Skip to main content

Mitigating harmful cyanobacterial blooms: strategies for control of nitrogen and phosphorus loads

Abstract

Harmful blooms of cyanobacteria (CyanoHABs) have increased globally and cyanotoxins associated with some CyanoHAB species pose serious health risks for animals and humans. CyanoHABs are sensitive to supply rates of both nitrogen and phosphorus, but sensitivity may vary among species (e.g., between diazotrophic and non-diazotrophic species) and a range of physiographic and environmental factors. A sustainable approach to manage CyanoHABs is therefore to limit the supply of nitrogen and phosphorus from catchments to receiving waters. Alternative approaches of within-lake treatment have increased risks and large capital and operational expenditure. The need to manage catchment nutrient loads will intensify with climate change, due to expected increases in nutrient remineralization rates, alteration in hydrological regimes, and increases in lake water temperature and density stratification. Many CyanoHAB species have physiological features that enable them to benefit from the effects of climate change, including positive buoyancy or buoyancy control, high replication rates at elevated water temperature, and nutrient uptake strategies adapted for the intermittency of nutrient supply with greater hydrological variability expected in the future. Greater attention needs to be focused on nonpoint sources of nutrients, including source control, particularly maintaining nitrogen and phosphorus in agricultural soils at or below agronomic optimum levels, and enhancing natural attenuation processes in water and solute transport pathways. Efforts to achieve effective catchment management and avert the dire ecological, human health and economic consequences of CyanoHABs must be intensified in an era of anthropogenically driven environmental change arising from increasing human population, climate change and agricultural intensification.

This is a preview of subscription content, access via your institution.

References

  • Abell JM, Hamilton DP, Paterson J (2011) Reducing the external environmental costs of pastoral farming in New Zealand: experiences from the Te Arawa lakes, Rotorua. Aust J Environ Manage 18:139–154

    Article  Google Scholar 

  • Ahrens TD, Beman JM, Harrison JA, Jewett PK, Matson PA (2008) A synthesis of nitrogen transformations and transfers from land to the sea in the Yaqui Valley agricultural region of northwest Mexico. Water Resour Res 44:W00A05

    Article  CAS  Google Scholar 

  • Alexander RB, Smith RA, Schwarz GE, Boyer EW, Nolan JV, Brakebill JW (2008) Differences in phosphorus and nitrogen delivery to the Gulf of Mexico from the Mississippi River basin. Environ Sci Technol 42:822–830

    CAS  PubMed  Article  Google Scholar 

  • Arheimer B, Löwgren M, Pers BC, Rosberg J (2005) Integrated catchment modeling for nutrient reduction: scenarios showing impacts, potential, and cost of measures. Ambio 34:513–520

    PubMed  Article  Google Scholar 

  • Arienzo M, Adamo P, Bianco MR, Violante P (2001) Impact of land use and urban runoff on the contamination of the Sarno River basin in southwestern Italy. Water Air Soil Poll 131:349–366

    CAS  Article  Google Scholar 

  • Bailey-Watts AE, Kirika A (1999) Poor water quality in Loch Leven (Scotland) in 1995 in spite of reduced phosphorus loadings since 1985: the influences of catchment management and inter-annual weather variation. Hydrobiologia 403:135–151

    CAS  Article  Google Scholar 

  • Baum R, Luh J, Bartram J (2013) Sanitation: a global estimate of sewerage connections without treatment and the resulting impact on MDG progress. Environ Sci Technol 47:1994–2000

    CAS  PubMed  Article  Google Scholar 

  • Benítez-Gilabert M, Alvarez-Cobelas M, Angeler DG (2010) Effects of climatic change on stream water quality in Spain. Clim Change 103:339–352

    Article  CAS  Google Scholar 

  • Borok A (1984) Oregon’s nutrient management program. Oregon Department of Environmental Quality, Oregon

    Google Scholar 

  • Boscaini A (2009) Natural and anthropogenic loads of nutrients. In: Bertin F, Bortoli A (eds) Environmental issues in Lake Garda: insights and proposals for restoration [in Italian]. ANSAC, Roma, pp 51–63

    Google Scholar 

  • Bouwman L, Klein Goldewijk K, Van Der Hoek KW, Beusen AHW, Van Vuuren DP, Willems J, Rufino MC, Stehfest E (2013) Exploring global changes in nitrogen and phosphorus cycles in agriculture induced by livestock production over the 1900–2050 period. P Natl Acad Sci USA 110:20882–20887

