Harmful algal blooms and eutrophication: Nutrient sources, composition, and consequences

Abstract

Although algal blooms, including those considered toxic or harmful, can be natural phenomena, the nature of the global problem of harmful algal blooms (HABs) has expanded both in extent and its public perception over the last several decades. Of concern, especially for resource managers, is the potential relationship between HABs and the accelerated eutrophication of coastal waters from human activities. We address current insights into the relationships between HABs and eutrophication, focusing on sources of nutrients, known effects of nutrient loading and reduction, new understanding of pathways of nutrient acquisition among HAB species, and relationships between nutrients and toxic algae. Through specific, regional, and global examples of these various relationships, we offer both an assessment of the state of understanding, and the uncertainties that require future research efforts. The sources of nutrients potentially stimulating algal blooms include sewage, atmospheric deposition, groundwater flow, as well as agricultural and aquaculture runoff and discharge. On a global basis, strong correlations have been demonstrated between total phosphorus inputs and phytoplankton production in freshwaters, and between total nitrogen input and phytoplankton production in estuarine and marine waters. There are also numerous examples in geographic regions ranging from the largest and second largest U.S. mainland estuaries (Chesapeake Bay and the Albemarle-Pamlico Estuarine System), to the Inland Sea of Japan, the Black Sea, and Chinese coastal waters, where increases in nutrient loading have been linked with the development of large biomass blooms, leading to anoxia and even toxic or harmful impacts on fisheries resources, ecosystems, and human health or recreation. Many of these regions have witnessed reductions in phytoplankton biomass (as chlorophylla) or HAB incidence when nutrient controls were put in place. Shifts in species composition have often been attributed to changes in nutrient supply ratios, primarily N∶P or N∶Si. Recently this concept has been extended to include organic forms of nutrients, and an elevation in the ratio of dissolved organic carbon to dissolved organic nitrogen (DOC∶DON) has been observed during several recent blooms. The physiological strategies by which different groups of species acquire their nutrients have become better understood, and alternate modes of nutrition such as heterotrophy and mixotrophy are now recognized as common among HAB species. Despite our increased understanding of the pathways by which nutrients are delivered to ecosystems and the pathways by which they are assimilated differentially by different groups of species, the relationships between nutrient delivery and the development of blooms and their potential toxicity or harmfulness remain poorly understood. Many factors such as algal species presence/abundance, degree of flushing or water exchange, weather conditions, and presence and abundance of grazers contribute to the success of a given species at a given point in time. Similar nutrient loads do not have the same impact in different environments or in the same environment at different points in time. Eutrophication is one of several mechanisms by which harmful algae appear to be increasing in extent and duration in many locations. Although important, it is not the only explanation for blooms or toxic outbreaks. Nutrient enrichment has been strongly linked to stimulation of some harmful species, but for others it has not been an apparent contributing factor. The overall effect of nutrient over-enrichment on harmful algal species is clearly species specific.

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

Literature Cited

  1. Anderson, D. M. 1989. Toxic algal blooms and red tides: A global perspective, p. 11–16.In T. Okaichi, D. M. Anderson, and T. Nemoto (eds.), Red Tides: Biology, Environmental Science and Toxicology. Elsevier, New York.

    Google Scholar 

  2. Anderson, D. M., D. M. Kulis, G. J. Doucette, J. C. Gallagher, andE. Balech. 1994. Biogeography of toxic dinoflagellates in the genusAlexandrium from the northeastern United States and Canada.Marine Biology 120:467–478.

    Article  Google Scholar 

  3. Anderson, D. M., D. M. Kulis, J. J. Sullivan, andS. Hall. 1990. Toxin composition variations in one isolate of the dinoflagellateAlexandrium fundyense.Toxicon 28:885–893.

    CAS  Article  Google Scholar 

  4. Ashworth, W. 1986. The Late, Great Lakes—An Environmental History. Alfred A. Knopf, Inc., New York.

    Google Scholar 

  5. Berg, G. M., P. M. Glibert, M. W. Lomas, andM. A. Burford. 1997. Organic nitrogen uptake and growth by the chrysophyteAureococcus anophagefferens during a brown tide event.Marine Biology 129:377–387.

    CAS  Article  Google Scholar 

  6. Bodeanu, N. 1993. Microalgal blooms in the Romanian area of the Black Sea and contemporary eutrophication conditions, p. 203–209.In T. J. Smayda and Y. Shimizu (eds.), Toxic Phytoplankton Blooms in the Sea. Proceedings of the Fifth International Conference on Toxic Marine Phytoplankton. Elsevier, Amsterdam, The Netherlands.

    Google Scholar 

  7. Bodeanu, N. andG. Ruta. 1998. Development of the planktonic algae in the Romanian Black Sea sector in 1981–1996, p. 188–191.In B. Reguera, J. Blanco, M. L. Fernandez, and T. Wyatt (eds.), Harmful Algae, Xunta de Galicia and Intergovernmental Oceanographic Commission of United Nations Educational, Scientific and Cultural Organization, Paris, France.

    Google Scholar 

  8. Boyer, G. L., J. J. Sullivan, R. J. Andersen, P. J. Harrison, andF. J. R. Taylor. 1987. Effects of nutrient limitation on toxin production and composition in the marine dinoflagellateProtogonyaulax tamarnsis.Marine Biology 96:123–128.

    CAS  Article  Google Scholar 

  9. Boynton, W. R., J. H. Garber, R. Summers, andW. M. Kemp. 1995. Inputs, transformations, and transport of nitrogen and phosphorus in Chesapeake Bay and selected tributaries.Estuaries 18:285–314.

    CAS  Article  Google Scholar 

  10. Boynton, W. R., W. M. Kemp, andC. W. Keefe. 1982. A comparative analysis of nutrients and other factors influencing estuarine phytoplankton production, p. 69–90.In V. S. Kennedy (ed.), Estuarine Comparisons. Academic Press, New York.

    Google Scholar 

  11. Burford, M. A. 1997. Phytoplankton dynamics in shrimp ponds.Aquaculture Research 28:351–360.

    Article  Google Scholar 

  12. Burford, M. A. andP. M. Glibert. 1999. Short-term nitrogen uptake and regeneration in early and late growth phase shrimp ponds.Aquaculture Research 30:215–227.

    Article  Google Scholar 

  13. Burkholder, J. M. 1998. Implications of harmful microalgae and heterotrophic dinoflagellates in management of sustainable marine fisheries.Ecological Applications 8:S37-S62.

    Google Scholar 

  14. Burkholder, J. M. 2000. Eutrophication and oligotrophication, p. 649–670.In S. Levin (ed.), Encyclopedia of biodiversity, Volume 2. Academic Press, New York.

    Google Scholar 

  15. Burkholder, J. M. andH. B. Glasgow. 1995. Interactions of a toxic estuarine dinoflagellate with microbial predators and prey.Archiv für Protistenkunde 145:177–188.

    Google Scholar 

  16. Burkholder, J. M. andH. B. Glasgow. 1997. The ichthyotoxic dinoflagellatePfiesteria piscicida: Behavior, impacts and environmental controls.Limnology and Oceanography 42:1052–1075.

    Google Scholar 

  17. Burkholder, J. M. andH. B. Glasgow. 2001. History of toxicPfiesteria in North Carolina estuaries from 1991 to the present.BioScience 51:827–841.

    Article  Google Scholar 

  18. Burkholder, J. M., H. B. Glasgow, andN. J. Deamer-Melia. 2001a. Overview and present status of the toxicPfiesteria complex.Phycologia 40:186–214.

    Google Scholar 

  19. Burkholder, J. M., H. B. Glasgow, N. J. Deamer-Melia, J. Springer, M. W. Parrow, C. Zheng, andP. Cancellieri. 2001b. Species of the toxicPfiesteria complex, and the importance of functional type in data interpretations.Environmental Health Perspectives 109:667–679.

