Skip to main content
SpringerLink
Log in

Key Questions and Recent Research Advances on Harmful Algal Blooms in Relation to Nutrients and Eutrophication

  • Chapter
  • First Online:
Global Ecology and Oceanography of Harmful Algal Blooms

Part of the book series: Ecological Studies ((ECOLSTUD,volume 232))

Abstract

The Core Research Project on HABs in Eutrophic Systems was one of the projects implemented under the Global Ecology and Oceanography of Harmful Algal Blooms (GEOHAB) program. Building on several Open Science Meetings and associated international efforts, this project focused on a number of key questions that related to the types of harmful algal species found in eutrophic systems, the drivers of nutrient changes and their effects, as well as interactions with community composition of all members of the food web. Substantial progress was made on all of the identified key questions and that progress is reviewed in this chapter. In all, the evidence is unequivocal that harmful algae can be directly and/or indirectly stimulated by nutrient over-enrichment and that chronic, subtle effects, such as changes in nutrient proportion or form, can be equally important or even more important than the obvious, acute effects. Furthermore, nutrient enrichment interacts with other major drivers, such as hydrology, food web interactions, and climate change, in both direct and indirect ways. Many questions remain, however. Much needs to be done in parameterizing rates, characterizing traits, and how they are both externally driven and internally dynamically regulated. Many species are understudied. Work needs to advance in understanding the physiological responses to excess nutrient availability and relationships with toxicity, among other physiological processes. A new emphasis on improved model formulations is needed, linking land-use models with regional ocean models and that incorporate dynamic physiological behavior. Given the pace at which nutrient loads continue to pollute the global landscape and the global expansion of HABs, continued international collaborative efforts in understanding changing nutrients and their relationships with HABs are not only necessary, but urgently needed.

Paul J. Harrison was deceased at the time of publication.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adolf JE, Bachvaroff T, Place AR (2008a) Cryptophyte abundance drives blooms of mixotrophic harmful algae: a hypothesis based on Karlodinium veneficum as a model system. Harmful Algae 8:119–128

    Article  CAS  Google Scholar 

  • Adolf JE, Bachvaroff T, Place AR (2008b) Can cryptophytes trigger toxic Karlodinium veneficum blooms in eutrophic estuaries? Harmful Algae 81:19–128

    Google Scholar 

  • Al-Azri A, Piontkovski SA, Al-Hashmi KA et al (2014) Mesoscale and nutrient conditions associated with the massive 2008 Cochlodinium polykrikoides bloom in the Sea of Oman/Arabian Gulf. Estuar Coasts 37:325–338

    Article  CAS  Google Scholar 

  • Allen JI, Polimene L (2011) Linking physiology to ecology: towards a new generation of plankton models. J Plankton Res 33:989–997. https://doi.org/10.1093/plankt/fbr032

    Article  Google Scholar 

  • Alonso-Rodríguez R, Páez-Osuna F (2003) Nutrients, phytoplankton and harmful algal blooms in shrimp ponds: a review with special reference to the situation in the Gulf of California. Aquaculture 219:317–336

    Article  Google Scholar 

  • Alvarez-Salgado XA, Figueiras FG, Perez FF et al (2003) The Portugal coastal counter current of NW Spain: new insights on its biogeochemical variability. Prog Oceanogr 56:281–321

    Article  Google Scholar 

  • Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:562–584

    Article  Google Scholar 

  • Azanza RV, Fukuyo Y, Yap LG et al (2005) Prorocentrum minimum bloom and its possible link to a massive fish kill in Bolinae, Pangasian, northern Philippines. Harmful Algae 4:519–524

    Article  Google Scholar 

  • Bates SS, de Freitas ASW, Milley JE et al (1991) Controls on domoic acid production by the diatom Nitzschia pungens c.f. multiseries in culture: nutrients and irradiance. Can J Fish Aquat Sci 48:1136–1144

    Article  CAS  Google Scholar 

  • Beusen AHW, Bouwman AF, Van Beek LPH et al (2016) Global riverine N and P transport to ocean increased during the 20th century despite increased retention along the aquatic continuum. Biogeosciences 13:2441–2451. https://doi.org/10.5194/bg-13-2441-2016

    Article  CAS  Google Scholar 

  • Beusen AHW, Van Beek LPH, Bouwman AF et al (2015) Coupling global models for hydrology and nutrient loading to simulate nitrogen and phosphorus retention in surface water. Description of IMAGE-GNM and analysis of performance. Geosci Model Dev 8:4045–4067. https://doi.org/10.5194/gmd-4048-4045-2015

    Article  CAS  Google Scholar 

  • Bond NA, Cronin MF, Freeland H et al (2015) Causes and impacts of the 2014 warm anomaly in the NE Pacific. Geophys Res Lett 42:3414–3420

    Article  Google Scholar 

  • Bouwman AF, Beusen AHW, Glibert PM et al (2013a) Mariculture: significant and expanding cause of coastal nutrient enrichment. Environ Res Lett 8(044026):5. https://doi.org/10.1088/1748-9326/8/4/044026

    Article  Google Scholar 

  • Bouwman AF, Beusen AHW, Lassaletta L et al (2017) Lessons from temporal and spatial patterns in global use of N and P fertilizer on cropland. Sci Rep. https://doi.org/10.1038/srep40366

  • Bouwman AF, Beusen AHW, Overbeek CC et al (2013b) Hindcasts and future projections of global inland and coastal nitrogen and phosphorus loads due to finfish aquaculture. Rev Fish Sci 21:112–158

    Article  CAS  Google Scholar 

  • Bouwman AF, Pawlowski M, Liu C et al (2011) Global hindcasts and future projections of coastal nitrogen and phosphorus loads due to shellfish and seaweed aquaculture. Rev Fish Sci 19:331–357

    Article  CAS  Google Scholar 

  • Boyd PW, Doney SC (2003) The impact of climate change and feedback processes on the ocean carbon cycle. In: Fasham MJR (ed) Ocean biogeochemistry – the role of the ocean carbon cycle in global change. Springer, Berlin, pp 157–193

