Temporal Variability in Ecological Stoichiometry and Material Exchange in a Tidally Dominated Estuary (North Inlet, South Carolina) and the Impact on Community Nutrient Status

  • Douglas W. Bell
  • Susan Denham
  • Erik M. Smith
  • Claudia R. Benitez-Nelson
Article

Abstract

Across the coastal zone, rates of carbon and nutrient exchange are defined by the spatiotemporal heterogeneity of individual estuarine systems. Elemental stoichiometry provides a mechanism for simplifying overlapping physical, chemical, and biological drivers into proxies that can be used to compare and monitor estuarine biogeochemistry. To this end, the seasonal and tidal variability of estuarine stoichiometry was examined over an annual cycle in North Inlet (NI), South Carolina. Surface samples for dissolved and particulate carbon (C), nitrogen (N), and phosphorus (P) were collected every 20 days (August 2014 to August 2015) over a semi-diurnal tidal cycle. Dissolved nutrient flux estimates of an individual tidal creek were also made. Overall, the results demonstrated the dominance of seasonal versus tidal forcing on water column C:N:P stoichiometry. This seasonal behavior mediated the relative exchange of N and P into and out of the tidal creek and influenced the nutrient status index (NSI) of NI plankton communities. These communities were largely N deficient with the magnitude of this deficiency impacted by assumptions of inorganic versus organic plankton P demand and nutrient supply. Persistent N deficiency appeared to help drive the net import of N, while temporary P surplus likely drives its seasonal export. Combined, these results indicate that material delivery must be considered on seasonal time frames, as net annual fluxes do not reflect the short-term deliveries of C and nutrients into nearshore ecosystems.

Keywords

Stoichiometry Tidal exchange Nutrient status Salt marsh tidal creek NERRS 

Notes

Acknowledgements

We give special thanks to Drs. Jay Pinckney and George Voulgaris for their helpful consultation regarding our statistical approaches and tidal exchange estimates. Additional thanks are given to Elise Van Mersche and Yuan Shen for thoughtful discussions and access to their respective bioassay and bioavailability data. We gratefully acknowledge the efforts of Tracy Buck in collecting and QA/QC’ing the meteorological and YSI water quality data. This is contribution #1852 to the Belle W. Baruch Institute for Marine and Coastal Sciences.

Funding Information

Portions of this work were supported by a National Oceanic and Atmospheric Administration operations grant to the North Inlet—Winyah Bay National Estuarine Research Reserve (Award # NA14NOS4200054). This work was additionally supported by the SPARC Graduate Research Grant program (Office of the Vice President for Research, University of South Carolina to DWB), the Kathryn D. Sullivan Earth and Marine Science Fellowship (S.C. Space Grant and Sea Grant Consortiums to DWB), and the Slocum-Lunz Foundation (to DWB).

Supplementary material

12237_2018_430_MOESM1_ESM.docx (35 kb)
ESM 1 (DOCX 35 kb)

