Oceanography The Official Magazine of
The Oceanography Society
Volume 30 Issue 01

View Issue TOC
Volume 30, No. 1
Pages 58 - 69

OpenAccess

Globally Changing Nutrient Loads and Harmful Algal Blooms: Recent Advances, New Paradigms, and Continuing Challenges

By Patricia M. Glibert  and Michele A. Burford 
Jump to
Article Abstract Citation References Copyright & Usage
Article Abstract

It is now well recognized that there are more harmful algal blooms (HABs), more often, in new and different places, often lasting longer, and with a range of toxicities, and that many of these blooms are related to nutrient pollution. Nutrient loads are increasing globally, but they are changing regionally in proportion and in the dominant form of nutrient. The fact that nutrient loads have generally increased is, in itself, insufficient for the promotion of HABs. The success of HABs lies at the intersection of the physiological adaptations of the harmful algal species, environmental conditions, and interactions with co-occurring organisms that alter abiotic conditions and/or aggregate or disperse cells, in turn promoting or inhibiting their growth. It is a change in the supply of the right nutrients at the right time that helps to create conditions conducive to specific HABs. Many dinoflagellate and cyanobacterial HABs appear to have adaptations that allow them to exploit environments—and potentially even become more toxic—where nutrients are not in balanced (Redfield) proportions. HABs are also changing in complex ways due to changes in climate and many other changes that affect the timing, amount, or proportions of nutrients. There is much work to be done to understand the physiological ecology of HABs and other co-occurring species. Climate change and altered CO2 levels, and their implications for altered productivity of the global ocean, should motivate both new models and new experimental investigations that support them. Based on current knowledge, the management implications are clear: the most effective actions to reduce HABs and their impacts will be continued efforts to reduce nutrients entering our waters.

Citation

Glibert, P.M., and M.A. Burford. 2017. Globally changing nutrient loads and harmful algal blooms: Recent advances, new paradigms, and continuing challenges. Oceanography 30(1):58–69, https://doi.org/10.5670/oceanog.2017.110.

References
    Acquisti, C., J.J. Elser, and S. Kumar. 2009. Ecological nitrogen limitation shapes the DNA composition of plant genomes. Molecular Biology and Evolution 26:953–956, https://doi.org/10.1093/molbev/msp038.
  1. Adolf, J.E., D. Krupatkina, and T. Bachvaroff. 2007. Karlotoxin mediates grazing by Oxyrrhis marina on strains of Karlodinium veneficum. Harmful Algae 6:400–412, https://doi.org/10.1016/​j.hal.2006.12.003.
  2. Allen, J.I., and L. Polimene. 2011. Linking physiology to ecology: Towards a new generation of plankton models. Journal of Plankton Research 33:989–997, https://doi.org/10.1093/plankt/fbr032.
  3. Armstrong-Howard, M.D., W.P. Cochlan, N. Ladizinsky, and R.M. Kudela. 2007. Nitrogenous preference of toxigenic Pseudo-nitzschia australis (Bacillariophyceae) from field and laboratory experiments. Harmful Algae 6:206–217, https:/doi.org/​10.1016/​j.hal.2006.06.003.
  4. Babin, M., J.J. Cullen, C.S. Roesler, P.L. Donaghay, G.J. Doucette, M. Kahru, M.R. Lewis, C.A. Scholin, M.E. Sieracki, and H.M. Sosik. 2005. New approaches and technologies for observing harmful algal blooms. Oceanography 18(2):210–227, https://doi.org/10.5670/oceanog.2005.55.
  5. Berg, G.M., P.M. Glibert, M.W. Lomas, and M.A. Burford. 1997. Organic N uptake and growth by the chrysophyte Aureococcus anaphogefferens during a brown tide event. Marine Biology 129:377–387, https://doi.org/10.1007/s002270050178.