    CAS  Article  Google Scholar 

  • Boxall AB, Hardy A, Beulke S, Boucard T, Burgin L, Falloon PD, Haygarth PM, Hutchinson T, Kovats RS, Leonardi G, Levy LS, Nichols G, Parsons SA, Potts L, Stone D, Topp E, Turley DB, Walsh K, Wellington EM, Williams RJ (2009) Impacts of climate change on indirect human exposure to pathogens and chemicals from agriculture. Environ Health Persp 117:508–514

    CAS  Article  Google Scholar 

  • Burger DF, Hamilton DP, Pilditch CA, Gibbs MM (2007) Benthic nutrient fluxes in a eutrophic, polymictic lake. Hydrobiologia 584:13–25

    CAS  Article  Google Scholar 

  • Carey CC, Ibelings BW, Hoffmann EP, Hamilton DP, Brookes JD (2012) Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Res 46:1394–1407

    CAS  PubMed  Article  Google Scholar 

  • Carey RO, Hochmutha GJ, Martinez CJ, Boyer TH, Dukes MD, Toord GS, Cisare JL (2013) Evaluating nutrient impacts in urban watersheds: challenges and research opportunities. Environ Pollut 173:138–149

    CAS  PubMed  Article  Google Scholar 

  • Cherry KA, Shepherd M, Withers PJA, Mooney SJ (2008) Assessing the effectiveness of actions to mitigate nutrient loss from agriculture: a review of methods. Sci Total Environ 406:1–23

    CAS  PubMed  Article  Google Scholar 

  • Cline WR (2007) Global warming and agriculture. Impact estimates by country. Center for Global Development—Peter G. Peterson Institute for International Economics, Washington

    Google Scholar 

  • Codd GA, Morrison LF, Metcalf JS (2005) Cyanobacterial toxins: risk management for health protection. Toxicol Appl Pharm 203:264–272

    CAS  Article  Google Scholar 

  • Conley DJ, Paerl HW, Howarth RW, Boesch DF, Seitzinger SP, Havens KE, Lancelot C, Likens GE (2009) Controlling eutrophication: nitrogen and phosphorus. Science 323:1014–1015

    CAS  PubMed  Article  Google Scholar 

  • Correll DL (1996) The role of phosphorus in the eutrophication of receiving waters. J Environ Qual 27:261–266

    Article  Google Scholar 

  • Cullen P, Forsberg C (1988) Experiences with reducing point sources of phosphorus to lakes. Hydrobiologia 170:321–336

    CAS  Article  Google Scholar 

  • Department of Environmental Protection (2014) Multi-tiered water quality modeling program annual status eport. New York Department of Environmental Protection of Water Supply, New York

    Google Scholar 

  • Dokulil MT, Jagsch A, George G, Anneville O, Jankowski T, Wahl B, Lenhart B, Blenckner T, Teubner K (2006) Twenty years of spatially coherent deepwater warming in lakes across Europe related to the North Atlantic Oscillation. Limnol Oceanogr 51:2787–2793

    Article  Google Scholar 

  • Drewry JJ, Newham LTH, Greene RSB, Jakeman AJ, Croke BFW (2006) A review of nitrogen and phosphorus export to waterways: context for catchment modelling. Mar Freshwat Res 58:757–774

    Article  Google Scholar 

  • Dudley BJ, Spears BM, Carvalho L, Gunn IDM, May L (2012) Water quality monitoring at Loch Leven 2008–2010—Report of results. Scottish Natural Heritage Commissioned Report No. 511. Scotish Natural Heritage, Inverness

  • Dziallas C, Grossart D (2011) Increasing oxygen radicals and water temperature select for toxic Microcystis sp. PLoS One 6:e25569

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Edmondson WT (1970) Phosphorus, nitrogen, and algae in Lake Washington after diversion of sewage. Science 169:690–691

    CAS  PubMed  Article  Google Scholar 

  • Edmondson WT, Lehman JT (1991) The effect of changes in the nutrient income on the condition of Lake Washington. Limnol Oceanogr 26:1–29

    Article  Google Scholar 

  • Edmonson WT (1961) Changes in Lake Washington following an increase in the nutrient income. Verh Int Ver Limnol 14:167–175