References

  1. Apple, J.K., E.M. Smith, and T.J. Boyd. 2008. Temperature, salinity, nutrients, and the covariation of bacterial production and chlorophyll-a in estuarine ecosystems. Journal of Coastal Research 55: 59–75.CrossRefGoogle Scholar
  2. Aspila, K.I., H. Agemian, and A.S.Y. Chau. 1976. A semi-automated method for the determination of inorganic, organic and total phosphate in sediments. Analyst 101 (1200): 187–197.CrossRefGoogle Scholar
  3. Barbier, E.B., S.D. Hacker, C. Kennedy, E.W. Koch, A.C. Stier, and B.R. Silliman. 2011. The value of estuarine and coastal ecosystem services. Ecological Monographs 81 (2): 169–193.CrossRefGoogle Scholar
  4. Beck, M., O. Dellwig, G. Liebezeit, B. Schnetger, and H.J. Brumsack. 2008. Spatial and seasonal variations of sulphate, dissolved organic carbon, and nutrients in deep pore waters of intertidal flat sediments. Estuarine, Coastal and Shelf Science 79 (2): 307–316.CrossRefGoogle Scholar
  5. Benitez-Nelson, C.R. 2000. The biogeochemical cycling of phosphorus in marine systems. Earth-Science Reviews 51 (1-4): 109–135.CrossRefGoogle Scholar
  6. Benner, R., and M. Strom. 1993. A critical evaluation of the analytical blank associated with DOC measurements by high-temperature catalytic oxidation. Marine Chemistry 41 (1-3): 153–160.CrossRefGoogle Scholar
  7. Berggren, M., R.A. Sponseller, A.R. Alves Soares, and A.K. Bergström. 2015. Toward an ecologically meaningful view of resource stoichiometry in DOM-dominated aquatic systems. Journal of Plankton Research 37 (3): 489–499.CrossRefGoogle Scholar
  8. Borja, A., M. Elliott, J.H. Andersen, A.C. Cardoso, J. Carstensen, J.G. Ferreira, A.S. Heiskanen, J.C. Marques, J.M. Neto, H. Teixeira, L. Uusitalo, M.C. Uyarra, and N. Zampoukas. 2013. Good environmental status of marine ecosystems: what is it and how do we know when we have attained it? Marine Pollution Bulletin 76 (1-2): 16–27.CrossRefGoogle Scholar
  9. Buzzelli, C., O. Akman, T. Buck, E. Koepfler, J. Morris, and A. Lewitus. 2004. Relationships among water-quality parameters from the North Inlet–Winyah Bay National Estuarine Research Reserve, South Carolina. Journal of Coastal Research 45: 59–74.CrossRefGoogle Scholar
  10. Cai, W.J., Y. Wang, J. Krest, and W.S. Moore. 2003. The geochemistry of dissolved inorganic carbon in a surficial groundwater aquifer in North Inlet, South Carolina, and the carbon fluxes to the coastal ocean. Geochimica et Cosmochimica Acta 67 (4): 631–639.CrossRefGoogle Scholar
  11. Childers, D.L., J.W. Day, and H.N. McKellar. 2002. Twenty more years of marsh and estuarine flux studies: revisiting Nixon (1980). In Concepts and controversies in tidal marsh ecology, ed. M.P Weinstein and Daniel A. Kreeger, 391–423. Netherlands: Springer.Google Scholar
  12. Christian, J.R. 2005. Biogeochemical cycling in the oligotrophic ocean: Redfield and non-Redfield models. Limnology and Oceanography 50 (2): 646–657.CrossRefGoogle Scholar
  13. Christian, J.R., M.R. Lewis, and D.M. Karl. 1997. Vertical fluxes of carbon, nitrogen, and phosphorus in the North Pacific Subtropical Gyre near Hawaii. Journal of Geophysical Research: Oceans 102 (C7): 15667–15677.CrossRefGoogle Scholar
  14. Clark, L.L., E.D. Ingall, and R. Benner. 1998. Marine phosphorus is selectively remineralized. Nature 393 (6684): 426–426.CrossRefGoogle Scholar
  15. Cloern, James E., Elizabeth A. Canuel, and David Harris. 2002. Stable carbon and nitrogen isotope composition of aquatic and terrestrial plants of the San Francisco Bay estuarine system. Limnology and Oceanography 47 (3): 713–729.CrossRefGoogle Scholar
