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Seasonal Nitrogen Uptake Dynamics and Harmful Algal Blooms in the York River, Virginia

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Abstract

During a 2-year study of planktonic nitrogen (N) nutrition, temporal variability of (1) ambient nutrient concentrations; (2) uptake rates of ammonium (NH4+), nitrate (NO3), nitrite (NO2), urea, and amino acids (AA) in three size fractions (> GF/F, > 5 μm, and 5–0.2 μm); (3) NH4+ regeneration and NO3 regeneration (nitrification); and (4) an unexpected bloom of Alexandrium monilatum were examined. Dissolved organic N (DON) was the most abundant form of fixed N. High concentrations of NH4+ and NO2 were detected during the late summer and fall, reaching maximums of 9.9 and 7.6 μmol N L−1, respectively. The highest uptake rates were for NH4+ at all stations, size fractions, and seasons sampled and ranged from 34 to 80% of total absolute N uptake. The magnitude of uptake rates in the > GF/F fraction generally followed the pattern of NH4+ > NO3 > urea > AA > NO2 with some exceptions when urea uptake rates were higher than NO3. Rates of NH4+ regeneration and nitrification often exceeded uptake rates, indicating autochthonous pathways for nutrient loading. Exceptionally high dinoflagellate biomass was found in late summer and corresponded with harmful algal blooms. Kinetic curves measured during an A. monilatum bloom showed high Vmax (33.7 ± 2.7 × 10−3 h−1) and high Ks (7.3 μmol N L−1) for NH4+ suggesting that it can rapidly utilize high concentrations when available but may be outcompeted by other phytoplankton when concentrations of NH4+ are low. However, A. monilatum demonstrated that it is capable of using a diverse suite of N substrates, giving it a potential competitive advantage under diverse nutrient conditions.

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References

  • Altman, J.C., and H.W. Paerl. 2012. Composition of inorganic and organic nutrient sources influences phytoplankton community structure in the New River Estuary, North Carolina. Aquatic Ecology 46 (3): 269–282.

    CAS  Google Scholar 

  • Aluwihare, L., and T. Meador. 2008. Chemical composition of marine dissolved organic nitrogen. In Nitrogen in the Marine Environment, ed. D.G. Capone, D.A. Bronk, M.R. Mulholland, and E.J. Carpenter, 2nd ed., 95–139. San Diego: Academic Press.

    Google Scholar 

  • Antia, N., P. Harrison, and L. Oliveira. 1991. The role of dissolved organic nitrogen in phytoplankton nutrition, cell biology, and ecology. Phycologia 30 (1): 1–89.

    Google Scholar 

  • Arar, E.J., and G.B. Collins. 1997. Method 445.0 in vitro determination of chlorophyll a and pheophytin a in marine and freshwater algae by fluorescence. Washington: U.S. Environmental Protection Agency.

    Google Scholar 

  • Berg, G., P.M. Glibert, M.W. Lomas, and M.A. Burford. 1997. Organic nitrogen uptake and growth by the chrysophyte Aureococcus anophagefferens during a brown tide event. Marine Biology 129 (2): 377–387.

    CAS  Google Scholar 

  • Boesch, D.F., E. Burreson, W. Dennison, E. Houde, M. Kemp, V. Kennedy, R. Newell, K. Paynter, R. Orth, and W. Ulanowicz. 2001. Factors in the decline of coastal ecosystems. Science 293: 629–638.

    Google Scholar 

  • Boynton, W.R., and W.M. Kemp. 2008. Nitrogen in estuaries. In Nitrogen in the marine environment, ed. D.G. Capone, D.A. Bronk, M.R. Mulholland, and E.J. Carpenter, 2nd ed., 809–866. San Diego: Elsevier Press.

    Google Scholar 

  • Bradley, P.B., M.W. Lomas, and D.A. Bronk. 2010. Inorganic and organic nitrogen use by phytoplankton along Chesapeake Bay, measured using a flow cytometric sorting approach. Estuaries and Coasts 33 (4): 971–984.

    CAS  Google Scholar 

  • Bronk, D.A., P.M. Glibert, T.C. Malone, E. Sahlstenand, and S. Banahan. 1998. Inorganic and organic nitrogen cycling in Chesapeake Bay: autotrophic versus heterotrophic processes and relationships to carbon flux. Aquatic Microbial Ecology 15: 177–189.

