Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Mitigating a global expansion of toxic cyanobacterial blooms: confounding effects and challenges posed by climate change

Hans W. Paerl A B F , Karl. E. Havens C , Nathan. S Hall A , Timothy G. Otten D , Mengyuan Zhu E , Hai Xu E , Guangwei Zhu E and Boqiang Qin E
+ Author Affiliations
- Author Affiliations

A Institute of Marine Sciences, University of North Carolina at Chapel Hill, 3431 Arendell Street, Morehead City, NC 28557, USA.

B College of Environment, Hohai University, 1 Xikang Road, Nanjing, 210098, PR China.

C Florida Sea Grant and University of Florida Institute of Food and Agricultural Sciences, Gainesville, FL 32611, USA.

D Bend Genetics, Sacramento, CA 95825, USA.

E State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, 210008, PR China.

F Corresponding author. Email: hpaerl@email.unc.edu

Marine and Freshwater Research 71(5) 579-592 https://doi.org/10.1071/MF18392
Submitted: 16 October 2018  Accepted: 11 January 2019   Published: 26 March 2019

Abstract

Managing and mitigating the global expansion of toxic cyanobacterial harmful algal blooms (CyanoHABs) is a major challenge facing researchers and water resource managers. Various approaches, including nutrient load reduction, artificial mixing and flushing, omnivorous fish removal, algaecide applications and sediment dredging, have been used to reduce bloom occurrences. However, managers now face the additional challenge of having to address the effects of climate change on watershed hydrological and nutrient load dynamics, water temperature, mixing regime and internal nutrient cycling. Rising temperatures and increasing frequencies and magnitudes of extreme weather events, including tropical cyclones, extratropical storms, floods and droughts, all promote CyanoHABs and affect the efficacy of ecosystem remediation measures. These climatic changes will likely require setting stricter nutrient (including both nitrogen and phosphorus) reduction targets for bloom control in affected waters. In addition, the efficacy of currently used methods to reduce CyanoHABs will need to be re-evaluated in light of the synergistic effects of climate change with nutrient enrichment.

Additional keywords: cyanobacterial harmful algal bloom dynamics, CyanoHAB dynamics, mitigation and management strategies, nutrients.


References

Bachmann, R. L., Hoyer, M. V., Vinzon, S. B., and Canfield, D. E. (2005). The origin of the fluid mud layer in Lake Apopka. Limnology and Oceanography 50, 629–635.
The origin of the fluid mud layer in Lake Apopka.Crossref | GoogleScholarGoogle Scholar |

Backer, L., Manassaram-Baptiste, D., LePrell, R., and Bolton, B. (2015). Cyanobacteria and algae blooms: review of health and environmental data from the harmful algal bloom-related illness surveillance system (HABISS) 2007–2011. Toxins 7, 1048–1064.
Cyanobacteria and algae blooms: review of health and environmental data from the harmful algal bloom-related illness surveillance system (HABISS) 2007–2011.Crossref | GoogleScholarGoogle Scholar | 25826054PubMed |

Bouvy, M., Molica, R. M., De Oliveira, S., Marinho, M., and Beker, M. (1999). Dynamics of a toxic cyanobacterial bloom (Cylindrospermopsis raciborskii) in a shallow reservoir in the semi-arid region of northern Brazil. Aquatic Microbial Ecology 20, 285–297.
Dynamics of a toxic cyanobacterial bloom (Cylindrospermopsis raciborskii) in a shallow reservoir in the semi-arid region of northern Brazil.Crossref | GoogleScholarGoogle Scholar |

Bouvy, M., Falcao, D., Marinho, M., Pagano, M., and Moura, A. (2000). Occurrence of Cylindrospermopsis (Cyanobacteria) in 39 Brazilian tropical reservoirs during the 1998 drought. Aquatic Microbiology 23, 13–27.
Occurrence of Cylindrospermopsis (Cyanobacteria) in 39 Brazilian tropical reservoirs during the 1998 drought.Crossref | GoogleScholarGoogle Scholar |

Bozarth, C. S., Schwartz, A. D., Shepardson, J. W., Colwell, F. S., and Dreher, T. W. (2010). Population turnover in a Microcystis bloom results in predominantly nontoxigenic variants late in the season. Applied and Environmental Microbiology 76, 5207–5213.
Population turnover in a Microcystis bloom results in predominantly nontoxigenic variants late in the season.Crossref | GoogleScholarGoogle Scholar | 20543038PubMed |

Briand, E., Bormans, M., Quiblier, C., Salençon, M. J., and Humbert, J. F. (2012). Evidence of the cost of the production of microcystins by Microcystis aeruginosa under differing light and nitrate environmental conditions. PLoS One 7, e29981.
Evidence of the cost of the production of microcystins by Microcystis aeruginosa under differing light and nitrate environmental conditions.Crossref | GoogleScholarGoogle Scholar | 22276137PubMed |