  16. Conley, D.J., H.W. Paerl, R.W. Howarth, D.F. Boesch, S.P. Seitzinger, K.E. Havens, C. Lancelot, and G.E. Likens. 2009. Controlling eutrophication: nitrogen and phosphorus. Science 323 (5917): 1014–1015.CrossRefGoogle Scholar
  17. Dame, R., and S. Libes. 1993. Oyster reefs and nutrient retention in tidal creeks. Journal of Experimental Marine Biology and Ecology 171 (2): 251–258.CrossRefGoogle Scholar
  18. Dame, R.F., J.D. Spurrier, T.M. Williams, B. Kjerfve, R.G. Zingmark, T.G. Wolaver, T.H. Chrzanowski, H.N. McKellar, and F.J. Vernberg. 1991. Annual material processing by a salt marsh-estuarine basin in South Carolina, USA. Marine Ecology Progress Series 76: 153–166.CrossRefGoogle Scholar
  19. Dame, R., D. Childers, and E. Koepfler. 1992. A geohydrologic continuum theory for the spatial and temporal evolution of marsh-estuarine ecosystems. Netherlands Journal of Sea Research 30: 63–72.CrossRefGoogle Scholar
  20. Dame, R., M. Alber, D. Allen, M. Mallin, C. Montague, A. Lewitus, A. Chalmers, R. Gardner, C. Gilman, B. Kjerfve, J. Pinckney, and N. Smith. 2000. Estuaries of the South Atlantic coast of North America: their geographical signatures. Estuaries 23 (6): 793–819.CrossRefGoogle Scholar
  21. Duarte, C.M., D.J. Conley, J. Carstensen, and M. Sánchez-Camacho. 2009. Return to Neverland: shifting baselines affect eutrophication restoration targets. Estuaries and Coasts 32 (1): 29–36.CrossRefGoogle Scholar
  22. Dürr, H.H., G.G. Laruelle, C.M. van Kempen, C.P. Slomp, M. Meybeck, and H. Middelkoop. 2011. Worldwide typology of nearshore coastal systems: defining the estuarine filter of river inputs to the oceans. Estuaries and Coasts 34 (3): 441–458.CrossRefGoogle Scholar
  23. Ember, L.M., D.F. Williams, and J.T. Morris. 1987. Processes that influence carbon isotope variations in salt marsh sediments. Marine Ecology Progress Series 36: 33–42.CrossRefGoogle Scholar
  24. Fagherazzi, S., P.L. Wiberg, S. Temmerman, E. Struyf, Y. Zhao, and P.A. Raymond. 2013. Fluxes of water, sediments, and biogeochemical compounds in salt marshes. Ecological Processes 2 (1): 3.CrossRefGoogle Scholar
  25. Falkowski, P.G., R.T. Barber, and V. Smetacek. 1998. Biogeochemical controls and feedbacks on ocean primary production. Science 281 (5374): 200–206.CrossRefGoogle Scholar
  26. Flynn, K.J. 2010. Ecological modelling in a sea of variable stoichiometry: dysfunctionality and the legacy of Redfield and Monod. Progress in Oceanography 84 (1-2): 52–65.CrossRefGoogle Scholar
  27. Frigstad, H., T. Andersen, D.O. Hessen, L.J. Naustvoll, T.M. Johnsen, and R.G. Bellerby. 2011. Seasonal variation in marine C: N: P stoichiometry: can the composition of seston explain stable Redfield ratios? Biogeosciences 8 (10): 2917–2933.CrossRefGoogle Scholar
  28. Gardner, L.R., and B. Kjerfve. 2006. Tidal fluxes of nutrients and suspended sediments at the North Inlet–Winyah Bay National Estuarine Research Reserve. Estuarine, Coastal and Shelf Science 70 (4): 682–692.CrossRefGoogle Scholar
  29. Gardner, L.R., B. Kjerfve, and D.M. Petrecca. 2006. Tidal fluxes of dissolved oxygen at the North Inlet—Winyah Bay national estuarine research Reserve. Estuarine, Coastal and Shelf Science 67 (3): 450–460.CrossRefGoogle Scholar
  30. Geider, R., and J. La Roche. 2002. Redfield revisited: variability of C: N: P in marine microalgae and its biochemical basis. European Journal of Phycology 37 (1): 1–17.CrossRefGoogle Scholar
  31. Glibert, P.M. 2012. Ecological stoichiometry and its implications for aquatic ecosystem sustainability. Current Opinion in Environmental Sustainability 4 (3): 272–277.CrossRefGoogle Scholar