    Google Scholar 

  • Bronk, D.A., M.W. Lomas, P.M. Glibert, K.J. Schukert, and M.P. Sanderson. 2000. Total dissolved nitrogen analysis: comparisons between the persulfate, UV and high temperature oxidation methods. Marine Chemistry 69 (1-2): 163–178.

    CAS  Google Scholar 

  • Bronk, D.A. 2002. Dynamics of organic nitrogen. In Biogeochemistry of marine dissolved organic matter, ed. D.A. Hansell and C.A. Carlson, 153–247. San Diego: Academic Press.

    Google Scholar 

  • Button, D.K. 1978. On the theory of control of microbial growth kinetics by limiting nutrient concentration. Deep Sea Research 25: 113–1177.

    Google Scholar 

  • Callender, E., and D.E. Hammond. 1982. Nutrient exchange across the sediment-water interface in the Potomac River estuary. Estuarine, Coastal and Shelf Science 15 (4): 395–413.

    CAS  Google Scholar 

  • Collos, Y., A. Vaquer, B. Bibent, P. Souchu, G. Slawyk, and N. Garcia. 2003. Response of coastal phytoplankton to ammonium and nitrate pulses: seasonal variations of nitrogen uptake and regeneration. Aquatic Ecology 37 (3): 227–236.

    CAS  Google Scholar 

  • Connell, C.H., and J.B. Cross. 1950. Mass mortality of the fish associated with the protozoan Gonyaulax in the Gulf of Mexico. Science. 112 (2909): 359–363.

    CAS  Google Scholar 

  • Dauer, D., H. Marshall, J. Donat, M. Lane, P. Morton, S. Doughten, and F. Hoffman. 2005. Status and trends in water quality and living resources in the Virginia Chesapeake Bay: York River (1985–2004). Final Report. Virginia Department of Environmental Quality, Richmond. 63 pp.

  • D’Elia, C.F., F.J. Sanders, and W.R. Boynton. 1986. Nutrient enrichment studies in a coastal plain estuary: phytoplankton growth in large scale, continuous cultures. Canadian Journal of Fisheries and Aquatic Sciences 43 (2): 397–406.

    Google Scholar 

  • Diaz, R.J., R.J. Neubauer, L.C. Schaffner, L. Pihl., and S.P. Baden. 1992. Continuous monitoring of dissolved oxygen in an estuary experiencing periodic hypoxia and the effect of hypoxia on macrobenthos and fish. Science of the Total Environment Supplement: 1055–1068.

  • Diaz, R.J., and R. Rosenberg. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321 (5891): 926–929.

    CAS  Google Scholar 

  • Dortch, Q. 1990. The interaction between ammonium and nitrate uptake in phytoplankton. Marine Ecology Progress Series 61: 183–201.

    CAS  Google Scholar 

  • Dudek, N., M.A. Brzezinski, and P.A. Wheeler. 1986. Recovery of ammonium nitrogen by solvent extraction for the determination of relative 15N abundance in regeneration experiments. Marine Chemistry 18 (1): 59–69.

    CAS  Google Scholar 

  • Dugdale, R.C., and J.J. Goering. 1967. Uptake of new and regenerated forms of nitrogen in primary productivity. Limnology and Oceanography 12 (2): 196–206.

    CAS  Google Scholar 

  • Fisher, T.R., P.R. Carlson, and R.T. Barber. 1982. Sediment nutrient regeneration in three North Carolina estuaries. Estuarine, Coastal and Shelf Science 14 (1): 101–116.

    CAS  Google Scholar 

  • Garside, C. 1981. Nitrate and ammonia uptake in the apex of the New York Bight. Limnology and Oceanography 26 (4): 731–739.

    CAS  Google Scholar 

  • Gasol, J.M., and X.A.G. Morán. 1999. Effects of filtration on bacterial activity and picoplankton community structure as assessed by flow cytometry. Aquatic Microbial Ecology 16: 251–264.

    Google Scholar 

  • Glibert, P.M., F. Lipschultz, J.J. McCarthy, and M.A. Altabet. 1982. Isotope dilution models of uptake and remineralization of ammonium by marine plankton. Limnology and Oceanography 27 (4): 639–650.

