Abstract
Coastal waters are severely threatened by nitrogen (N) loading from direct groundwater discharge. The subterranean estuary, the mixing zone of fresh groundwater and sea water in a coastal aquifer, has a high potential to remove substantial N. A network of piezometers was used to characterize the denitrification capacity and groundwater flow paths in the subterranean estuary below a Rhode Island fringing salt marsh.15N-enriched nitrate was injected into the subterranean estuary (in situ push-pull method) to evaluate the denitrification capacity of the saturated zone at multiple depths (125–300 cm) below different zones (upland-marsh transition zone, high marsh, and low marsh). From the upland to low marsh, the water table became shallower, groundwater dissolved oxygen decreased, and groundwater pH, soil organic carbon, and total root biomass increased. As groundwater approached the high and low marsh, the hydraulic gradient increased and deep groundwater upwelled. In the warm season (groundwater temperature >12 °C), elevated groundwater denitrification capacity within each zone was observed. The warm season low marsh groundwater denitrification capacity was significantly higher than all other zones and depths. In the cool season (groundwater temperature <10.5 °C), elevated groundwater denitrification capacity was only found in the low marsh. Additions of dissolved organic carbon did not alter groundwater denitrification capacity suggesting that an alternative electron donor, possibly transported by tidal inundation from the root zone, may be limiting. Combining flow paths with denitrification capacity and saturated porewater residence time, we estimated that as much as 29–60 mg N could be removed from 11 of water flowing through the subterranean estuary below the low marsh, arguing for the significance of subterranean estuaries in annual watershed scale N budgets.
Article PDF
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Literature Cited
Addy, K. L., D. Q. Kellogg, A. J. Gold, P. M. Groffman, G. Ferendo, andC. Sawyer. 2002. In situ push-pull method to determine ground water denitrification in riparian zones.Journal of Environmental Quality 31:1017–1024.
Aelion, C. M. andJ. N. Shaw. 2000. Denitrification in South Carolina (USA) coastal plain aquatic sediments.Journal of Environmental Quality 29:1696–1703.
An, S. andW. S. Gardner. 2002. Dissimilatory nitrate reduction to ammonium (DNRA) as a nitrogen link, versus denitrification as a sink in a shallow estuary (Laguna Madre/Baffin Bay, Texas).Marine Ecology Progress Series 237:41–50.
Anderson, I. C., C. R. Tobias, B. B. Neikirk, andR. L. Wetzel. 1997. Development of a process-based nitrogen mass balance model for a VirginiaSpartina alterniflora salt marsh: Implications for net DIN flux.Marine Ecology Progress Series 159:13–27.
American Public Health Association (APHA). 1998. Standard Methods for the Examination of Water and Wastewater. American Public Health Association. Washington, D.C.
Barlow, P. M. 2003. Ground Water in Freshwater-Saltwater Environments of the Atlantic Coast Circular 1262. U.S. Geological Survey, Reston, Virginia.
Beauchamp, E. G., J. T. Trevors, andJ. W. Paul 1989. Carbon sources for bacterial denitrification.Advances in Soil Science 10: 113–141.
Bertness, M. D., D. J. Ewanchuk, andB. R. Silliman. 2002. Anthropogenic modification of New England salt marsh landscapes.Proceedings of the National Academy of Science 99: 1395–1398.
Blicher-Mathiesen, G. andC. C. Hoffmann. 1999. Denitrification as a sink for dissolved nitrous oxide in a freshwater riparian fen.Journal of Environmental Quality 28:257–262.
Bradley, P. M., M. Fernandez, Jr., andF. H. Chapelle. 1992. Carbon limitation of denitrification rates in an anaerobic groundwater system.Environmental Science and Technology 26:2377–2381.
Brawley, J. W., G. Collins, J. N., Kremer, C. Sham, andI. Valiela. 2000. A time-dependent model of nitrogen loading to estuaries from coastal watersheds.Journal of Environmental Quality 29:1448–1461.
Burnett, W. C., M. Taniguchi, andJ. Oberdofer. 2001. Measurement and significance of the direct discharge of groundwater into the coastal zone.Journal of Sea Research 46: 109–116.
Capone, D. G. andM. F. Bautista. 1985. A groundwater source of nitrate in nearshore marine sediments.Nature 313:214–216.
Castro, M. S., C. T. Driscoll, T. E. Jordan, W. G. Reay, andW. R. Boynton. 2003. Sources of nitrogen to estuaries in the United States.Estuaries 26:803–814.