    Article  Google Scholar 

  20. Burkholder, J. M., H. B. Glasgow, andC. W. Hobbs. 1995. Fish kills linked to a toxic ambush-predator dinoflagellate: Distribution and environmental condition.Marine Ecology Progress Series 124:42–61.

    Article  Google Scholar 

  21. Burkholder, J. M., H. B. Glasgow, andA. J. Lewitus. 1998a. Physiological ecology ofPfiesteria piscicida with general comments on “ambush-predator” dinoflagellates, p. 175–191.In D. M. Anderson, A. D. Cembella, and G. M. Hallegraeff (eds.), Physiological Ecology of Harmful Algal Blooms. Springer-Verlag. New York.

    Google Scholar 

  22. Burkholder, J. M., L. M. Larsen, H. B. Glasgow, K. M. Mason, P. Gama, andJ. E. Parsons. 1998b. Influence of sediment and phosphorus loading on phytoplankton communities in an urban piedmont reservoir.Lake and Reservoir Management 14: 110–121.

    Google Scholar 

  23. Burkholder, J. M., M. A. Mallin, H. B. Glasgow, L. M. Larsen, M. R. McIver, Shank, N. Deamer-Melia, D. S. Briley, J. Springer, B. W. Touchette, andE. K. Hannon. 1997. Impacts to a coastal river and estuary from rupture of a large swine waste holding lagoon.Journal of Environmental Quality 26:1451–1466.

    CAS  Google Scholar 

  24. Cadée, G. C. andJ. Hegeman. 1986. Seasonal and annual variation inPhaeocystis poucheti (Haptophyceae) in the westernmost inlet of the Wadden Sea during the 1973 to 1985 period.Netherlands Journal of Sea Research 20:29–36.

    Article  Google Scholar 

  25. Canfield, Jr.,D. E. andR. W. Bachmann. 1981. Prediction of total phosphorus concentrations, chlorophylla and Secchi depths in natural and artificial lakes.Canadian Journal of Fisheries and Aquatic Sciences 38:414–423.

    Google Scholar 

  26. Caperon, J. S., S. A. Cattell, andG. Krasnick. 1971. Phytoplankton kinetics in a subtropical estuary: Eutrophication.Limnology and Oceanogrpahy 16:599–607.

    Google Scholar 

  27. Capone, D. G., M. D. Ferrier, andE. J. Carpenter. 1994. Amino acid cycling in colonies of the planktonic marine cyanobacteriumTrichodesmium theibauteii.Applied and Environmental Microbiology 60:3989–3995.

    CAS  Google Scholar 

  28. Caraco, N. F. 1995. Influence of human populations on P transfers to aquatic systems: A regional scale study using large rivers, p. 235–247.In H. Tiessen (ed.), Phosphorus in the Global Environment. SCOPE 54. John Wiley and Sons Ltd, New York.

    Google Scholar 

  29. Carlsson, P., H. Edling, andC. Bechemin. 1998. Interactions between a marine dinoflagellate (Alexandrium catenella) and a bacterial community utilizing riverine humic substances.Aquatic Microbial Ecology 16:65–80.

    Article  Google Scholar 

  30. Cho, B. C., M. G. Park, J. H. Shim, andF. Azam. 1996. Significance of bacteria in urea dynamics in coastal surface waters.Marine Ecology Progress Series 142:19–26.

    Article  Google Scholar 

  31. Chorus, I. andJ. Bartram (eds.). 1999. Toxic Cyanobacteria in Water—A Guide to Their Public Health Consequences, Monitoring, and Management, E & FN Spon, published on behalf of the World Health Organization, New York.

    Google Scholar 

  32. Church, T. M., J. M. Tramontano, D. M. Whelpdale, M. O. Andreae, J. N. Galloway, W. C. Keene, A. H. Knap, andJ. Tokos Jr. 1991. Atmospheric and precipitation chemistry over the north Atlantic Ocean: Shipboard results, April–May 1984.Journal of Geophysical Research 96:18705–18725.

    CAS  Article  Google Scholar 

  33. Cloern, J. E. 1982. Does the benthos control phytoplankton biomass in south San Francisco Bay?Marine Ecology Progress Series 9:191–202.

    Article  Google Scholar 

  34. Coale, K. H., K. S. Johnson, S. E. Fitzwater, R. M. Gordon, S. Tanner, F. P. Chavez, L. Ferioli, C. Sakamoto, P. Rogers, F. Millero, P. Steinberg, P. Nightingale, D. Cooper, W. P. Cochlan, andR. Kudela. 1996. A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the equatorial Pacific Ocean.Nature 383:495–501.

    CAS  Article  Google Scholar 

  35. Codd, G. A., C. J. Ward, andS. G. Bell. 1997. Cyanobacterial toxins: Occurrence, modes of action, health effects and exposure routes, p. 399–410.In J. P. Seiler and E. Vilanova (eds.), Applied Toxicology: Approaches Through Basic Science, Archives of Toxicology Supplement 19. Springer-Verlag, Berlin, Germany.

    Google Scholar 

  36. Constant, K. M. and W. F. Sheldrick. 1992. World nitrogen survey. World Bank Technical Paper Number 174. Washington, D.C.

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

    Google Scholar 

  38. Cullen, J. J. 1991. Hypotheses to explain high-nutrient conditions in the open sea.Limnology and Oceanogrpahy 36:1578–1599.

    CAS  Google Scholar 

  39. Dahl, E. andK. Tangen. 1993. 25 years experience withGyrodinium aureolum in Norwegian waters, p. 15–21.In T. J. Smayda and Y. Shimizu (eds.), Toxic Phytoplankton Blooms in the Sea. Elsevier, New York.

    Google Scholar 

  40. Day, J. W., C. A. S. Hall, W. M. Kemp, andA. Yanez-Arancibia. 1989. Estuarine Ecology. John Wiley and Sons, New York.

    Google Scholar 

  41. Dennison, W. C., G. J. Marshall, andC. Wigand. 1989. Effect of “brown tide” shading on eelgrass (Zostera marina L.) distributions, p. 675–692.In E. M. Cosper, V. M. Bricelj, and E. J. Carpenter (eds.), Novel Phytoplankton Blooms: Causes and Impacts of Recurrent Brown Tides and other Unusual Blooms. Lecture Notes on Coastal and Estuarine Studies. Springer-Verlag, New York.

    Google Scholar 

  42. DeYoe, H. R. andC. A. Suttle. 1994. The inability of the Texas “brown tide” alga to use nitrate and the role of nitrogen in the initiation of a persistent bloom of this organism.Journal of Phycology 30:800–806.

    Article  Google Scholar 

  43. Dillon, P. J. 1975. The phosphorus budget of Cameron Lake, Ontario: The importance of flushing rate to the degree of eutrophy of lakes.Limnology and Oceanography 20:28–39.

    CAS  Google Scholar 

  44. Dillon, P. J. andF. H. Rigler. 1975. A simple method for predicting the capacity of a lake for development based on lake trophic status.Journal of the Fisheries Research Board of Canada 32:1519–1531.

    Google Scholar 

  45. DiTullio, G. R., D. A. Hutchins, andK. W. Bruland. 1993. Interaction of iron and major nutrients controls phytoplankton growth and species composition in the tropical North Pacific Ocean.Limnology and Oceanography 38:495–508.

    CAS  Google Scholar 

  46. Dortch, Q., M. L. Parsons, G. J. Doucette, G. A. Fryxell, A. Maier, A. Thessen, C. L. Powell, andT. M. Soniat. 2000.Pseudo-nitzschia spp. in the northern Gulf of Mexico: Overview and response to increasing eutophication, p. 27.In Symposium on Harmful Marine Algae in the U.S., December 4–9, 2000. Marine Biological Laboratory, Woods Hole, Massachusetts.

