. Coveney, R. Deneker, M. T. Dokulil, B. Foy, D. Gerdeaux, S. E. Hampton, S. Hilt, K. Kangur, J. Köhler, E. H. H. R. Lammens, T. L. Lauridsen, M. Manca, M. R. Miracle, B. Moss, P. Nõges, G. Persson, G. Phillips, R. Portielje, S. Romo, C. L. Schelske, D. Straile, I. Tatrai, E. Willén & M. Winder, 2005. Lake response to reduced nutrient loading – an analysis of contemporary long-term data from 35 case studies. Freshwater Biology 50: 1747–1771.

    Article  Google Scholar 

  • Jeppesen, E., B. Kronvang, M. Meerhoff, M. Søndergaard, K. M. Hansen, H. E. Andersen, T. L. Lauridsen, M. Beklioglu, A. Özen & J. E. Olesen, 2009. Climate change effects on runoff, catchment phosphorus loading and lake ecological state, and potential adaptations. Journal of Environmental Quality 38: 1930–1941.

    Article  CAS  PubMed  Google Scholar 

  • Jeppesen, E., B. Kronvang, J. E. Olesen, J. Audet, M. Søndergaard, C. C. Hoffmann, H. E. Andersen, T. L. Lauridsen, L. Liboriussen, S. E. Larsen, M. Beklioglu, M. Meerhoff, A. Özen & K. Özkan, 2011. Climate change effects on nitrogen loading from cultivated catchments in Europe: implications for nitrogen retention, ecological state of lakes and adaptation. Hydrobiologia 663: 1–21.

    Article  CAS  Google Scholar 

  • Jeppesen, E., M. Meerhoff, T. A. Davidson, D. Trolle, M. Søndergaard, T. L. Lauridsen, M. Beklioglu, S. Brucet, P. Volta, I. González-Bergonzoni & A. Nielsen, 2014. Climate change impacts on lakes: an integrated ecological perspective based on a multi-faceted approach, with special focus on shallow lakes. Journal of Limnology 73: 88–111.

    Article  Google Scholar 

  • Jeppesen, E., S. Brucet, L. Naselli-Flores, E. Papastergiadou, K. Stefanidis, T. Nõges, P. Nõges, J. L. Attayde, T. Zohary, J. Coppens, T. Bucak, R. F. Menezes, F. R. S. Freitas, M. Kernan, M. Søndergaard & M. Beklioglu, 2015. Ecological impacts of global warming and water abstraction on lakes and reservoirs due to changes in water level and related changes in salinity. Hydrobiologia 750: 201–227.

    Article  Google Scholar 

  • Jespersen, A. M. & K. Christoffersen, 1988. Measurements of chlorophyll-a from phytoplankton using ethanol as extraction solvent. Archiv für Hydrobiologie 109: 445–454.

    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 

  • Kosten, S., V. L. M. Huszar, N. Mazzeo, M. Scheffer, L. S. S. Sternberg & E. Jeppesen, 2009. Lake and watershed characteristics rather than climate influence nutrient limitation in shallow lakes. Ecological Applications 19: 1791–1804.

    Article  PubMed  Google Scholar 

  • 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. D. 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 

  • Leal, I. R., J. M. C. Silva, M. Tabarelli & T. E. Lacher Jr, 2005. Changing the course of biodiversity conservation in the Caatinga of northeastern Brazil. Conservation Biology 19: 701–706.

    Article  Google Scholar 

  • Leão, P. N., M. T. S. D. Vasconcelos & V. M. Vasconcelos, 2009. Allelopathy in freshwater cyanobacteria. Critical Reviews in Microbiology 35: 271–282.

    Article  PubMed  Google Scholar 

  • Legendre, P. & L. Legendre, 2012. Numerical Ecology. Elsevier, Amsterdam.

    Google Scholar 

  • Lewis Jr, W. M., 2000. Basis for the protection and management of tropical lakes. Lakes Reservoirs: Research and Management 5: 35–48.

    Article  Google Scholar 

  • Lewis Jr, W. M. & W. A. Wurtsbaugh, 2008. Control of lacustrine phytoplankton by nutrients: erosion of the phosphorus paradigm. International Review of Hydrobiology 93: 446–465.

    Article  CAS  Google Scholar 

  • Loverde-Oliveira, S. M., V. L. M. Huszar, N. Mazzeo & M. Scheffer, 2009. Hydrology-driven regime shifts in a shallow tropical lake. Ecosystems 12: 807–819.