Cervantes, F. J., D. A. De la Rosa, andJ. Gomez. 2001. Nitrogen removal from wastewaters at low C/N ratios with ammonium and acetate as electron donors.Bioresource Technology 79: 165–170.
Cey, E. E., D. L. Rudolph, R. Aravena, andG. Parkin. 1999. Role of the riparian zone in controlling the distribution and fate of agricultural nitrogen near a small stream in southern Ontario.Journal of Contaminant Hydrology 37:45–67.
Childers, D. L. 1994. Fifteen years of marsh flumes—A review of marsh-water column interactions in Southeastern USA estuaries, p. 277–294.In W. Mitsch (ed.), Global Wetlands. Elsevier Publishers, Amsterdam, The Netherlands.
Childers, D. L. andJ. W. Day, Jr. 1988 A flow-through flume technique for quantifying nutrient and materials fluxes in microtidal estuaries.Estuarine Coastal and Shelf Science 27: 483–494.
Cirmo, C. P. andJ. J. McDonnell. 1997. Linking the hydrologic and biogeochemical controls of nitrogen transport in nearstream zones of temperate-forested catchments: A review.Journal of Hydrology 199:88–120.
Glough, T. J., S. C. Jarvis, E. R. Dixon, R. J. Stevens, R. J. Laughlin, andD. J. Hatch. 1999. Carbon induced subsoil denitrification of 15N-labelled nitrate in 1 m deep soil columns.Soil Biology and Biochemistry 31:31–41.
Correll, D. L. 1997. Buffer zones and water quality protection: General principles p. 7–20.In N. E. Haycock, et al. (eds.), Buffer Zones: Their Processes and Potential in Water Protection. Quest Environmental, Harpenden, Hertfordshire, U.K.
Davidson, E. A. andM. K. Firestone. 1988. Measurement of nitroux oxide dissolved in soil solution.Soil Science Society of America Journal 52:1201–1203.
DeCatanzaro, J. B. andE. G. Beauchamp. 1985. The effect of some carbon substrates on denitrification rates and carbon utilization in soil.Biology and Fertility of Soils 1:183–187.
Devito, K. J., D. Fitzgerald, A. R. Hill, andR. Aravena. 2000. Nitrate dynamics in relation to lithology and hydrologic flow path in a river riparian zone.Journal of Environmental Quality 29:1075–1084.
Drexler, J. Z. andK. C. Ewel. 2001. Effect of the 1997–1998 ENSO-related drought on hydrology and salinity in a micronesian wetland complex.Estuaries 24:347–356.
Duff, J. H. andF. J. Triska. 2000. Nitrogen biogeochemistry and surface-subsurface exchange in streams, p. 197–220.In J. B. Jones and P. J. Mulholland (eds.), Streams and Ground Waters. Academic Press, San Diego, California.
Ford, T. E. andR. G. Naiman. 1989. Groundwater-surface water relationship in boreal forest watersheds—Dissolved organic carbon and inorganic nutrient dynamics.Canadian Journal of Fisheries and Aquatic Sciences 46:41–49.
Freeze, R. A. andJ. A. Cherry. 1979. Groundwater. Prentice Hall, Englewood Cliffs, New Jersey.
Gardner, L. R. andH. W. Reeves. 2002. Spatial patterns in soil water fluxes along a forest-marsh transect in the southeastern United States.Aquatic Science 64:141–155.
Gardner, L. R., H. W. Reeves, andP. M. Thibodeau. 2002. Groundwater dynamics along forest-marsh transects in a southeastern salt marsh, USA: Description, interpretation and challenges for numerical modeling.Wetland Ecology and Management 10:145–159.
Gayle, B. P., G. D. Boardman, J. H. Sherrard, andR. E. Benoit. 1989. Biological denitrification of water.Journal of Environmental Engineering 115:930–943.
Giblin, A. E. andA. G. Gaines. 1990. Nitrogen inputs to a marine embayment: The importance of groundwater.Biogeochemistry 10:309–328.
Gold, A. J., P. M. Groffman, K. Addy, D. Q. Kellogg, M. Stolt, andA. E. Rosenblatt. 2001. Landscape attributes as controls on ground water nitrate removal capacity of riparian zones.Journal of the American Water Resources Association 37:1457–1464.