Bullerjahn, G. S., McKay, R. M., Davis, T. W., Baker, D. B., Boyer, G. L., D’Anglada, L. V., Doucette, G. J., Ho, J. C., Irwin, E. G., Kling, C. L., Kudela, R. M., Kurmayer, R., Michalak, A. M., Ortiz, J. D., Otten, T. G., Paerl, H. W., Qin, B., Sohngen, B. L., Stumpf, R. P., Visser, P. M., and Wilhelm, S. W. (2016). Global solutions to regional problems: collecting global expertise to address the problem of harmful cyanobacterial blooms. A Lake Erie case study. Harmful Algae 54, 223–238.
Global solutions to regional problems: collecting global expertise to address the problem of harmful cyanobacterial blooms. A Lake Erie case study.Crossref | GoogleScholarGoogle Scholar | 28073479PubMed |

Burch, M. D., Baker, P. D., Steffensen, D., Bursill, D. B., Bain, D. B., Ganf, G. G., and Brookes, J. D. (1994). Critical flow and blooms of the cyanobacterium Anabaena circinalis in the River Murray, South Australia. In ‘Proceedings of Environmental Flows Seminar’, 25–26 August 1994, Canberra, ACT, Australia. pp. 44–51. (Australian Water and Wastewater Association: Sydney, NSW, Australia.)

Cai, W., Santoso, A., Wang, G., Yeh, S. W., An, S. I., Cobb, K., Collins, M., Guilyardi, E., Jin, F. F., Kug, J. S., Lengaigne, M., McPhaden, M. J., Takahashi, K., Timmermann, A., Vecchi, G., Watanabe, M., and Wu, L. (2015). ENSO and greenhouse warming. Nature Climate Change 5, 849–859.
ENSO and greenhouse warming.Crossref | GoogleScholarGoogle Scholar |

Carmichael, W. W. (2001). Health effects of toxin producing cyanobacteria: the cyanoHABs. Human and Ecological Risk Assessment 7, 1393–1407.
Health effects of toxin producing cyanobacteria: the cyanoHABs.Crossref | GoogleScholarGoogle Scholar |

Chaffin, J. D., Bridgeman, T. B., and Bade, D. L. (2013). Nitrogen constrains the growth of late summer cyanobacterial blooms in Lake Erie. Advances in Microbiology 3, 16–26.
Nitrogen constrains the growth of late summer cyanobacterial blooms in Lake Erie.Crossref | GoogleScholarGoogle Scholar |

Chorus, I., and Bartram, J. (Eds) (1999). ‘Toxic Cyanobacteria in Water.’ (E&F Spon: London, UK.)

Conley, D. J., Bonsdorff, E., Carstensen, J., Destouni, G., Gustafsson, B. G., Hansson, L. A., Rabalais, N. N., Voss, M., and Zillén, L. (2009a). Tackling hypoxia in the Baltic Sea: is engineering a solution? Environmental Science & Technology 43, 3407–3411.
Tackling hypoxia in the Baltic Sea: is engineering a solution?Crossref | GoogleScholarGoogle Scholar |

Conley, D. J., Paerl, H. W., Howarth, R. W., Boesch, D. F., Seitzinger, S. P., Havens, K. E., Lancelot, C., and Likens, G. E. (2009b). Controlling eutrophication: nitrogen and phosphorus. Science 323, 1014–1015.
Controlling eutrophication: nitrogen and phosphorus.Crossref | GoogleScholarGoogle Scholar | 19229022PubMed |

Cooke, G. D., Welch, E. B., Peterson, S. A., and Newroth, P. R. (1993). ‘Restoration and Management of Lakes and Reservoirs.’ 2nd edn. (Lewis Publishers: Boca Raton, FL, USA.)

Cózar, A., Bruno, M., Bergamino, N., Ubeda, B., Bracchini, L., Dattilo, A. M., and Loiselle, S. (2012). Basin-scale control on the phytoplankton biomass in Lake Victoria, Africa. PLoS One 7, e29962.
Basin-scale control on the phytoplankton biomass in Lake Victoria, Africa.Crossref | GoogleScholarGoogle Scholar | 22253837PubMed |

Cronberg, G. (1982). Changes in the phytoplankton of Lake Trummen induced by restoration. Hydrobiologia 86, 185–193.
Changes in the phytoplankton of Lake Trummen induced by restoration.Crossref | GoogleScholarGoogle Scholar |

Davis, T. W., Harke, M. J., Marcoval, M. A., Goleski, J., Orano-Dawson, C., Berry, D. L., and Gobler, C. J. (2010). Effects of nitrogenous compounds and phosphorus on the growth of toxic and nontoxic strains of Microcystis during cyanobacterial blooms. Aquatic Microbial Ecology 61, 149–162.
Effects of nitrogenous compounds and phosphorus on the growth of toxic and nontoxic strains of Microcystis during cyanobacterial blooms.Crossref | GoogleScholarGoogle Scholar |

Davis, T. W., Bullerjahn, G. S., Tuttle, T., McKay, R. M., and Watson, S. B. (2015). Effects of increasing nitrogen and phosphorus concentrations on phytoplankton community growth and toxicity during planktothrix blooms in Sandusky Bay, Lake Erie. Environmental Science & Technology 49, 7197–7207.
Effects of increasing nitrogen and phosphorus concentrations on phytoplankton community growth and toxicity during planktothrix blooms in Sandusky Bay, Lake Erie.Crossref | GoogleScholarGoogle Scholar |