    Google Scholar 

  • Elliott JA, May L (2007) The sensitivity of phytoplankton in Loch Leven (U.K.) to changes in nutrient load and water temperature. Freshwat Biol 53:32–41

    Google Scholar 

  • Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Bgai JT, Seabloom EW, Shurin JB, Smith JE (2009) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1124–1134

    Google Scholar 

  • Elsgaard L, Børgesen CD, Olesen JE, Siebert S, Ewert F, Peltonen-Sainio P, Rötter RP, Skjelvåg AO (2012) Shifts in comparative advantages for maize, oat, and wheat cropping under climate change in Europe. Food Addit Contam 29:1514–1526

    CAS  Article  Google Scholar 

  • Fastner J, Abella S, Litt A et al (2015) Combating cyanobacterial proliferation by avoiding or treating inflows with high P load—experiences from eight case studies. Aquat Ecol. doi:10.1007/s10452-015-9558-8

    Google Scholar 

  • Finger D, Wüest A, Bossard P (2013) Effects of oligotrophication on primary production in peri-alpine lakes. Water Resour Res 49:4700–4710

    CAS  Article  Google Scholar 

  • Galloway JN, Cowling EB, Seitzinger SP, Sokolow RH (2002) Reactive nitrogen: too much of a good thing. Ambio 31:60–66

    PubMed  Article  Google Scholar 

  • Garcia AM, Alexander RB, Arnold JG, Norfleet L, White M, Robertson DM, Schwarz G (2016) Regional effects of agricultural conservation practices on nutrient transport in the Upper Mississippi River Basin. Environ Sci Technol 50:6991–7000

    CAS  PubMed  Article  Google Scholar 

  • Gascuel-Odoux C, Aurousseau P, Durand P, Ruiz L, Molenat J (2010) The role of climate on inter-annual variation in stream nitrate fluxes and concentrations. Sci Total Environ 408:5657–5666

    CAS  PubMed  Article  Google Scholar 

  • Hamilton DP, Wood SA, Dietrich DR, Puddick J (2014) Costs of harmful blooms of freshwater cyanobacteria. In: Sharma NK, Rai AK, Stal LJ (eds) Cyanobacteria. Wiley, Hoboken, pp 245–256

    Google Scholar 

  • Harke MJ, Steffen MM, Gobler CJ, Otten TG, Wilhelm SW, Wood SA, Paerl HW (2016) Global expansion of harmful cyanobacterial blooms: diversity, ecology, causes, and controls. Harmful Algae 54:4–20

    Article  Google Scholar 

  • Havens KE, Paerl HW (2015) Climate change at a crossroad for control of harmful algal blooms. Environ Sci Technol 49:12605–12606

    CAS  PubMed  Article  Google Scholar 

  • Haynes RJ, Williams PH (1993) Nutrient cycling and soil fertility in the grazed pasture ecosystem. Adv Agron 49:119–199

    CAS  Article  Google Scholar 

  • Heaney DJC (1987) Occurrence of phosphorus and its potential remobilization in the littoral sediments of a productive English lake. Freshwat Biol 17:513–523

    Article  Google Scholar 

  • Heaney SI, Smyly WJP, Tailing JF (1986) Interactions of physical, chemical and biological processes in depth and time within a productive English lake during summer stratification. Int Rev ges Hydrobio 17:441–494

    Article  Google Scholar 

  • Her Y, Chaubey I, Frankenberger J, Smith D (2016) Effect of conservation practices implemented by USDA programs at field and watershed scales. J Soil Water Conserv 71:249–266

    Article  Google Scholar 

  • Intergovernmental Panel on Climate Change (2015) IPCC Fifth Assessment synthesis report—IPCC. IPCC, c/o World Meteorological Organization (WMO), Geneva

    Google Scholar 

  • Jacquet S, Briand J-F, Leboulanger C, Avois-Jacquet C, Oberhaus L, Tassin B, Vinçon-Leite B, Paolini G, Druart J-C, Anneville O, Humbert J-F (2005) The proliferation of the toxic cyanobacterium Planktothrix rubescens following restoration of the largest natural French lake (Lac du Bourget). Harmful Algae 4:651–672