    Google Scholar 

  • Boyd PW, Hutchins DA (2012) Understanding the responses of ocean biota to a complex matrix of cumulative anthropogenic change. Mar Ecol Prog Ser 470:125–135

    Article  Google Scholar 

  • Bricker SB, Longstaff B, Dennison W et al (2007) Effects of nutrient enrichment in the Nation’s estuaries: a decade of change, NOAA coastal ocean program decision analysis series No. 26. National Center for Coastal Ocean Science, Silver Spring, MD, p 328

    Google Scholar 

  • Burford MA, Davis TW, Orr PT et al (2014) Nutrient-related changes in the toxicity of field blooms of the cyanobacterium Cylindrospermopsis raciborskii. FEMS Microbiol Ecol 89:135–148

    Article  PubMed  CAS  Google Scholar 

  • Burford MA, Longmore AR (2001) High ammonium production from sediments in hypereutrophic aquaculture ponds. Mar Ecol Prog Ser 224:187

    Article  CAS  Google Scholar 

  • Burford MA, Pearson D (1998) Effect of different nitrogen sources on phytoplankton composition in aquaculture ponds. Aquat Microb Ecol 15:277–284

    Article  Google Scholar 

  • Burford MA, Williams KC (2001) The fate of nitrogenous waste from shrimp feeding. Aquaculture 198:79–93

    Article  CAS  Google Scholar 

  • Burkholder JM, Dickey DA, Kinder C et al (2006) Comprehensive trend analysis of nutrients and related variables in a large eutrophic estuary: a decadal study of anthropogenic and climatic influences. Limnol Oceanogr 51:463–487

    Article  CAS  Google Scholar 

  • Burkholder JM, Eggleston D, Glasgow H et al (2004) Comparative impacts of two major hurricane seasons on the Neuse River and western Pamlico Sound ecosystems. Proc Natl Acad Sci USA 101:9291–9296

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Burkholder JM, Glibert PM, Skelton H (2008) Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8:77–93

    Article  CAS  Google Scholar 

  • Burkholder JM, Shumway SE, Glibert PM (2018) Food webs and ecosystem impacts of harmful algae. In: Shumway S, Burkholder JM, Morton SL (eds) Harmful algal blooms: a compendium desk reference. Wiley

    Google Scholar 

  • Buskey EJ, Liu H, Collumb C et al (2001) The decline and recovery of a persistent Texas brown tide algal bloom in the Laguna Madre (Texas, USA). Estuaries 24:337–346

    Article  Google Scholar 

  • Cannon JA (1990) Development and dispersal of red tides in the Port River, South Australia. In: Granéli E, Sundstroem B, Edler L et al (eds) Toxic marine phytoplankton. Elsevier, New York, pp 110–115

    Google Scholar 

  • Chen C-C, Gong G-C, Shiah F-K (2007) Hypoxia in the East China Sea: one of the largest coastal low oxygen areas in the world. Mar Environ Res 64:399–408

    Article  PubMed  CAS  Google Scholar 

  • Cloern JE (2001) Our evolving conceptual model of the coastal eutrophication problem. Mar Ecol Prog Ser 210:223–253

    Article  CAS  Google Scholar 

  • Davis TL, Berry DL, Boyer GL et al (2009) The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 8:715–725

    Article  CAS  Google Scholar 

  • Doney SC (2010) The growing human footprint on coastal and open ocean biogeochemistry. Science 328:1512–1516

    Article  PubMed  CAS  Google Scholar 

  • Duan SW, Liang T, Zhang S et al (2008) Seasonal changes in nitrogen and phosphorus transport in the lower Changjiang River before the construction of the Three Gorges Dam. Estuar Coast Shelf Sci 79:239–250

    Article  Google Scholar 

  • Dumont E, Harrison JA, Kroeze C et al (2005) Global distribution and sources of dissolved inorganic nitrogen export to the coastal zone: results from a spatially explicit, global model. Global Biogeochem Cycles 19:GB4S02

    Article  CAS  Google Scholar 

  • Dürr HH, Laruelle GG, van Kempen CM et al (2011) Worldwide typology of nearshore coastal sys tems: defining the estuarine filter of river inputs to the oceans. Estuar Coasts 34:441–458

    Article  Google Scholar 

  • Elser JJ, Sterner RW, Gorokhova E et al (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3:540–550

    Article  Google Scholar 

  • Fang TH (2004) Phosphorus speciation and budget of the East China Sea. Cont Shelf Res 24:1285–1299

    Article  Google Scholar 

  • Flynn KA, Clark DR, Mitra A et al (2015) Ocean acidification with (de)eutrophication will alter future phytoplankton growth and succession. Philos Trans R Soc B 282:20142604

    Google Scholar 

  • Flynn KJ, Mitra A, Glibert PM et al (2018) Mixotrophy by HABs: by whom, on whom, when, why and what next. In: Glibert PM, Berdalet E, Burford M et al (eds) Global ecology and oceanography of harmful algal blooms. Springer, Cham, pp 113–132

    Chapter  Google Scholar 

  • Flynn KJ, Stoecker DK, Mitra A et al (2013) Misuse of the phytoplankton-zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. J Plankton Res 35:3–11

    Article  Google Scholar 

  • Freeland H, Whitney F (2014) Unusual warming in the Gulf of Alaska. North Pac Mar Org (PICES) Press 22:51–52

    Google Scholar 

  • Fu M, Wang Z, Pu X et al (2012) Changes in nutrient concentrations and N:P:Si ratios and their possible impacts on the Huanghai Sea ecosystem. Acta Oceanol Sinica 31:101–112

    Article  CAS  Google Scholar 

  • Galloway JN, Cowling EB, Seitzinger SP et al (2002) Reactive nitrogen: too much of a good thing? Ambio 31:60–63

    Article  PubMed  Google Scholar 

  • GEOHAB (2001) Global ecology and oceanography of harmful algal blooms, science plan. Glibert P, Pitcher G (eds) SCOR and IOC, Baltimore and Paris, 86 pp