  6. Burford, M.A., T.W. Davis, P.T. Orr, R. Sinha, A. Willis, and B.A. Neilan. 2014. Nutrient-related changes in the toxicity of field blooms of the cyanobacterium Cylindrospermopsis raciborskii. FEMS Microbiology and Ecology 89:135–148, https://doi.org/10.1111/1574-6941.12341.
  7. Burkholder, J.M., P.M. Glibert, and H. Skelton. 2008. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8:77–93, https://doi.org/10.1016/​j.hal.2008.08.010.
  8. Cloern, J.E. 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210:223–253, https://doi.org/10.3354/meps210223.
  9. Cochlan, W.P., J. Herndon, and R.M. Kudela. 2008. Inorganic and organic nitrogen uptake by the toxigenic diatom Pseudo-nitzschia australis (Bacillariophyceae). Harmful Algae 8:111–118, https://doi.org/10.1016/j.hal.2008.08.008.
  10. Conley, D.J., H.W. Paerl, R.W. Howarth, D.F. Boesch, S.P. Seitzinger, K.E. Havens, C. Lancelot, and G.E. Likens. 2009. Controlling eutrophication: Nitrogen and phosphorus. Science 323:1,014–1,015, https://doi.org/10.1126/science.1167755.
  11. Davis, T.W., M.J. Harke, M.A. Marcoval, J. Goleski, C. Orano-Dawson, D.L. Berry, and C.J. Gobler. 2010. Effects of nitrogenous compounds and phosphorus on the growth of toxic and non-toxic strains of Microcystis during bloom events. Aquatic Microbial Ecology 61:149–162, https://doi.org/10.3354/ame01445.
  12. Donald, D.B., M.J. Bogard, K. Finlay, L. Bunting, and P.R. Leavitt. 2013. Phytoplankton-specific response to enrichment of phosphorus-rich surface waters with ammonium, nitrate, and urea. PLoS ONE 8(1):e53277, https://doi.org/10.1371/​journal.pone.0053277.
  13. Donald, D.B., M.J. Bogard, K. Finlay, and P.R. Leavitt. 2011. Comparative effects of urea, ammonium and nitrate on phytoplankton dominance, community composition and toxicity in a hypereutrophic freshwater. Limnology and Oceanography 56:2,161–2,175, https://doi.org/10.4319/lo.2011.56.6.2161.
  14. Erisman, J.W., M.A. Sutton, J.N. Galloway, Z. Klimont, and W. Winiwater. 2008. How a century of ammonia synthesis changed the world. Nature Geoscience 1:636–639, https://doi.org/10.1038/ngeo325.
  15. Finkel, Z.V., J. Beardall, K.J. Flynn, A. Quiqq, T.A.V. Rees, and J.A. Raven. 2010. Phytoplankton in a changing world: Cell size and elemental stoichiometry. Journal of Plankton Research 32:119–137, https://doi.org/10.1093/plankt/fbp098.
  16. Finlay, K., A. Patoine, D.B. Donald, M.J. Bogard, and P.R. Leavitt. 2010. Experimental evidence that pollution with urea can degrade water quality in phosphorus-rich lakes of the Northern Great Plains. Limnology and Oceanography 55:1,213–1,230, https://doi.org/10.4319/lo.2010.55.3.1213.
  17. Flynn, K.J. 2010. Do external resource ratios matter? Implications for modelling eutrophication events and controlling harmful algal blooms. Journal of Marine Systems 83:170–180, https://doi.org/10.1016/j.jmarsys.2010.04.007.
  18. Flynn, K.J., D.K. Stoecker, A. Mitra, J.A. Raven, P.M. Glibert, P.J. Hansen, E. Granéli, and J.M. Burkholder. 2013. Misuse of the phytoplankton-zooplankton dichotomy: The need to assign organisms as mixotrophs within plankton functional types. Journal of Plankton Research 35:3–11, https://doi.org/10.1093/plankt/fbs062.