Dodds, W. K., and Smith, V. H. (2016). Nitrogen, phosphorus, and eutrophication in streams. Inland Waters 6, 155–164.
Nitrogen, phosphorus, and eutrophication in streams.Crossref | GoogleScholarGoogle Scholar |

Dodds, W. K., Bouska, W. W., Eitzmann, J. L., Pilger, T. J., Pitts, K. L., Riley, A. J., Schloesser, J. T., and Thornburgh, D. J. (2009). Eutrophication of US freshwaters: analysis of potential economic damages. Environmental Science & Technology 43, 12–19.
Eutrophication of US freshwaters: analysis of potential economic damages.Crossref | GoogleScholarGoogle Scholar |

Douglas, G. B., Adeney, J. A., and Robb, M. (1999). A novel technique for reducing bioavailable phosphorus in water and sediments. International Association of Water Quality Diffuse Pollution Conference 1999, 517–523.

Egemose, S., Reitzel, K., Andersen, F., and Flindt, M. R. (2010). Chemical lake restoration products: sediment stability and phosphorous dynamics. Environmental Science & Technology 44, 985–991.
Chemical lake restoration products: sediment stability and phosphorous dynamics.Crossref | GoogleScholarGoogle Scholar |

Elmgren, R., and Larsson, U. (2001). Nitrogen and the Baltic Sea: managing nitrogen in relation to phosphorus. Scientific World 1, 371–377.
Nitrogen and the Baltic Sea: managing nitrogen in relation to phosphorus.Crossref | GoogleScholarGoogle Scholar |

Elser, J. J., Bracken, M. E. S., Cleland, E. E., Gruner, D. S., Harpole, W. S., Hillebrand, H., Bgai, J. T., Seabloom, E. W., Shurin, J. B., and Smith, J. E. (2007). Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10, 1135–1142.
Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems.Crossref | GoogleScholarGoogle Scholar | 17922835PubMed |

Flores, E., and Herrero, A. (2005). Nitrogen assimilation and nitrogen control in cyanobacteria. Biochemical Society Transactions 33, 164–167.
Nitrogen assimilation and nitrogen control in cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 15667295PubMed |

Fogg, G. E. (1969). The physiology of an algal nuisance. Proceedings of the Royal Society of London. Series B, Biological Sciences 173, 175–189.

Foy, R. H., Gibson, C. E., and Smith, R. V. (1976). The influence of day length, light intensity and temperature on the growth rates of planktonic blue-green algae. British Psychological Journal 11, 151–163.
The influence of day length, light intensity and temperature on the growth rates of planktonic blue-green algae.Crossref | GoogleScholarGoogle Scholar |

Galloway, J. N., Cowling, E. B., Seitzinger, S. P., and Sokolow, R. H. (2002). Reactive nitrogen: too much of a good thing. Ambio 31, 60–63.
Reactive nitrogen: too much of a good thing.Crossref | GoogleScholarGoogle Scholar | 12078010PubMed |

Haghseresht, F., Wang, S., and Do, D. D. (2009). A novel lanthanum-modified bentonite, Phoslock, for phosphate removal from wastewaters. Applied Clay Science 46, 369–375.
A novel lanthanum-modified bentonite, Phoslock, for phosphate removal from wastewaters.Crossref | GoogleScholarGoogle Scholar |

Harke, M. J., Steffen, M. M., Gobler, C. J., Otten, T. G., Wilhelm, S. W., Wood, S. A., and Paerl, H. W. (2016). A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae 54, 4–20.
A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp.Crossref | GoogleScholarGoogle Scholar | 28073480PubMed |

Havens, K. E., and Ji, G. (2018). Multiyear oscillations in depth affect water quality in Lake Apopka. Inland Waters 8, 1–9.
Multiyear oscillations in depth affect water quality in Lake Apopka.Crossref | GoogleScholarGoogle Scholar |

Havens, K. E., Fukushima, T., Xie, P., Iwakuma, T., James, R. T., Takamura, N., Hanazato, T., and Yamamoto, T. (2001). Nutrient dynamics and the eutrophication of shallow lakes Kasumigaura (Japan), Donghu (PR China), and Okeechobee (USA). Environmental Pollution 111, 263–272.
Nutrient dynamics and the eutrophication of shallow lakes Kasumigaura (Japan), Donghu (PR China), and Okeechobee (USA).Crossref | GoogleScholarGoogle Scholar | 11202730PubMed |

Havens, K. E., Fulton, R. S., Beaver, J., Samples, E., and Colee, J. (2016). Effects of climate variability on cladoceran zooplankton and cyanobacteria in a shallow subtropical lake. Journal of Plankton Research 38, 418–430.
Effects of climate variability on cladoceran zooplankton and cyanobacteria in a shallow subtropical lake.Crossref | GoogleScholarGoogle Scholar |

Hense, I. (2007). Regulative feedback mechanisms in cyanobacteria-driven systems: a model study. Marine Ecology Progress Series 339, 41–47.
Regulative feedback mechanisms in cyanobacteria-driven systems: a model study.Crossref | GoogleScholarGoogle Scholar |

Holland, G. J., and Webster, P. J. (2007). Heightened tropical cyclone activity in the North Atlantic: natural variability of climate trend? Philosophical Transactions of the Royal Society – A. Mathematical and Physical Sciences 365, 2695–2716.
Heightened tropical cyclone activity in the North Atlantic: natural variability of climate trend?Crossref | GoogleScholarGoogle Scholar |

Howarth, R. W., Marino, R., Lane, J., and Cole, J. J. (1988). Nitrogen fixation rates in freshwater, estuarine, and marine ecosystems. Limnology and Oceanography 33, 669–687.