    Article  Google Scholar 

  • Jacquet S, Kerimoglu O, Rimet F, Paolini G, Anneville O (2014) Cyanobacterial bloom termination: the disappearance of Planktothrix rubescens from Lake Bourget (France) after restoration. Freshwat Biol 59:2472–2487

    Article  Google Scholar 

  • Jarvie HP, Sharpley AN, Spears B, Buda AR, May L, Kleinman PJA (2013) Water quality remediation faces unprecedented challenges from “legacy phosphorus”. Environ Sci Technol 47:8997–8998

    CAS  PubMed  Article  Google Scholar 

  • Jensen HS, Andersen FO (1992) Importance of temperature, nitrate and pH for phosphate release from aerobic sediments of four shallow, eutrophic lakes. Limnol Oceanogr 37:577–589

    Article  Google Scholar 

  • Jeppesen E, Kronvang B, MeerhoffM Søndergaard M, Hansen KM, Andersen HE, Lauridsen TL, Liboriussen L, Beklioglu M, Özen A, Olesen JE (2009) Climate change effects on runoff, catchment phosphorus loading and lake ecological state, and potential adaptations. J Environ Qual 38:1930–1941

    CAS  PubMed  Article  Google Scholar 

  • Jeppesen E, Kronvang B, Olesen JE, Audet J, Søndergaard M, Hoffmann CC, Andersen HE, Lauridsen TL, Liboriussen L, Larsen SE, Beklioglu M, Meerhoff M, Özen A, Özkan K (2010) 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 

  • Jiménez Cisneros BE, Oki T, Arnell NW et al (2014) Freshwater resources. In: Field CB, Barros VR, Dokken DJ et al (eds) Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA. pp 229–269

  • Kartal B, Kuenen GJ, van Loosdrecht MCM (2010) Sewage treatment with anammox. Science 328:702–703

    CAS  PubMed  Article  Google Scholar 

  • Katsiapi M, Mazaris AD, Charalampous E, Moustaka-Gouni M (2012) Watershed land use types as drivers of freshwater phytoplankton structure. Hydrobiologia 698:121–131

    CAS  Article  Google Scholar 

  • Kingwell R (2006) Climate change in Australia: agricultural impacts and adaptation. Australasian Agribusiness Review 14: Paper 1

  • Kleinman PJA, Sharpley AN, McDowell RW, Flaten DN, Buda AR, Tao L, Bergstrom L, Zhu Q (2011) Managing agricultural phosphorus for water quality protection: principles for progress. Plant Soil 349:169–182

    CAS  Article  Google Scholar 

  • Knight RL, Walton WE, O’Meara GF, Reisend WK, Wasse R (2003) Strategies for effective mosquito control in constructed treatment wetlands. Ecol Eng 21:211–232

    Article  Google Scholar 

  • Kohler J, Hilt S, Adrian R, Nicklisch A, Kozerski HP, Walz N (2005) Long-term response of a shallow, moderately flushed lake to reduced external phosphorus and nitrogen loading. Freshwat Biol 50:1639–1650

    Article  CAS  Google Scholar 

  • Kosten S, Huszar VLM, Mazzeo N, Scheffer M, Sternberg SL, Jeppesen E (2009) Lake and watershed characteristics rather than climate influence nutrient limitation in shallow lakes. Ecol Appl 19:1791–1804

    PubMed  Article  Google Scholar 

  • Kpodonu ATKN, Hamilton DP, Hartland A, Laughlin DC, Lusk CH (2016) Coupled use of sediment phosphorus speciation and pigment composition to infer phytoplankton phenology over 700 years in a deep oligotrophic lake. Biochemistry. doi:10.1007/s10533-016-0227-3

    Google Scholar 

  • Kristiana R, Vilhena LC, Begg G, Antenucci JP, Imberger J (2011) The management of Lake Burragorang in a changing climate: the application of the Index of Sustainable Functionality. Lake Reserve Manage 27:70–86

    Article  Google Scholar 

  • Lang U, Schick R, Schröder G (2010) The decision support system Bodenseeonline for hydrodynamics and water quality in Lake Constance. In: Devlin R (ed) Decision support systems, advances in. Intech, Croatia, pp 81–98

    Google Scholar 

  • Lewis WM, Wurtsbaugh WA, Paerl HW (2011) Rationale for control of anthropogenic nitrogen and phosphorus in inland waters. Environ Sci Technol 45:10030–10035

