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Long-term trends and causal factors associated with Microcystis abundance and toxicity in San Francisco Estuary and implications for climate change impacts

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Abstract

The impacts of climate change on Microcystis blooms in San Francisco Estuary are uncertain because factors associated with the abundance and distribution of Microcystis blooms since their inception in 1999 are poorly understood. Discrete and continuous data collected between 2004 and 2008 were used to assess what factors controlled bloom initiation and persistence, if there was an impact of the bloom on mesozooplankton abundance and toxicity or dissolved organic carbon concentration, and how these might vary with climate change. Microcystis abundance was greater in dry years than wet years and both total microcystins concentration and the microcystins content of mesozooplankton tissue increased with abundance. The bloom began in the upstream portions of the estuary and spread farther west during dry years. Bloom initiation required water temperature above 19°C and surface irradiance in the visible range above 100 W m−2. The bloom persisted during a wide range of water quality conditions but was closely correlated with low turbidity. The intensity of Microcystis blooms will likely increase with climate change due to increased water temperature and low streamflow during droughts. Elevated water temperature earlier in the spring could also extend the duration of Microcystis blooms by up to 3 months.

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References

  • Acuna, S. C., D.-F. Deng, P. W. Lehman & S. J. Teh, 2012a. Dietary effects of Microcystis on Sacramento splittail, Pogonichthys macrolepidotus. Aquatic Toxicology 110–111: 1–8.

    Article  PubMed  Google Scholar 

  • Acuna, S., D. Baxa & S. Teh, 2012b. Sublethal dietary effects of microcystin producing Microcystis on threadfin shad, Dorosoma petenense. Toxicon 60: 1191–1202.

    Article  PubMed  CAS  Google Scholar 

  • American Public Health Association, American Water Works Association & Water Environment Association, 1998. Standard Methods for the Examination of Water and Wastewater, 20th ed. American Public Health Association, Washington, D.C.

    Google Scholar 

  • Baldia, S. F., A. D. Evangelista, E. V. Aralar & A. E. Santiago, 2007. Nitrogen and phosphorus utilization in the cyanobacterium Microcystis aeruginosa isolated from Laguna de Bay, Philippines. Journal of Applied Phycology 19: 607–613.

    Article  CAS  Google Scholar 

  • Baxa, D. V., T. Kurobe, K. A. Ger, P. W. Lehman & S. J. Teh, 2010. Estimating the abundance of toxic Microcystis in the San Francisco Estuary using quantitative Q-PCR. Harmful Algal Blooms 9: 342–349.

    Article  CAS  Google Scholar 

  • Black, K., M. Yilmaz & E. J. Phlips, 2011. Growth and toxin production by Microcystis aeruginosa PCC 7806 (Kutzing) Lemmerman at elevated salt concentrations. Journal of Environmental Protection 2: 669–674.

    Article  CAS  Google Scholar 

  • Boyer, G. L., 2007. The occurrence of cyanobacterial toxins in New York Lakes: lessons from the MERHAB-Lower Great lakes program. Lake and Reservoir Management 23: 153–160.

    Article  Google Scholar 

  • Bozarth, C. S., A. D. Schwartz, J. W. Shepardson, F. S. Colwell & T. W. Dreher, 2010. Population Turnover in a Microcystis bloom results in predominantly non-toxigenic variants late in the season. Applied and Environmental Microbiology 76: 5207–5213.

    Article  PubMed  CAS  Google Scholar 

  • Briand, E., N. Escoffier, C. Straub, M. Sabart, C. Quiblier & J.-F. Humbert, 2008. Spatiotemporal changes in the genetic diversity of a bloom-forming Microcystis aeruginosa (cyanobacteria) population. International Society for Microbial Ecology Journal 3: 419–429.

    Google Scholar 

  • Brookes, J. D. & G. G. Ganf, 2001. Variations in the buoyancy response of Microcystis aeruginosa to nitrogen, phosphorus and light. Journal of Plankton Research 23: 1399–1411.