Huisman, J., Sharples, J., Stroom, J., Visser, P. M., Kardinaal, W. E. A., Verspagen, J. M. H., and Sommeijer, B. (2004). Changes in turbulent mixing shift competition for light between phytoplankton species. Ecology 85, 2960–2970.
Changes in turbulent mixing shift competition for light between phytoplankton species.Crossref | GoogleScholarGoogle Scholar |

Huisman, J., Matthijs, H. C. P., and Visser, P. M. (2005). ‘Harmful Cyanobacteria.’ (Springer: Dordrecht, Netherlands.)

Huisman, J., Codd, G. A., Paerl, H. W., Ibelings, B. W., Verspagen, J. M. H., and Visser, P. M. (2018). Cyanobacterial blooms. Nature Reviews. Microbiology 16, 471–483.
Cyanobacterial blooms.Crossref | GoogleScholarGoogle Scholar | 29946124PubMed |

Ibelings, B. W., and Maberly, S. C. (1998). Photoinhibition and the availability of inorganic carbon restrict photosynthesis by surface blooms of cyanobacteria. Limnology and Oceanography 43, 408–419.
Photoinhibition and the availability of inorganic carbon restrict photosynthesis by surface blooms of cyanobacteria.Crossref | GoogleScholarGoogle Scholar |

Ibelings, B. W., Vonk, M., Los, H. F. J., van der Molen, D. T., and Mooij, W. M. (2003). Fuzzy modeling of cyanobacterial surface waterblooms: validation with NOAA-AVHRR satellite images. Ecological Applications 13, 1456–1472.
Fuzzy modeling of cyanobacterial surface waterblooms: validation with NOAA-AVHRR satellite images.Crossref | GoogleScholarGoogle Scholar |

Kaebernick, M., and Neilan, B. A. (2001). Ecolocial and molecular investigations of cyanotoxin production. FEMS Microbiology Ecology 35, 1–9.
Ecolocial and molecular investigations of cyanotoxin production.Crossref | GoogleScholarGoogle Scholar | 11248384PubMed |

Kahru, M., Leppänen, J. M., and Rud, O. (1993). Cyanobacterial blooms cause heating of the sea surface. Marine Ecology Progress Series 101, 1–7.
Cyanobacterial blooms cause heating of the sea surface.Crossref | GoogleScholarGoogle Scholar |

Kosten, S., Huszar, V. L. M., Bécares, E., Costa, L. S., van Donk, E., Hansson, L. A., Jeppesen, E., Kruk, C., Lacerot, G., Mazzeo, N., De Meester, L., Moss, B., Lürling, M., Nõges, T., Romo, S., and Scheffer, M. (2012). Warmer climates boost cyanobacterial dominance in shallow lakes. Global Change Biology 18, 118–126.
Warmer climates boost cyanobacterial dominance in shallow lakes.Crossref | GoogleScholarGoogle Scholar |

Kratzer, C. R., and Brezonik, P. L. (1981). A Carlson-type trophic state index for nitrogen in Florida lakes. Journal of the American Water Research Association 17, 713–715.
A Carlson-type trophic state index for nitrogen in Florida lakes.Crossref | GoogleScholarGoogle Scholar |

Lewis, W. M., and Wurtsbaugh, W. A. (2008). Control of lacustrine phytoplankton by nutrients: erosion of the phosphorus paradigm. International Review of Hydrobiology 93, 446–465.
Control of lacustrine phytoplankton by nutrients: erosion of the phosphorus paradigm.Crossref | GoogleScholarGoogle Scholar |

Lürling, M., and Faassen, E. J. (2012). Controlling toxic cyanobacteria: effects of dredging and phosphorus-binding clay on cyanobacteria and microcystins. Water Research 46, 1447–1459.
Controlling toxic cyanobacteria: effects of dredging and phosphorus-binding clay on cyanobacteria and microcystins.Crossref | GoogleScholarGoogle Scholar | 22137447PubMed |

Maier, H. R., Kingston, G. B., Clark, T., Frazer, A., and Sanderson, A. (2004). Risk-based approach for assessing the effectiveness of flow management in controlling cyanobacterial blooms in rivers. River Research and Applications 20, 459–471.
Risk-based approach for assessing the effectiveness of flow management in controlling cyanobacterial blooms in rivers.Crossref | GoogleScholarGoogle Scholar |

McCarthy, M. J., Lavrentyev, P. J., Yang, L., Zhang, L., Chen, Y., Qin, B., and Gardner, W. S. (2007). Nitrogen dynamics and microbial food web structure during a summer cyanobacterial bloom in a subtropical, shallow, well-mixed, eutrophic lake (Lake Taihu, China). Hydrobiologia 581, 195–207.
Nitrogen dynamics and microbial food web structure during a summer cyanobacterial bloom in a subtropical, shallow, well-mixed, eutrophic lake (Lake Taihu, China).Crossref | GoogleScholarGoogle Scholar |