  19. Franks, P. In press. Recent advances in modeling of harmful algal blooms. In Ecology and Oceanography of Harmful Algal Blooms (GEOHAB). P.M. Glibert, E. Berdalet, M. Burford, G. Pitcher, and M. Zhou, eds, Springer.
  20. Frigstad, H., T. Andersen, D.O. Hessen, L.-J. Naustvoll, T.M. Johnsen, and R.G.J. Bellerby. 2011. Seasonal variation in marine stoichiometry: Can the composition of seston explain stable Redfield ratios? Biogeosciences 8:2,917–2,933, https://doi.org/​10.5194/bg-8-2917-2011.
  21. Fu, F.X., A.O. Tatters, and D.A. Hutchins. 2012. Global change and the future of harmful algal blooms in the ocean. Marine Ecology Progress Series 470:207–233, https://doi.org/10.3354/meps10047.
  22. Galloway, J.N., and E.B. Cowling. 2002. Reactive nitrogen and the world: 200 years of change. Ambio 31:64–71, https://doi.org/10.1579/​0044-7447-31.2.64.
  23. Glibert, P.M. 2016. Margalef revisited: A new phytoplankton mandala incorporating twelve dimensions including nutritional physiology. Harmful Algae 55:25–30, https://doi.org/10.1016/​j.hal.2016.01.008.
  24. Glibert, P.M., J.I. Allen, Y. Artioli, A. Beusen, L. Bouwman, J. Harle, R. Holmes, and J. Holt. 2014a. Vulnerability of coastal ecosystems to changes in harmful algal bloom distribution in response to climate change: Projections based on model analysis. Global Change Biology 20:3,845–3,858, https://doi.org/10.1111/gcb.12662.
  25. Glibert, P.M., and J.M. Burkholder. 2011. Harmful algal blooms and eutrophication: “Strategies” for nutrient uptake and growth outside the Redfield comfort zone. Chinese Journal of Oceanology and Limnology 29:724–738, https://doi.org/10.1007/s00343-011-0502-z.
  26. Glibert, P.M., and J.M. Burkholder. In press. Causes of harmful algal blooms. In Harmful Algal Blooms: A Compendium Desk Reference. S. Shumway, ed., Wiley.
  27. Glibert, P.M., J.M. Burkholder, T.M. Kana, J. Alexander, H. Skelton, and C. Shillings. 2009. Grazing by Karenia brevis on Synechococcus enhances their growth rate and may help to sustain blooms. Aquatic Microbial Ecology 55:17–30, https://doi.org/10.3354/ame01279.
  28. Glibert, P.M., J. Harrison, C. Heil, and S. Seitzinger. 2006. Escalating worldwide use of urea: A global change contributing to coastal eutrophication. Biogeochemistry 77:441–463, https://doi.org/​10.1007/s10533-005-3070-5.
  29. Glibert, P.M., T.M. Kana, and K. Brown. 2013. From limitation to excess: Consequences of substrate excess and stoichiometry for phytoplankton physiology, trophodynamics and biogeochemistry, and implications for modeling. Journal of Marine Systems 125:14–28, https://doi.org/10.1016/​j.jmarsys.2012.10.004.
  30. Glibert, P.M., R. Manager, D.J. Sobota, and L. Bouwman. 2014b. The Haber-Bosch-Harmful Algal Bloom (HB-HAB) link. Environmental Research Letters 9:105001, https://doi.org/​10.1088/1748-9326/9/10/105001.
  31. Glibert, P.M., S. Seitzinger, C.A. Heil, J.M. Burkholder, M.W. Parrow, L.A. Codispoti, and V. Kelly. 2005. The role of eutrophication in the global proliferation of harmful algal blooms: New perspectives and new approaches. Oceanography 18(2):198–209, https://doi.org/10.5670/oceanog.2005.54.