    Google Scholar 

  47. Dortch, Q., R. Robichaux, S. Pool, D. Milsted, G. Mire, N. N. Rabalais, T. M. Soniat, G. A. Fryxell, R. E. Turner, andM. L. Parsons. 1997. Abundance and vertical flux ofPseudonitzschia in the northern Gulf of Mexico.Marine Ecology Progress Series 146:249–264.

    Article  Google Scholar 

  48. Doucette, G. J. andP. J. Harrison. 1991. Aspects of iron and nitrogen nutrition in the red tide dinoflagellateGymnodinium sanguineum. Effects of iron depletion and nitrogen source on biochemical composition.Marine Biology 110:165–173.

    CAS  Article  Google Scholar 

  49. Driscoll, C. T., G. B. Lawrence, A. J. Bulger, T. J. Butler, C. S. Cronan, C. Eager, K. F. Lambert, G. E. Likens, J. L. Stoddard, andK. C. Weathers. 2001. Acidic deposition in the northeastern United States: Sources and inputs, ecosystem effects, and management strategies.BioScience 51:180–198.

    Article  Google Scholar 

  50. Duce, R. A. 1986. The impact of atmospheric nitrogen, phosphorus, and iron species on marine biological productivity, p. 497–529.In P., Baut-Menard (ed.), The Role of Air-Sea Exchange in Geochemical Cycling. Reidel, Dordrecht, Germany.

    Google Scholar 

  51. Duce, R. A. andN. W. Tindale. 1991. Atmospheric transport of iron and its deposition in the ocean.Limnology and Ocea nography 36:1715–1726.

    CAS  Google Scholar 

  52. Dugdale, R. C. andJ. J. Goering. 1967. Uptake of new and regenerated forms of nitrogen in primary productivity.Limnology and Oceanography 12:196–206.

    CAS  Google Scholar 

  53. Edmondson, W. T. 1970. Phosphorus, nitrogen, and algae and Lake Washington after diversion of sewage.Science 169:690–691.

    CAS  Article  Google Scholar 

  54. Fisher, D. C. andM. P. Oppenheimer. 1991. Atmospheric nitrogen deposition and the Chesapeake Bay estuary.Ambio 20: 102–108.

    Google Scholar 

  55. Fisher, T. R., P. R. Carlson, andR. T. Barber. 1982. Carbon and nitrogen primary productivity in three North Carolina estuaries.Estuarine, Coastal, and Shelf Science 15:621–644.

    CAS  Article  Google Scholar 

  56. Fisher, T. R., P. R. Carlson, andR. T. Barber. 1982. Carbon and nitrogen primary productivity in three North Carolina estuaries, andEstuarine, Coastal, and Shelf Science 15:621–644.

    CAS  Article  Google Scholar 

  57. Fisher, T. R., L. Harding, D. W. Stanley, andL. G. Ward. 1988. Phytoplankton, nutrients, and turbidity in the Chesapeake, Delaware, and Hudson estuaries.Estuarine, Coastal, and Shelf Science 27:61–93.

    CAS  Article  Google Scholar 

  58. Fisher, T. R., E. R. Peele, J. W. Ammerman, andL. W. Harding. 1992. Nutrient limitation of phytoplankton in Chesapeake Bay.Marine Ecology Progress Series 82:51–63.

    Article  Google Scholar 

  59. Gallagher, S. M., D. K. Stoecker, andV. M. Bricelj. 1989. Effects of the brown tide alga on growth, feeding physiology and locomotory behavior of scallop larvae (Argopectin irradians). p. 511–541.In E. M. Cosper, V. M. Bricelj, and E. J. Carpenter (eds.), Novel Phytoplankton Blooms: Causes and Impacts of Recurrent Brown Tides and other Unusual Blooms. Lecture Notes on Coastal and Estuarine Studies. Springer-Verlag, Berlin, Germany.

    Google Scholar 

  60. Glasgow, H. B. andJ. M. Burkholder. 2000. Water quality trends and management implications from a five-year study of a eutrophic estuary.Ecological Applications 10:1024–1046.

    Article  Google Scholar 

  61. Glasgow, H. B., J. M. Burkholder, M. A. Mallin, N. J. Deamermelia, andR. E. Reed. 2001a. Field ecology of toxicPfiesteria complex species, and a conservative analysis of their role in estuarine fish kills.Environmental Health Perspectives 109:715–730.

    CAS  Article  Google Scholar 

  62. Glasgow, H. B., J. M. Burkholder, S. L. Morton, J. Springer, andM. W. Parrow: 2001b. The fish-killing activity and nutrient stimulation of a second toxicPfiesteria species.In G. M. Hallegraeff, S. Blackburn, C. Bolch, and R. Lewis (eds.), Proceedings of the Ninth International Conference on Algal Blooms. Intergovernmental Oceanographic Commission, United Nations Educational, Scientific and Cultural Organization, Paris, France.

    Google Scholar 

  63. Glasgow, H. B., A. J. Burkholder, J. Springer, andS. L. Morton. 2001c. A new species of ichthyotoxicPfiesteria.Phycologia 40:234–245.

    Google Scholar 

  64. Glasgow, H. B., A. J. Lewitus, andJ. M. Burkholder. 1998. Feeding behavior of the ichthyotoxic estuarine dinoflagellate,Pfiesteria piscicida, on amino acids, algal prey, and fish vs. mammalian erythrocytes, p. 394–398.In B. Reguera, J. Blanco, M. L. Fernandez, and T. Wyatt (eds.), Harmful Microalgae. Proceedings VIIth International Conference on Harmful Algal Blooms. Xunta de Galicia and Intergovernmental Oceanographic Commission of United Nations Educational, Scientific and Cultural Organization, Paris, France.

    Google Scholar 

  65. Gilbert, P. M. 1988. Primary productivity and pelagic nitrogen cycling. p. 3–31.In T. H. Blackburn and J. Sorensen (eds.), Nitrogen Cycling in Coastal Marine Environments. John Wiley and Sons, Inc., Chichester, U.K.

    Google Scholar 

  66. Gilbert, P. M. 1988. Interactions of top-down and bottom-up control in planktonic nitrogen cycling.Hydrobiologia 363:1–12.

    Article  Google Scholar 

  67. Gilbert, P. M. andD. A. Bronk. 1994. Release of dissolved organic nitrogen by marine diazotrophic cyanobacteria,Trichodesmium spp.Applied and Environmental Microbiology 60:3996–4000.

    Google Scholar 

  68. Glibert, P. M., D. J. Conley, T. R. Fisher, L. W. Harding, and T. C. Malone. 1995. Dynamics of the 1995 winter/spring bloom in Chesapeake Bay.Marine Ecology Progress Series 122: 27–43.

    Article  Google Scholar 

  69. Glibert, P. M., R. Magnien, M. W. Lomas, J. Alexander, C. Fan, E. Haramoto, M. Trice, and T. M. Kana. 2001. Harmful algal blooms in the Chesapeake and coastal bays of Maryland, USA: Comparison of 1997, 1998, and 1999 events.Estuaries 24:875–883.

    CAS  Article  Google Scholar 

  70. Gilbert, P. M. and J. M. O’Neil. 1999. Dissolved organic nitrogen release and amino acid oxidase activity byTrichodesium spp., p. 265–271.In L. Charpy and A. W. D. Larkum (eds.), Marine Cyanobacteria. Bulletin de l’Institute Oceanographique, Monaco Musee Oceanographique, Monaco.