Goni, M. A. andL. R. Gardner. 2003. Seasonal dynamics in dissolved organic carbon concentrations in a coastal water-table aquifer at the forest-marsh interface.Aquatic Geochemistry 9: 209–232.
Gould, W. D. andG. L. McCready. 1982. Denitrification in several soils: Inhibition by sulfur anions.Canadian Journal of Microbiology 28:334–340.
Groffman, P. M. 1994. Denitrification in freshwater wetlands.Current Topics in Wetland Biogeochemistry 1:15–35.
Groffman, P. M., A. J. Gold, andK. Addy. 2000. Nitrous oxide production in riparian zones and its importance to national emission inventories.Chemosphere-Global Change Science 2: 291–299.
Groffman, P. M., A. J. Gold, andP. A. Jacinthe. 1998. Nitrous oxide production in riparian zones and groundwater.Nutrient Cycling in Agroecosystems 52:179–186.
Gross, M. F., M. A. Hardisky, P. L. Wolf, andV. Klemas. 1991. Relationship between aboveground and belowground biomass ofSpartina alterniflora (smooth cordgrass).Estuaries 14:180–191.
Hackney, C. T. andA. A. de la Cruz. 1986. Belowground productivity of roots and rhizomes in a giant cordgrass marsh.Estuaries 9:112–116.
Harvey, J. W. andB. J. Wagner. 2000. Quantifying hydrologic interactions between streams and their subsurface hyporheic zones, p. 3–44.In J. B. Jones and P. J. Mulholland (eds.), Streams and Ground Waters. Academic Press, San Diego, California.
Hedin, L. O., J. C. von Fischer, N. E. Ostrom, B. P. Kennedy, M. G. Brown, andG. P. Robertson. 1998. Thermodynamic constraints on nitrogen transformations and other biogeochemical processes at soil-stream interfaces.Ecology 79:684–703.
Hefting, M. M., R. Bobbink, andH. de Caluwe. 2003. Nitrous oxide emission and denitrification in chronically nitrate-loaded riparian buffer zones.Journal of Environmental Quality 32: 1194–1203.
Hill, A. R. 1996. Nitrate removal in stream riparian zones.Journal of Environmental Quality 25:743–755.
Hill, A. R., K. J. Devito, S. Campagnolo, andK. Sanmugadas. 2000. Subsurface denitrification in a forest riparian zone: Interactions between hydrology and supplies of nitrate and organic carbon.Biogeochemistry 51:193–223.
Howarth, R. W., G. Downing, D. Swaney, A. Townsend, N. Jaworski, K. Lajtha, J. A. Downing, R. Elmgren, N. Caraco, T. Jordan, F. Berendse, J. Freney, V. Kudeyarov, P. Murdoch, andZ. Zhao-Liang. 1996. Regional nitrogen budgets and riverine N and P fluxes for the drainages to the North Atlantic Ocean: Natural and human influences.Biogeochemistry 35:75–139.
Howarth, R., R. Marino, andD. Scavia. 2003. Priority Topics for Nutrient Pollution Coastal Waters: An Integrated National Research Programs for the United States. National Oceanic and Atmospheric Administration, Silver Spring, Maryland.
Howarth, R. W., A. Sharpley, andD. Walker. 2002. Sources of nutrient pollution to coastal waters in the United States: Implications for achieving coastal water quality goals.Estuaries 25:656–676.
Howes, B. L., P. K. Weiskel, D. D. Goehringer, andJ. M. Teal. 1996. Interception of freshwater and nitrogen transport from uplands to coastal waters: The role of saltmarshes, p. 287–310.In K. F. Nordstrom and C. T. Roman (eds.), Estuarine Shores: Evolution, Environments, and Human Alterations. John Wiley and Sons Limited, New York.
Istok, J. D., M. D. Humphrey, M. H. Schroth, M. R. Hyman, andK. T. O’Reilly. 1997. Single-well, “push-pull” test for in situ determination of microbial activities.Ground Water 35:619–631.
Joye, S. B. 2002. Denitrification in the marine environment, p. 1010–1019.In G. Britton (ed.), Encyclopedia of Environmental Microbiology, Wiley Publishers, New York.
Joye, S. B. andJ. T. Hollibaugh. 1995. Sulfide inhibition of nitrification influences nitrogen regeneration in sediments.Science 270:623–625.
Kaplan, W., I. Valiela, andJ. M. Teal. 1979. Denitrification in a salt marsh ecosystem.Limnology and Oceanography 24:726–734.