    CAS  Google Scholar 

  • Glibert, P.M., C. Garside, J.A. Fuhrman, and M.R. Roman. 1991. Time-dependent coupling of inorganic and organic nitrogen uptake and regeneration in the plume of the Chesapeake Bay estuary and its regulation by large heterotrophs. Limnology and Oceanography 36 (5): 895–909.

    Google Scholar 

  • 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 (6): 875–883.

    CAS  Google Scholar 

  • Glibert, P., J. Harrison, C. Heil, and S. Seitzinger. 2006. Escalating worldwide use of urea—a global change contributing to coastal eutrophication. Biogeochemistry 77 (3): 441–463.

    CAS  Google Scholar 

  • Glibert, P.M., and C. Legrand. 2006. The diverse nutrient strategies of harmful algae: Focus on osmotrophy. In Ecology of harmful algae, ed. E. Granéli and J.T. Turner, 163–175. New York: Springer-Verlag.

    Google Scholar 

  • Glibert, P.M., F.P. Wilkerson, R.C. Dugdale, J.A. Raven, C.L. Dupont, P.R. Leavitt, A.E. Parker, J.M. Burkholder, and T.M. Kana. 2016. Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition, with emphasis on nitrogen-enriched conditions. Limnology and Oceanography 61 (1): 165–197.

    Google Scholar 

  • Gobler, C.J., A. Burson, F. Koch, Y. Tang, and M. Mulholland. 2012. The role of nitrogenous nutrients in the occurrence of harmful algal blooms caused by Cochlodinium polykrikoides in New York estuaries (USA). Harmful Algae 17: 64–74.

    CAS  Google Scholar 

  • Gruber, N. 2008. The marine nitrogen cycle: overview and challenges. In Nitrogen in the marine environment, ed. D.G. Capone, D.A. Bronk, M.R. Mulholland, and E.J. Carpenter, 2nd ed., 1–50. San Diego: Elsevier Press.

    Google Scholar 

  • Haas, L.W. 1975. Plankton dynamics in a temperate estuary with observations on a variable hydrographic conditions. Doctoral dissertation. School of Marine Science. The College of William & Mary, Gloucester Point, VA. 202 pp.

  • Hagy, J.D., W.R. Boynton, C.W. Keefe, and K.V. Wood. 2004. Hypoxia in Chesapeake Bay, 1950-2001: long term change in relation to nutrient loading and river flow. Estuaries 27 (4): 634–658.

    CAS  Google Scholar 

  • Hansell, D.A. 1993. Results and observations from the measurement of DOC and DON in seawater using a high-temperature catalytic oxidation technique. Marine Chemistry 41 (1-3): 195–202.

    CAS  Google Scholar 

  • Harding, J.M., R. Mann, P. Moeller, and M.S. Hsia. 2009. Mortality of the veined rapa whelk, Rapana venosa, in relation to a bloom of Alexandrium monilatum in the York River, United States. Journal of Shellfish Research 28 (2): 363–367.

    Google Scholar 

  • Healey, F.P. 1980. Slope of the Monod equation as an indicator of advantage in nutrient competition. Microbial Ecology l5: 281–286.

    Google Scholar 

  • Hecky, R., and P. Kilham. 1988. Nutrient limitation of phytoplankton in freshwater and marine environments: a review of recent evidence of the effects of enrichment. Limnology and Oceanography 33: 796–822.

    CAS  Google Scholar 

  • Ho, M., and P. Zubkoff. 1979. The effects of a Cochlodinium heterolobatum bloom on the survival and calcium uptake by larvae of the American oyster, Crassostrea virginica. In: Toxic dinoflagellate blooms, eds. F. Taylor and H.H. Seliger. 409-412, New York.

  • Hopkinson, C.S., and R.L. Wetzel. 1982. In situ measurements of nutrient and oxygen fluxes in a coastal marine benthic community. Marine Ecology Progress Series 10: 29–35.

    CAS  Google Scholar 

  • Hsia, M.H., S.L. Morton, L.L. Smith, K.R. Beauchense, K.M. Huncik, and P.D.R. Moeller. 2006. Production of goniodomin A by the planktonic, chain-forming dinoflagellate Alexandrium monilatum (Howell) Balech isolated from the Gulf Coast of the United States. Harmful Algae 5 (3): 290–299.