    Article  Google Scholar 

  • Lund, J. W. G., C. Kipling & E. D. Lecren, 1958. The inverted microscope method of estimating algae number and the statistical basis of estimating by counting. Hydrobiologia 11: 143–170.

    Article  Google Scholar 

  • Lürling, M. & F. van Oosterhout, 2013. Controlling eutrophication by combined bloom precipitation and sediment phosphorus inactivation. Water Research 47: 6527–6537.

    Article  PubMed  Google Scholar 

  • Lürling, M., F. Eshetu, E. J. Faassen, S. Kosten & V. L. M. Huszar, 2013. Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshwater Biology 58: 552–559.

    Article  Google Scholar 

  • Mackereth, F. J. H., J. Heron & J. F. Talling, 1978. Water Analysis: Some Revised Methods for Limnologists. Freshwater Biological Association, Cumbria.

    Google Scholar 

  • Marengo, J. A., R. Jones, L. M. Alves & M. C. Valverde, 2009. Future change of temperature and precipitation extremes in South America as derived from the PRECIS regional climate modeling system. International Journal of Climatology 29: 2241–2255.

    Article  Google Scholar 

  • Marengo, J. A., T. Ambrizzi, R. P. Rocha, L. M. Alves, S. V. Cuadra, M. C. Valverde, R. R. Torres, D. C. Santos & S. E. T. Ferraz, 2010. Future change of climate in South America in the late twenty-first century: intercomparison of scenarios from three regional climate models. Climate Dynamics 35: 1073–1097.

    Article  Google Scholar 

  • Massana, R., J. M. Gasol, P. K. Bjørnsen, N. Blackburn, A. Hagstrom, S. Hietanen, B. H. Hygum, J. Kuparinen & C. PedrosAlio, 1997. Measurement of bacterial size via image analysis of epifluorescence preparations: description of an inexpensive system and solutions to some of the most common problems. Scientia Marina 61: 397–407.

    Google Scholar 

  • Medeiros, L. C. M., A. Mattos, M. Lürling & V. Becker, 2015. Is the future blue-green or brown? The effects of extreme events on phytoplankton dynamics in a semi-arid man-made lake. Aquatic Ecology 49: 293–307.

    Article  CAS  Google Scholar 

  • Molica, R. J. R., E. J. A. Oliveira, P. V. V. C. Carvalho, A. N. S. F. Costa, M. C. C. Cunha, G. L. Melo & S. M. F. O. Azevedo, 2005. Occurrence of saxitoxins and an anatoxin-a(s)-like anticholinesterase in a Brazilian drinking water supply. Harmful Algae 4: 743–753.

    Article  CAS  Google Scholar 

  • Morris, D. P. & W. M. Lewis Jr, 1988. Phytoplankton nutrient limitation in Colorado mountain lakes. Freshwater Biology 20: 315–327.

    Article  Google Scholar 

  • Moss, B., S. Kosten, M. Meerhoff, R. W. Battarbee, E. Jeppesen, N. Mazzeo, K. Havens, G. Lacerot, Z. Liu, L. De Meester, H. Paerl & M. Scheffer, 2011. Allied attack: climate change and eutrophication. Inland Waters 1: 101–105.

    Article  Google Scholar 

  • Moss, B., E. Jeppesen, M. Søndergaard, T. L. Lauridsen & Z. Liu, 2013. Nitrogen, macrophytes, shallow lakes and nutrient limitation: resolution of a current controversy? Hydrobiologia 710: 3–21.

    Article  CAS  Google Scholar 

  • Norland, S., 1993. The relationship between biomass and volume of bacteria. In Kemp, P. F., B. F. Sherr, E. B. Sherr & J. J. Cole (eds), Aquatic Microbial Ecology. Lewis Publishers, Boca Raton: 303–307.

    Google Scholar 

  • Nürnberg, G. K., 1996. Trophic state of clear and colored, soft- and hardwater lakes with special consideration of nutrients, anoxia, phytoplankton and fish. Lake and Reservoir Management 12: 432–447.

    Article  Google Scholar 

  • 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 

  • Özen, A., B. Karapınar, I. Kucuk, E. Jeppesen & M. Beklioglu, 2010. Drought-induced changes in nutrient concentrations and retention in two shallow Mediterranean lakes subjected to different degrees of management. Hydrobiologia 646: 61–72.

    Article  Google Scholar 

  • Pace, M. L. & J. D. Orcutt Jr, 1981. The relative importance of protozoans, rotifers and crustaceans in a freshwater zooplankton community. Limnology and Oceanography 26: 822–830.