    Article  CAS  Google Scholar 

  • Liu AJ, Goodrich JA, Tong SY (2000) Land use as a mitigation strategy for the water quality impacts of global warming: a scenario analysis on two watersheds in the Ohio River basin. Environ Eng Policy 2:65–76

    Google Scholar 

  • Løvik JE, Kjellberg G (2003) Long-term changes of the crustacean zooplankton community in Lake Mjøsa, the largest lake in Norway. J Limnol 62:143–150

    Article  Google Scholar 

  • Mackay EB, Maberly SC, Pan G, Reitzel K, Bruere A, Corker N, Douglas G, Egemose S, Hamilton D, Hatton-Ellis T, Huser B, Li W, Meis S, Moss B, Lürling M, Phillips G, Yasseri S, Spears BM (2014) Geoengineering in lakes: welcome attraction or fatal distraction? Inland Waters 4:349–356

    Article  Google Scholar 

  • Matthijs HC, Visser PM, Reeze B, Meeuse J, Slot PC, Wijn G, Talens R, Huisman J (2012) Selective suppression of harmful cyanobacteria in an entire lake with hydrogen peroxide. Water Res 46(5):1460–1472

    CAS  PubMed  Article  Google Scholar 

  • McComas S (2003) Lake and pond management guidebook, 1st edn. CRC Press, Taylor and Francis, Boca Raton

    Google Scholar 

  • McDowell RW, Houlbrooke DJ (2009) Management options to decrease phosphorus and sediment losses from irrigated cropland grazed by cattle and sheep. Soil Use Manage 25:224–233

    Article  Google Scholar 

  • McDowell RD, Moreau P, Salmon-Monviola J, Durand P, Letermee P, Merot P (2014) Contrasting spatial management of nitrogen and phosphorus for improved water quality: modelling studies in Nw Zealand and France. Eur J Agron 57:52–61

    CAS  Article  Google Scholar 

  • Michalak AM, Anderson EJ, Beletsky D, Boland S, Bosche S, Bridgeman TB, Chaffin JD, Chog K, Confesor R, Daloğlu I, DePinto JV, Evans MA, Fahnenstiel GL, Hek L, Hol JC, Jenkins L, Johengen TH, Kuod KC, LaPorten E, Liud X, McWilliams MR, Moore MR, Posselt DJ, Richards RP, Scavia D, Steiner AL, Verhammei E, Wright DM, Zagorski MA (2013) Record-setting algal bloom in Lake Erie caused by agricultural and meteorological trends consistent with expected future conditions. P Natl Acad Sci USA 110:6448–6452

    CAS  Article  Google Scholar 

  • Mino T (2000) Microbial selection of polyphosphate-accumulating bacteria in activated sludge wastewater treatment processes for enhanced biological phosphate removal. Biochemistry (Moscow) 65:341–348

    CAS  Google Scholar 

  • Molina-Navarro E, Trolle D, Martínez-Pérez S, Jeppesen E (2014) Hydrological and water quality impact assessment of a Mediterranean limno-reservoir under climate change and land use management scenarios. J Hydrol 509:354–366

    Article  Google Scholar 

  • Morée AL, Beusen AHW, Bouwman AF, Willems WJ (2013) Exploring global nitrogen and phosphorus flows in urban wastes during the twentieth century. Glob Biogeochem Cycl 27:836–846

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Muñoz-Huerta RF, Guevara-Gonzalez RG, Contreras-Medina LM, Torres-Pacheco I, Prado-Olivarez J, Ocampo-Velazquez RV (2013) A review of methods for sensing the nitrogen status in plants: advantages, disadvantages and recent advances. Sensors 13:10823–10843

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • O’Neil JM, Davis TW, Burford MA, Gobler CJ (2012) The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14:313–334

    Article  CAS  Google Scholar 

  • O’Reilly CM, Sharma S, Gray DK et al (2015) Rapid and highly variable warming of lake surface waters around the globe. Geophys Res Lett 42:GL066235

    Google Scholar 

  • OECD (1982) Eutrophication of Waters. Monitoring, Assessment and Control. Organisation for Economic Co-Operation and Development, Paris

    Google Scholar 

  • Oldham WK, Stevens GM (1984) Initial operating experiences of nutrient removal process (modified Bardenpho) at Kelowna, British Columbia. Can J Civil Eng 11:474–479