    Google Scholar 

  • GEOHAB (2005) Global ecology and oceanography of harmful algal blooms: HABs in eutrophic systems. Glibert PM (ed) IOC and SCOR, Paris and Baltimore, 74 pp

    Google Scholar 

  • GEOHAB (2010) Global ecology and oceanography of harmful algal blooms in Asia. Furuya K, Glibert PM, Zhou M et al (eds) IOC and SCOR, Paris and Newark, Delaware, 68 pp

    Google Scholar 

  • Glibert PM (1998) Interactions of top-down and bottom-up control in planktonic nitrogen cycling. Hydrobiology 363:1–12

    Article  Google Scholar 

  • Glibert PM (2017) Eutrophication, harmful algae and biodiversity – challenging paradigms in a world of complex nutrient changes. Mar Pollut Bull 124:591–606. https://doi.org/10.1016/j.marpolbul.2017.04.027

    Article  PubMed  CAS  Google Scholar 

  • Glibert PM, Allen JI, Artioli Y et al (2014b) Vulnerability of coastal ecosystems to changes in harmful algal bloom distribution in response to climate change: projections based on model ana lysis. Glob Chang Biol 20:3845–3858. https://doi.org/10.1111/gcb.12662

    Article  PubMed  Google Scholar 

  • Glibert PM, Beusen AHW, Harrison JA et al (2018) Changing land-, sea- and airscapes: sources of nutrient pollution affecting habitat suitability for harmful algae. In: Glibert PM, Berdalet E, Burford M et al (eds) Global ecology and oceanography of harmful algal blooms. Springer, Cham, pp 53–76

    Chapter  Google Scholar 

  • Glibert PM, Boyer J, Heil C et al (2010) Blooms in lagoons: different from those of river-dominated estuaries. In: Kennish M, Paerl H (eds) Coastal lagoons: critical habitats of environmental change. Taylor and Francis, Boca Raton, FL, pp 91–114

    Chapter  Google Scholar 

  • Glibert PM, Burford MA (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

    Article  Google Scholar 

  • Glibert PM, Burkholder JM (2006) The complex relationships between increasing fertilization of the earth, coastal eutrophication and proliferation of harmful algal blooms. In: Granéli E, Turner J (eds) Ecology of harmful algae. Springer, New York, NY, pp 341–354

    Chapter  Google Scholar 

  • Glibert PM, Burkholder JM (2011) Eutrophication and HABs: strategies for nutrient uptake and growth outside the Redfield comfort zone. Chin J Oceanol Limnol 29:724–738

    Article  Google Scholar 

  • Glibert PM, Burkholder JM (2017) Causes of harmful algal blooms. In: Shumway S, Burkholder JM, Morton SL (eds) Harmful algal blooms: a compendium desk reference. Wiley (in press)

    Google Scholar 

  • Glibert PM, Burkholder JM, Granéli E et al (2008a) Advances and insights in the complex relationships between eutrophication and HABs: preface to the special issue. Harmful Algae 8:1–2

    Article  Google Scholar 

  • Glibert PM, Burkholder JM, Kana TM et al (2009a) Grazing by Karenia brevis on Synechococcus enhances their growth rate and may help to sustain blooms. Aquat Microb Ecol 55:17–30

    Article  Google Scholar 

  • Glibert PM, Burkholder JM, Kana TM (2012) Recent advances in understanding of relationships between nutrient availability, forms and stoichiometry and the biogeographical distribution, ecophysiology, and food web effects of pelagic and benthic Prorocentrum spp. Harmful Algae 14:231–259

    Article  Google Scholar 

  • Glibert PM, Fullerton D, Burkholder JM et al (2011) Ecological stoichiometry, biogeochemical cycling, invasive species and aquatic food webs: San Francisco Estuary and comparative systems. Rev Fish Sci 19:358–417

    Article  Google Scholar 

  • Glibert PM, Harrison JA, Heil CA et al (2006) Escalating worldwide use of urea – a global change contributing to coastal eutrophication. Biogeochemistry 77:441–463

    Article  CAS  Google Scholar 

  • Glibert PM, Heil CA, Hollander D et al (2004) Evidence for dissolved organic nitrogen and phosphorus uptake during a cyanobacterial bloom in Florida Bay. Mar Ecol Prog Ser 280:73–83

    Article  Google Scholar 

  • Glibert PM, Heil CA, Rudnick D et al (2009b) Florida Bay: status, trends, new blooms, recurrent problems. Contrib Mar Sci 38:5–17

    Google Scholar 

  • Glibert PM, Kana TM, Brown K (2013) From limitation to excess: consequences of substrate excess and stoichiometry for phytoplankton physiology, trophodynamics and biogeochemistry, and implications for modelling. J Mar Syst 125:14–28. https://doi.org/10.1016/j.jmarsys.2012.10.004

    Article  Google Scholar 

  • Glibert PM, Maranger R, Sobota DJ et al (2014a) The Haber-Bosch–harmful algal bloom (HB-HAB) link. Environ Res Lett 9:105001 (13 p). https://doi.org/10.1088/1748-9326/9/10/105001

    Article  CAS  Google Scholar 

  • Glibert PM, Mayorga E, Seitzinger S (2008b) Prorocentrum minimum tracks anthropogenic nitrogen and phosphorus inputs on a global basis: application of spatially explicit nutrient export models. Harmful Algae 8:33–38

    Article  CAS  Google Scholar 

  • Glibert PM, Seitzinger S, Heil CA et al (2005) The role of eutrophication in the global proliferation of harmful algal blooms: new perspectives and new approaches. Oceanography 18(2):198–209

    Article  Google Scholar 

  • Glibert PM, Wilkerson FP, Dugdale RC et al (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. Limnol Oceanogr 61:165–197

    Article  CAS  Google Scholar 

  • Gobler CJ, Burkholder JM, Davis TW et al (2016) The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms. Harmful Algae 54:87–97

    Article  PubMed  CAS  Google Scholar 

  • Goolsby DA, Battaglin WA (2001) Long-term changes in concentrations and flux of nitrogen in the Mississippi River basin, USA. Hydrol Process 15:1209–1226