    Google Scholar 

  71. Glibert, P. M. and D. E. Terlizzi. 1999. Co-occurrence of elevated urea levels and dinoflagellate blooms in temperate estuarine aquaculture ponds.Applied and Environmental Microbiology 65:5594–5596.

    CAS  Google Scholar 

  72. Gobler, C. J. 1999. A biogeochemical investigation ofAureococcus anophagefferens blooms: Interactions with organic nutrients and trace metals. Ph.D. Dissertation, State University of New York, Stony Brook, New York.

    Google Scholar 

  73. Goldman, J. C. 1993. Potential role of large oceanic diatoms in new primary production.Deep-Sea Research 40:159–168.

    Article  Google Scholar 

  74. Granéli, E., D. M. Anderson, P. Carlsson, andS. Y. Maestrini. 1997. Light and dark carbon uptake byDinophysis species in comparison to other photosynthetic and heterotrophic dinoflagellates.Aquatic Microbial Ecology 13:177–186.

    Article  Google Scholar 

  75. Granéli, E. andP. Carlsson. 1998. The ecological significance of phagotrophy in photosynthetic flagellates, p. 540–557,In D. M. Anderson, A. D. Cembella, and G. M. Hallegraeff (eds.), Physiological Ecology of Harmful Algal Blooms. Springer-Verlag, Berlin, Germany.

    Google Scholar 

  76. Hallegraeff, G. M. 1993. A review of harmful algal blooms and their apparent global increase.Phycologia 32:79–99.

    Google Scholar 

  77. Hallegraeff, G. M. andC. J. Bolch. 1992. Transport of diatom and dinoflagellate resting spores via ship’s ballast water: Implications for plankton biogeography and aquaculture.Journal of Plankton Research 14:1067–1084.

    Article  Google Scholar 

  78. Harlin, M. M. 1993. Changes in major plant groups following nutrient enrichment, p. 173–187.In A. J. McComb (ed.), Eutrophic Shallow Estuaries and Lagoons, CRC Press, Inc., Boca Raton, Florida.

    Google Scholar 

  79. Harper, D. 1992. Eutrophication of Freshwaters—Principles, Problems and Restoration. Chapman and Hall, New York.

    Google Scholar 

  80. Hecky, P. E. andP. Kilham. 1988. Nutrient limitation of phytoplankton in freshwater and marine environments: A review of recent evidence on the effects of enrichment.Limnology and Oceanography 33:796–822.

    CAS  Google Scholar 

  81. Heil, C. A., P. M. Glibert, M. A. Al-Sarawi, M. Faraj, M. Behbehani, andM. Husain. 2001. First record of a fish-killingGymnodinium sp. bloom in Kuwait Bay, Arabian Sea: Chronology and potential causes.Marine Ecology Progress Series 214:15–23.

    CAS  Article  Google Scholar 

  82. Hodgkiss, I. J. 2001. The N∶P ratio revisited.In K. C. Ho and Z. D. Wang (eds.) Prevention and Management of Harmful Algal Blooms in the South China Sea. School of Science and Technology, The Open University of Hong Kong. China.

    Google Scholar 

  83. Hodgkiss, I. J. andK. C. Ho. 1997. Are changes in N∶P ratios in coastal waters the key to increased red tide blooms?Hydrobiologia 852:141–147.

    Article  Google Scholar 

  84. Hollibaugh, J. T. andF. Azam. 1983. Microbial degradation of dissolved proteins in seawater.Limnology and Oceanography 28: 1104–1116.

    CAS  Google Scholar 

  85. Horner, R. A., D. L. Garrison, andF. G. Plumley. 1997. Harmful algal blooms and red tide problems on the U.S. west coast.Limnology and Oceanography 42:1076–1088.

    Google Scholar 

  86. Howarth, R. W. 1998. An assessment of human influences on inputs of nitrogen to the estuaries and continental shelves of the North Atlantic Ocean.Nutrient Cycling in Agroecosystems 52: 213–223.

    Article  Google Scholar 

  87. Howarth, R. W., G. Billen, D. Swaney, A. Townsend, N. Jaworski, K. Lajtha, J. A. Downing, R. Elmgren, N. Caraco, T. Jordan, F. Berendse, J. Freney, V. Kudeyarov, P. Murdoch, andZ. Zhao-Liang. 1996. Regional nitrogen budgets and riverine nitrogen and phosphorus fluxes for the drainages to the North Atlantic Ocean: Natural and human influences.Biogeochemistry 35:75–79.

    CAS  Article  Google Scholar 

  88. Jacobson, D. M. andD. M. Anderson. 1996. Widespread phagocytosis of ciliates and other protists by marine mixotrophic and heterotrophic thecate dinoflagellates.Journal of Phycology 32:279–285.

    Article  Google Scholar 

  89. Jaworski, N. 1990. Retrospective of the water quality issues of the upper Potomac estuary.Aquatic Science 3:11–40.

    Google Scholar 

  90. Johansson, N. andE. Granéli. 1999a. Cell density, chemical composition and toxicity ofChrysochromulina polylepis (Haptophyta) in relation to different N∶P supply ratios.Marine Biology 135:209–217.

    CAS  Article  Google Scholar 

  91. Johansson, N. andE. Granéli. 1999b. Influence of different nutrient conditions on cell density, chemical composition and toxicity ofPrymnesium parvum (Haptophyta) in semi-continuous cultures.Journal of Experimental Marine Biology and Ecology 239:243–258.

    CAS  Article  Google Scholar 

  92. Johansson, N., E. Granéli, T. Yasumoto, P. Carlsson, andC. Legrand. 1996. Toxin production byDinophysis acuminata andD. acuta cells grown under nutrient sufficient and deficient conditions, p. 227–280.In T. Yasumoto, Y. Oshima, and Y. Fukuyo (eds.), Harmful and Toxic Algal Blooms. Intergovernmental Oceanographic Commission of United Nations Educational, Scientific and Cultural Organization, Paris, France.

    Google Scholar 

  93. Jones, J. R. andR. W. Bachmann. 1974. Prediction of phosphorus and chlorophyll levels in lakes.Journal of the Water Pollution Control Federation 48:2176–2182.

    Google Scholar 

  94. Karl, D. M., R. Letelier, D. V. Hebel, D. F. Bird, andC. D. Winn. 1992.Trichodesmium blooms and new nitrogen in the North Pacific Gyre, p. 219–238.In E. J. Carpenter, D. G. Capone, and J. G. Reuter (eds.), Marine Pelagic Cyanobacteria:Trichodesmium and Other Diazotrophs. NATO ASI Series, Volume 362. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

  95. Keil, R. G. andD. L. Kirchman. 1992. Bacterial hydrolysis of protein and methylated protein and its implications for studies of protein degradation in aquatic systems.Applied Environmental Microbiology 58:1374–1375.

    CAS  Google Scholar 

  96. Keller, A. A. andR. L. Rice. 1980. Effects of nutrient enrichment on natural populations of the brown tide phytoplanktonAureococcus anophagefferens (Chrysophyceae).Journal of Phycology 25:636–646.

    Article  Google Scholar 

  97. Kilham, P. 1982. Acid precipitation: Its role in the alkalization of a lake in Michigan.Limnology and Oceanography 27:856–867.

    CAS  Google Scholar 

  98. Kilham, S. S., D. A. Kreeger, C. E. Goulden, andS. G. Lynn. 1997. Effects of algal food quality on fecundity and population growth rates ofDaphnia.Freshwater Biology 38:639–647.

    Article  Google Scholar 

  99. Lam, C. W. Y. andK. C. Ho. 1989. Red tides in Tolo Harbour, Hong Kong, p. 49–52.In T. Okaichi, D. M. Anderson, and T. Nemoto (eds.), Red Tides: Biology, Environmental Science and Toxicology, Elsevier, New York.