  32. Glibert, P.M., F.P. Wilkerson, R.C. Dugdale, J.A. Raven, C. Dupont, P.R. Leavitt, A.E. Parker, J.M. Burkholder, and T.M. Kana. 2016. Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition, with emphasis on nitrogen-enriched conditions. Limnology and Oceanography 61:165–197, https://doi.org/10.1002/lno.10203.
  33. Gobler, C.J., D.L. Berry, S.T. Dyhrman, S.W. Wilhelm, A. Salamov, A.V. Lobanov, Y. Zhang, J. L. Collier, L.L. Wurch, A.B. Kustka, and others. 2011. Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics. Proceedings of the National Academy of Sciences of the United States of America 108:4,352–4,357, https://doi.org/10.1073/pnas.1016106108.
  34. Gobler, C.J., J.M. Burkholder, T.W. Davis, M.J. Harke, T. Johengen, C.A. Snow, and D.B. van de Waal. 2016. The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms. Harmful Algae 54:87–97, https://doi.org/10.1016/​j.hal.2016.01.010.
  35. Goes, J., and H.d.R. Gomes. 2016. An ecosystem in transition: The emergence of mixotrophy in the Arabian Sea. Pp. 155–183 in Aquatic Microbial Ecology and Biogeochemistry: A Dual Perspective. P.M. Glibert and T.M. Kana, eds, Springer International Publication, Geneva, Switzerland. 
  36. Goes, J.I., P.G. Thoppil, H.d.R. Gomes, and J.T. Fasullo. 2005. Warming of the Eurasian landmass is making the Arabian Sea more productive. Science 308:545–547, https://doi.org/10.1126/science.1106610.
  37. Gomes, H.d.R., J.I. Goes, S.G.P. Matondkar, E.J. Buskey, S. Basu, S. Parab, and P. Thoppil. 2014. Massive outbreaks of Noctiluca scintillans blooms in the Arabian Sea due to spread of hypoxia. Nature Communications 5:4862, https://doi.org/10.1038/ncomms5862.
  38. Gomes, H.d.R., J.I. Goes, P. Matondkar, S. Parab, A. Al-Azri, and P. Thoppil. 2008. Blooms of Noctiluca miliaris in the Arabian Sea: An in situ and satellite study. Deep Sea Research 55:751–765, https://doi.org/10.1016/j.dsr.2008.03.003.
  39. Granéli, E., P. Carlsson, and C. Legrand. 1999. The role of C, N and P in dissolved and particulate matter as a nutritional source for phytoplankton growth, including toxic species. Aquatic Ecology 33:17–27, https://doi.org/10.1023/A:1009925515059.
  40. Granéli, E., and K.J. Flynn. 2006. Chemical and physical factors influencing toxin content. Pp. 229–241 in Ecology of Harmful Algae. E. Granéli, and J.T. Turner, eds, Springer, Heidelberg, Germany.
  41. Hardison, D.R., W.G. Sunda, R.W. Litaker, D. Shea, and P.A. Tester. 2012. Nitrogen limitation increases brevetoxins in Karenia brevis (Dinophyceae): Implications for bloom toxicity. Journal of Phycology 48:844–858, https://doi.org/​10.1111/j.1529-8817.2012.01186.x.
  42. Hardison, D.R., W.G. Sunda, D. Shea, and R.W. Litaker. 2013. Increased toxicity of Karenia brevis during phosphate limited growth: Ecological and evolutionary implications. PLoS ONE 8(3):e58545, https://doi.org/10.1371/journal.pone.0058545
  43. Harke, M.J., D.L. Berry, J.W. Ammerman, and C.H. Gobler. 2012. Molecular response of the bloom-forming cyanobacterium, Microcystis aeruginosa, to phosphorus limitation. Microbial Ecology 63:188–189, https://doi.org/10.1007/s00248-011-9894-8.