    CAS  Google Scholar 

  • Hudson, K. 2018. Virginia shellfish aquaculture situation and outlook report. VIMS Marine Resources Report No. 2018-9. VSG-18-3. 20pp.

  • Juhl, A.R. 2005. Growth rates and elemental composition of Alexandrium monilatum, a red-tide dinoflagellate. Harmful Algae 4 (2): 287–295.

    Google Scholar 

  • Kemp, W.M., and W.R. Boynton. 1981. External and internal factors regulating metabolic rates of an estuarine benthic community. Oecologia. 51 (1): 19–27.

    Google Scholar 

  • Kemp, W.M., W.R. Boynton, J.E. Adolf, D.F. Boesch, W.C. Boicourt, G. Brush, J.C. Cornwell, T.R. Fisher, P.M. Glibert, J.D. Hagy, and L.W. Harding. 2005. Eutrophication of Chesapeake Bay: historical trends and ecological interactions. Marine Ecology Progress Series 303: 1–29.

    Google Scholar 

  • Killberg-Thoreson, L., R.E. Sipler, and D.A. Bronk. 2013. Anthropogenic nutrient sources supplied to a Chesapeake Bay tributary support algal growth: a bioassay and high resolution mass spectrometry approach. Estuaries and Coasts 36 (5): 966–980.

    CAS  Google Scholar 

  • Killberg-Thoreson, L., M.R. Mulholland, C.A. Heil, M.P. Sanderson, J.M. O’Neil, and D.A. Bronk. 2014. Nitrogen uptake kinetics in field populations and cultured strains of Karenia brevis. Harmful Algae 38: 73–85.

    CAS  Google Scholar 

  • Koroleff, F. 1983. Simultaneous oxidation of nitrogen and phosphorus compounds by persulfate. In In: Methods of seawater analysis, ed. K. Grasshoff, M. Eberhardt, and F. Kremling, 2nd ed. Weinheimer: GMB: Verlag Chemie.

    Google Scholar 

  • Kuo, A.Y., and B.J. Neilson. 1987. Hypoxia and salinity in Virginia estuaries. Estuaries 10 (4): 277–283.

    CAS  Google Scholar 

  • Lewitus, A.J., B.M. Willis, K.C. Hayes, J.M. Burkholder, H.B. Glasgow Jr., P.M. Glibert, and M.K. Burke. 1999. Mixotrophy and nitrogen uptake by Pfiesteria piscicida (Dinophyceae). Journal of Phycology 35 (6): 1430–1437.

    CAS  Google Scholar 

  • Lin, J., and A.Y. Kuo. 2001. Secondary turbidity maximum in a partially mixed microtidal estuary. Estuaries 24 (5): 707–720.

    Google Scholar 

  • Lomas, M.W., and P.M. Glibert. 1999. Interactions between NH4+ and NO3 uptake and assimilation: comparison of diatoms and dinoflagellates at several growth temperatures. Marine Biology 133 (3): 541–551.

    CAS  Google Scholar 

  • Mackiernan, G. 1968. Seasonal distribution of dinoflagellates in the lower York River, Virginia. Thesis. The College of William and Mary. 104 pp.

  • Malone, T.C., D.J. Conley, T.R. Fisher, P.M. Glibert, L.W. Harding, and K.G. Sellner. 1996. Scales of nutrient-limited phytoplankton productivity in Chesapeake Bay. Estuaries 19 (2): 371–385.

    CAS  Google Scholar 

  • Marshall, H.G. 1994. Succession of dinoflagellate blooms in the Chesapeake Bay, U.S.A. In In: Harmful marine algal blooms, Proceedings of the 6th International Conference on Toxic Marine Phytoplankton, ed. P. Lassus et al., 615–620. Andover: Intercept Ltd.

    Google Scholar 

  • Marshall, H.G., L. Burchardt, T.A. Egerton, and M. Lane. 2008. Status of potentially harmful algae in the lower Chesapeake Bay estuarine system. In In: Proc. 12th International Conference on Harmful Algae, ed. O. Moestrup et al., 203–205. Copenhagen: UNESCO.

