Abstract
Seasonal wind-driven upwelling along the U.S. West Coast supplies large concentrations of nitrogen to surface waters that drives high primary production. However, the influence of coastal upwelled nutrients on phytoplankton productivity in adjacent small estuaries and bays is poorly understood. This study was conducted in Drakes Estero, California, a low inflow estuary located in the Point Reyes National Seashore and the site of an oyster mariculture facility that produces 40 % of the oysters harvested in California. Measurements of nutrients, chlorophyll a, phytoplankton functional groups, and phytoplankton carbon and nitrogen uptake were made between May 2010 and June 2011. A sea-to-land gradient in nutrient concentrations was observed with elevated nitrate at the coast and higher ammonium at the landward region. Larger phytoplankton cells (>5 μm diameter) were dominant within the outer and middle Estero where phytoplankton primary productivity was fueled by nitrate and f-ratios were >0.5; the greatest primary production rates were in the middle Estero. Primary production was lowest within the inner Estero, where smaller phytoplankton cells (<5 μm) were dominant, and nitrogen uptake was dominated by ammonium. Phytoplankton blooms occurred at the outer and middle Estero and were dominated by diatoms during the spring and dry-upwelling seasons but dinoflagellates during the fall. Small flagellated algae (>2 μm) were dominant at the inner Estero where no blooms occurred. These results indicate that coastal nitrate and phytoplankton are imported into Drakes Estero and lead to periods of high new production that can support the oyster mariculture; a likely scenario also for other small estuaries and bays.
Similar content being viewed by others
References
Arar, E.J. and G.B. Collins.1992. In vitro determination of chlorophyll a and pheophytin a in marine and freshwater phytoplankton by fluorescence. In: Methods for the Determination of Chemical Substances in Marine and Estuarine Environmental Samples. Report # EPA/600/R-92/121. Cincinnati, OH: Environmental Monitoring and Support Laboratory, Office of Research and Development, U.S. Environmental Protection Agency.
Bakun, A. 1973. Coastal upwelling indices, west coast of North America, 1946–1971. U.S. Department of Commerce, NOAA technical report, NMFS SSRF-671.
Banas, N.S., B.M. Hickey, J.A. Newton, and J.L. Ruesink. 2007. Tidal exchange, bivalve grazing, and patterns of primary production in Willapa Bay, Washington, USA. Marine Ecology Progress Series 341: 123–139.
Bran and Luebbe Inc. 1999a. Silicate in water and seawater. AutoAnalyzer Method No. G-177-96. Buffalo Grove, IL: Bran and Luebbe, Inc.
Bran and Luebbe Inc. 1999b. Bran Luebbe AutoAnalyzer Applications: AutoAnalyzer Method No. G-175-96 phosphate in water and seawater. Buffalo Grove, IL: Bran and Luebbe Inc.
Bran and Luebbe Inc. 1999c. Bran Luebbe AutoAnalyzer Applications: AutoAnalyzer Method No. G-172-96 nitrate and nitrite in water and seawater. Buffalo Grove, IL: Bran and Luebbe Inc.
Brown, C.A., and R.J. Ozretich. 2009. Coupling between the coastal ocean and Yaquina Bay, Oregon: Importance of oceanic inputs relative to other nitrogen sources. Estuaries and Coasts 32: 219–237.
Caffrey, J.M., N. Harrington, and B. Ward. 2002. Biogeochemical processes in a small California estuary: 1. Benthic fluxes and pore water constituents reflect high nutrient freshwater inputs. Marine Ecology Progress Series 233: 39–53.
California Department of Public Health. 2010. 2010 Management Plan for Commercial Shellfishing in Drakes Estero. Technical Report 10–05.
Dortch, Q. 1990. The interaction between ammonium and nitrate uptake in phytoplankton. Marine Biology 331: 221–232.
Dugdale, R.C., and J.J. Goering. 1967. Uptake of new and regenerated forms of nitrogen in primary productivity. Limnology and Oceanography 12: 196–207.