    Google Scholar 

  100. Lancelot, C. 1995. The mucilage phenomenon in the continental coastal waters of the North Sea.Science of the Total Environment 165:83–102.

    CAS  Article  Google Scholar 

  101. LaRoche, J., R. Nuzzi, R. Waters, K. Wyman, P. G. Falkkowski, andD. W. R. Wallace. 1997. Brown tide blooms in Long Island’s coastal waters linked to variability in groundwater flow.Global Change Biology 3:397–410.

    Article  Google Scholar 

  102. LeGrand, C., S. Semundsdottir, andE. Granéli. 1996. Phagotrophy inChrysochromulina polylepis (Prymnesiophyceae): Ingestion of fluorescent labelled algae (FLA) under different nutrient conditions, p. 339–342.In T. Yasumoto, Y. Oshima, and Y. Fukuyo (eds.), Harmful and Toxic Algal Blooms. Intergovernmental Oceanographic Commission of United Nations Educational, Scientific and Cultural Organization, Paris, France.

    Google Scholar 

  103. Lenes, J. M., B. P. Darrow, C. Cattrall, C. A. Heil, M. Callahan, G. A. Vargo, R. H. Byrne, J. M. Prospero, D. E. Bates, K. A. Fanning, andJ. J. Walsh. 2001. Iron fertilization and theTrichodesmium response on the West Florida shelf.Limnology and Oceanography 46:1261–1277.

    CAS  Google Scholar 

  104. Le Pape, O., Y. Del Amo, A. Ménesguen, A. Aminot, B. Quéguiner, andP. Tréguer. 1996. Resistance of a coastal ecosystem to increasing eutrophic conditions: The Bay of Brest (France), a semienclosed zone of western Europe.Continental Shelf Research 16:1885–1907.

    Article  Google Scholar 

  105. Le Pape, O. andA. Ménesguen. 1997. Hydrodynamic prevention of eutrophication in the Bay of Brest (France), A modeling approach.Journal of Marine Systems 12:171–186.

    Article  Google Scholar 

  106. Lewitus, A. J., J. M. Burkholder, H. B. Glasgow, P. M. Glibert, B. M. Willis, K. C. Hayes, andM. Burke. 1999a. Mixotrophy and nitrogen uptake byPfiesteria piscidida (Dinophyceae).Journal of Phycology 35:1430–1437.

    CAS  Article  Google Scholar 

  107. Lewitus, A. J., H. G. Glasgow, Jr., andJ. M. Burkholder. 1999b. Kleptoplastidy in the toxic dinoflagellate,Pfiesteria piscicida (Dinophyceae).Journal of Phycology 35:303–312.

    Article  Google Scholar 

  108. Lewitus, A. J., K. C. Hayes, S. G. Gransden, H. B. Glasgow, Jr.,J. M. Burkholder, P. M. Glibert, andS. L. Morton. 2001. Ecologicla characterization of a widespreadScrippsiella red tide in South Carolina estuaries: A newly observed phenomenon.In G. M. Hallegraeff, S. Blackburn, C. Bolch, and R. Lewis (eds.), Proceedings of the Ninth International Conference on Harmful Algal Blooms. Intergovernmental Oceanographic Commission, United Nations Educational, Scientific and Cultural Organization, Paris, France.

    Google Scholar 

  109. Lewitus, A. J., R. V. Jesien, T. M. Kana, J. M. Burkholder, H. B. Glasgow, Jr., andE. May. 1995. Discovery of the “phantom” dinoflagellate in Chesapeake Bay.Estuaries 18:373–378.

    Article  Google Scholar 

  110. Lewitus, A. J. andT. M. Kana. 1994. Responses of estuarine phytoplankton to exogenous glucose: Stimulatin versus inhibition of photosynthesis and respiration.Limnology and Oceanography 39:182–188.

    CAS  Google Scholar 

  111. Li, A., D. K. Stoecker, andD. W. Coats. 2000. Spatial and temporal aspects ofGyrodinium galatheanum in Chesapeake Bay: Distribution and mixotrophy.Journal of Plankton Research 22:2105–2124.

    Article  Google Scholar 

  112. Li, A., D. K. Stoecker, andD. W. Coats. 2001. Mixotrophy inGyrodinium galatheanum (Dinophyceae): Grazing responses to light intensity and inorganic nutrients.Journal of Phycology 36 33–45.

    Article  Google Scholar 

  113. Likens, G. E., J. N. Wright, J. N. Galloway, andT. J. Butler. 1979. Acid rain.Scientific American 241:43–48.

    CAS  Google Scholar 

  114. Lomas, M. W. andP. M. Glibert. 1999a. Temperature regulation of NO3 uptake: A novel hypothesis about NO3 uptake and cool-water diatoms.Limnology and Oceanography 44:556–572.

    CAS  Google Scholar 

  115. Lomas, M. W. andP. M. Glibert. 1999b. Interactions between NH4+ and NO3 uptake and assimilation: Comparisons of diatoms and dinoflagellates at several growth temperatures.Marine Biology 133:541–551.

    CAS  Article  Google Scholar 

  116. Lomas, M. W. andP. M. Glibert. 2000. Comparisons of nitrate uptake, storage, and reduction in marine diatoms and flagellates.Journal of Phycology 36:903–913.

    CAS  Article  Google Scholar 

  117. Lomas, M. W., P. M. Glibert, D. A. Clougherty, D. A. Huber, J. Jones, J. Alexander, andE. Haramoto. 2001. Elevated organic nutrient ratios associated with brown tide blooms ofAureococcus anophagefferens (Pelagophyceae).Journal of Plankton Research 23:1339–1344.

    Article  Google Scholar 

  118. MacIsaac, J. J. andR. C. Dugdale. 1972. Interactions of light and inorganic nitrogen in controlling nitrogen uptake in the sea.Deep-Sea Research 19:209–232.

    CAS  Google Scholar 

  119. Magnien, R., D. Goshorn, B. Michael, P. Tango, andR. Karrh. 2000. Associations BetweenPfiesteria, Fish Health and Environmental Conditions in Maryland. Tidewater Ecosystem Assessment, Maryland Department of Natural Resources, Annapolis, Maryland.

    Google Scholar 

  120. Magnien, R. E., R. M. Summers, andK. G. Sellner. 1992. External sources, internal nutrient pools, and phytoplankton production in Chesapeake Bay.Estuaries 15:497–516.

    CAS  Article  Google Scholar 

  121. Mallin, M. A. 2000. Impacts of industrial animal production on rivers and estuaries.American Scientist 88:2–13.

    Google Scholar 

  122. Mallin, M. A., H. W. Paerl, J. Rudek, andP. W. Bates. 1993. Regulation of estuarine primary production by watershed rainfall and river flow.Marine Ecology Progress Series 93:199–203.

    Article  Google Scholar 

  123. Malone, T. C., D. J. Conley, T. R. Fisher, P. M. Glibert, L. W. Harding, andK. G. Sellner. 1996. Scales of nutrient-limited phytoplankton productivity in Chesapeake Bay.Estuaries 19: 371–385.

    CAS  Article  Google Scholar 

  124. Malone, T. C., P. G. Falkowski, T. S. Hopkins, G. T. Rowe, andT. E. Whitledge. 1983. Mesoscale response of diatom populations to wind events in the plume of the Hudson River.Deep-Sea Research 30:149–170.

    Article  Google Scholar 

  125. Malone, T. C., W. M. Kemp, H. W. Ducklow, W. R. Boynton, J. H. Tuttle, andR. B. Jonas. 1986. Lateral variability in the production and fate of phytoplankton in a partially stratified estuary.Marine Ecology Progress Series 32:149–160.

