, Volume 541, Issue 1, pp 87–99 | Cite as

Distribution and toxicity of a new colonial Microcystis aeruginosa bloom in the San Francisco Bay Estuary, California

  • P. W. LehmanEmail author
  • G. Boyer
  • C. Hall
  • S. Waller
  • K. Gehrts
Primary Research Paper


The first distribution, biomass and toxicity study of a newly established bloom of the colonial cyanobacteria Microcystis aeruginosa was conducted on October 15, 2003 in the upper San Francisco Bay Estuary. Microcystis aeruginosa was widely distributed throughout 180 km of waterways in the upper San Francisco Bay Estuary from freshwater to brackish water environments and contained hepatotoxic microcystins at all stations. Other cyanobacteria toxins were absent or only present in trace amounts. The composition of the microcystins among stations was similar and dominated by demethyl microcystin-LR followed by microcystin-LR. In situ toxicity computed for the >75 μm cell diameter size fraction was well below the 1 μg l−1 advisory level set by the World Health Organization for water quality, but the toxicity of the full population is unknown. The toxicity may have been greater earlier in the year when biomass was visibly higher. Toxicity was highest at low water temperature, water transparency and salinity. Microcystins from the bloom entered the food web and were present in both total zooplankton and clam tissue. Initial laboratory feeding tests suggested the cyanobacteria was not consumed by the adult copepod Eurytemora affinis, an important fishery food source in the estuary.