Mitrovic, S. M., Oliver, R. L., Rees, C., Bowling, L. C., and Buckney, R. T. (2003). Critical velocities for the growth and dominance of Anabaena circinalis in some turbid freshwater rivers. Freshwater Biology 48, 164–174.
Critical velocities for the growth and dominance of Anabaena circinalis in some turbid freshwater rivers.Crossref | GoogleScholarGoogle Scholar |

Mitrovic, S. M., Hardwick, L., and Dorani, F. (2011). Use of flow management to mitigate cyanobacterial blooms in the Lower Darling River, Australia. Journal of Plankton Research 33, 229–241.
Use of flow management to mitigate cyanobacterial blooms in the Lower Darling River, Australia.Crossref | GoogleScholarGoogle Scholar |

Moisander, P. H., McClinton, E., and Paerl, H. W. (2002). Salinity effects on growth, photosynthetic parameters, and nitrogenase activity in estuarine planktonic Cyanobacteria. Microbial Ecology 43, 432–442.
Salinity effects on growth, photosynthetic parameters, and nitrogenase activity in estuarine planktonic Cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 12043002PubMed |

Moisander, P. H., Cheshire, L. A., Braddy, J., Calandrino, E. S., Hoffman, M., Piehler, M. F., and Paerl, H. W. (2012). Facultative diazotrophy increases Cylindrospermopsis raciborskii competitiveness under fluctuating nitrogen availability. FEMS Microbiology Ecology 79, 800–811.
Facultative diazotrophy increases Cylindrospermopsis raciborskii competitiveness under fluctuating nitrogen availability.Crossref | GoogleScholarGoogle Scholar | 22126519PubMed |

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

National Academy of Sciences, Engineering and Medicine (2016). ‘Progress Towards Restoring the Everglades, The Sixth Biennial Review.’ (The National Academies Press: Washington DC, USA.)

Neilan, B. A., Pearson, L. A., Muenchhoff, J., Moffitt, M. C., and Dittmann, E. (2013). Environmental conditions that influence toxin biosynthesis in cyanobacteria. Environmental Microbiology 15, 1239–1253.
Environmental conditions that influence toxin biosynthesis in cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 22429476PubMed |

Nõges, T., Nõges, P., and Laugaste, R. (2003). Water level as a the mediator between climate change and phytoplankton composition in a large shallow temperate lake. Hydrobiologia 506–509, 257–263.
Water level as a the mediator between climate change and phytoplankton composition in a large shallow temperate lake.Crossref | GoogleScholarGoogle Scholar |

North, R. L., Guildford, S. J., Smith, R. E. H., Havens, S. M., and Twiss, M. R. (2007). Evidence for phosphorus, nitrogen, and iron colimitation of phytoplankton communities in Lake Erie. Limnology and Oceanography 52, 315–328.
Evidence for phosphorus, nitrogen, and iron colimitation of phytoplankton communities in Lake Erie.Crossref | GoogleScholarGoogle Scholar |

O’Conner, B., Lichtenstein, S., and Cross, E. (2015). The impact of water quality on Florida’s home values. March 2015, Final Report. (Florida Association of Realtors.) Available at https://www.floridarealtors.org/ResearchAndStatistics/Other-Research-Reports/upload/FR_WaterQuality_Final_Mar2015.pdf [Verified 8 February 2019].

O’Reilly, C. M., Sharma, S., Gray, D., Hampton, S. E., Read, J. S., Rowley, R. J., Schneider, P., Lenters, J. D., McIntyre, P. B., Kraemer, B. M., Weyhenmeyer, G. A., Straile, D., Dong, B., Adrian, R., Allan, M. G., Anneville, O., Arvola, L., Austin, J., Bailey, J. L., Baron, J. S., Brookes, J. D., Eyto, E., Dokulil, M. T., Hamilton, D. P., Havens, K., Hetherington, A. L., Higgins, S. N., Hook, S., Izmest’eva, L. R., Joehnk, K. D., Kangur, K., Kasprzak, P., Kumagai, M., Kuusisto, E., Leshkevich, G., Livingstone, D. M., MacIntyre, S., May, L., Melack, J. M., Mueller-Navarra, D. C., Naumenko, M., Noges, P., Noges, T., North, R. P., Plisnier, P. D., Rigosi, A., Rimmer, A., Rogora, M., Rudstam, L. G., Rusak, J. A., Salmaso, N., Samal, N. R., Schindler, D. E., Schladow, S. G., Schmid, M., Schmidt, S. R., Silow, E., Soylu, M. E., Teubner, K., Verburg, P., Voutilainen, A., Watkinson, A., Williamson, C. E., and Zhang, G. (2015). Rapid and highly variable warming of lake surface waters around the globe. Geophysical Research Letters 42, 10773–10781.
Rapid and highly variable warming of lake surface waters around the globe.Crossref | GoogleScholarGoogle Scholar |

Ochumba, P. B. O., and Kibaara, D. I. (1989). Observations of blue–green algal blooms in the open waters of Lake Victoria, Kenya. African Journal of Ecology 27, 23–34.
Observations of blue–green algal blooms in the open waters of Lake Victoria, Kenya.Crossref | GoogleScholarGoogle Scholar |