  32. Glibert, P.L., and T.C. Loder. 1977. Automated analysis of nutrients in seawater: a manual of techniques 77: 47. Woods Hole Oceanographic Institution.Google Scholar
  33. Goñi, M.A., and K.A. Thomas. 2000. Sources and transformations of organic matter in surface soils and sediments from a tidal estuary (North Inlet, South Carolina, USA). Estuaries 23 (4): 548–564.CrossRefGoogle Scholar
  34. Gruber, N., and J.L. Sarmiento. 1997. Global patterns of marine nitrogen fixation and denitrification. Global Biogeochemical Cycles 11 (2): 235–266.CrossRefGoogle Scholar
  35. Herrmann, M., R.G. Najjar, W.M. Kemp, R.B. Alexander, E.W. Boyer, W.J. Cai, P.C. Griffith, K.D. Kroeger, S.L. McCallister, and R.A. Smith. 2015. Net ecosystem production and organic carbon balance of US East Coast estuaries: a synthesis approach. Global Biogeochemical Cycles 29 (1): 96–111.CrossRefGoogle Scholar
  36. Hillebrand, H., G. Steinert, M. Boersma, A. Malzahn, C.L. Meunier, C. Plum, and R. Ptacnik. 2013. Goldman revisited: faster-growing phytoplankton has lower N: P and lower stoichiometric flexibility. Limnology and Oceanography 58 (6): 2076–2088.CrossRefGoogle Scholar
  37. Howarth, R., F. Chan, D.J. Conley, J. Garnier, S.C. Doney, R. Marino, and G. Billen. 2011. Coupled biogeochemical cycles: eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Frontiers in Ecology and the Environment 9 (1): 18–26.CrossRefGoogle Scholar
  38. Hutchinson, S.E., F.H. Sklar, and F. H. 1993. Lunar periods as grouping variables for temporally fixed sampling regimes in a tidally dominated estuary. Estuaries and Coasts 16 (4): 789–798.CrossRefGoogle Scholar
  39. Jickells, T.D., J.E. Andrews, D.J. Parkes, S. Suratman, A.A. Aziz, and Y.Y. Hee. 2014. Nutrient transport through estuaries: the importance of the estuarine geography. Estuarine, Coastal and Shelf Science 150: 215–229.CrossRefGoogle Scholar
  40. Kaiser, Christina, Oskar Franklin, Ulf Dieckmann, Andreas Richter, and Nancy Johnson. 2014. Microbial community dynamics alleviate stoichiometric constraints during litter decay. Ecology Letters 17 (6):680–690.Google Scholar
  41. Karl, D.M., K.M. Björkman, J.E. Dore, L. Fujieki, D.V. Hebel, T. Houlihan, R.M. Letelier, and L.M. Tupas. 2001. Ecological nitrogen-to-phosphorus stoichiometry at station ALOHA. Deep Sea Research Part II: Topical Studies in Oceanography 48 (8-9): 1529–1566.CrossRefGoogle Scholar
  42. Kennish, M.J., M.J. Brush, and K.A. Moore. 2014. Drivers of change in shallow coastal photic systems: an introduction to a special issue. Estuaries and Coasts 37 (S1): 3–19.CrossRefGoogle Scholar
  43. Kjerfve, B. 1986. Circulation and salt flux in a well mixed estuary. In Physics of shallow estuaries and bays, ed. J. Van de Kreeke, 22–29. Berlin: Springer Verlag.CrossRefGoogle Scholar
  44. Kjerfve, B., and K.E. Magill. 1989. Geographic and hydrodynamic characteristics of shallow coastal lagoons. Marine Geology 88 (3-4): 187–199.CrossRefGoogle Scholar
  45. Klausmeier, C.A., E. Litchman, and S.A. Levin. 2004. Phytoplankton growth and stoichiometry under multiple nutrient limitation. Limnology and Oceanography 49 (4part2): 1463–1470.CrossRefGoogle Scholar
  46. Krest, J.M., W.S. Moore, L.R. Gardner, and J.T. Morris. 2000. Marsh nutrient export supplied by groundwater discharge: evidence from radium measurements. Global Biogeochemical Cycles 14 (1): 167–176.CrossRefGoogle Scholar