    Article  Google Scholar 

  • Brooks, M. L., E. Fleishman, L. R. Brown, P. W. Lehman, I. Werner, N. Scholz, C. Mitchelmore, J. R. Loworn, M. L. Johnson, D. Schlenk, et al., 2012. Life histories, salinity zones and sublethal contributions of contaminants to pelagic fish declines illustrated with a case study of San Francisco Estuary, California, USA. Estuaries and Coasts. doi:10.1007/s12237-011-9459-6.

  • Carey, C. C., B. W. Ibelings, E. P. Hoffmann, D. P. Hamilton & J. D. Brookes, 2012. Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Research 46: 1394–1407.

    Article  PubMed  CAS  Google Scholar 

  • Chaffin, J. D., T. B. Bridgeman, S. A. Heckathorn & S. Mishra, 2011. Assessment of Microcystis growth rate potential and nutrient status across a trophic gradient in western Lake Erie. Journal of Great Lakes Research 37: 92–100.

    Article  CAS  Google Scholar 

  • Christian, R. R., W. L. Bryant & D. W. Stanley, 1986. Relationship between river flow and Microcystis aeruginosa blooms in the Neuse River, North Carolina. North Carolina Water Resources Research Institute, Raleigh, NC. Report 223. National Technical Information Service, Springfield, VA 22161. PB86-222445.

  • Clarke, K. R., 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18: 117–143.

    Article  Google Scholar 

  • Clarke, K. R. & R. N. Gorley, 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth.

    Google Scholar 

  • Cloern, J. E., 1987. Turbidity as a control on phytoplankton biomass and productivity in estuaries. Continental Shelf Research 7: 1367–1381.

    Article  Google Scholar 

  • Cloern, J. E., N. Knowles, L. R. Brown, D. Cayan, M. D. Dettinger, et al., 2011. Projected evolution of California’s San Francisco Bay-Delta-River System in a century of climate change. PLoS One 6(9): e24465.

    Article  PubMed  CAS  Google Scholar 

  • Davis, T. W., D. L. Berry, G. L. Boyer & C. J. Gobler, 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 

  • Deng, D.-F., K. Zheng, F. Teh, P. W. Lehman & S. J. Teh, 2010. Toxic threshold of dietary microcystin-LR for quart Medaka. Toxicon 55: 787–794.

    Article  PubMed  CAS  Google Scholar 

  • Elliott, J. A., 2012. Is the future blue-green? A review of the current model predictions of how climate change could affect pelagic freshwater cyanobacteria. Water Research 46: 1364–1371.

    Article  PubMed  CAS  Google Scholar 

  • Fastner, J., U. Neumann, B. Wirsing, J. Weckesser, C. Wiedner, B. Nixdorf & I. Chorus, 1999. Microcystins (hepatotoxic heptapeptides) in German fresh water bodies. Environmental Toxicology 14: 13–22.

    Article  CAS  Google Scholar 

  • Ger, K. A., S. J. Teh & C. R. Goldman, 2009. Microcystin-LR toxicity on dominant copepods Eurytemora affinis and Pseudodiaptomus forbesi of the upper San Francisco Estuary. Science of the Total Environment 407: 4852–4857.

    Article  PubMed  CAS  Google Scholar 

  • Glibert, P. M., D. Fullerton, J. M. Burkholder, J. C. Cornwell & T. M. Kana, 2011. Ecological stoichiometry, biogeochemical cycling, invasive species and aquatic food webs: San Francisco Estuary and comparative systems. Reviews in Fisheries Science 19: 358–417.

    Article  Google Scholar 

  • Ibelings, B. W. & K. E. Havens, 2008. Cyanobacterial toxins: a qualitative meta-analysis of concentrations, dosage and effects in freshwater estuarine and marine biota. In Hudnell, H. K. (ed.), Cyanobacterial harmful algal blooms: state of the science and research needs. Advances in Experimental Medicine and Biology 619:675–732.

  • International Agency for Research on Cancer, 2006. Carcinogenicity of nitrate, nitrite, and cyanobacterial peptide toxins. The Lancet Oncology 7: 628–629.