  44. Harris, T.D., V.H. Smith, J.L. Graham, D. Van de Waal, L.P. Tedesco, and N. Clercin. 2016. Combined effects of nitrogen to phosphorus and nitrate to ammonia ratios on cyanobacterial metabolite concentrations in eutrophic Midwestern USA reservoirs. Inland Waters 6:199–210, https://doi.org/​10.5268/iw-6.2.938
  45. Harrison, P.J., K. Furuya, P.M. Glibert, J. Xu, H.B. Liu, K. Yin, J.H.W. Lee, D.M. Anderson, R. Gowen, A.R. Al-Azri, and A.Y.T. Ho. 2011. Geographical distribution of red and green Noctiluca scintillans. Chinese Journal of Oceanology and Limnology 29:807–831, https://doi.org/10.1007/s00343-011-0510-z.
  46. Heisler, J., P.M. Glibert, J.M. Burkholder, D.A. Anderson, W.P. Cochlan, W.C. Dennison, Q. Dortch, C. Gobler, C.A. Heil, E. Humphries, and others. 2008. Eutrophication and harmful algal blooms: A scientific consensus. Harmful Algae 8:3–13, https://doi.org/10.1016/​j.hal.2008.08.006.
  47. Holt, J., J. Harle, R. Proctor, S. Michel, M. Ashworth, C. Batstone, I. Allen, R. Holmes, T. Smyth, K. Haines, and others. 2009. Modelling the global coastal ocean. Philosophical Transactions of the Royal Society A 367:939–951, https://doi.org/10.1098/rsta.2008.0210.
  48. Hoos, A.B., and G. McMahon. 2009. Spatial analysis of instream nitrogen loads and factors controlling nitrogen delivery to streams in the southeastern United Stated using spatially referenced regression on watershed attributes (SPARROW) and regional classification frameworks. Hydrological Processes 23:2,275–2,294, https://doi.org/10.1002/hyp.7323.
  49. Howarth, R.W. 2008. Coastal nitrogen pollution: A review of sources and trends globally and regionally. Harmful Algae 8:14–20, https://doi.org/​10.1016/j.hal.2008.08.015.
  50. Howarth, R.W., A. Sharpley, and D. Walker. 2002. Sources of nutrient pollution to coastal waters in the United States: Implications for achieving coastal water quality goals. Estuaries 25:656–676, https://doi.org/10.1007/BF02804898.
  51. Illikchyan, N., R.M.L. McKay, J.P. Zehr, S.T. Dyhrman, and G.S. Bullerjahn. 2009. Detection and expression of the phosphonate transporter gene phnD in marine and freshwater picocyanobacteria. Environmental Microbiology 11:1,314–1,324, https://doi.org/10.1111/j.1462-2920.2009.01869.x.
  52. IPCC (Intergovernmental Panel on Climate Change). 2007. Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt, M. Tignor, and H.L. Miller, eds, Cambridge University Press, Cambridge, UK, and New York, NY, USA, 996 pp.
  53. Jeong, H.J., Y.D. Yoo, J.S. Kim, K.A. Seong, N.S. Kang, and T.H. Kim. 2010. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Science Journal 45:65–91, https://doi.org/10.1007/s12601-010-0007-2
  54. Johansson, N., and E. Granéli. 1999. Cell density, chemical composition and toxicity of Chrysochromulina polylepis (Haptophyta) in relation to different N:P supply ratios. Marine Biology 135:209–217, https://doi.org/10.1007/s002270050618.
  55. Kana, T.M., and P.M. Glibert. 2016. On saturating response curves from the dual perspectives of photosynthesis and nitrogen acquisition. Pp. 93–104 in Aquatic Microbial Ecology and Biogeochemistry: A Dual Perspective. P.M. Glibert and T.M. Kana, eds, Springer International Publishing, Switzerland. 
  56. Klausmeier, C.A., E. Litchman, T. Daufresne, and S.A. Levin. 2004. Optimal nitrogen-to-​phosphorus stoichiometry of phytoplankton. Nature 429:171–174, https://doi.org/​10.1038/nature02454.