  47. Krom, M.D., and R.A. Berner. 1980. Adsorption of phosphate in anoxic marine sediments. Limnology and Oceanography 25 (5): 797–806.CrossRefGoogle Scholar
  48. Lawrenz, E., E.M. Smith, and T.L. Richardson. 2013. Spectral irradiance, phytoplankton community composition and primary productivity in a salt marsh estuary, North Inlet, South Carolina, USA. Estuaries and Coasts 36 (2): 347–364.CrossRefGoogle Scholar
  49. Leonardos, N., and R.J. Geider. 2004a. Responses of elemental and biochemical composition of Chaetoceros muelleri to growth under varying light and nitrate: phosphate supply ratios and their influence on critical N: P. Limnology and Oceanography 49 (6): 2105–2114.CrossRefGoogle Scholar
  50. Leonardos, N., and R.J. Geider. 2004b. Effects of nitrate: phosphate supply ratio and irradiance on the C: N: P stoichiometry of Chaetoceros muelleri. European Journal of Phycology 39 (2): 173–180.CrossRefGoogle Scholar
  51. Lewitus, A.J., E.T. Koepfler, and J.T. Morris. 1998. Seasonal variation in the regulation of phytoplankton by nitrogen and grazing in a salt-marsh estuary. Limnology and Oceanography 43 (4): 636–646.CrossRefGoogle Scholar
  52. Lillebø, A.I., J.M. Neto, M.R. Flindt, J.C. Marques, and M.A. Pardal. 2004. Phosphorous dynamics in a temperate intertidal estuary. Estuarine, Coastal and Shelf Science 61 (1): 101–109.CrossRefGoogle Scholar
  53. Lønborg, C., and X.A. Álvarez-Salgado. 2012. Recycling versus export of bioavailable dissolved organic matter in the coastal ocean and efficiency of the continental shelf pump. Global Biogeochemical Cycles. 26 (3).  https://doi.org/10.1029/2012GB004353.
  54. Mallin, M.A., D.C. Parsons, V.L. Johnson, M.R. McIver, and H.A. CoVan. 2004. Nutrient limitation and algal blooms in urbanizing tidal creeks. Journal of Experimental Marine Biology and Ecology 298 (2): 211–231.CrossRefGoogle Scholar
  55. Martiny, A.C., C.T. Pham, F.W. Primeau, J.A. Vrugt, J.K. Moore, S.A. Levin, and M.W. Lomas. 2013. Strong latitudinal patterns in the elemental ratios of marine plankton and organic matter. Nature Geoscience 6 (4): 279–283.CrossRefGoogle Scholar
  56. McCrackin, M.L., J.A. Harrison, and J.E. Compton. 2014. Factors influencing export of dissolved inorganic nitrogen by major rivers: a new, seasonal spatially explicit, global model. Global Biogeochemical Cycles. 28 (3): 269–285.  https://doi.org/10.1002/2013GB004723.CrossRefGoogle Scholar
  57. Monaghan, E.J., and K.C. Ruttenberg. 1999. Dissolved organic phosphorus in the coastal ocean: reassessment of available methods and seasonal phosphorus profiles from the Eel River Shelf. Limnology and Oceanography 44 (7): 1702–1714.CrossRefGoogle Scholar
  58. Montani, S., P. Magni, and N. Abe. 2003. Seasonal and interannual patterns of intertidal microphytobenthos in combination with laboratory and areal production estimates. Marine Ecology Progress Series 249: 79–91.CrossRefGoogle Scholar
  59. Moore, C.M., M.M. Mills, K.R. Arrigo, I. Berman-Frank, L. Bopp, P.W. Boyd, E.D. Galbraith, R.J. Geider, C. Cuieu, S.L. Jaccard, T.D. Jickells, J. La Roche, T.M. Lenton, N.M. Mahowald, E. Marañon, I. Marinov, J.K. Moore, T. Nakatsuka, A. Oschiles, M.A. Saito, T.F. Thingstad, A. Tsuda, and O. Ulloa. 2013. Processes and patterns of oceanic nutrient limitation. Nature Geoscience 6 (9): 701–710.CrossRefGoogle Scholar
  60. Morris, J.T., P.V. Sundareshwar, C.T. Nietch, B. Kjerfve, and D.R. Cahoon. 2002. Responses of coastal wetlands to rising sea level. Ecology 83 (10): 2869–2877.CrossRefGoogle Scholar