    Article  Google Scholar 

  • Padisák, J. & C. S. Reynolds, 1998. Selection of phytoplankton associations in Lake Balaton, Hungary, in response to eutrophication and restoration measures, with special reference to cyanoprokaryotes. Hydrobiologia 384: 41–53.

    Article  Google Scholar 

  • Padisák, J., W. Scheffler, P. Kasprzak, R. Koschel & L. Krienitz, 2003. Interannual variability in the phytoplankton composition of Lake Stechlin (1994-2000). Archiv für Hydrobiologie Special Issues in Advanced Limnology 58: 101–133.

    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 

  • Paerl, H. W., H. Xu, M. J. McCarthy, G. Zhu, B. Qin, Y. Li & W. S. Gardner, 2011. Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N & P) management strategy. Water Research 45: 1973–1983.

    Article  CAS  PubMed  Google Scholar 

  • Rangel, L. M., L. H. S. Silva, P. Rosa, F. Roland & V. L. M. Huszar, 2012. Phytoplankton biomass is mainly controlled by hydrology and phosphorus concentrations in tropical hydroelectric reservoirs. Hydrobiologia 693: 13–28.

    Article  CAS  Google Scholar 

  • Reynolds, C. S., 1999. Non-determinism to probability, or N: p in the community ecology of phytoplankton. Archiv für Hydrobiologie 146: 23–35.

    CAS  Google Scholar 

  • Reynolds, C. S., 2006. Ecology of Phytoplankton. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Rigosi, A., C. C. Carey, B. W. Ibelings & J. D. Brookes, 2014. The interaction between climate warming and eutrophication to promote cyanobacteria is dependent on trophic state and varies among taxa. Limnology and Oceanography 59: 99–114.

    Article  Google Scholar 

  • Romo, S., J. Soria, F. Fernández, Y. Ouahid & A. Barón-Solá, 2012. Water residence time and the dynamics of toxic cyanobacteria. Freshwater Biology 58: 513–522.

    Article  Google Scholar 

  • Ruttner-Kolisko, A., 1977. Suggestions for biomass calculation of plankton rotifers. Archiv für Hydrobiologie, Beihefte Ergebnisse der Limnologie 8: 71–76.

    Google Scholar 

  • 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 

  • Santos, A. C. 2014. Efeitos das características do uso do solo da bacia de drenagem sobre a qualidade da água e biodiversidade de ecossistemas aquáticos. Master thesis. Universidade Federal do Rio Grande do Norte, Natal.

  • Sarmento, H., A. M. Amado, J. P. Descy, et al., 2013. Climate change in tropical freshwaters (comment on the paper ‘Plankton dynamics under different climatic conditions in space and time’ by de Senerpont Domis. Freshwater Biology 58: 2208–2210.

    Article  Google Scholar 

  • Sas, H., 1989. Lake Restoration by Reduction of nutRient Loading: Expectations, Experiences, Extrapolations. Academia Verlag Richarz, St. Augustin.

    Google Scholar 

  • Scheffer, M., 1998. Ecology of Shallow Lakes. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • Scheffer, M., S. Rinaldi, A. Gragnani, L. R. Mur & E. H. van Nes, 1997. On the dominance of filamentous cyanobacteria in shallow, turbid lakes. Ecology 78: 272–282.

    Article  Google Scholar 

  • Schindler, D. W., 1977. Evolution of phosphorus limitation in lakes. Science 195: 260–262.

    Article  CAS  PubMed  Google Scholar 

  • Schindler, D. W., 2012. The dilemma of controlling cultural eutrophication of lakes. Proceedings of The Royal Society B 279: 4322–4333.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 105: 11254–11258.

    Article  CAS  Google Scholar 

  • Scott, J. T. & M. McCarthy, 2010. Nitrogen fixation may not balance the nitrogen pool in lakes over timescales relevant to eutrophication management. Limnology and Oceanography 55: 1265–1270.

    Article  CAS  Google Scholar 

  • Shapiro, J., 1990. Current beliefs regarding dominance by blue-greens: the case for the importance of CO2 and pH. Verhandlungen of Internationale Vereinigung für Theoretische und Angewandte Limnologie 24: 38–54.

    Google Scholar 

  • Smith, V. H., 1983. Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Science 221: 669–671.

    Article  CAS  PubMed  Google Scholar 

  • Smith, V. H., 1998. Cultural eutrophication of inland, estuarine, and coastal waters. In Pace, M. L. & P. M. Groffman (eds), Successes, Limitations and Frontiers in Ecosystem Science. Springer-Verlag, New York: 7–49.