  57. Leong, S.C.Y., A. Murata, Y. Nagashima, and S. Taguchi. 2004. Variability in toxicity of the dinoflagellate Alexandrium tamarense in response to different nitrogen sources and concentrations. Toxicon 43:407–415, https://doi.org/10.1016/​j.toxicon.2004.01.015.
  58. Lewis, N.I., S.S. Bates, J.L. McLachlan, and J.C. Smith. 1993. Temperature effects on growth, domoic acid production, and morphology of the diatom Nitzschia-pungens f. multiseries. Pp. 601–606 in Toxic Phytoplankton Blooms in the Sea. T.J. Smayda and Y. Shimizu, eds, Elsevier Science Publisher BV, Amsterdam, The Netherlands.
  59. Lin, C.-H., S. Accoroni, and P.M. Glibert. In press. Mixotrophy in the dinoflagellate Karlodinium veneficum under variable nitrogen:phosphorus stoichiometry: Feeding response and effects on larvae of the eastern oyster (Crassostrea virginica). Aquatic Microbial Ecology.
  60. Litke, D.W. 1999. Review of phosphorus control measures in the United States and their effects on water quality. US Geological Survey Water–Resources Investigations Report 99-4007. US Geological Survey, Denver, Colorado.
  61. Lomas, M.W., and P.M. Glibert. 1999. Temperature regulation of nitrate uptake: A novel hypothesis about nitrate uptake and reduction in cool-water diatoms. Limnology and Oceanography 44:556–572, https://doi.org/10.4319/lo.1999.44.3.0556.
  62. Lundgren, V., P.M. Glibert, E. Granéli, N.K. Vidyarathna, E. Fiori, L. Ou, K.J. Flynn, A. Mitra, D.K. Stoecker, and P.J. Hansen. 2016. Metabolic and physiological changes in Prymnesium parvum when grown under, and grazing on, prey of variable nitrogen:phosphorus stoichiometry. Harmful Algae 55:1–12, https://doi.org/10.1016/​j.hal.2016.01.002.
  63. Margalef, R. 1978. Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanologica Acta 1:493–509.
  64. Margalef, R., M. Estrada, and D. Blasco. 1979. Functional morphology of organisms involved in red tides, as adapted to decaying turbulence. Pp. 89–94 in Toxic Dinoflagellate Blooms. D. Taylor and H. Seliger, eds, Elsevier, New York.
  65. Mitra, A., and K.J. Flynn. 2005. Predator-prey interactions: Is “ecological stoichiometry” sufficient when good food goes bad? Journal of Plankton Research 27:393–399, https://doi.org/10.1093/plankt/fbi022.
  66. Mitra, A., and K.J. Flynn. 2006. Promotion of harmful algal blooms by zooplankton predatory activity. Biology Letters 2:194–197, https://doi.org/10.1098/rsbl.2006.0447.
  67. Mitra, A., K.J. Flynn, J.M. Burkholder, T. Berge, A. Calbet, J.A. Raven, E. Granéli, P.M. Glibert, P.J. Hansen, D.K. Stoecker, and others. 2014. The role of mixotrophic protists in the biological carbon pump. Biogeosciences 11:995–1,005, https://doi.org/10.5194/bg-11-995-2014.
  68. Monchamp, M.E., F.R. Pick, B.E. Beisner, and R. Maranger. 2014. Nitrogen forms influence microcystin concentration and composition via changes in cyanobacterial community structure. PLoS ONE 9(1):e85573, https://doi.org/​10.1371/​journal.pone.0085573.
  69. Nixon, S.W. 1995. Coastal marine eutrophication: A definition, social causes, and future concerns. Ophelia 41:199–219, https://doi.org/10.1080/​00785236.1995.10422044
  70. Ogata, T., M. Kodama, and T. Ishimaru. 1989. Effect of water temperature and light intensity on growth rate and toxin production of toxic dinoflagellates. Pp. 423–426 in Red Tides, Biology, Environmental Science and Toxicology. T. Okaichi, D.M. Anderson, and T. Nemoto, eds, Elsevier, New York, NY.