    Google Scholar 

  • Marshall, H.G. 2009. Phytoplankton of the York River. Journal of Coastal Research, SI 57: 59–65.

    Google Scholar 

  • McCarthy, J.J., W.R. Taylor, and J.L. Taft. 1975. The dynamics of nitrogen and phosphorus cycling in the open waters of the Chesapeake Bay. In: Marine chemistry in the coastal environment. ed. T.M. Church. 664–681. Am. Chem. Soc.

  • McCarthy, J.J., W.R. Taylor, and J.L. Taft. 1977. Nitrogenous nutrition of the plankton in the Chesapeake Bay. 1. Nutrient availability and phytoplankton preferences. Limnology and Oceanography 22 (6): 996–1011.

    CAS  Google Scholar 

  • McCarthy, J.J., W. Kaplan, and J.L. Nevins. 1984. Chesapeake Bay nutrient and plankton dynamics. 2. Sources and sinks of nitrite. Limnology and Oceanography 29 (1): 84–98.

    CAS  Google Scholar 

  • Moore, K., B. Anderson, and D.J. Wilcox. (2003) Intensive water quality mapping of nearshore and midchannel regions of the James River relative to SAV growth and survival using the DataFlow surface water quality mapping system. Special Reports in Applied Marine Science and Ocean Engineering (SRAMSOE) No. 385. Virginia Institute of Marine Science, William & Mary. https://doi.org/10.21220/V5JX79.

  • Morse, D.C. 1947. Some observations on variations in plankton populations, Patuxent River, Maryland 1943–1945. Chesapeake Biological Laboratory 65. Solomons, MD. pp. 1–31.

  • Morse, R.E., S. Jian, J.L. Blanco-Garcia, W.S. Hunley, S. Fentress, M. Wiggins, and M.R. Mulholland. 2011. Environmental and physical controls on the formation and transport of blooms of the dinoflagellate Cochlodinium polykrikoides Margalef in the lower Chesapeake Bay and its tributaries. Estuaries and Coasts 34 (5): 1006–1025.

    Google Scholar 

  • Morse, R.E., M.R. Mulholland, W.S. Hunley, S. Fentress, M. Wiggins, and J.L. Blanco-Garcia. 2013. Controls on the initiation and development of blooms of the dinoflagellate Cochlodinium polykrikoides Margalef in lower Chesapeake Bay and its tributaries. Harmful Algae 28: 71–82.

    CAS  Google Scholar 

  • Mulholland, M.R., C.J. Gobler, and C. Lee. 2002. Peptide hydrolysis, amino acid oxidation, and nitrogen uptake in communities seasonally dominated by Aureococcus anophagefferens. Limnology and Oceanography 47 (4): 1094–1108.

    Google Scholar 

  • Mulholland, M.R., G. Boneillo, and E. Minor. 2004. A comparison of N and C uptake during brown tide (Aureococcus anophagefferens) blooms from two coastal bays on the east coast of the USA. Harmful Algae 3 (4): 361–376.

    CAS  Google Scholar 

  • Mulholland, M., and M.W. Lomas. 2008. Nitrogen uptake and assimilation. In In: Nitrogen in the marine environment, ed. D.G. Capone, D.A. Bronk, M. Mulholland, and E.J. Carpenter, 2nd ed., 303–384. San Diego: Elsevier Press.

    Google Scholar 

  • Mulholland, M.R., R.E. Morse, G.E. Boneillo, P.W. Bernhardt, K.C. Filippino, L.A. Procise, J.L. Blanco-Garcia, H.G. Marshall, T.A. Egerton, W.S. Hunley, K.A. Moore, D.L. Berrry, and C.J. Gobler. 2009. Understanding causes and impacts of the dinoflagellate, Cochlodinium polykrikoides, blooms in the Chesapeake Bay. Estuaries and Coasts 32 (4): 734–747.

    CAS  Google Scholar 

  • Najjar, R.G., C.R. Pyke, M.B. Adams, D. Breitburg, C. Hershner, M. Kemp, R. Howarth, M.R. Mulholland, M. Paolisso, D. Secor, K. Sellner, D. Wardrop, and R. Wood. 2010. Potential climate-change impacts on the Chesapeake Bay. Estuarine, Coastal and Shelf Science 86 (1): 1–20.