    Article  Google Scholar 

  • Granéli E, Edler L, Gedziorowska D et al (1985) Influence of humic and fulvic acids on Prorocentrum minimum (Pav.) Schiller. In: Anderson DM, White AW, Baden DG (eds) Toxic dino flagellates. Elsevier, New York, NY, pp 201–206

    Google Scholar 

  • Granéli E, Flynn K (2006) Chemical and physical factors influencing toxin content. In: Granéli E, Turner J (eds) The ecology of harmful algae. Springer, New York, NY, pp 229–241

    Chapter  Google Scholar 

  • Granéli E, Johansson N (2003) Increase in the production of allelopathic substances by Prymnesium parvum cells grown under N- or P-deficient conditions. Harmful Algae 2:135–145

    Article  CAS  Google Scholar 

  • Granéli E, Olsson P, Sundstrøm B et al (1989) In situ studies of the effects of humic acids on dinoflagellates and diatoms. In: Okaichi T, Anderson DM, Nomoto T (eds) Red tides: biology, environmental science and toxicology. Elsevier, New York, NY, pp 209–212

    Google Scholar 

  • Hajdu S, Pertola S, Kuosa H (2005) Prorocentrum minimum (Dinophyceae) in the Baltic Sea: morphology, occurrence – a review. Harmful Algae 4:471–480

    Article  CAS  Google Scholar 

  • Hansen PJ (2011) The role of photosynthesis and food uptake for the growth of marine mixotrophic dinoflagellates. J Eukaryot Microbiol 58:203–214

    Article  PubMed  CAS  Google Scholar 

  • Hardison DR, Sunda WG, Litaker RW et al (2012) Nitrogen limitation increases brevetoxins in Karenia brevis (Dinophyceae): implications for bloom toxicity. J Phycol 48:844–858

    Article  CAS  Google Scholar 

  • Hardison DR, Sunda WG, Shea D et al (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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Harris GP (1986) Phytoplankton ecology: structure, function and fluctuation. Chapman and Hall, London

    Book  Google Scholar 

  • Harris TD, Smith VH, Graham JL et al (2016) Combined effects of nitrogen to phosphorus and nitrate to ammonia ratios on cyanobacterial metabolite concentrations in eutrophic Midwestern USA reservoirs. Inland Wat 6:199–210

    Article  CAS  Google Scholar 

  • Harrison JA, Caraco NF, Seitzinger SP (2005a) Global patterns and sources of dissolved organic matter export to the coastal zone: results from a spatially explicit, global model. Global Biogeochem Cycles 19:GB4S04

    Google Scholar 

  • Harrison JA, Seitzinger SP, Caraco N et al (2005b) Dissolved inorganic phosphorous export to the coastal zone: results from a new, spatially explicit, global model (NEWS-SRP). Global Biogeochem Cycles 19:GB4S03

    Google Scholar 

  • Heil CA, Glibert PM, Fan C (2005) Prorocentrum minimum (Pavillard) Schiller – a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae 4:449–470

    Article  CAS  Google Scholar 

  • Heisler J, Glibert PM, Burkholder JM et al (2008) Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae 8:3–13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hitchcock G, Phlips E, Brand L et al (2007) Plankton blooms. In: Hunt JH, Nuttle W (eds) Florida Bay science program: a synthesis of research on Florida Bay. Fish and Wildlife Research Institute Technical Report TR-11. Florida Fish and Wildlife Research Institute, St Petersburg, FL, pp 77–91

    Google Scholar 

  • Holland E, Dentener F, Braswell B et al (1999) Contemporary and preindustrial global reactive nitrogen budgets. Biogeochemistry 4:7–43

    Google Scholar 

  • Honkanen T, Helminen H (2000) Impacts of fish farming on eutrophication: comparisons among different characteristics of ecosystem. Int Rev Hydrobiol 85:673–686

    Article  Google Scholar 

  • Howarth RW (2008) Coastal nitrogen pollution: a review of sources and trends globally and regionally. Harmful Algae 8:14–20

    Article  CAS  Google Scholar 

  • Howarth RW, Billen G, Swaney D et al (1996) Regional nitrogen budgets and riverine N & P fluxes for the drainages to the North Atlantic Ocean: natural and human in influences. Biogeochemistry 35:75–139

    Article  CAS  Google Scholar 

  • Howarth RW, Sharpley A, Walker D (2002) Sources of nutrient pollution to coastal waters in the United States: implications for achieving coastal water quality goals. Estuaries 25:656–676

    Article  CAS  Google Scholar 

  • Hu C, Li D, Chen C et al (2010) On the recurrent Ulva prolifera blooms in the Yellow Sea and East China Sea. Marine Science Faculty Publications Paper 58. http://scholarcommons.usf.edu/msc_facpub/58

  • Intergovernmental Panel on Climate Change (IPCC) Core Writing Team (2007) Climate change 2007: synthesis report. In: Pachauri RK, Reisinger A (eds) Contribution of working groups I, II and III to the fourth assessment report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, p 104

    Google Scholar 

  • Intergovernmental Panel on Climate Change (IPCC) core Writing Team (2014) Climate change 2014: synthesis report. In: Pachauri RK, Meyer LA (eds) Contribution of working groups I, II and III to the fifth assessment report of the Intergovernmental Panel on Climate Change. IPCC, Geneva

    Google Scholar 

  • Jeong HJ, Park JY, Nho JH et al (2005) Feeding by red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquat Microb Ecol 41:131–143

    Article  Google Scholar 

  • Jeong HJ, Yoo YD, Kim TH et al (2004) Mixotrophy in the phototrophic harmful alga Cochlodinium polykrikoides (Dinophyceae): prey species, the effects of prey concentration and grazing impact. J Eukaryot Microbiol 51:563–569

    Article  PubMed  Google Scholar 

  • Jeong HJ, Yoo YD, Kim JS et al (2010) Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci J 45:65–91