    Article  Google Scholar 

  • IPCC (International Panel on Climate Change), 2007. Climate Change 2007: The Scientific Basis. Contribution of Working Group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, New York.

    Book  Google Scholar 

  • Jacoby, J. M., D. C. Collier, E. B. Welch, F. J. Hardy & M. Crayton, 2000. Environmental factors associated with a toxic bloom of Microcystis aeruginosa. Canadian Journal of Fisheries and Aquatic Science 57: 231–240.

    Article  Google Scholar 

  • Jassby, A. D., 2005. Phytoplankton regulation in a eutrophic tidal river (San Joaquin River, California). San Francisco Estuary and Watershed Science 3, Issue 1, Article 3.

  • Jiang, Y., B. Ji, R. N. S. Wong & M. H. Wong, 2008. Statistical study on the effects of environmental factors on the growth and microcystins production of bloom-forming cyanobacterium-Microcystis aeruginosa. Harmful Algae 7: 127–136.

    Article  CAS  Google Scholar 

  • Latour, D., O. Sabido, M. Salencon & H. Giraudet, 2004. Dynamics and metabolic activity of the benthic cyanobacterium Microcystis aeruginosa in the Grangent reservoir (France). Journal of Plankton Research 26: 719–726.

    Article  CAS  Google Scholar 

  • Lehman, P. W., 2000. The influence of climate on phytoplankton community carbon in San Francisco Bay Estuary. Limnology and Oceanography 45: 580–590.

    Article  CAS  Google Scholar 

  • Lehman, P. W., 2004. The influence of climate on mechanisms that affect lower food web production in estuaries. Estuaries 27: 312–325.

    Google Scholar 

  • Lehman, P. W., G. Boyer, C. Hall, S. Waller & K. Gehrts, 2005. Distribution and toxicity of a new colonial Microcystis aeruginosa bloom in the San Francisco Bay Estuary, California. Hydrobiologia 541: 87–90.

    Article  CAS  Google Scholar 

  • Lehman, P. W., G. Boyer, M. Satchwell & S. Waller, 2008. The influence of environmental conditions on the seasonal variation of Microcystis abundance and microcystins concentration in San Francisco Estuary. Hydrobiologia 600: 187–204.

    Article  CAS  Google Scholar 

  • Lehman, P. W., S. J. Teh, G. L. Boyer, M. Nobriga, E. Bass & C. Hogle, 2010. Initial impacts of Microcystis on the aquatic food web in the San Francisco Estuary. Hydrobiologia 637: 229–248.

    Article  CAS  Google Scholar 

  • Miller, M. A., R. M. Kudela, A. Mekebri, D. Crane, S. C. Oates, et al., 2010. Evidence for a novel marine harmful algal bloom: cyanotoxin (microcystin) transfer from land to sea Otters. PLoS One 5: e12576.

    Article  PubMed  Google Scholar 

  • Moisander, P. H., P. W. Lehman, M. Ochiai & S. Corum, 2009. Diversity of the toxic cyanobacterium Microcystis aeruginosa in the Klamath River and San Francisco Bay delta, California. Aquatic Microbial Ecology 57: 19–31.

    Article  Google Scholar 

  • O’Brien, K. R., D. L. Meyer, A. M. Waite, G. N. Ivey & D. P. Hamilton, 2004. Disaggregation of Microcystis aeruginosa colonies under turbulent mixing: laboratory experiments in a grid-stirred tank. Hydrobiologia 519: 143–152.

    Article  Google Scholar 

  • O’Neil, J. M., T. W. Davis, M. A. Burford & C. J. Gobler, 2012. The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14: 313–334.

    Article  Google Scholar 

  • Parker, A. E., R. C. Dugdale & F. P. Wilkerson, 2012. Elevated ammonium concentrations from wastewater discharge depress primary productivity in the Sacramento River and the Northern San Francisco Estuary. Marine Pollution Bulletin 64: 574–586.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Paerl, H. W., R. S. Fulton, P. H. Moisander & J. Dyble, 2001. Harmful freshwater algal blooms, with an emphasis on cyanobacteria. The Scientific World 1: 76–113.