Oh, H. M., Lee, S. J., Jang, M. H., and Yoon, B. D. (2000). Microcystin production by Microcystis aeruginosa in a phosphorus-limited chemostat. Applied and Environmental Microbiology 66, 176–179.
Microcystin production by Microcystis aeruginosa in a phosphorus-limited chemostat.Crossref | GoogleScholarGoogle Scholar | 10618220PubMed |

Orr, P. T., and Jones, G. J. (1998). Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures. Limnology and Oceanography 43, 1604–1614.
Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures.Crossref | GoogleScholarGoogle Scholar |

Pachauri, R. K., and Meyer, L. A. (Eds) (2014). ‘Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.’ (Intergovernmental Panel on Climate Change: Geneva, Switzerland.)

Padisák, J. (1997). Cylindrospermopsis raciborskii (Woloszynska) Seenaya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Archiv für Hydrobiologie 107, 563–593.

Paerl, H. W. (1984). Transfer of N2 and CO2 fixation products from Anabaena oscillarioides to associated bacteria during inorganic carbon sufficiency and deficiency. Journal of Phycology 20, 600–608.
Transfer of N2 and CO2 fixation products from Anabaena oscillarioides to associated bacteria during inorganic carbon sufficiency and deficiency.Crossref | GoogleScholarGoogle Scholar |

Paerl, H. W. (1988). Nuisance phytoplankton blooms in coastal, estuarine, and inland waters. Limnology and Oceanography 33, 823–847.

Paerl, H. W. (1990). Physiological ecology and regulation of N2 fixation in natural waters. Advances in Microbial Ecology 11, 305–344.
Physiological ecology and regulation of N2 fixation in natural waters.Crossref | GoogleScholarGoogle Scholar |

Paerl, H. W. (2009). Controlling eutrophication along the freshwater–marine continuum: dual nutrient (N and P) reductions are essential. Estuaries and Coasts 32, 593–601.
Controlling eutrophication along the freshwater–marine continuum: dual nutrient (N and P) reductions are essential.Crossref | GoogleScholarGoogle Scholar |

Paerl, H. W., and Huisman, J. (2008). Blooms like it hot. Science 320, 57–58.
Blooms like it hot.Crossref | GoogleScholarGoogle Scholar | 18388279PubMed |

Paerl, H. W., and Huisman, J. (2009). Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environmental Microbiology Reports 1, 27–37.
Climate change: a catalyst for global expansion of harmful cyanobacterial blooms.Crossref | GoogleScholarGoogle Scholar | 23765717PubMed |

Paerl, H. W., and Millie, D. F. (1996). Physiological ecology of toxic cyanobacteria. Phycologia 35, 160–167.
Physiological ecology of toxic cyanobacteria.Crossref | GoogleScholarGoogle Scholar |

Paerl, H. W., and Otten, T. G. (2013). Harmful cyanobacterial blooms: causes, consequences, and controls. Microbial Ecology 65, 995–1010.
Harmful cyanobacterial blooms: causes, consequences, and controls.Crossref | GoogleScholarGoogle Scholar | 23314096PubMed |

Paerl, H. W., and Ustach, J. (1982). Blue–green algal scums: an explanation for their occurrence during freshwater blooms. Limnology and Oceanography 27, 212–217.
Blue–green algal scums: an explanation for their occurrence during freshwater blooms.Crossref | GoogleScholarGoogle Scholar |

Paerl, H. W., Xu, H., Hall, N. S., Rossignol, K. L., Joyner, A. R., Zhu, G., and Qin, B. (2015). Nutrient limitation dynamics examined on a multi-annual scale in Lake Taihu, China: implications for controlling eutrophication and harmful algal blooms. Journal of Freshwater Ecology 30, 5–24.
Nutrient limitation dynamics examined on a multi-annual scale in Lake Taihu, China: implications for controlling eutrophication and harmful algal blooms.Crossref | GoogleScholarGoogle Scholar |

Paerl, H. W., Otten, T. G., and Joyner, A. R. (2016a). Moving towards adaptive management of cyanotoxin-impaired water bodies. Microbial Biotechnology 9, 641–651.
Moving towards adaptive management of cyanotoxin-impaired water bodies.Crossref | GoogleScholarGoogle Scholar | 27418325PubMed |

Paerl, H. W., Scott, J. T., McCarthy, M. J., Newell, S. E., Gardner, W. S., Havens, K. E., Hoffman, D. K., Wilhelm, S. W., and Wurtsbaugh, W. A. (2016b). It takes two to tango: when and where dual nutrient (N & P) reductions are needed to protect lakes and downstream ecosystems. Environmental Science & Technology 50, 10805–10813.
It takes two to tango: when and where dual nutrient (N & P) reductions are needed to protect lakes and downstream ecosystems.Crossref | GoogleScholarGoogle Scholar |