    Article  Google Scholar 

  • Olesen JE (2005) Climate change and CO2 effects on productivity of Danish agricultural systems. J Crop Improv 13:257–274

    CAS  Article  Google Scholar 

  • Olesen JE, Rubæk GH, Heidmann T, Hansen S, Børgensen CD (2004) Effect of climate change on greenhouse gas emissions from arable crop rotations. Nut Cycl Agroecosys 70:147–160

    CAS  Article  Google Scholar 

  • Olesen JE, Carter TR, Díaz-Ambrona CH et al (2007) Uncertainties in projected impacts of climate change on European agriculture and terrestrial ecosystems based on scenarios from regional climate models. Clim Change 81:123–143

    Article  Google Scholar 

  • Paerl HW, Huisman J (2008) Blooms like it hot. Science 320:57–58

    CAS  PubMed  Article  Google Scholar 

  • Paerl HW, Huisman J (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1:27–37

    CAS  PubMed  Article  Google Scholar 

  • Paerl HW, Otten TG (2016) Duelling “CyanoHABs”: unravelling the environmental drivers controlling dominance and succession among diazotrophic and non-N2 -fixing harmful cyanobacteria. Environ Microbiol 18:316–324

    CAS  PubMed  Article  Google Scholar 

  • Paerl HW, Gardner WS, Havens KE, Joyner AR, McCarthy MJ, Newell SE, Qin B, Scott JT (2016) Mitigating cyanobacterial harmful algal blooms in aquatic ecosystems impacted by climate change and anthropogenic nutrients. Harmful Algae 54:213–222

    Article  Google Scholar 

  • Park S-R, Lee H-J, Lee S-W, Hwanga S-J, Byeona M-S, Jooa G-J, Jeonga K-S, Konga D-S, Kim M-C (2011) Relationships between land use and multi-dimensional characteristics of streams and rivers at two different scales. Ann Limnol—Int J Lim 47:S107–S116

    Article  Google Scholar 

  • Paul WJ, Hamilton DP, Ostrovsky I, Miller SD, Zhang A, Muraoka K (2012) Catchment land use and trophic state impacts on phytoplankton composition: a case study from the Rotorua lakes’ district, New Zealand. Hydrobiologia 698:133–146

    CAS  Article  Google Scholar 

  • Pienitz R, Roberge K, Vincent WF (2006) Three hundred years of human-induced change in an urban lake: paleolimnological analysis of Lac Saint-Augustin, Que´bec City, Canada. Can J Bot 84:303–320

    CAS  Article  Google Scholar 

  • Pierson DC, Samal N, Owens E, Schneiderman EM, Zion MS (2013) Changes in the timing of snowmelt, and the seasonality of nutrient loading: can models simulate the impacts on freshwater trophic status? Hydrol Process 27:3083–3093

    CAS  Article  Google Scholar 

  • Prasuhn V, Sieber U (2005) Changes in diffuse phosphorus and nitrogen inputs into surface waters in the Rhine watershed in Switzerland. Aquat Sci 67:363–371

    CAS  Article  Google Scholar 

  • Proestos Y, Christophides GK, Ergüler K, Tanarhte M, Waldock J, Lelieveld J (2015) Present and future projections of habitat suitability of the Asian tiger mosquito, a vector of viral pathogens, from global climate simulation. Philos T R Soc Lon B, Biol Sci 370:20130554

    Article  Google Scholar 

  • Quinn JM, Stroud MJ (2002) Water quality and sediment and nutrient export from New Zealand hill-land catchments of contrasting land use. N Zeal J Mar Freshw Res 36:409–429

    CAS  Article  Google Scholar 

  • Rasouli S, Whalen JK, Madramootoo CA (2014) Review: reducing residual soil nitrogen losses from agroecosystems for surface water protection in Quebec and Ontario, Canada: Best management practices, policies and perspectives. Can J Soil Sci 94:109–127

    CAS  Article  Google Scholar 

  • Reddy KR, Newman S, Osborne TZ, White JR, Fitz HC (2011) Phosphorus cycling in the greater Everglades ecosystem: legacy phosphorus implications for management and restoration. Crit Rev Env Sci Tec 41:149–186