Dugdale, R.C., and F.P. Wilkerson. 1986. The use of 15 N to measure nitrogen uptake in eutrophic oceans: Experimental considerations. Limnology and Oceanography 31: 673–689.
Dugdale, R.C., F.P. Wilkerson, and A. Morel. 1990. Realization of new production in coastal upwelling areas: A means to compare relative performance. Limnology and Oceanography 35(4): 822–829.
Dugdale, R.C., F.P. Wilkerson, V. Hogue, and A. Marchi. 2006. Nutrient controls on new production in the Bodega Bay, California, coastal upwelling plume. Deep Sea Research 53: 3049–3062.
Dugdale, R.C., F.P. Wilkerson, V.E. Hogue, and A. Marchi. 2007. Spring phytoplankton bloom development in San Francisco Estuary: the role of ammonium and nitrate. Estuarine, Coastal and Shelf Science 73: 17–29.
Dumbauld, B.R., J.L. Ruesink, and S.S. Rumbrill. 2009. The ecological role of bivalve shellfish aquaculture in the estuarine environment: A review with application to oyster and clam culture in West Coast (USA) estuaries. Aquaculture 290: 196–223.
Figueiras, F.G., U. Larbarta, and M.J. Fernandez Reiriz. 2002. Coastal upwelling, primary production and mussel growth in the Rias Baixas of Galicia. Hydrobiologia 484: 121–131.
Glibert, P.M., J.M. Burkholder, and T.M. Kana. 2012. Recent insights about relationships between nutrient availability, forms, and stoichiometry, and the distribution, ecophysiology, and food web effects of pelagic and benthic Prorocentrum species. Harmful Algae 14: 231–259.
Glover, H.E., D.A. Bhinney, and C.S. Yentsch. 1986. Photosynthetic characteristics of picoplankton compared with those of larger phytoplankton populations in various water masses in the gulf of Maine. Biological Oceanography 3: 223–248.
Hall, J.A., and W.F. Vincent. 1990. Vertical and horizontal structure in the picophytoplankton communities of a coastal upwelling system. Marine Biology 106(3): 465–471.
Hickey, B.M. 1989. Patterns and processes of circulation over the Washington continental shelf and slope. Oceanography 47: 41–115.
Hickey, B., and N. Banas. 2003. Oceanography of the U.S. Pacific Northwest coastal ocean and estuaries with application to coastal ecology. Estuaries and Coasts 26: 1010–1031.
Horner, R.A., D.L. Garrison, and F.G. Plumley. 1997. Harmful algal blooms and red tide problems on the US west coast. Limnology and Oceanography 42: 1076–1088.
Jeong, H.J., J.Y. Park, J. Nho, M.O. Park, J.H. Ha, K.A. Seong, C. Jeng, C.N. Seong, K.Y. Lee, and W.H. Yih. 2005. Feeding by red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquatic Microbial Ecology 41: 131–143.
Kimbro, D., J. Largier, and E. Grosholz. 2009. Coastal oceanographic processes influence the growth and size of a key estuarine species, the Olympia oyster. Limnology and Oceanography 54: 1425–1437.
Kimmerer, W.J., A.E. Parker, U.E. Lidström, and E.J. Carpenter. 2012. Short-term interannual variability in primary production in the low-salinity zone of the San Francisco Estuary. Estuaries and Coasts 25: 913–929.
Largier, J. 2004. The importance of retention zones in the dispersal of larvae. American Fisheries Society Symposium 42: 105–122.
Largier, J. 2010. Low-Inflow estuaries: hypersaline, inverse and thermal scenarios. In Contemporary Issues in Estuarine Physics, ed. A. Valle-Levinson, A., 247–272. Cambridge University Press.
Largier, J.L., S.V. Smith, and J.T. Hollibaugh. 1997. Seasonally hypersaline estuaries in Mediterranean climate regions. Estuarine, Coastal and Shelf Science 45: 789–797.