    Article  CAS  Google Scholar 

  • Johansson N, Granéli E (1999) Influence of different nutrient conditions on cell density, chemical composition and toxicity of Prymnesium parvum (Haptophyta) in semi-continuous cultures. J Exp Mar Biol Ecol 239:243–258

    Article  CAS  Google Scholar 

  • Kaushik SJ, Cowey CB (1991) Dietary factors affecting nitrogen excretion by fish. In: Cowey CB, Cho CY (eds) Nutritional strategies and aquaculture waste. Proceedings of the 1st International symposium on nutritional strategies in management of aquaculture waste. University of Guelph, Ontario, Canada, pp 3–19

    Google Scholar 

  • Kimmerer WJ (2002) Physical, biological and management responses to variable freshwater flow into the San Francisco Estuary. Estuaries 25:1275–1290

    Article  Google Scholar 

  • Kremp A, Godhe A, Egardt J et al (2012) Strain variability in the response of bloom-forming marine microalgae to changed climate conditions. Ecol Evol 2:1195–1207

    Article  PubMed  PubMed Central  Google Scholar 

  • Kudela RM, Gobler CJ (2012) Harmful dinoflagellate blooms caused by Cochlodinium sp.: global expansion and ecological strategies facilitating bloom formation. Harmful Algae 14:71–86

    Article  Google Scholar 

  • Kudela RM, Lane JQ, Cochlan WP (2008a) The potential role of anthropogenically derived nitrogen in the growth of harmful algae in California, USA. Harmful Algae 8:103–110

    Article  CAS  Google Scholar 

  • Kudela RM, Ryan JP, Blakeley MD et al (2008b) Linking the physiology and ecology of Cochlodinium to better understand harmful algal bloom events: a comparative approach. Harmful Algae 7:278–292

    Article  CAS  Google Scholar 

  • Larsen J, Eikrem W, Paasche E (1993) Growth and toxicity in Prymnesium patelliferum (Prymnesiophycae) isolated from Norwegian waters. Can J Bot 71:1357–1362

    Article  CAS  Google Scholar 

  • Larsen J, Sournia A (1991) Diversity of heterotrophic dinoflagellates. In: Patterson DJ, Larsen J (eds) The biology of free-living heterotrophic dinoflagellates. Clarendon Press, Oxford, pp 313–332

    Google Scholar 

  • Laruelle GG (2009) Quantifying nutrient cycling and retention in coastal waster at the global scale. PhD dissertation, Geologica Ultraiectina. Mededelingen van de Faculteit Geowetenschappen Universiteit Utrecht No. 312, Utrecht University, Utrecht, p 226

    Google Scholar 

  • Lee MO, Kim JK (2008) Characteristics of algal blooms in the southern coastal waters of Korea. Mar Environ Res 65:128–147

    Article  PubMed  CAS  Google Scholar 

  • Lehman PW, Boyer G, Hall C et al (2005) Distribution and toxicity of a new colonial Microcystis aeruginosa bloom in the San Francisco Bay Estuary, California. Hydrobiologia 541:87–99

    Article  CAS  Google Scholar 

  • Lehman PW, Boyer G, Stachwell M et al (2008) The influence of environmental conditions on seasonal variation of Microcystis abundance and microcystins concentration in San Francisco Estuary. Hydrobiologia 600:187–204

    Article  CAS  Google Scholar 

  • Lehner B, Liermann CR, Revenga C et al (2011) High-resolution mapping of the world’s reservoirs and dams for sustainable river-flow management. Front Ecol Environ 9:494–502

    Article  Google Scholar 

  • Lewis NI, Bates SS, McLachlan JL et al (1993) Temperature effects on growth, domoic acid production, and morphology of the diatom Nitzschia-pungens f. multiseries. In: Smayda TJ, Shimizu Y (eds) Toxic phytoplankton blooms in the sea. Elsevier Science Publications B V, Amsterdam, pp 601–606

    Google Scholar 

  • Li J, Glibert PM, Zhou M et al (2009) Relationships between nitrogen and phosphorus forms and ratios and the development of dinoflagellate blooms in the East China Sea. Mar Ecol Prog Ser 383:11–26

    Article  CAS  Google Scholar 

  • Li J, Glibert PM, Zhou M (2010) Temporal and spatial variability in nitrogen uptake kinetics during harmful dinoflagellate blooms in the East China Sea. Harmful Algae 9:531–539

    Article  CAS  Google Scholar 

  • Liermann CR, Nilsson C, Robertson J et al (2012) Implications of dam obstruction for global freshwater fish diversity. Biosciences 62:539–548

    Article  Google Scholar 

  • Lin C-H, Accoroni S, Glibert PM (2017) Mixotrophy in the dinoflagellate Karlodinium veneficum under variable nitrogen:phosphorus stoichiometry: feeding response and effects on larvae of the eastern oyster (Crassostrea virginica). Aquat Microb Ecol 79:101–114. https://doi.org/10.3354/ameo01823.

    Article  Google Scholar 

  • Liu D, Zhou MJ (2018) Green tides of the Yellow Sea: massive free-floating blooms of Ulva prolifera. In: Glibert PM, Berdalet E, Burford M et al (eds) Global ecology and oceanography of harmful algal blooms. Springer, Cham, pp 317–326

    Chapter  Google Scholar 

  • Lomas MW, Glibert PM (1999) Temperature regulation of nitrate uptake: a novel hypothesis about nitrate uptake and reduction in cool-water diatoms. Limnol Oceanogr 44:556–572

    Article  CAS  Google Scholar 

  • Lu D, Goebel J (2001) Five red tide species in genus Prorocentrum including the description of Prorocentrum donghaiense Lu sp. nov. from the East China Sea. China Chin J Oceanol Limnol 19:337–344

    Article  Google Scholar 

  • Lu D, Goebel J, Qi Y et al (2005) Morphology and genetic study of Prorocentrum donghaiense Lu from the East China Sea, and comparison with some related Prorocentrum species. Harmful Algae 4:493–506

    Article  CAS  Google Scholar 

  • Lu D, Wang H, Huang H et al (2011) Morphological and genetic comparison of two strains of a Prorocentrum species isolated from Zhejiang coastal water of China and Masan Bay of Korea. Chin J Oceanol Limnol 29:832–839