    Article  Google Scholar 

  126. Martin, J. H. andS. E. Fitzwater. 1988. Iron deficiency limits phytoplankton growth in the north-east Pacific subarctic.Nature 331:341–343.

    CAS  Article  Google Scholar 

  127. Matson, P. A., W. J. Parton, A. G. Power, andM. J. Swift. 1997. Agricultural intensification and ecosystem properties.Science 277:504–509.

    CAS  Article  Google Scholar 

  128. McElroy, A. (Ed.). 1996. Proceedings of the Brown Tide Summit. Publication No. NYSGI-W-95-001. New York Sea Grant Institute, New York.

    Google Scholar 

  129. Miller, Jr.,G. T. 2000. Living in the Environment, 11th edition. Brooks/Cole Publishing Company, New York.

    Google Scholar 

  130. Mulholland, M. R., P. M. Glibert, G. M. Berg, L. Van Heukelem, S. Pantoja, andC. Lee. 1998. Extracellular amino acid oxidation by microplankton: A cross-ecosystem comparison.Aquatic Microbial Ecology 15:141–152.

    Article  Google Scholar 

  131. Mulholland, M. R., C. Gobler, andC. Lee. 2000. Amino acid oxidation and peptide hydrolysis in populations seasonally dominated byAureococcus anophagefferens, p. 56. Symposium on Harmful Marine Algae in the U.S., December 4–9, 2000. Marine Biological Laboratory, Woods Hole, Massachusetts.

    Google Scholar 

  132. National Research Council. 1993. Managing Wastewater in Coastal Urban Areas. National Academy Press, Washington, D.C.

    Google Scholar 

  133. National Research Council. 2000. Clean Coastal Waters—Understanding and Reducing the Effects of Nutrient Pollution. National Academy Press, Washington, D.C.

    Google Scholar 

  134. Newell, R. I. E. 1988. Ecological changes in Chesapeake Bay: Are they the result of over-harvesting the American oyster,Crassostrea virginica?, p. 29–31.In Proceedings of Understanding the Estuary: Advances in Chesapeake Bay Research (March 1988). Chesapeake Bay Consortium, Baltimore, Maryland.

    Google Scholar 

  135. Nixon, S. W. 1992. Quantifying the relationship between nitrogen input and the productivity of marine ecosystems.Proceedings of Advancements in Marine Science Conference 5:57–83.

    Google Scholar 

  136. Nixon, S. W.. 1995. Coastal marine eutrophication: A definition, social causes, and future concerns.Ophelia 41:199–219.

    Google Scholar 

  137. Nixon, S. W. andM. Q. Pilson. 1983. Nitrogen in estuarine and coastal marine ecosystems, p. 565–648.In E. J. Carpenter and D. G. Capone (eds.), Nitrogen in the Marine Environment. Academic Press, New York.

    Google Scholar 

  138. North Carolina Department of Environment, Health and Natural Resources (NC DEHNR). 1994. Water Quality Progress in North Carolina: 1992–1993 305(b) Report. NC DEHNR, Raleigh, North Carolina.

    Google Scholar 

  139. Nygaard, K. andA. Tobiesen. 1993. Bacterivory in algae: A survival strategydduring nutrient limitation.Limnology and Oceanography 38:273–279.

    Google Scholar 

  140. Officer, C. B. andJ. H. Ryther. 1980. The possible importance of silicon in marine eutrophication.Marine Ecology Progress Series 3:83–91.

    CAS  Article  Google Scholar 

  141. Okaichi, T. 1997. Red tides in the Seto Inland Sea, p. 251–304.In T. Okaichi and Y. Yanagi (eds.), Sustainable Development in the Seto Inland Sea—From the Viewpoint of Fisheries. Tera Scientific Publishing Company, Tokyo, Japan.

    Google Scholar 

  142. O’Neil, J. M., C. A. Heil, P. M. Glibert, J. Greenwood, C. A. Miller, and J. G. Greenwood. Submitted. Plankton community changes and nutrient dynamics associated with a bloom of the pelagic cyanobacteriumTrichodesmium: A Eulerian study.Journal of Plankton Research.

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

    CAS  Google Scholar 

  144. Paerl, H. W. 1995. Coastal eutrophication in relation to atmospheric nitrogen deposition: Current perspectives.Ophelia 41: 237–259.

    Google Scholar 

  145. Paerl, H. W. 1997. Coastal eutrophication and harmful algal blooms: Importance of atmospheric deposition and ground-water as “new” nitrogen and other nutrient sources.Limnology and Oceanography 42:1154–1165.

    CAS  Google Scholar 

  146. Paerl, H. W., W. R. Boynton, R. L. Dennis, C. T. Driscoll, H. S. Greening, J. N. Kremer, N. N. Rabalais, andS. P. Seitzinger. 2000. Atmospheric deposition of nitrogen in coastal waters: Biogeochemical and ecological implications, p. 11–53.In R. A. Valigura, R. B. Alexander, M. S. Castro, T. P. Meyers, H. W. Paerl, P. E. Stacey, and R. E. Turner (eds.), Nitrogen Loading in Coastal Water Bodies. An Atmospheric Perspective. Coastal and Esturaine Studies 57. American Geophysical Union, Washington, D.C.

    Google Scholar 

  147. Palenik, B. andF. M. M. Morel. 1990a. Comparison of cell-surface L-amino acid oxidases from several marine phytoplankton.Marine Ecology Progress Series 59:195–201.

    CAS  Article  Google Scholar 

  148. Palenik, B. andF. M. M. Morel. 1990b. Amino acid utilization by marine phytoplankton: A novel mechanism.Limnology and Oceanography 35:260–269.

    CAS  Google Scholar 

  149. Pan, Y., M. L. Parsons, M. Busman, P. Moller, Q. Dortch, C. L. Powell, G. A. Fryxell, andG. J. Doucette. 2001.Pseudonitzschia Pseudodelicatissima—A confirmed producer of domoic acid from the northern Gulf of Mexico.Marine Ecology Progress Series 220:83–92.

    CAS  Article  Google Scholar 

  150. Pan, Y., D. V. Subba Rao, K. H. Mann, R. G. Brown, and R. Pocklington . 1996a. Effects of silicate limitation on production of domoic acid, a neurotoxin, by the diatomPseudo-nitschia multiseries. I. Batch culture studies.Marine Ecology Progress Series 131:225–233.

    CAS  Article  Google Scholar 

  151. Pan, Y., D. V. Subba Rao, K. H. Mann, R. G. Brown, andR. Pocklington. 1996b. Effects of silicate limitation on production of domoic acid, a neurotoxin, by the diatomPseudo-nitzschia multiseries. II. Continuous culture studies.Marine Ecology Progress Series 131:235–243.

    CAS  Article  Google Scholar 

  152. Pantoja, S. andC. Lee. 1994. Cell-surface oxidation of amino acids in seawater.Limnology and Oceanography 39:1718–1726.

    CAS  Google Scholar 

  153. Pantoja, S. andC. Lee. 1999. Peptide decomposition by extracellular hydrolysis in coastal seawater and salt marsh sediment.Marine Chemistry 63:273–291.

    CAS  Article  Google Scholar 

  154. Pantoja, S., C. Lee, andJ. F. Marecek. 1997. Hydrolysis of peptides in seawater and sediments.Marine Chemistry 57:25–40.

    Article  Google Scholar 

  155. Parrow, M. W., H. B. Glasgow, J. M. Burkholder, andC. Zhang. 2001. Comparative response to algal prey byPfiesteria piscicida, Pfiesteria shumwayae sp. nov., and an estuarine ‘lookalike’ species.In G. M. Hallegraeff, S. Blackburn, C. Bolch, and R. Lewis (eds.), Proceedings of the Ninth International Conference on Harmful Algal Blooms. Intergovernmental Oceanographic Commission, United Nations, Educational, Scientific and Cultural Organization, Paris, France.