Paerl, H. W., Gardner, W. S., Havens, K. E., Joyner, A. R., McCarthy, M. J., Newell, S. E., Qin, B., and Scott, J. T. (2016c). Mitigating cyanobacterial harmful algal blooms in aquatic ecosystems impacted by climate change and anthropogenic nutrients. Harmful Algae 54, 213–222.
Mitigating cyanobacterial harmful algal blooms in aquatic ecosystems impacted by climate change and anthropogenic nutrients.Crossref | GoogleScholarGoogle Scholar | 28073478PubMed |

Peierls, B. L., Caraco, N. F., Pace, M. L., and Cole, J. J. (1991). Human influence on river nitrogen. Nature 350, 386–387.
Human influence on river nitrogen.Crossref | GoogleScholarGoogle Scholar |

Peterson, S. A. (1982). Lake restoration by sediment removal. Water Resources Bulletin. American Water Resources Association 18, 423–436.
Lake restoration by sediment removal.Crossref | GoogleScholarGoogle Scholar |

Potts, M. (1994). Desiccation tolerance of prokaryotes. Microbiological Reviews 58, 755–805.
| 7854254PubMed |

Qin, B., Zhu, G., Gao, G., Zhang, Y., Li, W., Paerl, H. W., and Carmichael, W. W. (2010). A drinking water crisis in Lake Taihu, China: linkage to climatic variability and lake management. Environmental Management 45, 105–112.
A drinking water crisis in Lake Taihu, China: linkage to climatic variability and lake management.Crossref | GoogleScholarGoogle Scholar | 19915899PubMed |

Rabalais, N. N. (2002). Nitrogen in aquatic ecosystems. Ambio 31, 102–112.
Nitrogen in aquatic ecosystems.Crossref | GoogleScholarGoogle Scholar | 12077998PubMed |

Reynolds, C. S. (1987). Cyanobacterial water blooms. Advances in Botanical Research 13, 67–143.
Cyanobacterial water blooms.Crossref | GoogleScholarGoogle Scholar |

Robb, M., Greenop, B., Goss, Z., Douglas, G., and Adeney, J. (2003). Application of Phoslock, an innovative phosphorous binding clay, to two Western Australian waterways: preliminary findings. Hydrobiologia 494, 237–243.
Application of Phoslock, an innovative phosphorous binding clay, to two Western Australian waterways: preliminary findings.Crossref | GoogleScholarGoogle Scholar |

Schindler, D. W., and Vallentine, J. R. (2008). ‘The Algal Bowl: Overfertilization of the World’s Freshwaters and Estuaries.’ (University of Alberta Press: Edmonton, AB, Canada.)

Schindler, D. W., Hecky, R. E., Findlay, D. L., Stainton, M. P., Parker, B. R., Paterson, M., Beaty, K. G., Lyng, M., and Kasian, S. E. M. (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 of the United States of America 105, 11254–11258.
Eutrophication of lakes cannot be controlled by reducing nitrogen input: results of a 37 year whole ecosystem experiment.Crossref | GoogleScholarGoogle Scholar | 18667696PubMed |

Schopf, J. W. (2000). The fossil record: tracing the roots of the cyanobacterial lineage. In ‘The Ecology of Cyanobacteria’. (Eds B. A. Whitton and M. Potts.) pp. 13–35. (Kluwer Academic Publishers: Dordrecht, Netherlands.)

Schutten, J., Dainty, J., and Davy, A. J. (2005). Root anchorage and its significance for submerged plants in shallow lakes. Journal of Ecology 93, 556–571.
Root anchorage and its significance for submerged plants in shallow lakes.Crossref | GoogleScholarGoogle Scholar |

Scott, J. T., and McCarthy, M. J. (2010). Nitrogen fixation may not balance the nitrogen pool in lakes over timescales relevant to eutrophication management. Limnology and Oceanography 55, 1265–1270.
Nitrogen fixation may not balance the nitrogen pool in lakes over timescales relevant to eutrophication management.Crossref | GoogleScholarGoogle Scholar |

Seitzinger, S. P. (1988). Denitrification in freshwater and coastal marine systems: ecological and geochemical significance. Limnology and Oceanography 33, 702–724.

Seneviratne, S., Nicholls, N., Easterling, D., Goodess, C., Kanae, S., Kossin, J., Luo, Y., Marengo, J., McInnes, K., Rahimi, M., Reichstein, M., Sorteberg, A., Vera, C., and Zhang, X. (2012). Changes in climate extremes and their impacts on the natural physical environment. In ‘Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation. A Special Report of Working Groups I and II of the Intergovernmental Panel on Climate Change (IPCC)’. (Eds C. B. Field, V. Barros, T. F. Stocker, D. Qin, D. J. Dokken, K. L. Ebi, M. D. Mastrandrea, K. J. Mach, G. -K. Plattner, S. K. Allen, M. Tignor, and P. M. Midgley.) pp. 109–230. (Cambridge University Press: New York, NY, USA.)

Shapiro, J. (1990). Current beliefs regarding dominance of blue-greens: the case for the importance of CO2 and pH. Verhandlungen: Internationale Verein fur Theoretische Angewante Limnology 24, 38–54.