    Article  CAS  Google Scholar 

  • Paerl, H. W. & J. Huisman, 2008. Blooms like it hot. Science 320: 57–58.

    Article  PubMed  CAS  Google Scholar 

  • Paerl, H. W. & V. J. Paul, 2012. Climate change: links to global expansion of harmful cyanobacteria. Water Research 46: 1349–1363.

    Article  PubMed  CAS  Google Scholar 

  • Raikow, D. F., O. Sarnelle, A. E. Wilson & S. K. Hamilton, 2004. Dominance of the noxious cyanobacterium Microcystis aeruginosa in low-nutrient lakes is associated with exotic zebra mussels. Limnology and Oceanography 49: 482–487.

    Article  Google Scholar 

  • Reichwaldt, E. S. & A. Ghadouani, 2012. Effects of rainfall patterns on toxic cyanobacterial blooms in a changing climate: between simplistic scenarios and complex dynamics. Water Research 46: 1372–1393.

    Article  PubMed  CAS  Google Scholar 

  • Reynolds, C. S., 1997. Vegetation processes in the pelagic: a model for ecosystem theory. In Kinne, O. (ed.), Excellence in Ecology. Ecology Institute, Germany.

    Google Scholar 

  • Reynolds, C. S., 2006. Ecology of Phytoplankton. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Rinta-Kanto, J. M., E. A. Konopko, J. M. DeBruyn, R. A. Bourbonniere, G. L. Boyer & S. W. Wilhelm, 2009. Lake Erie Microcystis: relationship between microcystin production, dynamics of genotypes and environmental parameters in a large lake. Harmful Algae 8: 665–673.

    Article  CAS  Google Scholar 

  • Robarts, R. D. & T. Zohary, 1987. Temperature effects on photosynthetic capacity, respiration, and growth rates of bloom-forming cyanobacteria. New Zealand Journal of Marine and Freshwater Research 21: 391–399.

    Article  CAS  Google Scholar 

  • Robson, B. J. & D. P. Hamilton, 2003. Summer flow event induces a cyanobacterial bloom in a seasonal Western Australia estuary. Marine and Freshwater Research 54: 139–151.

    Article  Google Scholar 

  • Rocha, C., H. Galvão & A. Barbosa, 2002. Role of transient silicon limitation in the development of cyanobacteria blooms in the Guadiana estuary, south-western Iberia. Marine Ecology Progress Series 228: 35–45.

    Article  CAS  Google Scholar 

  • SAS Institute, 2004. SAS/STAT User’s Guide, Version 8. SAS Institute Inc., Cary, USA.

    Google Scholar 

  • Sellner, K. G., R. V. Lacouture & K. G. Parlish, 1988. Effect of increasing salinity on a cyanobacteria bloom in the Potomac River Estuary. Journal of Plankton Research 10: 49–61.

    Article  CAS  Google Scholar 

  • Shen, H. & L. Song, 2007. Comparative studies on physiological responses to phosphorus in two phenotypes of bloom-forming Microcystis. Hydrobiologia 592: 475–486.

    Article  CAS  Google Scholar 

  • Sieracki, C. K., M. E. Sieracki & C. S. Yentsch, 1998. An imaging-in-flow system for automated analysis of marine microplankton. Marine Ecology Progress Series 168: 285–296.

    Article  Google Scholar 

  • Sigee, D. C., 2005. Freshwater Microbiology. Wiley, West Sussex.

    Google Scholar 

  • Sommer, T. R., C. Armor, R. Baxter, R. Breuer, L. Brown, M. Chotkowski, S. Culberson, F. Feyrer, M. Gingras, B. Herbold, W. Kimmerer, A. Mueller-solger, M. Nobriga & K. Souza, 2007. The collapse of pelagic fishes in the upper San Francisco Estuary. Fisheries 32: 270–277.

    Article  Google Scholar 

  • Takamura, N., T. Iwakuma & M. Yasuno, 1987. Uptake of 13C and 15N (ammonium, nitrate and urea) by Microcystis in Lake Kasumigaura. Journal of Plankton Research 9: 151–165.