    Google Scholar 

  156. Parsons, M. L., Q. Dortch, andG. A. Fryxell. 1998. A multi-year study of the presence of potential domoic acid-producingPseudo-nitzschia species in the coastal and estuarine waters of Lousiana, USA, p. 184–187.In B. Reguera, J. Blance, M. L. Fernandez, and T. Wyatt (eds.), Harmful Algae. Xunta de Galicia and Intergovernmental Oceanographic Commission of United Nations Educational, Scientific and Cultural Organization, Paris, France.

    Google Scholar 

  157. Parsons, M. L., Q. Dortch, andR. E. Turner. 2002. Sedimentological evidence of an increase inPseudo-nitzschia (Bacillariophyceae) abundance in response to coastal eutrophication.Limnology and Oceanography 47:551–558.

    Google Scholar 

  158. Parsons, M. L., C. A. Scholin, P. E. Miller, G. J. Doucette, C. L. Powell, G. A. Fryxell, Q. Dortch, andT. M. Soniat. 1999.Pseudo-nitzschia in Lousianna coastal waters: Molecular probe field trials, genetic variability, and domoic acid analyses.Journal of Phycology 35:1368–1378.

    Article  Google Scholar 

  159. Prakash, A., J. C. Medcof, andA. D. Tenant. 1971. Paralytic shellfish poisoning in eastern Canada. Fisheries Research Board of Canada, Bulletin 177. Fisheries Research Board of Canada, Ottawa, Canada.

    Google Scholar 

  160. Qi, Y. Z., Z. Zhang, Y. Hong, S. Lu, C. Zhu, andY. Li 1993. Occurrence of red tides on the coasts of China, p. 43–46.In T. Smayda and Y. Shimizu (eds.), Toxic Phytoplankton Blooms in the Sea. Elsevier, Amsterdam, The Netherlands.

    Google Scholar 

  161. Rabalais, N. N., W. J. Wiseman, Jr,R. E. Turner, D. Justic, B. K. Sen Gupta, andQ. Dortch. 1996. Nutrient changes in the Mississippi River and system responses on the adjacent continental shelf.Estuaries 19:386–407.

    CAS  Article  Google Scholar 

  162. Radach, G., J. Berg, andE. Hagmeier. 1990. Long-term changes of the annual cycles of meteorological, hydrographic nutrient and phytoplankton time series at Helgoland and at LV Elbe 1 in the German Bight.Continental Shelf Research 10:305–328.

    Article  Google Scholar 

  163. Rensel, J. E. 1993. Factors controlling paralytic shellfish poisoning (PSP) in Puget Sound, Washington.Journal of Shellfish Research 12:371–376.

    Google Scholar 

  164. Richardson, K. 1997. Harmful or exceptional phytoplankton blooms in the marine ecosystem, p. 302–386.In J. H. S. Blaxter and A. J. Southworth (eds.), Advances in Marine Biology, Volume 31. Academic Press, San Diego, California.

    Google Scholar 

  165. Richardson, K. andB. B. Jorgensen. 1996. Eutrophication: Definition, history and effects, p. 1–19.In B. B. Jorgensen and K. Richardson (eds.), Eutrophication in Coastal Marine Ecosystems. Coastal and Estuarine Studies, Volume 52. American Geophysical Union, Washington, D.C.

    Google Scholar 

  166. Riegman, R. 1995. Nutrient-related selection mechanisms in marine phytoplankton communities and the impact of eutrophication on the planktonic food web.Water Science and Technology 32:63–75.

    CAS  Article  Google Scholar 

  167. Romdhane, M. S., H. C. Eilertsen, O. K. D. Yahia, andM. N. D. Yahia. 1998. Toxic dinoflagellate blooms in Tunisian lagoons: Causes and consequences for aquaculture, p. 80–83.In B. Reguera, J. Blance, M. L. Fernandez, and T. Wyatt (eds.), Harmful Algae. Xunta de Galicia and Intergovernmental Oceanographic and Cultural Organization, Paris, France.

    Google Scholar 

  168. Rothschild, B. J., J. S. Ault, P. Goulletquer, andM. Heral. 1994. Decline of the Chesapeake Bay oyster population: A century of habitat destruction and overfishing.Marine Ecology Progress Series 111:29–39.

    Article  Google Scholar 

  169. Rudek, J., H. W. Paerl, M. A. Mallin, andP. W. Bates. 1991. Seasonal and hydrological control of phytoplankton nutrient limitation in the lower Neuse River estuary, North Carolina.Marine Ecology Progress Series 75:133–142.

    Article  Google Scholar 

  170. Sakamoto, I. 1986. N and P load control from the viewpoint of pisciculture, p. 86–133.In A. Murakami (ed.), Regulation of Nitrogen and Phosphorus Pollution Load into Partially Enclosed Fishing Ground for the Development of Fisheries. Kouseisha Kouseikaku, Tokyo, Japan.

    Google Scholar 

  171. Schell, D. M. 1974. Uptake and regeneration of free amino acids in marine waters of southeast Alaska.Limnology and Oceanography 19:260–270.

    CAS  Google Scholar 

  172. Schelske, C. L., E. F. Stoermer, G. L. Fahnenstiel, andM. Haibach. 1986. Phosphorus enrichment, silica utilization, and biogeochemical silica depletion in the Great Lakes.Canadian Journal of Fisheries and Aquatic Sciences 43:407–415.

    CAS  Google Scholar 

  173. Schindler, D. W. 1977. Evolution of phosphorus limitation in lakes.Science 196:260–262.

    Article  Google Scholar 

  174. Schnepf, E. andM. Elbrachter. 1992. Nutritional strategies in dinoflagellates: A review with emphasis on cell biological aspects.European Journal of Protistology 28:3–24.

    Google Scholar 

  175. Shiah, F.-K. andH. W. Ducklow. 1994. Temperature regulation of heterotrophic bacterioplankton abundance, production, and specific growth rate in Chesapeake Bay.Limnology and Oceanography 39:1243–1258.

    Google Scholar 

  176. Shimizu, Y., N. Watanabe, andG. Wrensford. 1993. Biosynthesis of brevetoxins and heterotrophic metabolism inGymnodinium breve, p. 351–357.In P. Lassus, G. Arzul, E. Erard-Le-Denn, P. Gentien, and C. Marcaillou (eds.), Harmful Marine Algal Blooms, Lavoisier Publishing, Paris, France.

    Google Scholar 

  177. Skovgaard, A. 1998. Role of chloroplast retention in a marine dinoflagellate.Aquatic Microbial Ecology 15:293–301.

    Article  Google Scholar 

  178. Skulberg, O. M., W. W. Carmichael, G. A. Codd, andR. Skulberg. 1993. Taxonomy of toxic Cyanophyceae (cyanobacteria), p. 1–28, 145–164.In I. R. Falconer (ed.), Algal Toxins in Seafood and Drinking Water. Academic Press, New York.

    Google Scholar 

  179. Smayda, T. J. 1989. Primary production and the global epidemic of phytoplankton blooms in the sea: A linkage?, p. 449–484.In. E. M. Cosper, V. M. Bricelj, and E. J. Carpenter (eds.), Novel Phytoplankton, Blooms, Coastal and Estuarine Studies Number 35. Springer-Verlag, New York.

    Google Scholar 

  180. Smayda, T. 1990. Novel and nuisance phytoplankton blooms in the sea: Evidence for a global epidemic, p. 29–40.In E. Graneli, B. Sundstrom, L. Edler and D. M. Anderson (eds.), Toxic Marine Phytoplankton, Elsevier, New York.