    Chapter  Google Scholar 

  • Smith, V. H. & D. W. Schindler, 2009. Eutrophication science: where do we go from here? Trends in Ecology & Evolution 24: 201–207.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Soares, M. C. S., V. L. M. Huszar, M. N. Miranda, M. M. Mello, F. Roland & M. Lürling, 2013. Cyanobacterial dominance in Brazil: distribution and environmental preferences. Hydrobiologia 717: 1–12.

    Article  CAS  Google Scholar 

  • Stumm, W. & J. J. Morgan, 1996. Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters. Wiley Interscience, Hoboken.

    Google Scholar 

  • Teferi, M., S. A. J. Declerck, T. De Bie, P. Lemmens, A. Gebrekidan, T. Asmelash, T. Dejenie, K. Gebrehiwot, H. Bauer, J. A. Deckers, J. Snoeks & L. D. Meester, 2014. Strong effects of occasional drying on subsequent water clarity and cyanobacterial blooms in cool tropical reservoirs. Freshwater Biology 59: 870–884.

    Article  Google Scholar 

  • Thornton, J. A. & W. Rast, 1993. A test of hypothesis relating to the comparative limnology and assessment of eutrophication in semi-arid man-made lakes. In Straškraba, M., J. G. Tundisi & A. Duncan (eds), Comparative Reservoir Limnology and Water Quality Management. Kluwer Academic Publishers, Dordrecht: 1–24.

    Chapter  Google Scholar 

  • Uehlinger, V., 1964. Étude statistique des méthodes de dénobrement planctonique. Archives des Sciences 77: 121–123.

    Google Scholar 

  • Utermöhl, H., 1958. Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitteillungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 9: 1–38.

    Google Scholar 

  • Veraart, A. J., J. J. M. de Klein & M. Scheffer, 2011. Warming can boost denitrification disproportionately due to altered oxygen dynamics. PloS One 6(3): e18508. doi:10.1371/journal.pone.0018508.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiss, R. F., 1974. Carbon dioxide in water and seawater: the solubility of a non-ideal gas. Marine Chemistry 2: 203–215.

    Article  CAS  Google Scholar 

  • Wetzel, R. G. & G. E. Likens, 2000. LIMNOLOGICAL Analyses, Book 3. Springer-Verlag, New York.

    Book  Google Scholar 

  • Wilson, A. E., O. Sarnelle & A. R. Tillmanns, 2006. Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: meta-analyses of laboratory experiments. Limnology and Oceanography 51: 1915–1924.

    Article  Google Scholar 

  • Zar, J. H., 2010. Biostatistical Analysis, 5th ed. Prentice Hall, New Jersey.

    Google Scholar 

Download references

Acknowledgments

The authors thank the staff of the Secretaria Estadual do Meio Ambiente e dos Recursos Hídricos do Rio Grande do Norte (SEMARH), especially Celso Veiga, Gláucia Costa, Maria Pereira, Selma Silva, Antônio Paiva, Josenilton Silva, and Fernando Silva for their logistical assistance during the sampling work and for providing data from the lakes. We thank the staff of the Empresa de Pesquisa Agropecuária do Rio Grande do Norte (EMPARN) and the Companhia de Águas e Esgotos do Rio Grande do Norte for providing climatological and sewage treatment data, respectively. We are especially grateful to Fabiana Araújo and Jamila Pereira for laboratory assistance, and to Fábio Roland, Natália Noyma, Luciana Vidal, Anderson Freitas, Lúcia Lobão and Guilherme Dias for the nutrient and bacteria analyses. We thank Janet Reid for English correction. We also thank Mariana Meerhoff and two anonymous reviewers for their suggestions that helped improve the quality of the manuscript. JB was partially supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/CT-HIDRO, doctoral grant 141682/2007-8) and the Coordenadoria de Aperfeiçoamento de Pessoal Superior (CAPES/WUR, PhD sandwich scholarship grant BEX2977/09-5). VLMH was partially supported by CNPq (Grant 307727/2009-2).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jandeson Brasil.

Additional information

Handling editor: Mariana Meerhoff

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brasil, J., Attayde, J.L., Vasconcelos, F.R. et al. Drought-induced water-level reduction favors cyanobacteria blooms in tropical shallow lakes. Hydrobiologia 770, 145–164 (2016). https://doi.org/10.1007/s10750-015-2578-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-015-2578-5

Keywords

Navigation