  61. Moulton, O.M., M.A. Altabet, J.M. Beman, L.A. Deegan, J. Lloret, M.K. Lyons, J.A. Nelson, and C.A. Pfister. 2016. Microbial associations with macrobiota in coastal ecosystems: patterns and implications for nitrogen cycling. Frontiers in Ecology and the Environment 14 (4): 200–208.CrossRefGoogle Scholar
  62. NOAA Center for Operational Oceanographic Products and Services (CO-OPS). 2017. Environmental measurement systems: sensor specifications and measurement algorithms. NOAA’s Ocean Service. NOAA. Jul. 2013. Web. Feb. 2017.Google Scholar
  63. NOAA National Estuarine Research Reserve (NERRS). 2017a. Nutrient and Chlorophyll Monitoring Program and Database Design, v1.8. Centralized Data Management Office: www.nerrsdata.org. 17pp.
  64. NOAA National Estuarine Research Reserve (NERRS). 2017b. YSI 6-Series Multi-Parameter Water Quality Monitoring Standard Operating Procedure, v4.6. Centralized Data Management Office: www.nerrsdata.org. 46pp.
  65. Odum, E.P. 1980. The status of three ecosystem-level hypotheses regarding salt marsh estuaries: tidal subsidy, outwelling and detritus based food chains. In Estuarine perspectives, ed. V.S. Kennedy, 485–495. New York: Academic Press.CrossRefGoogle Scholar
  66. Pinckney, J.L., D.F. Millie, K.E. Howe, H.W. Paerl, and J.P. Hurley. 1996. Flow scintillation counting of 14C-labeled microalgal photosynthetic pigments. Journal of Plankton Research 18 (10): 1867–1880.CrossRefGoogle Scholar
  67. Pinckney, J.L., H.W. Paerl, P. Tester, and T.L. Richardson. 2001. The role of nutrient loading and eutrophication in estuarine ecology. Environmental Health Perspectives 109 (s5): 699–706.CrossRefGoogle Scholar
  68. Pomeroy, L.R., J.E. Sheldon, W.M. Sheldon, J.O. Blanton, J. Amft, and F. Peters. 2000. Seasonal changes in microbial processes in estuarine and continental shelf waters of the south-eastern USA. Estuarine, Coastal and Shelf Science 51 (4): 415–428.CrossRefGoogle Scholar
  69. Redfield, A.C. 1958. The biological control of chemical factors in the environment. American Scientist 46: 205–221.Google Scholar
  70. Ruttenberg, K.C. 1992. Development of a sequential extraction method for different forms of phosphorus in marine sediments. Limnology and Oceanography 37 (7): 1460–1482.CrossRefGoogle Scholar
  71. Saito, M.A., T.J. Goepfert, and J.T. Ritt. 2008. Some thoughts on the concept of colimitation: three definitions and the importance of bioavailability. Limnology and Oceanography 53 (1): 276–290.CrossRefGoogle Scholar
  72. Sañudo-Wilhelmy, S.A., A. Tovar-Sanchez, F.X. Fu, D.G. Capone, E.J. Carpenter, and D.A. Hutchins. 2004. The impact of surface-adsorbed phosphorus on phytoplankton Redfield stoichiometry. Nature 432 (7019): 897–901.CrossRefGoogle Scholar
  73. Scavia, D., J.C. Field, D.F. Boesch, R.W. Buddemeier, V. Burkett, D.R. Cayan, M. Fogarty, M.A. Harwell, R.W. Howart, C. Mason, D.J. Reed, T.C. Royer, A.H. Sallenger, and J.G. Titus. 2002. Climate change impacts on US coastal and marine ecosystems. Estuaries 25 (2): 149–164.CrossRefGoogle Scholar
  74. Seitzinger, S.P., J.A. Harrison, E. Dumont, A.H. Beusen, and A.F. Bouwman. 2005. Sources and delivery of carbon, nitrogen, and phosphorus to the coastal zone: an overview of global nutrient export from watersheds (NEWS) models and their application. Global Biogeochemical Cycles 19 (4).Google Scholar
  75. Sharples, J., J.J. Middelburg, K. Fennel, and T.D. Jickells. 2017. What proportion of riverine nutrients reaches the open ocean? Global Biogeochemical Cycles. 31 (1): 39–58.  https://doi.org/10.1002/2016GB005483.CrossRefGoogle Scholar