Lassiter, A.M., F.P. Wilkerson, R.C. Dugdale, and V.E. Hogue. 2006. Phytoplankton assemblages in the CoOP-WEST coastal upwelling area. Deep-Sea Research 53: 3063–3077.
Legendre, L., and M. Gosselin. 1996. Estimation of N or C uptake rates by phytoplankton using 15 N or 13C: Revisiting the usual computation formulae. Journal of Plankton Research 19: 263–271.
Li, William K.W. 1994. Primary production of prochlorophytes, cyanobacteria, and eukaryotic ultraphytoplankton: Measurements from a flow cytometric sorting. Limnology and Oceanography 39(1): 169–175.
Lomas, M.W., and P.M. Glibert. 1999. Interaction between ambient NH4 and NO3uptake and assimilation: Comparison of diatoms and dinoflagellates at several growth temperature. Marine Biology 133: 541–555.
Lund, J.W., G.C. Kipling, and E.D. Le Cren. 1958. The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11: 143–170.
MacDonald, R.W., F.A. McLaughlin, and C.S. Wong. 1986. The storage of reactive silicate samples by freezing. Limnology and Oceanography 31: 1139–1142.
Margalef, R. 1978. Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanologica Acta 134: 493–509.
Monteiro, P.M.S., B. Spolander, G.B. Brundt, and G. Nelson. 1998. Shellfish mariculture in the Benguela system: Estimates of nitrogen-driven new production in Saldahna Bay using two physical models. Journal of Shellfish Research 17: 3–13.
Montes-Hugo, M.A. 2007. Two decades of aquaculture has not altered the phytoplankton communities of a coastal lagoon influenced by coastal upwelling. Hidrobiologica 17: 213–224.
Moore, L.R., A.F. Post, G. Rocap, and S.W. Chistholm. 2002. Utilization of different nitrogen sources by the marine cyanobacteria Prochlorococcus and Synechococcus. Limnology and Oceanography 47(4): 989–996.
Mortazavi, B., R.L. Iverson, W. Huang, F.G. Lewis, and J.M. Caffrey. 2000. Nitrogen budget of Apalachicola Bay, a bar-built estuary in the northeastern Gulf of Mexico. Marine Ecology Progress Series 195: 1–14.
Newton, J.A., and R.A. Horner. 2003. Use of phytoplankton species indicators to track the origin of phytoplankton blooms in Willapa Bay, Washington. Estuaries 26: 1071–1078.
Oczkowski, A., F. Lewis, S. Nixon, H. Edmiston, R. Robinson, and J. Chanton. 2011. Fresh water inflow and oyster productivity in Apalachicola Bay, FL (USA). Estuaries and Coasts 34: 993–1005.
Packard, T., T.R. Blasco, J.J. MacIsaac, and R.C. Dugdale. 1971. Variations in nitrate reductase activity in marine phytoplankton. Investigacion Pesquera 35(1): 209–219.
Parker, A.E., V.E. Hogue, F.P. Wilkerson, and R.C. Dugdale. 2012. The effect of inorganic nitrogen speciation on primary production in the San Francisco Estuary. Estuarine, Coastal and Shelf Science 104–105: 91–101.
Pitcher, G.C., and D. Calder. 1998. Shellfish mariculture in the Benguela system: Phytoplankton and the availability of food for commercial mussel farms in Saldahna Bay, South Africa. Journal of Shellfish Research 17(1): 15–24.
Probyn, T.A. 1992. The inorganic nitrogen nutrition of phytoplankton in the southern Benguela: New phytoplankton, phytoplankton size and implications for pelagic food webs. South African Journal of Marine Science 12(1): 411–420.
Revilla, M., J. Alexander, and P.M. Glibert. 2005. Urea analysis in coastal waters: Comparison of enzymatic and direct methods. Limnology and Oceanography: Methods 3: 290–299.
Roegner, G.C., and A.L. Shanks. 2001. Import of coastally-derived chlorophyll a to South Slough, Oregon. Estuaries 24: 244–256.