    Article  Google Scholar 

  • Tonk, L., K. Bosch, P. M. Visser & J. Huisman, 2007. Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa. Aquatic Microbial Ecology 46: 117–123.

    Article  Google Scholar 

  • United States Environmental Protection Agency, 1983. Methods for chemical analysis of water and wastes. Technical Report EPA-600/4-79-020. United States Environmental Protection Agency, Washington, D.C., USA.

  • United States Geological Survey, 1985. Methods for determination of inorganic substances in water and fluvial sediments. Open file report 85–495.

  • Utermöhl, H., 1958. Zur Vervollkommnung der quantitativen Phytoplankton-methodik. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 9: 1–38.

    Google Scholar 

  • Verspagen, J. M. H., E. O. F. M. Snelder, P. M. Visser, K. D. Jöhnk, B. W. Ibelings, L. R. Mur & J. Huisman, 2005. Benthic–pelagic coupling in the population dynamics of the harmful cyanobacterium Microcystis. Freshwater Biology 50: 854–867.

    Article  Google Scholar 

  • Verspagen, J. M. H., J. Passarge, K. D. Jöhnk, P. M. Visser, L. Peperzak, P. Boers, H. J. Laanbroek & J. Huisman, 2006. Water management strategies against toxic Microcystis blooms in the Dutch Delta. Ecological Applications 16: 313–327.

    Article  PubMed  Google Scholar 

  • Wang, X., B. Qin, G. Gao & H. W. Paerl, 2010. Nutrient enrichment and selective predation by zooplankton promote Microcystis (Cyanobacteria) bloom formation. Journal of Plankton Research 32: 457–470.

    Article  Google Scholar 

  • Wright, S. A. & D. H. Schoellhamer, 2004. Trends in the sediment yield of the Sacramento River, California, 1957–2001. San Francisco Estuary and Watershed Science 2, Issue 2, Article 2.

  • Wu, X., F. Kong & M. Zhang, 2011. Photoinhibition of colonial and unicellular Microcystis cells in a summer bloom in Lake Taihu. Limnology 12: 55–61.

    Article  Google Scholar 

  • Yoshida, M., T. Togashi, K. Takeya, J. Yoshimura & M. Tatsuo, 2007. Ammonium supply mode and the competitive interaction between the cyanobacterium Microcystis novacekii and the green alga Scenedesmus quadricauda. Fundamental and Applied Limnology 170: 133–140.

    Article  Google Scholar 

  • Zegura, B., B. Sedmak & M. Filipi, 2003. Microcystin-LR induces oxidative DNA damage in human hepatoma cell line HepG2. Toxicon 41: 41–48.

    Google Scholar 

  • Zhang, M., H. Duan, X. Shi, Y. Yu & F. Kong, 2012. Contributions of meteorology to the phenology of cyanobacterial blooms: implications for future climate change. Water Research 46: 442–452.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was funded by grants from the San Francisco Bay Delta Interagency Ecological Program and the Delta Science Program. The study was facilitated by sampling assistance from the California Department of Water Resources Real-Time Monitoring Section and Bay-Delta and Analysis Monitoring Program, U. S. Fish and Wildlife Service as well as the University of California at Davis Department of Veterinary Medicine.

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  1. Division of Environmental Services, California Department of Water Resources, West Sacramento, CA, USA

    P. W. Lehman & K. Marr

  2. Department of Veterinary Medicine, University of California, Davis, CA, USA

    S. Acuna & S. J. Teh

  3. College of Environmental Science and Forestry, State University of New York, Syracuse, NY, USA

    G. L. Boyer

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  1. P. W. Lehman
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  2. K. Marr
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  3. G. L. Boyer
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  4. S. Acuna
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  5. S. J. Teh
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Correspondence to P. W. Lehman.

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Lehman, P.W., Marr, K., Boyer, G.L. et al. Long-term trends and causal factors associated with Microcystis abundance and toxicity in San Francisco Estuary and implications for climate change impacts. Hydrobiologia 718, 141–158 (2013). https://doi.org/10.1007/s10750-013-1612-8

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