  76. Spivak, A.C., and J. Ossolinski. 2016. Limited effects of nutrient enrichment on bacterial carbon sources in salt marsh tidal creek sediments. Marine Ecology Progress Series 544: 107–130.CrossRefGoogle Scholar
  77. Statham, P.J. 2012. Nutrients in estuaries—an overview and the potential impacts of climate change. Science of the Total Environment 434: 213–227.CrossRefGoogle Scholar
  78. Sundareshwar, P.V., J.T. Morris, E.K. Koepfler, and B. Fornwalt. 2003. Phosphorus limitation of coastal ecosystem processes. Science 299 (5606): 563–565.CrossRefGoogle Scholar
  79. Talarmin, A., M.W. Lomas, Y. Bozec, N. Savoye, H. Frigstad, D.M. Karl, and A.C. Martiny. 2016. Seasonal and long-term changes in elemental concentrations and ratios of marine particulate organic matter. Global Biogeochemical Cycles 30 (11): 1699–1711.CrossRefGoogle Scholar
  80. Tappin, A.D. 2002. An examination of the fluxes of nitrogen and phosphorus in temperate and tropical estuaries: current estimates and uncertainties. Estuarine, Coastal and Shelf Science 55 (6): 885–901.CrossRefGoogle Scholar
  81. Thunell, R.C., R. Varela, M. Llano, J. Collister, F.M. Karger, and R. Bohrer. 2000. Organic carbon fluxes, degradation, and accumulation in an anoxic basin: sediment trap results from the Cariaco Basin. Limnology and Oceanography 45 (2): 300–308.CrossRefGoogle Scholar
  82. Tyrrell, T. 1999. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400 (6744): 525–531.CrossRefGoogle Scholar
  83. Ulanowicz, R.E., and D. Baird. 1999. Nutrient controls on ecosystem dynamics: the Chesapeake mesohaline community. Journal of Marine Systems 19 (1-3): 159–172.CrossRefGoogle Scholar
  84. Welschmeyer, N.A. 1994. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnology and Oceanography 39 (8): 1985–1992.CrossRefGoogle Scholar
  85. Weston, N.B., W.P. Porubsky, V.A. Samarkin, M. Erickson, S.E. Macavoy, and S.B. Joye. 2006. Porewater stoichiometry of terminal metabolic products, sulfate, and dissolved organic carbon and nitrogen in estuarine intertidal creek-bank sediments. Biogeochemistry 77 (3): 375–408.CrossRefGoogle Scholar
  86. Wilson, A.M., and J.T. Morris. 2012. The influence of tidal forcing on groundwater flow and nutrient exchange in a salt marsh-dominated estuary. Biogeochemistry 108 (1-3): 27–38.CrossRefGoogle Scholar
  87. Wolaver, T.G., W. Johnson, and M. Marozas. 1984. Nitrogen and phosphorus concentrations within North Inlet, South Carolina—speculation as to sources and sinks. Estuarine, Coastal and Shelf Science 19 (2): 243–255.CrossRefGoogle Scholar
  88. Wolaver, T. G., Dame, R. F., Spurrier, J. D., and A.B. Miller. (1988). Sediment exchange between a euhaline salt marsh in South Carolina and the adjacent tidal creek. Journal of Coastal Research 4 (1): 17–26.Google Scholar
  89. Zohary, T., B. Herut, M.D. Krom, R.F.C. Mantoura, P. Pitta, S. Psarra, F. Rassoulzadegan, N. Stambler, T. Tanaka, T.F. Thingstad, and E.M.S. Woodward. 2005. P-limited bacteria but N and P co-limited phytoplankton in the Eastern Mediterranean—a microcosm experiment. Deep Sea Research Part II: Topical Studies in Oceanography 52 (22-23): 3011–3023.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2018

Authors and Affiliations

  1. 1.School of Earth, Ocean, and EnvironmentUniversity of South CarolinaColumbiaUSA
  2. 2.School of the Earth, Ocean, and EnvironmentUniversity of South CarolinaColumbiaUSA
  3. 3.Belle W. Baruch Institute for Marine and Coastal SciencesUniversity of South CarolinaColumbiaUSA
  4. 4.North Inlet-Winyah Bay National Estuarine Research ReserveGeorgetownUSA

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