    Article  Google Scholar 

  • Lundgren V, Glibert PM, Granéli E et al (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

    Article  PubMed  CAS  Google Scholar 

  • Madden CJ, Smith R, Dettmann E et al (2010) Estuarine typology development and application. In: Glibert P, Madden C, Boynton W et al (eds) Estuarine nutrient criteria development: state of the science. EPA Office of Water. http://www2.epa.gov/sites/production/files/documents/nutrients-in-estuaries-november-2010.pdf

  • Malone TC, Conley DJ, Glibert PM et al (1996) Scales of nutrient limited phytoplankton productivity: the Chesapeake Bay example. Estuaries 19:371–385

    Article  CAS  Google Scholar 

  • Marasović I, Pucher-Petkovic T, Petrova-Karadjova V (1990) Prorocentrum minimum (Dinophyceae) in the Adriatic and Black Sea. J Mar Biol Assoc UK 70:473–476

    Article  Google Scholar 

  • Martinez-Lopez A, Escobedo-Urias DC, Ulloa-Perez AE et al (2008) Dynamics of a Prorocentrum minimum bloom along the northern coast of Sinaloa, Mexico. Cont Shelf Res 28:1693–1701

    Article  Google Scholar 

  • Matsuoka K, Takano Y, Kamrani E et al (2010) Study on Cochlodinium polykrikoides Margalef in the Oman Sea and the Persian Gulf from August 2008 to August 2009. Curr Dev Oceanogr 1:153–171

    Google Scholar 

  • Mayorga E, Seitzinger SP, Harrison JA et al (2010) Global nutrient export from WaterSheds 2 (NEWS 2): model development and implementation. Environ Model Softw 25(7):837–853

    Article  Google Scholar 

  • McCabe RM, Hickey BM, Kudela RM et al (2016) An unprecedented coastwide toxic algal bloom linked to anomalous ocean conditions. Geophys Res Lett. https://doi.org/10.1002/2016GL070023

  • Miller, WD, Harding LW, Adolf JE (2005) The influence of Hurricane Isabel on Chesapeake Bay phytoplankton dynamics. In: Sellner KG (ed) Hurricane Isabel in perspective, Chesapeake Research Consortium Publication 05-160, Edgewater, Maryland, pp 155–160

    Google Scholar 

  • Miller WD, Harding LW, Adolf JE (2006) Hurricane Isabel generated an unusual fall bloom in Chesapeake Bay. Geophys Res Lett 33:LO6612. https://doi.org/10.1029/2005GL025658

    Article  Google Scholar 

  • Minnhagen S, Kim M, Salomon P et al (2011) Active uptake of kleptoplastids by Dinophysis caudata from its ciliate prey Myrionecta rubra. Aquat Microb Ecol 62:99–108

    Article  Google Scholar 

  • Monchamp ME, Pick FR, Beisner BE et al (2014) Variation in microcystin concentration and composition in relation to cyanobacterial community structure. PLoS One 9(1):e85573. https://doi.org/10.1371/journal.pone0085573

    Article  PubMed  PubMed Central  Google Scholar 

  • Moncheva D, Petrova Kardjova V, Palasov A (1995) Harmful algal blooms along the Bulgarian sea coast and possible patterns of fish and zoobenthos mortalities. In: Lassus P, Arzul G, Erard-Le Denn E et al (eds) Harmful marine algal blooms. Lavoisier, Paris, pp 193–198

    Google Scholar 

  • Moore SK, Trainer VL, Mantua NJ et al (2008) Impacts of climate variability and future change on harmful algal blooms and human health. Environ Health 7:S4. https://doi.org/10.1186/1476-069X-7-S2-S4

    Article  PubMed  PubMed Central  Google Scholar 

  • Mulholland MR, Morse RE, Boneillo GE et al (2009) Understanding causes and impacts of the dinoflagellate, Cochlodinium polykrikoides, blooms in the Chesapeake Bay. Estuaries 32:734–747

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ogata T, Kodama M, Ishimaru T (1989) Effect of water temperature and light intensity on growth rate and toxin production of toxic dinoflagellates. In: Okaichi T, Anderson DM, Nemoto T (eds) Red tides, biology, environmental science and toxicology. Elsevier, New York, NY, pp 423–426

    Google Scholar 

  • Olenina I, Wasmund N, Hajdu S et al (2010) Assessing impacts of invasive phytoplankton: the Baltic Sea case. Mar Pollut Bull 60:1691–1700

    Article  PubMed  CAS  Google Scholar 

  • Paerl HW, Huisman J (2008) Blooms like it hot. Science 3320:57–58

    Article  Google Scholar 

  • Paerl HW, Scott JT (2010) Throwing fuel on the fire: synergistic effects of excessive nitrogen inputs and global warming on harmful algal blooms. Environ Sci Technol 44:7756–7758

    Article  PubMed  CAS  Google Scholar 

  • Pan YL, Subba Rao DV, Mann KH (1996) Changes in domoic acid production and cellular chemical composition of the toxigenic diatom Pseudo-nitzschia multiseries under phosphate limitation. J Phycol 32:371–381

    Article  CAS  Google Scholar 

  • Pennock JR (1985) Chlorophyll distributions in the Delaware Estuary: regulation by light limitation. Estuar Coast Shelf Sci 21:711–725

    Article  CAS  Google Scholar 

  • Peñuelas J, Sardans J, Rivas-Ubach A et al (2012) The human-induced imbalance between C, N and P in Earth’s life system. Glob Chang Biol 18:3–6

    Article  Google Scholar 

  • Pertola S, Kuosa H, Olsonen R (2005) Is the invasion of Prorocentrum minimum (Dinophyceae) related to the nitrogen enrichment of the Baltic Sea? Harmful Algae 4:481–492

    Article  CAS  Google Scholar 

  • Raven JA, Beardall J, Flynn KJ et al (2009) Phagotrophy in the origins of photosynthesis in eukaryotes and as a complementary mode of nutrition in phototrophs: relation to Darwin’s insectivorous plants. J Exp Bot 60:3975–3987. https://doi.org/10.1093/jxb/erp282