    CAS  Article  Google Scholar 

  • Romo S, Villena M-J, Sahuquillo M, Soria JM, Giménez M, Alfonson T, Vicente E, Mirale MR (2005) Response of a shallow Mediterranean lake to nutrient diversion: does it follow similar patterns as in northern shallow lakes? Freshwat Biol 50:1706–1717

    CAS  Article  Google Scholar 

  • Ryding S-O, Rast W (1989) The control of eutrophication of lakes and reservoirs. UNESCO and The Parthenon Publishing Group, Paris

    Google Scholar 

  • Salmaso N, Cerasino L (2012) Long-term trends and fine year-to-year tuning of phytoplankton in large lakes are ruled by eutrophication and atmospheric modes of variability. Hydrobiologia 698:17–28

    CAS  Article  Google Scholar 

  • Salmaso N, Naselli-Flores L, Padisák J (2012) Impairing the largest and most productive forest on our planet: how do human activities impact phytoplankton? Hydrobiologia 698:375–384

    Article  Google Scholar 

  • Salmaso N, Naselli-Flores L, Padisák J (2015) Functional classifications and their application in phytoplankton ecology. Freshwat Biol 60:603–619

    Article  Google Scholar 

  • Schindler DW (2006) Recent advances in the understanding and management of eutrophication. Limnol Oceanogr 51:356–363

    Article  Google Scholar 

  • Schindler DW, Hecky RE, FindlayDL StaintonMP, Parker BR, Paterson M, Beaty KG, Lyng M, Kasian SEM (2008) Eutrophication of lakes cannot be controlled by reducing nitrogen input: results of a 37 year whole ecosystem experiment. P Natl Acad Sci USA 105:11254–11258

    CAS  Article  Google Scholar 

  • Schneider P, Hook SJ (2010) Space observations of inland water bodies show rapid surface warming since 1985. Geophys Res Lett 37:GL045059

    Article  Google Scholar 

  • Schoumansa OF, Chardona WJ, Bechmann ME, Gascuel-Odoux C, Hofmand G, Kronvange B, Rubækf GH, Uléng B, Doriozh J-M (2014) Mitigation options to reduce phosphorus losses from the agricultural sector and improve surface water quality: a review. Sci Total Environ 468–469:1255–1266

    Article  CAS  Google Scholar 

  • Sedlak RI (1991) Phosphorus and nitrogen removal from municipal wastewater: principles and practice, 2nd edn. CRC Press, Boca Raton

    Google Scholar 

  • Sharpley AN, Chapra SC, Wedepohl R, Sims JT, Daniel TC, Reddy KR (1994) Managing agricultural phosphorus for protection of surface waters: issues and options. J Environ Qual 23:437–451

    CAS  Article  Google Scholar 

  • Shimoda Y, Arhonditsis GB (2016) Phytoplankton functional type modelling: running before we can walk? A critical evaluation of the current state of knowledge. Ecol Modell 320:29–43

    CAS  Article  Google Scholar 

  • Smith VH, Wood SA, McBride CG, Atalah J, Hamilton DP, Abell J (2016) Phosphorus and nitrogen loading restraints are essential for successful eutrophication control of Lake Rotorua, New Zealand. Inland Waters 6:273–283

    Article  Google Scholar 

  • Spears BM, Maberly SC, Pan G, Mackay E, Bruere A, Corker N, Douglas G, Egemose S, Hamilton D, Hatton-Ellis T, Huser B, Li W, Meis S, Moss B, Lürling M, Phillips G, Yasseri S, Reitzel K (2014) Geo-engineering in lakes: a crisis of confidence? Environ Sci Technol 48:9977–9979

    CAS  PubMed  Article  Google Scholar 

  • Stern N (2006) Stern review on the economics of climate change. Cambridge University Press, London

    Google Scholar 

  • Sukenik A, Hadas O, Kaplan A, Quesada A (2012) Invasion of Nostocales (cyanobacteria) to subtropical and temperate freshwater lakes—Physiological, regional, and global driving forces. Front Microbiol 3:86

    PubMed  PubMed Central  Article  Google Scholar 

  • Takacs I, Murthy S, Smith S, McGrath M (2006) Chemical phosphorus removal to extremely low levels: experience at two plants in the Washington, D.C. area. Water Sci Technol 53:21–28