Roegner, G.C., B. Hickey, J.A. Newton, A. Shanks, and D.A. Armstrong. 2002. Wind-induced plume and blume intrusions into Willapa Bay, Washington. Limnology and Oceanography 47(4): 1033–1042.
Ruesink, J.L., G.C. Roegner, B.R. Dumbauld, J.A. Newton, and D.A. Armstrong. 2003. Contributions of coastal and watershed energy sources to secondary production in a northeastern Pacific estuary. Estuaries 26: 1079–1093.
Shapira, M., M.J. Buscot, T. Pollet, S.C. Leterme, and L. Seuront. 2010. Distribution of picophytoplankton communities from brackish to hypersaline waters in a south Australian coastal lagoon. Saline sytems 6(2).
Shipe, R.F., A. Leinweber, and N. Gruber. 2008. Abiotic controls of potentially harmful algal blooms in Santa Monica Bay, California. Continental Shelf Research 28: 2584–2593.
Solórzano, L. 1969. Determination of ammonia in natural waters by phenol hypochlorite method. Limnology and Oceanography 14: 799–801.
Smith, S.V., and J.T. Hollibaugh. 1997. Annual cycle and interannual variability of ecosystem metabolism in a temperate climate embayment. Ecological Monographs 67(4): 509–533.
U.S. Department of the Interior. 2012. Secretary Salazar issues decision on Point Reyes National Seashore permit. DOI news release. http://www.doi.gov/news/pressreleases/secretary-salazar-issues-decision-on-point-reyes-national-seashore-permit.cfm#. Accessed 1 Dec. 2012.
Vander Woude, A.J., J.L. Largier, and R.M. Kudela. 2006. Nearshore retention of upwelled waters north and south of Point Reyes (northern California) — Patterns of surface temperature and chlorophyll observed in CoOP WEST. Deep Sea Research, Part II 53: 2985–2998.
Whitledge, T.E., S.C. Malloy, C.J. Patton, and C.D. Wirick. 1981. Automated nutrient analyses in seawater. Brookhaven Natl. Lab. Formal Rep. BNL 51398.
Wilkerson, F.P., R.C. Dugdale, F.P. Chavez, and R.M. Kudela. 2000. Biomass and productivity in Monterey Bay, CA: Contribution of the larger autotrophs. Deep-Sea Research II 47: 1003–1022.
Wilkerson, F.P., R.C. Dugdale, V.E. Hogue, and A. Marchi. 2006a. Phytoplankton blooms and nitrogen productivity in San Francisco estuary. Estuaries and Coasts 29: 401–416.
Wilkerson, F.P., A. Lassiter, R.C. Dugdale, A. Marchi, and V. Hogue. 2006b. The phytoplankton bloom response to wind events and upwelled nutrients during the CoOP WEST study. Deep Sea Research, Part II 53: 3023–3048.
Acknowledgments
Research and academic experiences were funded in part by the PADI Foundation, Achievement Rewards for College Scientists, California State Universities (CSU) Council on Ocean Affairs, Science & Technology (COAST), College of Science and Engineering and Department of Biology at SFSU, a CSU Pre-Doctoral Scholarship, and the Sally Cassanova Scholarship. A thank you for assisting with the laboratory, field, or logistics of this project goes to J. Largier, A. Marchi, Drakes Bay Oyster Company, B. Becker of the National Park Service; the RTC community, E. Carpenter, S. Blaser, E. Kress, J. Fuller, A. Johnson, J. Lee, J. Huggans, M. Maheigan and A. Pimenta.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by James L Pinckney
Rights and permissions
About this article
Cite this article
Buck, C.M., Wilkerson, F.P., Parker, A.E. et al. The Influence of Coastal Nutrients on Phytoplankton Productivity in a Shallow Low Inflow Estuary, Drakes Estero, California (USA). Estuaries and Coasts 37, 847–863 (2014). https://doi.org/10.1007/s12237-013-9737-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12237-013-9737-6