    CAS  Google Scholar 

  • Nixon, S.W., J.R. Kelly, B.N. Furnas, C.A. Oviatt, and S.S. Hale. 1980. Phosphorus regeneration and the metabolism of coastal marine bottom communities. In In: Marine benthic dynamics, ed. K.R. Tenore and B.C. Coull, 219–242. Columbia: Univ. South Carolina Press.

    Google Scholar 

  • Nixon, S.W. 1995. Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41 (1): 199–219.

    Google Scholar 

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

    CAS  Google Scholar 

  • Paerl, H.W., and M.F. Piehler. 2008. Nitrogen and marine eutrophication. In: Nitrogen in the marine environment. In , ed. D.G. Capone, D.A. Bronk, M.R. Mulholland, and E.J. Carpenter, 2nd ed., 529–568. San Diego: Elsevier Press.

    Google Scholar 

  • Paerl, H.W., N.S. Hall, B.L. Peierls, and K.L. Rossignol. 2014. Evolving paradigms and challenges in estuarine and coastal eutrophication dynamics in a culturally and climatically stressed world. Estuaries and Coasts 37 (2): 243–258.

    Google Scholar 

  • Parsons, T., Y. Maita, and C. Lalli. 1984. A manual of chemical and biological methods for seawater analysis. New York: Islands Pergamon Press.

    Google Scholar 

  • Pease, S.K.D. 2016. Alexandrium monilatum in the Lower Chesapeake Bay: sediment cyst distribution and potential health impacts on Crassostrea virginica. Master’s Thesis, Virginia Institute of Marine Science.

  • Philips, S., H.J. Laanbroek, and W. Verstraete. 2002. Origin, causes and effects of increased nitrite concentrations in aquatic environments. Rev. Environ. Sci. Bio/Technology 1 (2): 115–141.

    CAS  Google Scholar 

  • Press, W.H., S.A. Teukolsky, W.T. Vetterling, and B.P. Flannery. 1992. Numerical recipes. New York: Cambridge University Press.

    Google Scholar 

  • Price, N., and P. Harrison. 1987. A comparison of methods for the measurement of dissolved urea concentrations in seawater. Marine Biology 94 (2): 307–317.

    CAS  Google Scholar 

  • Ptacnik, R., T. Anderson, and T. Tamminen. 2010. Performance of the Redfield ratio and a family of nutrient limitation indicators as thresholds of phytoplankton N vs P limitation. Ecosystems 12: 1201–1214.

    Google Scholar 

  • Reay, W. 2009. Water quality within the York River estuary. Journal of Coastal Research 57: 23–39.

    CAS  Google Scholar 

  • Reece, K.S. 2009. Monitoring for HAB species in VA waters of Chesapeake Bay during 2008: emerging HAB species in Chesapeake Bay. Annual report submitted to the Virginia Dept. of Health.

  • Reece, K.S. 2010. Monitoring for HAB species in VA waters of Chesapeake Bay during 2009: emerging HAB species in Chesapeake Bay. Annual report submitted to the Virginia Dept. of Health.

  • Reed, M.L., J.L. Pinckney, C.J. Keppler, L.M. Brock, S.B. Hogan, and D.I. Greenfield. 2016. The influence of nitrogen and phosphorus on phytoplankton growth and assemblage composition in four coastal, southeastern USA systems. Estuarine, Coastal and Shelf Science 177: 71–82.

    CAS  Google Scholar 

  • Rizzo, W.M. 1990. Nutrient exchanges between the water column and a subtidal benthic microalgal community. Estuaries and Coasts 13 (3): 219–226.

    CAS  Google Scholar 

  • Ryther, J., and W. Dunstan. 1971. Nitrogen, phosphorus, and eutrophication in the coastal marine environment. Science. 171 (3975): 1008–1112.

    CAS  Google Scholar 

  • Schaefer, S.C., and J.T. Hollibaugh. 2017. Temperature decouples ammonium and nitrite oxidation in coastal waters. Environmental Science & Technology 51 (6): 3157–3164.

    CAS  Google Scholar 

  • Shen, J., and L. Haas. 2004. Calculating age and residence time in the tidal York River using three-dimensional model experiments. Estuarine, Coastal and Shelf Science 61 (3): 449–461.