    Article  PubMed  CAS  Google Scholar 

  • Redfield AC (1934) On the proportions of organic derivatives in sea water and their relation to the composition of plankton. In: James Johnstone memorial volume. University of Liverpool Press, Liverpool, pp 176–192

    Google Scholar 

  • Richlen ML, Morton SL, Jamali EA et al (2010) The catastrophic 2008-2009 red tide in the Arabian Gulf region, with observations on the identification and phylogeny of the fish-killing dinoflagellate Cochlodinium polykrikoides. Harmful Algae 9:163–172

    Article  Google Scholar 

  • Seitzinger SP, Harrison JA, Dumont E et al (2005) Sources and delivery of carbon, nitrogen, and phosphorus to the coastal zone: an overview of global nutrient export from Watersheds (NEWS) models and their application. Global Biogeochem Cycles 19:GB4S01. https://doi.org/10.1029/2005gb002606

    Article  Google Scholar 

  • Seitzinger SP, Kroeze C, Bouwman AF et al (2002) Global patterns of dissolved in organic and particulate nitrogen inputs to coastal systems: recent conditions and future projections. Estuaries 25:640–655

    Article  CAS  Google Scholar 

  • Seitzinger SP, Mayorga E, Bouwman AF et al (2010) Global river nutrient export: a scenario analysis of past and future trends. Global Biogeochem Cycles 24:GB0A08. https://doi.org/10.1029/2009GB003587

    Article  CAS  Google Scholar 

  • Shackeroff JM, Hazen EL, Crowder LB (2009) The oceans as peopled seascapes. In: McLeod K, Leslie H (eds) Ecosystem based management for the oceans. Island Press, Washington, DC, pp 33–54

    Google Scholar 

  • Shangguan Y, Glibert PM, Alexander JA et al (2017) Nutrients and phytoplankton community composition in semi-enclosed lagoon systems in Florida Bay and their responses to changes in flow from Everglades restoration. Limnol Oceanogr 62:S327–S347. https://doi.org/10.1002/lno.10599

  • Sierra-Beltran AP, Cortes-Altamirano R, Cortes-Lara MC (2005) Occurrences of Prorocentrum minimum (Pavillard) in Mexico. Harmful Algae 4:507–518

    Article  Google Scholar 

  • Silva ES (1985) Ecological factors related to Prorocentrum minimum blooms in Obidos Lagoon (Portugal). In: Anderson DM, White A, Baden D (eds) Toxic dinoflagellates. Elsevier, New York, NY, pp 251–256

    Google Scholar 

  • Smil V (2001) Enriching the Earth: Fritz Haber, Carl Bosch, and the transformation of world food. The MIT Press, Cambridge

    Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton, NJ, p 439

    Google Scholar 

  • Stonik IV (1995) A potentially toxic dinoflagellate, Prorocentrum minimum, in Amurskii Bay of the Sea of Japan. Russ J Mar Biol Assoc UK 20:314–320

    Google Scholar 

  • Stukel MR, Landry MR, Selph KE (2011) Nanoplankton mixotrophy in the eastern equatorial Pacific. Deep Sea Res Part II 58:378–386

    Article  CAS  Google Scholar 

  • Sun J, Hutchins DA, Feng YY et al (2011) Effects of changing pCO2 and phosphate availability on domoic acid production and physiology of the marine harmful bloom diatom Pseudo-nitzschia multiseries. Limnol Oceanogr 56:829–840

    Article  CAS  Google Scholar 

  • Sunda WG, Granéli E, Gobler CJ (2006) Positive feedback and the development and persistence of ecosystem disruptive algal blooms. J Phycol 42:963–974

    Article  Google Scholar 

  • Sutton MA, Bleeker A, Howard CM et al (2013) Our nutrient world: the challenge to produce more food and energy with less pollution. Centre for Ecology and Hydrology, Edinburgh

    Google Scholar 

  • Swaney DP, Hong B, Paneer Selvam A et al (2014) Net anthropogenic nitrogen inputs and nitrogen fluxes from Indian watersheds: an initial assessment. J Mar Syst. https://doi.org/10.1016/j.marsys.2014.09.004

  • Tang TY, Tai JH, Yang YJ (2000) The flow pattern north of Taiwan and the migration of the Kuroshio. Cont Shelf Res 20:349–371

    Article  Google Scholar 

  • Tango PJ, Magnien R, Butler W et al (2005) Impacts and potential effects due to Prorocentrum minimum blooms in Chesapeake Bay. Harmful Algae 4:525–531

    Article  Google Scholar 

  • Tatters AO, Fu F-X, Hutchins (2012) High CO2 and silicate limitation synergistically increase the toxicity of Pseudo-nitzschia fraudulenta. PLoS One 7(2):e32116. https://doi.org/10.1371/journal.pone.0032116

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ti C, Yan X (2013) Spatial and temporal variations of river nitrogen exports from major basins in China. Environ Sci Pollut Res 20:6509–6520

    Article  CAS  Google Scholar 

  • Unrein F, Massana R, Alonso-Saez L et al (2007) Significant year-round effect of small mixotrophic flagellates on bacterioplankton in an oligotrophic coastal system. Limnol Oceanogr 52:456–469

    Article  Google Scholar 

  • Van de Waal DB, Ferreruela G, Tonk L et al (2010) Pulsed nitrogen supply induces dynamic changes in the amino acid composition and microcystin production of the harmful cyanobacterium Planktothrix agardhii. FEMS Microbiol Ecol 74:430–438

    Article  PubMed  CAS  Google Scholar 

  • Van de Waal DB, Verspagen JM, Finke JF et al (2011) Reversal in competitive dominance of a toxic versus non-toxic cyanobacterium in response to rising CO2. ISME J 5:1438–1450

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van de Waal DB, Verspagen JMH, Lürling M et al (2009) The ecological stoichiometry of toxins produced by harmful cyanobacteria: an experimental test of the carbon-nutrient balance hypothesis. Ecol Lett 12:1326–1335