    Google Scholar 

  181. Smayda, T. J. 1997. Harmful algal blooms: Their ecophysiology and general relevance to phytoplankton blooms in the sea.Limnology and Oceanography 42:1137–1153.

    Article  Google Scholar 

  182. Smil, V. 2001. Enriching the Earth: Fritz Haber, Carl Bosch, and the Transformation of World Food. The MIT Press, Cambridge, U.K.

    Google Scholar 

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

    Article  CAS  Google Scholar 

  184. Starr, M., J. H. Himmelman, andJ.-C., Therriault. 1990. Direct coupling of marine invertebrate spawning with phytoplankton blooms.Science 247:1701–1704.

    Article  Google Scholar 

  185. Stickney, H. L., R. R. Hood, andD. K. Stoecker. 2000. The impact of mixotrophy on planktonic trophic dynamics in marine ecosystems.Ecological Modelling 125:203–230.

    CAS  Article  Google Scholar 

  186. Stoecker, D. K. 1998. Conceptual models of mixotrophy in planktonic protests and some ecological and evolutionary implications.European Journal of Protistology 34:281–290.

    Google Scholar 

  187. Stoecker, D. K. 1999. Mixotrophy among dinoflagellates.Journal of Eukaryotic Microbiology 46:397–401.

    Article  Google Scholar 

  188. Swedish Ministry of Agriculture. 1982. Acidification Today and Tomorrow. Environment ’82 Committee, Risbergs Tryckeri AB, Uddevalla, Sweden.

  189. Takahashi, M., I. Koike, K. Iseki, P. K. Bienfang, andA. Hattori. 1982. Phytoplankton species responses to nutrient changes in experimental enclosures and coastal waters, p. 333–340.In G. D. Grice and M. R. Reeve (eds.), Marine Mesocosms: Biological and Chemical Research in Experimental Ecosystems. Springer-Verlag, New York.

    Google Scholar 

  190. Tang, S., I. J. Hodgkiss, andM. D. Dickman. 2001. Distribution of chlorophyll biomass in reverse to the nutrient gradient in Hong Kong waters.In K. C. Ho and Z. D. Wang (eds.), Prevention and Management of Harmful Algal Blooms in the South China Sea. School of Science and Technology, The Open University of Hong Kong, Hong Kong, China.

    Google Scholar 

  191. Thornton, K. W., B. L. Kimmel, andF. E. Payne, (eds.) 1990. Reservoir Limnology—Ecological Perspectives. John Wiley and Sons, New York.

    Google Scholar 

  192. Tilman, D. 1977. Resource competition between planktonic algae: An experimental and theoretical approach.Ecology 58: 338–348.

    CAS  Article  Google Scholar 

  193. Timperley, M. H., R. J. Vigor-Brown, M. Kawashima, andM. Ishigami. 1985. Organic nitrogen compounds in atmospheric precipitation: Their chemistry and availability to phytoplankton.Canadian Journal of Fisheries and Aquatic Science 42:1171–1177.

    CAS  Google Scholar 

  194. Tracey, G. A. 1988. Feeding reduction, reproductive failure, and mortality inMytilus edulis during the 1985 “brown tide” in Narragansett Bay, Rhode Island.Marine Ecology Progress Series 50:73–81.

    Article  Google Scholar 

  195. Turner, R. E. andN. N. Rabalais. 1991. Changes in Mississippi River water quality this century.BioScience 41:140–147.

    Article  Google Scholar 

  196. Turner, R. E. andN. N. Rabalais. 1994. Coastal eutrophication near the Mississippi river delta.Nature 368:619–621.

    Article  Google Scholar 

  197. Vallentyne, J. R. 1974. The Algal Bowl—Lakes and Man. Miscellaneous Special Publication 22. Department of the Environment, Fisheries and Marine Service, Ottawa, Canada.

    Google Scholar 

  198. Vancouver, G. 1798. A Voyage of Discovery to the North Pacific Ocean and Around the World, Volume 2. G. C. and J. Robinson, London, U.K.

    Google Scholar 

  199. Vitousek, P. M., J. Aber, R. W. Howarth, G. E. Likens, P. A. Matson, D. W. Schindler, W. H. Schlesinger, andG. D. Tilman. 1997. Human alteration of the global nitrogen cycle: Causes and consequences.Ecological Applications 7:737–750.

    Google Scholar 

  200. Walsh, J. J. andK. A. Steidinger. 2001. Saharan dust and Florida red: The cyanophyte connection.Journal of Geophysical Research 106:597–601.

    Article  Google Scholar 

  201. Wells, M. L. 1999. Manipulating iron availability in nearshore waters.Limnology and Oceanography 44:1002–1008.

    CAS  Google Scholar 

  202. Wetzel, R. G. 1983. Limnology. Saunders College Publishing. Philadelphia, Pennsylvania.

    Google Scholar 

  203. Wheeler, P. A., B. B. North, andG. C. Stephens. 1974. Amino acid uptake by marine phytoplankton.Limnology and Oceanography 19:249–259.

    CAS  Article  Google Scholar 

  204. Wilhelm, S. W. 1995. Ecology of iron-limited cyanobacteria: A review of physiological responses and implications for aquatic systems.Aquatic Microbial Ecology 9:295–303.

    Article  Google Scholar 

  205. Wu, R. S. S., P. K. S. Lam, D. W. Mackay, T. C. Lau, andV. Yam. 1994. Impact of marine fish farming on water quality and bottom sediment: A case study in the subtropical environment.Marine Environmental Research 38:115–145.

    Article  Google Scholar 

  206. Yung, Y. K., C. K. Wong, M. J. Broom, J. A. Ogden, S. C. M. Chan, andY. Leung. 1997. Long-term, changes in hydrography, nutrients, and phytoplankton in Tolo Harbour, Hong Kong.Hydrobiologia 352:107–115.

    CAS  Article  Google Scholar 

  207. Zhang, J. 1994. Atmospheric wet depositions of nutrient elements: Correlations with harmful biological blooms in the Northwest Pacific coastal zones.Ambio 23:464–468.

    Google Scholar 

  208. Zhang, J., Z. F. Zhang, S. M. Liu, Y. Wu, H. Xiong, andH. T. Chen. 1999. Human impacts on the large world rivers: Would the Changjiang (Yangtze River) be an illustration?Global Biogeochemical Cycles 13:1099–1105.

    CAS  Article  Google Scholar 

  209. Zohary, T. andR. D. Robarts. 1989. Diurnal mixed layers and the long-term dominance ofMicrocystis, aeruginosa.Journal of Plankton Research 11:25–48.

    Article  Google Scholar 

Sources of Unpublished Materials

  1. Borkman, D. and T. J. Smayda. Unpublished Data. Graduate School of Oceanography, University of Rhode Island, Kingston, Rhode Island.

  2. Dortch, Q. Unpublished Data. Louisiana Universities Marine Consortium, Chauvin, Louisiana.

  3. Fukuyo, Y. Personal Communication. The University of Tokyo, Tokyo, Japan.

  4. Lewitus, A. J. Unpublished Data. Marine Resources Research Institute, Charleston, South Carolina.

  5. Rensel, J. E. Personal Communication. Rensel Associates Aquatic Science Consultants, Arlington, West Virginia.

  6. Rue, E. and M. Wells. Unpublished Data. University of California, Santa Cruz, California and University of Maine, Orono, Maine.

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Donald M. Anderson.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Anderson, D.M., Glibert, P.M. & Burkholder, J.M. Harmful algal blooms and eutrophication: Nutrient sources, composition, and consequences. Estuaries 25, 704–726 (2002). https://doi.org/10.1007/BF02804901

Download citation

Keywords

  • Phytoplankton
  • Dinoflagellate
  • Algal Bloom
  • Dissolve Organic Nitrogen
  • Phytoplankton Bloom