    CAS  Google Scholar 

  • Sigman, D.M., K.L. Casciotti, M. Andreani, C. Barford, M. Galanter, and J.K. Böhlke. 2001. A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Analytical Chemistry 73 (17): 4145–4153.

    CAS  Google Scholar 

  • Sin, Y., R. Wetzel, and I. Anderson. 1999. Spatial and temporal characteristics of nutrient and phytoplankton dynamics in the York River estuary, Virginia: analyses of long-term data. Estuaries. 22 (2A): 260–275.

    Google Scholar 

  • Sin, Y., R.L. Wetzel, and I.C. Anderson. 2000. Seasonal variations of size-fractionated phytoplankton along the salinity gradient in the York River estuary, Virginia (USA). Journal of Plankton Research 22 (10): 1945–1960.

    Google Scholar 

  • Sipler, R., and D. Bronk. 2015. Dynamics of dissolved organic nitrogen. In: Biogeochemistry of marine dissolved organic matter. In , ed. D.A. Hansell and C.A. Carlson, 2nd ed., 127–232. San Diego: Academic Press.

    Google Scholar 

  • Slawyk, G., and P. Raimbault. 1995. Simple procedure for simultaneous recovery of dissolved inorganic and organic nitrogen in 15N tracer experiments and improving the isotopic mass balance. Marine Ecology Progress Series 124: 289–299.

    CAS  Google Scholar 

  • Smith, E.M., and W.M. Kemp. 1995. Seasonal and regional variations in plankton community production and respiration for Chesapeake Bay. Marine Ecology Progress Series 116: 217–231.

    Google Scholar 

  • Stanley, D.W., and J.E. Hobbie. 1981. Nitrogen recycling in a North Carolina coastal river. Limnology and Oceanography 26 (1): 30–42.

    CAS  Google Scholar 

  • Tang, Y.Z., and C.J. Gobler. 2012. The toxic dinoflagellate Cochlodinium polykrikoides (Dinophyceae) produces resting cysts. Harmful Algae 20: 71–80.

    Google Scholar 

  • Twomey, L.J., M.F. Piehler, and H.W. Paerl. 2005. Phytoplankton uptake of ammonium, nitrate and urea in the Neuse River Estuary, NC, USA. Hydrobiologia 533 (1-3): 123–134.

    CAS  Google Scholar 

  • Walker, L.M., and K.A. Steidinger. 1979. Sexual reproduction in the toxic dinoflagellate Gonyaulax monilata. Journal of Phycology 15 (s1): 312–315.

    Google Scholar 

  • Webb, K.L., and C.F. D’Elia. 1980. Nutrient and oxygen redistribution during a spring neap tidal cycle in a temperate estuary. Science. 207 (4434): 983–985.

    CAS  Google Scholar 

  • Zubkoff, P., J. Munday, R. Rhodes, and J. Warinner. 1979. Mesoscale features of summer (1975-1979) dinoflagellate blooms in the York River, Virginia (Chesapeake Bay estuary). In In: Toxic dinoflagellate blooms, ed. D. Taylor and H. Seliger, 279–286. New York: Elsevier, Inc.

    Google Scholar 

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Acknowledgments

Thanks to K. Reece and W. Jones for species composition data from q-PCR analyses. Thanks to L. Ott for assistance with phytoplankton enumeration, C. Funkey for assistance in conducting experiments and with sample analysis, D. Parrish and M. Garrett for help with figures, and B. Conroy for manuscript comments and edits. Appreciation is also extended to D. Parrish, B. Neikirk, J. Barber, and A. Miller for supporting lab, field, and mapping aspects of the YSI-associated data. This research was supported by NOAA Sea Grant NA07NAOAR4170047 to D. Bronk. This paper is Contribution No. 3922 of the Virginia Institute of Marine Science, William & Mary.

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Killberg-Thoreson, L., Baer, S.E., Sipler, R.E. et al. Seasonal Nitrogen Uptake Dynamics and Harmful Algal Blooms in the York River, Virginia. Estuaries and Coasts 44, 750–768 (2021). https://doi.org/10.1007/s12237-020-00802-4

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  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-020-00802-4

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