    CAS  PubMed  Article  Google Scholar 

  • Tiemeyer B, Kahle P (2014) Nitrogen and dissolved organic carbon (DOC) losses from an artificially drained grassland on organic soils. Biogeosciences 11:4123–4137

    CAS  Article  Google Scholar 

  • Trájer A, Farkas-Iványi K, Padisák J (2015) Area-based historical modeling of the effects of the river bank regulation on the potential abundance of eleven mosquito species in the River Danube between Hungary and Slovakia. Adv Oceanogr Limnol. doi:10.4081/aiol.2015.5439

    Google Scholar 

  • Trolle D, Skovgaard H, Jeppesen E (2008) The Water Framework Directive: setting the phosphorus loading target for a deep lake in Denmark using the 1D lake ecosystem model DYRESM–CAEDYM. Ecol Model 219:138–152

    CAS  Article  Google Scholar 

  • Trolle D, Hamilton DP, Pilditch CA, Duggan IC, Jeppesen E (2011) Predicting the effects of climate change on trophic status of three morphologically varying lakes: implications for lake restoration and management. Environ Modell Softw 26:354–370

    Article  Google Scholar 

  • United Nations (2014) Population facts. United Nations Department of Economic and Social Affairs Population Division No. 2014/3. www.un.org/en/development/desa/population/publications/pdf/popfacts/PopFacts_2014-3.pdf

  • US Environmental Protection Agency (2007) Fact sheets on biological nutrient removal processes and costs. EPA-823-R-07-002. Washington, DC

  • Van Drecht G, Bouwman AF, Harrison J, Knoop JM (2009), Global nitrogen and phosphate in urban wastewater for the period 1970 to 2050, Global Biogeochem Cycl 23:03

  • Van Drecht G, Bouwman AF, Harrison J, Knoop JM (2009b) Global nitrogen and phosphate in urban wastewater for the period 1970 to 2050. Global Biogeochem Cycl 23:GB0A03

    Google Scholar 

  • Wang L, Lyons J, Kanehl P, Bannerman R (2001) Impacts of urbanization on stream habitat and fish across multiple spatial scales. Env Manage 28:255–266

    CAS  Article  Google Scholar 

  • White I (2010) Water and the city: risk, resilience and planning for a sustainable future. Routledge, London

    Google Scholar 

  • Wilson D, Hisdal H, Lawrence D (2010) Has streamflow changed in the Nordic countries?—Recent trends and comparisons to hydrological projections. J Hydrol 394:334–346

    Article  Google Scholar 

  • Wood SA, Puddick J, Borges H, Dietrich DR, Hamilton DP (2015) Potential effects of climate change on cyanobacterial toxin production. In: Botana LM, Louzao C, Vilarino N (eds) Climate change and marine and freshwater toxins. Walter de Gruyter Publishers, Berlin

    Google Scholar 

  • Zhu M, Paerl HW, Zhu G, Wu T, Li W, Shi K, Zhao L, Zhang Y, Qin B, Caruso AM (2014) The role of tropical cyclones in stimulating cyanobacterial (Microcystis spp.) blooms in hypertrophic Lake Taihu. China. Harmful Algae 39:310–321

    Article  Google Scholar 

Download references

Acknowledgments

DPH acknowledges support from the New Zealand Ministry of Business, Innovation and Employment (UOWX1503; Enhancing the health and resilience of New Zealand lakes) and the Royal Society of New Zealand International Research Staff Exchange Scheme Fellowship (MEAT Agreement 295223). HWP was supported by the US National Science Foundation (Projects 1230543, and 1240851) and the Chinese Ministry of Science and Technology (Contract 2014zx07101-011).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David P. Hamilton.

Additional information

Guest editors: Petra M. Visser, Bas W. Ibelings, Jutta Fastner and Myriam Bormans/Cyanobacterial blooms. Ecology, prevention, mitigation and control.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hamilton, D.P., Salmaso, N. & Paerl, H.W. Mitigating harmful cyanobacterial blooms: strategies for control of nitrogen and phosphorus loads. Aquat Ecol 50, 351–366 (2016). https://doi.org/10.1007/s10452-016-9594-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10452-016-9594-z

Keywords

  • CyanoHABs
  • Nitrogen
  • Phosphorus
  • Lakes
  • Climate change
  • Land use change
  • Cyanotoxins