Microcystis cyanobacteria toxic estuary harmful algal bloom 


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  1. American Public Health Association, American Water Works Association and Water Environment Association. 1998. Standard Methods for the Examination of Water and Wastewater. 20th edn. American Public Health Association, Washington, DC.Google Scholar
  2. Anderson, D.M., Garrison, D.J. 1997The ecology and oceanography of harmful algal bloomsSpecial issue. Limnology and Oceanography4210091305Google Scholar
  3. Bennett, W. A., Moyle, P. B. 1996Where have all the fishes gone? Interactive factors producing fish declines in the Sacramento-San Joaquin EstuaryHollibaugh, J. T. eds. San Francisco Bay: The Ecosystem.Pacific Division of the American Association for the Advancement of ScienceSan Francisco, California519542Google Scholar
  4. Brunberg, A., Blomqvist, P. 2003Recruitment of Microcystis (Cyanophyceae) from lake sediments: The importance of littoral inoculaJournal of Phycology395863CrossRefGoogle Scholar
  5. Boyer, G. L., Goddard, G. D. 1999High performance liquid chromatography (HPLC) coupled with post-column electrochemical oxidation (ECOS) for the detection of PSP toxinsNatural Toxins7353359CrossRefPubMedGoogle Scholar
  6. Breitburg, D. 2002Effects of hypoxia, and the balance between hypoxia and enrichment, on coastal fishes and fisheriesEstuaries25767781Google Scholar
  7. California Bay-Delta Authority, 2000. Programatic Record of Decision. Technical Report. California Bay-Delta Authority, Sacramento, CA. URL: Scholar
  8. Carmichael, W. W. 1995Toxic microcystis in the environmentWatanabe, M. F.Harada, K.Carmichael, W. W.Fujiki, H. eds. Toxic Microcystis.CRC PressNew York112Google Scholar
  9. Carmichael, W. W., An, J. 1999Using an enzyme linked immunosorbent assay (ELISA) and a protein phosphatase inhibition assay (PP1A) for the detection of microcystins and nodularinsNatural Toxins7377385CrossRefPubMedGoogle Scholar
  10. Christian, R. R., W. L. Bryant Jr. & D. W. Stanley, 1986. The relationship between river flow and Microcystis aeruginosablooms in the Neuse River, North Carolina. Water Resources Research Institute Report 223. North Carolina State University.Google Scholar
  11. Cohen, A. N. & J. T. Carlton, 1995. Indigenous aquatic species in a United States estuary: study of the biological invasions of the San Francisco Bay and Delta. United States Fish and Wildlife Service, Washington, DC and the National Sea Grant College Program, Connecticut Sea Grant.Google Scholar
  12. DeMott, W. R., Zhang, Q., Carmichael, W. W. 1991Effects of toxic cyanobacteria and purified toxins on the survival and feeding of a copepod and three species of DaphniaLimnology and Oceanography3613461357Google Scholar
  13. Downing, J. A., Watson, S. B., McCauley, E. 2001Predicting cyanobacterial dominance in lakesCanadian Journal of Fisheries and Aquatic Science5819051908CrossRefGoogle Scholar
  14. Feyrer, F., Herbold, B., Matern, S. A., Moyle, P. 2003Dietary shifts in a stressed fish assemblage: consequences of a bivalve invasion in the San Francisco EstuaryEnvironmental Biology of Fishes67277288CrossRefGoogle Scholar
  15. Ghadouani, A., Pinel-Alloul, B., Plath, K., Codd, G. A., Lampert, W. 2004Effects of Microcystis aeruginosaand purified microcystin-LR on the feeding behavior of Daphnia pulicariaLimnology and Oceanography49666679Google Scholar
  16. Hallock, R. J., Elwell, R. F., Fry, D. H. 1970Migrations of Adult King Salmon Oncorhynchus tshawytscha in the San Joaquin Delta, as Demonstrated by the Use of Sonic Tags. Bulletin 151California Department of Fish and Game FishSacramento, CaliforniaGoogle Scholar
  17. Harada, K. 1995Chemistry and detection of microcystinsWatanabe, M. F.Harada, K.Carmichael, W. W.Fujiki, H. eds. Toxic MicrocystisCRC PressNew York103148Google Scholar
  18. Hanazato, T. 1995Toxic cyanobacteria and the zooplankton communityWatanabe, M. F.Harada, K.Carmichael, W. W.Fujiki, H. eds. Toxic Microcystis.CRC PressNew York79102Google Scholar
  19. Horner, R. A., Garrison, D. L., Plumley, F. G. 1997Harmful algal blooms and red tide problems on the US west coastLimnology and Oceanography4210761088Google Scholar
  20. James, K. J., Sherlock, I. R. 1996Determination of the cyanobacterial neurotoxin, anatoxin-a, by derivatization using 7-fluoro-4-nitro-2,1,3-benzoxadiazole (NBD-F) and HPLC analysis with fluorimetric detectionBiomedical Chromatography104647CrossRefPubMedGoogle Scholar
  21. Jassby, A. D., Cloern, J. E., Cole, B. E. 2002Annual primary production: patterns and mechanisms of change in a nutrient-rich tidal ecosystemLimnology and Oceanography47698712Google Scholar
  22. Kaya, K. 1995Toxicology of MicrocystinsWatanabe, M. F.Harada, K.Carmichael, W. W.Fujiki, H. eds. Toxic Microcystis.CRC PressNew York175202Google Scholar
  23. Lehman, P. W. 1992Environmental factors associated with long-term changes in chlorophyll concentration in the Sacramento-San Joaquin Delta and Suisun Bay, CaliforniaEstuaries15335348Google Scholar
  24. Lehman P.W. (1996). Changes in chlorophyll a concentration and phytoplankton community composition with water-year type in the upper San Francisco Bay Estuary. In: Hollibaugh J.T. (eds), San Francisco Bay: The Ecosystem. Pacific Division of the American Association for the Advancement of Science. San Francisco, California, pp. 351–374.Google Scholar