  71. Paerl, H.W., and J. Huisman. 2008. Blooms like it hot. Science 320:57–58, https://doi.org/10.1126/science.1155398.
  72. Paerl, H.W., and J.T. Scott. 2010. Throwing fuel on the fire: Synergistic effects of excessive nitrogen inputs and global warming on harmful algal blooms. Environmental Science & Technology 44:7,756–7,758, https://doi.org/10.1021/es102665e.
  73. Paerl, H.W., J.T. Scott, M.J. McCarthy, S.E. Newell, W.S. Gardner, K.E. Havens, D.K. Hoffman, S.W. Wilhelm, and W.A. Wurtsbaugh. 2016. It takes two to tango: When and where dual nutrient (N & P) reductions are needed to protect lakes and downstream ecosystems. Environmental Science & Technology 50:10,805–10,813, https://doi.org/​10.1021/acs.est.6b02575 
  74. Parry, G.D. 1981. The meaning of r- and K-selection. Oecologia 48:260–264, https://doi.org/10.1007/BF00347974.
  75. Peñuelas, J., J. Sardans, A. Rivas-Ubach, and I.A. Janssens. 2012. The human-induced imbalance between C, N and P in Earth’s life system. Global Change Biology 18:3–6, https://doi.org/10.1111/j.1365-2486.2011.02568.x.
  76. Peoples, M.B., J.R. Freney, and A.R. Mosier. 1995. Minimizing gaseous losses of nitrogen. Pp. 565–602 in Nitrogen Fertilization and the Environment. P.E. Bacon, ed., Marcel Dekker, NY. 
  77. Richardson, K., and B.B. Jørgensen. 1996. Eutrophication: Definition, history and effects. Pp. 1–19 in Eutrophication in Coastal Marine Ecosystems. B.B. Jørgensen and K. Richardson, eds, American Geophysical Union, Coastal and Estuarine Studies 52, Washington, DC. 
  78. Robertson, D.M., G.E. Schwarz, D.A. Saad, and R.B. Alexander. 2009. Incorporating uncertainty into the ranking of SPARROW Model nutrient yields from Mississippi/Atchafalya River basin. Journal of the American Water Resources Association 45:534–549, https://doi.org/​10.1111/j.1752-1688.2009.00310.x.
  79. Seitzinger, S.P., J.A. Harrison, E. Dumont, A.H.W. Beusen, and A.F. Bouwman. 2005. Sources and delivery of carbon, nitrogen and phosphorous to the coastal zone: An overview of global nutrient export from watersheds (NEWS) models and their application. Global Biogeochemical Cycles 19, GB4S01, https://doi.org/10.1029/2005GB002606.
  80. Seitzinger, S.P., E. Mayorga, A.F. Bouwman, C. Kroeze, A.H.W. Beusen, G. Billen, G. Van Drecht, E. Dumont, B.M. Fekete, J. Garnier, and others. 2010. Global river nutrient export: A scenario analysis of past and future trends. Global Biogeochemical Cycles 24, GB0A08, https://doi.org/​10.1029/​2009GB003587.
  81. Smayda, T.J. 1990. Novel and nuisance phytoplankton blooms in the sea: Evidence for a global epidemic. Pp. 29–40 in Toxic Marine Phytoplankton: Proceedings of the Fourth International Conference on Toxic Marine Phytoplankton, Held June 26-30 in Lund, Sweden. E. Granéli, B. Sundstrom, L. Edler, D.M. Anderson, eds, Elsevier, New York. 
  82. Smil, V. 2001. Enriching the Earth: Fritz Haber, Carl Bosch, and the Transformation of World Food. The MIT Press, Cambridge, MA, 338 pp.
  83. Stoecker, D.K., U. Tillmann, and E. Granéli. 2006. Phagotrophy in harmful algae. Pp. 177–187 in Ecology of Harmful Algae. E. Granéli and J.T. Turner, eds, Springer, Heidelberg, Germany.