    Article  PubMed  Google Scholar 

  • Visser PM, Verspagen JMH, Sandrini G et al (2016) How rising CO2 and global warming may stimulate harmful cyanobacterial blooms. Harmful Algae 54:145–159

    Article  PubMed  CAS  Google Scholar 

  • Vörösmarty CJ, McIntyre PB, Gessner MO et al (2010) Global threats to human water security and river biodiversity. Nature 467:555–561

    Article  PubMed  CAS  Google Scholar 

  • Walsby T (1975) Gas vesicles. Annu Rev Plant Physiol 26:427–439

    Article  CAS  Google Scholar 

  • Wazniak CE, Glibert PM (2004) Potential impacts of brown tide, Aureococcus anophagefferens, on juvenile hard clams, Mercenaria mercenaria, in the Coastal Bays of Maryland, USA. Harmful Algae 3:321–329

    Article  CAS  Google Scholar 

  • Wells ML, Karlson B (2018) Harmful algal blooms in a changing ocean. In: Glibert PM, Berdalet E, Burford M et al (eds) Global ecology and oceanography of harmful algal blooms. Springer, Cham, pp 77–90

    Chapter  Google Scholar 

  • Wells ML, Trainer VL, Smayda TJ et al (2015) Harmful algal blooms and climate change: learning from the past and present to forecast the future. Harmful Algae 49:68–93

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu RSS, Lam KS, Mackay DW et al (1994) Impact of marine fish farming on water quality and bottom sediment: a case study in the sub-tropical environment. Mar Environ Res 38:115–145

    Article  Google Scholar 

  • Yu R-C, Lü S-H, Liang Y-B (2018) Harmful algal blooms in the coastal waters of China. In: Glibert PM, Berdalet E, Burford M et al (eds) Global ecology and oceanography of harmful algal blooms. Springer, Cham, pp 309–316

    Chapter  Google Scholar 

  • Zarfl C, Lumsdon AE, Berlekamp J et al (2015) A global boom in hydropower dam construction. Aquat Sci 77:161–170

    Article  Google Scholar 

  • Zhang QC, Qiu LM, Yu RC et al (2012) Emergence of brown tides caused by Aureococcus anophagefferens Hargraves et Sieburth in China. Harmful Algae 19:117–124

    Article  Google Scholar 

  • Zhang J, Wu Y, Zhang YY (2015) Plant nutrients and trace elements from the Changjiang watersheds and East China Sea Shelf. In: Zhang J (ed) Ecological continuum from the Changjiang (Yangtze River) watersheds to the East China Sea continental margin. Springer International Publishing, Switzerland, pp 93–118

    Google Scholar 

  • Zhou M, Yan T, Zou J (2003) Preliminary analysis of the characteristics of red tide areas in Changjiang River estuary and its adjacent sea. Chin J Appl Ecol 14:1031–1038

    CAS  Google Scholar 

  • Zhou MJ, Shen ZL, RC Y (2008) Responses of a coastal phytoplankton community to increased nutrient input from the Changjiang (Yangtze) River. Cont Shelf Res 28:1483–1489

    Article  Google Scholar 

  • Zhu Z-Y, Zhang J, Wu Y et al (2011) Hypoxia off the Changjiang (Yangtze River) estuary: oxygen depletion and organic matter decomposition. Mar Chem 125:108–116

    Article  CAS  Google Scholar 

  • Zubkov MV, Tarran GA (2008) High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455:224–226

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This is a contribution of the GEOHAB Core Research project on HABs in Eutrophic Systems and of SCOR WG 132 on Land-Based Nutrient Pollution and Harmful Algal Blooms. It is contribution number 5407 from the University of Maryland Center for Environmental Science.

Author information

Authors and Affiliations

  1. University of Maryland Center for Environmental Science, Horn Point Laboratory, Cambridge, MD, USA

    Patricia M. Glibert

  2. College of Agricultural and Marine Sciences, Sultan Qaboos University, Muscat, Sultanate of Oman

    Adnan Al-Azri

  3. Plymouth Marine Laboratory, Plymouth, UK

    J. Icarus Allen

  4. Faculty of Geosciences, Department of Earth Sciences—Geochemistry, Utrecht University, Utrecht, The Netherlands

    Alexander F. Bouwman & Arthur H. W. Beusen

  5. PBL Netherlands Environmental Assessment Agency, Bilthoven, The Netherlands

    Alexander F. Bouwman & Arthur H. W. Beusen

  6. Australian Rivers Institute and School of Environment, Griffith University, Nathan, Australia

    Michele A. Burford

  7. Department of Earth and Ocean Sciences, University of British Columbia, Vancouver, BC, Canada

    Paul J. Harrison

  8. Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China

    Mingjiang Zhou

Authors
  1. Patricia M. Glibert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adnan Al-Azri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Icarus Allen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexander F. Bouwman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Arthur H. W. Beusen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michele A. Burford
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Paul J. Harrison
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mingjiang Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Patricia M. Glibert .

Editor information

Editors and Affiliations

  1. Horn Point Laboratory, University of Maryland Center for Environmental Science, Cambridge, Maryland, USA

    Patricia M. Glibert

  2. Institute of Marine Sciences (CSIC), Barcelona, Catalonia, Spain

    Elisa Berdalet

  3. Australian Rivers Institute, Griffith University, Nathan, Queensland, Australia

    Michele A. Burford

  4. Fisheries Research and Development, Cape Town, South Africa

    Grant C. Pitcher

  5. Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China

    Mingjiang Zhou

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Glibert, P.M. et al. (2018). Key Questions and Recent Research Advances on Harmful Algal Blooms in Relation to Nutrients and Eutrophication. In: Glibert, P., Berdalet, E., Burford, M., Pitcher, G., Zhou, M. (eds) Global Ecology and Oceanography of Harmful Algal Blooms . Ecological Studies, vol 232. Springer, Cham. https://doi.org/10.1007/978-3-319-70069-4_12

Download citation

Publish with us

Policies and ethics

Search

Navigation