  25. Lehman, P. W. 2000The influence of climate on phytoplankton community carbon in San Francisco Bay EstuaryLimnology and Oceanography45580590Google Scholar
  26. Lehman, P. W. 2004The influence of climate on mechanistic pathways that impact lower food web production in northern San Francisco Bay estuaryEstuaries27311324Google Scholar
  27. Lehman, P. W., Smith, R. W. 1991Environmental factors associated with phytoplankton succession for the Sacramento-San Joaquin Delta and Suisun Bay EstuaryCalifornia. Estuarine Coastal and Shelf Science32105128Google Scholar
  28. Lehman, P. W., Waller, S. 2003Microcystis blooms in the DeltaInteragency Ecological Program for the San Francisco Estuary Newsletter161819Google Scholar
  29. Lindstrom, K. 1983Selenium as a growth factor for plankton algae in laboratory experiments and in some Swedish lakesHydrobiologia1013548Google Scholar
  30. Magalhaes, V. F., Marinho, M. M., Domingos, P., Oliveira, A. C., Costa, S. M., Azevedo, L. O., Azevedo, S. M. F. O. 2003Microcystins (cyanobacteria hepatotoxins) bioacccumulation in fish and crustaceans from Sepetiba Bay (Brazil, RJ)Toxicon42289295CrossRefPubMedGoogle Scholar
  31. Marker, A. F., Crowther, C. A., Gunn, R. J. M. 1980Methanol and acetone as solvents for estimating chlorophyll aand phaeopigments by spectrophotometryAchiv fuer Hydrobiologie supplement145259Google Scholar
  32. Mueller-Solger, A. B., Jassby, A. D., Mueller-Navarra, D. C. 2002Nutritional quality for zooplankton (Daphnia) in a tidal freshwater system (Sacramento-San Joaquin River Delta, USA)Limnology and Oceanography4714681476Google Scholar
  33. O’Brien, K. R., Meyer, D. L., Waite, A. M., Ivey, G. N., Hamilton, D. P. 2004Disaggregation of Microcystis aeruginosa colonies under turbulent mixing: laboratory experiments in a grid-stirred tankHydrobiologia519143152CrossRefGoogle Scholar
  34. Paerl, H. W. 1988Nuisance phytoplankton blooms in coastal, estuarine and inland watersLimnology and Oceanography33823847Google Scholar
  35. Park, H., Watanabe, M. F. 1995Toxic Microcystis in Eutrophic lakesWatanabe, M. F.Harada, K.Carmichael, W. W.Fujiki, H. eds. Toxic MicrocystisCRC PressNew York5778Google Scholar
  36. Reinikainen, M., Ketola, M., Walls, M. 1994Effects of the concentrations of toxic Microcystis aeruginosa and an alternative food on the survival of Daphnia pulexLimnology and Oceanography39424432Google Scholar
  37. Reynolds, C. S., Jaworski, G. H. M., Cmiech, H. A., Leedale, G. F. 1981On the annual cycle of the blue-green alga Microcystis aeruginosa KutzEmend. Elenkin. Philosophical Transactions of the Royal Society of London. Series B. Biological Sciences293419477Google Scholar
  38. Robarts, R. D., Zohary, T. 1992The influence of temperature and light on the upper limit of Microcystis aeruginosa production in a hypertrophic reservoirJournal of Plankton Research14235247Google Scholar
  39. Robson, B. J., Hamilton, D. P. 2003Summer flow event induces a cyanobacterial bloom in a seasonal Western Australia estuaryMarine and Freshwater Research54139151CrossRefGoogle Scholar
  40. SAS Institute, Inc., 2004. SAS/STAT User’s Guide, Version 8. SAS Institute Inc., SAS Campus Drive, Cary, NC.Google Scholar
  41. Sellner, K. G., Brownleee, D. C., Bundy, M. H., Brownlee, S. G., Braun, K. R. 1993Zooplankton grazing in a Potomac River cyanobacteria bloomEstuaries16859872Google Scholar
  42. Sivonen, K., Jones, G. 1999Cyaonbacterial toxinsChorus, I.Bartram, J. eds. Toxic Cyanobacteria in Water.World Health OrganizationLondon41112Google Scholar
  43. United States Environmental Protection Agency (US EPA), 1983. Methods for Chemical Analysis of Water and Wastes. Washington, DC. Technical Report EPA-600/4-79-020.Google Scholar
  44. Utermohl, H. 1958Zur Vervollkommung der quantitativen Phytoplankton-methodikMitteilumgen Internationale Verejunigung fur Theoretische und Angewandtet Limnologie9138Google Scholar
  45. Westhuizen, A. J., Eloff, J. N. 1985Effect of temperature and light on the toxicity and growth of the blue-green alga Microcystis aeruginosa (UV-006)Planta1635559CrossRefGoogle Scholar
  46. Watanabe, M. M. 1995Isolation, cultivation and classification of bloom-forming Microcystis in JapanWatanabe, M. F.Harada, K.Carmichael, W. W.Fujiki, H. eds. Toxic Microcystis.CRC PressNew York1334Google Scholar
  47. Watanabe, M. M., Kaya, K., Takamura, N. 1992Fate of the toxic cyclic heptapepetides, the microcystins, from blooms of Microcystis (cyanobacteria) in a hypertrophic lakeJournal of Phycology28761775CrossRefGoogle Scholar
  48. World Health Organization1998Guidelines for Safe Recreational-Water Environments: Coastal and Freshwaters. Draft for consultationWorld Health OrganizationGenevaGoogle Scholar
  49. Yunes, J. S., Salomon, P. S., Matthiensen, A., Beattie, K. A., Raggett, S. L., Codd, G. A. 1996Toxic blooms of cyanobacteria in the Patos Lagoon Estuary, Southern BrazilJournal of Aquatic Ecosystem Health5223229CrossRefGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • P. W. Lehman
    • 1
    Email author
  • G. Boyer
    • 2
  • C. Hall
    • 3
  • S. Waller
    • 1
  • K. Gehrts
    • 1
  1. 1.California Department of Water ResourcesSacramentoUSA
  2. 2.College of Environmental Science and ForestryState University of New YorkSyracuseUSA
  3. 3.Environmental Science and PolicyUniversity of CaliforniaDavisUSA

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