Smith, V. H., Dodds, W. K., Havens, K. E., Engstrom, D. R., Paerl, H. W., Moss, B., and Likens, G. E. (2014). Cultural eutrophication of natural lakes in the United States is real and widespread. Limnology and Oceanography 59, 2217–2225.
Cultural eutrophication of natural lakes in the United States is real and widespread.Crossref | GoogleScholarGoogle Scholar |

Steffen, M. M., Belisle, B. S., Watson, S. B., Boyer, G. L., and Wilhelm, S. W. (2014). Status, causes and controls of cyanobacterial blooms in Lake Erie. Journal of Great Lakes Research 40, 215–225.
Status, causes and controls of cyanobacterial blooms in Lake Erie.Crossref | GoogleScholarGoogle Scholar |

Trenberth, K. E. (2008). The impact of climate change and variability on heavy precipitation, floods, and droughts. In ‘Encyclopedia of Hydrological Sciences’. (Ed. M. G. Anderson.) pp. 1–11. (Wiley: Chichester, UK.)

Van Cleave, K., Lenters, J. D., Wang, J., and Verhamme, E. M. (2014). A regime shift in Lake Superior ice cover, evaporation, and water temperature following the warm El Niño winter of 1997–1998. Limnology and Oceanography 59, 1889–1898.
A regime shift in Lake Superior ice cover, evaporation, and water temperature following the warm El Niño winter of 1997–1998.Crossref | GoogleScholarGoogle Scholar |

Verspagen, J. M. H., Van de Waal, D. B., Finke, J. F., Visser, P. M., Van Donk, E., and Huisman, J. (2014). Rising CO2 levels will intensify phytoplankton blooms in eutrophic and hypertrophic lakes. PLoS One 9, e104325.
Rising CO2 levels will intensify phytoplankton blooms in eutrophic and hypertrophic lakes.Crossref | GoogleScholarGoogle Scholar |

Visser, P. M., Ibelings, B. W., Van der Veer, B., Koedood, J., and Mur, L. R. (1996). Artificial mixing prevents nuisance blooms of the cyanobacterium Microcystis in Lake Nieuwe Meer, the Netherlands. Freshwater Biology 36, 435–450.
Artificial mixing prevents nuisance blooms of the cyanobacterium Microcystis in Lake Nieuwe Meer, the Netherlands.Crossref | GoogleScholarGoogle Scholar |

Vopel, K., Gibbs, M., Hickey, C. W., and Quinn, J. (2008). Modification of sediment–water solute exchange by sediment-capping materials: effects on O2 and pH. Marine and Freshwater Research 59, 1101–1110.
Modification of sediment–water solute exchange by sediment-capping materials: effects on O2 and pH.Crossref | GoogleScholarGoogle Scholar |

Webster, P. J., Holland, G. J., Curry, J. A., and Chang, H. R. (2005). Changes in tropical cyclone number, duration, and intensity in a warming environment. Science 309, 1844–1846.
Changes in tropical cyclone number, duration, and intensity in a warming environment.Crossref | GoogleScholarGoogle Scholar | 16166514PubMed |

Wood, S. A., Dietrich, D. R., Cary, S. C., and Hamilton, D. P. (2012). Increasing Microcystis cell density enhances microcystin synthesis: a mesocosm study. Inland Waters 2, 17–22.
Increasing Microcystis cell density enhances microcystin synthesis: a mesocosm study.Crossref | GoogleScholarGoogle Scholar |

Wuebbles, D., Meehl, G., Hayhoe, K., Karl, T. R., Kunkel, K., Santer, B., Wehner, M., Colle, B., Fischer, E. M., Fu, R., Goodman, A., Janssen, E., Kharin, V., Lee, H., Li, W., Long, L. N., Olsen, S. C., Pan, Z., Seth, A., Sheffield, J., and Sun, L. (2014). CMIP5 climate model analyses: climate extremes in the United States. Bulletin of the American Meteorological Society 95, 571–583.
CMIP5 climate model analyses: climate extremes in the United States.Crossref | GoogleScholarGoogle Scholar |

Xu, H., Paerl, H. W., Qin, B., Zhu, G., and Gao, G. (2010). Nitrogen and phosphorus inputs control phytoplankton growth in eutrophic Lake Taihu, China. Limnology and Oceanography 55, 420–432.
Nitrogen and phosphorus inputs control phytoplankton growth in eutrophic Lake Taihu, China.Crossref | GoogleScholarGoogle Scholar |

Xu, H., Paerl, H. W., Qin, B., Zhu, G., Hall, N. S., and Wu, Y. (2015). Determining critical nutrient thresholds needed to control harmful cyanobacterial blooms in hypertrophic Lake Taihu, China. Environmental Science & Technology 49, 1051–1059.
Determining critical nutrient thresholds needed to control harmful cyanobacterial blooms in hypertrophic Lake Taihu, China.Crossref | GoogleScholarGoogle Scholar |

Zhu, M., Paerl, H. W., Zhu, G., Wu, T., Li, W., Shi, K., Zhao, L., Zhang, Y., Qin, B., and Caruso, A. M. (2014). The role of tropical cyclones in stimulating Cyanobacteria (Microcystis spp.) blooms in hypertrophic Lake Taihu, China. Harmful Algae 39, 310–321.
The role of tropical cyclones in stimulating Cyanobacteria (Microcystis spp.) blooms in hypertrophic Lake Taihu, China.Crossref | GoogleScholarGoogle Scholar |