  84. Sutton, M.A., A. Bleeker, C.M. Howard, M. Bekunka, B. Grizzetti, W. de Vries, H.J.M. van Grinsven, Y.P. Abrol, T.K. Adhya, G. Billen, and others. 2013. Our Nutrient World: The Challenge to Produce More Food and Energy with Less Pollution. Centre for Ecology and Hydrology, Edinburgh, UK, 114 pp.
  85. Swaney, D.P., B. Hong, A. Paneer Selvam, R.W. Howarth, R. Ramesh, and R. Purvaja. 2014. Net anthropogenic nitrogen inputs and nitrogen fluxes from Indian watersheds: An initial assessment. Journal of Marine Systems 141:45–58, https://doi.org/10.1016/j.jmarsys.2014.09.004.
  86. Tilman, D. 1977. Resource competition between planktonic algae: An experimental and theoretical approach. Ecology 58:338–348, https://doi.org/​10.2307/1935608.
  87. Van de Waal, D.B., G. Ferreruela, L. Tonk, E. Van Donk, J. Huisman, P.M. Visser, and H.C.P. Matthijs. 2010. Pulsed nitrogen supply induces dynamic changes in the amino acid composition and microcystin production of the harmful cyanobacterium Planktothrix agardhii. FEMS Microbiology Ecology 74:430–438, https://doi.org/10.1111/j.1574-6941.2010.00958.x.
  88. Van de Waal, D.B., J.M.H. Verspagen, M. Lürling, E. Van Donk, P.M. Visser, and J. Huisman. 2009. The ecological stoichiometry of toxins produced by harmful cyanobacteria: An experimental test of the carbon-nutrient balance hypothesis. Ecology Letters 12:1,326–1,335, https://doi.org/10.1111/j.1461-0248.2009.01383.x.
  89. Van Mooy, B.A.S., H.F. Fredricks, B.E. Pedler, S.T. Dyhrman, D.M. Karl, M. Koblížek, M.W. Lomas, T.J. Mincer, L.R. Moore, T. Moutin, and others. 2009. Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458:69–72, https://doi.org/10.1038/nature07659.
  90. Wells, M.L., V.L. Trainer, T.J. Smayda, B.S.O. Karlson, C.G. Trick, R.M. Kudela, A. Ishikawa, S. Bernard, A. Wulff, D.M. Anderson, and W.P. Cochlan. 2015. Harmful algal blooms and climate change: Learning from the past and present to forecast the future. Harmful Algae 49:68–93, https://doi.org/10.1016/​j.hal.2015.07.009.
  91. Willis, A., M.P. Adams, A.W. Chuang, P.T. Orr, K.R. O’Brien, and M.A. Burford. 2015. Constitutive toxin production under various nitrogen and phosphorus regimes of three ecotypes of Cylindrospermopsis raciborskii ((Wołoszyńska) Seenayya et Subba Raju). Harmful Algae 47:27–34, https://doi.org/10.1016/j.hal.2015.05.011.
  92. Wilhelm, C., C. Büchel, J. Fisahn, R. Goss, T. Jakob, J. LaRoche, J. Lavaud, M. Lohr, U. Riesbesell, K. Stehfest, and others. 2006. The regulation of carbon and nutrient assimilation in diatoms is significantly different from green algae. Protist 157:91–124, https://doi.org/10.1016/​j.protis.2006.02.003.
Copyright & Usage

This is an open access article made available under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution, and reproduction in any medium or format as long as users cite the materials appropriately, provide a link to the Creative Commons license, and indicate the changes that were made to the original content. Images, animations, videos, or other third-party material used in articles are included in the Creative Commons license unless indicated otherwise in a credit line to the material. If the material is not included in the article’s Creative Commons license, users will need to obtain permission directly from the license holder to reproduce the material.