Kellogg, D. Q., A. J. Gold, P. M. Groffman, K. Addy, M. H. Stolt, andG. Blazejewski. 2005. In situ ground water denitrification in stratified, permeable soils underlying riparian wetlands.Journal of Environmental Quality 34:524–533.
Kellogg, D. Q. N. 2005. The influence of geomorphic setting on ground water denitrification in forested riparian wetlands. Ph.D. Dissertation, University of Rhode Island, Kingston, Rhode Island.
Kilmer, V. J. andL. T. Alexander. 1949. Methods of making analyses of soils.Soil Science 68:15–24.
Koretsky, C. M., C. M. Moore, K. L. Lowe, C. Meile, T. J. DiChristina, andP. Van Cappellen. 2003. Seasonal oscillation of microbial iron and sulfate reduction in saltmarsh sediments (Sapelo Island, GA, USA).Biogeochemistry 64:179–203.
Korom, S. F. 1992. Natural denitrification in the saturated zone: A review.Water Resources Research 28:1657–1668.
LaMontagne, M., V. Astorga, A. E. Giblin, andI. Valiela. 2002. Denit and the stoichiometry of nutrient regeneration in Waquoit Bay, Massachusetts.Estuaries 25:272–281.
LaMontagne, M. G. andI. Valiela. 1995. Denitrification measured by a direct N2 flux method in sediments of Waquoit Bay, MA.Biogeochemistry 31:63–83.
Lemon, E. 1981. Nitrous oxide in freshwaters of the Great Lakes Basin.Limnology and Oceanography 26:867–879.
Lowrance, R., L. S. Altier, J. D. Newbold, R. R. Schnabel, P. M. Groffman, J. M. Denver, D. L. Correll, J. W. Gilliam, J. L. Robinson, R. B. Brinsfield, K. W. Staver, W. Lucas, andA. H. Todd. 1997. Water quality functions of riparian forest buffers in Chesapeake Bay watersheds.Environmental Management 21: 687–712.
Maitre, V., A. C. Cossandey, E. Desagher, andA. Parriaux. 2003. Effectiveness of groundwater nitrate removal in a river riparian area: The importance of hydrogeological conditions.Journal of Hydrology 278:76–93.
McCarty, G. W. andJ. M. Bremner. 1992. Availability of organic carbon for denitrification of nitrate in subsoils.Biology and Fertility of Soils 14:219–222.
Mohseni-Bandpi, A., D. J. Elliott, andA. Momeny-Mazdeh. 1999. Denitrification of groundwater using acetic acid as a carbon source.Water Science and Technology 40:53–59.
Moore, W. S. 1999. The subterranean estuary: A reaction zone of ground water and sea water.Marine Chemistry 65:111–125.
Mosier, A. R. andL. Klemedtsson. 1994. Measuring denitrification in the field, p. 1047–1065.In R. W. Weaver, et al. (eds.), Methods of Soil Analysis, Part 2: Microbiological and Biochemical Properties, 2nd edition. Soil Science Society of America, Madison, Wisconsin.
Nelson, W. M., A. J. Gold, andP. M. Groffman. 1995. Spatial and temporal variation in groundwater nitrate removal in a riparian forest.Journal of Environmental Quality 24:691–699.
Nixon, S. W. 1995. Coastal marine eutrophication: A definition, social causes and future concerns.Ophelia, International Journal of Marine Biology 41:199–219.
Nixon, S. W., B. Buckley, S. Granger, andJ. Bintz. 2001. Responses of very shallow marine ecosystems to nutrient enrichment.Human and Ecological Risk Assessment 7:1457–1481.
Nowicki, B. L., E. Requintina, D. Van Keuren, andJ. Portnoy. 1999. The role of sediment denitrification in reducing groundwater-derived nitrate inputs to Nauset Marsh Estuary, Cape Cod, Massachusetts.Estuaries 22:245–259.
Ott, R. L. 1993. An Introduction to Statistical Methods and Data Analysis, 4th edition. Duxbury Press, Belmont, California.
Otto, S., P. M. Groffman, S. E. G. Findlay, andA. Arreola. 1999. Invasive plant species and microbial processes in a tidal freshwater marsh.Journal of Environmental Quality 28:1252–1257.
Oviatt, C., P. Doering, B. Nowicki, L. Reed, J. Cole, andJ. Frithsen. 1995. An ecosystem level experiment on nutrient limitation in temperate coastal marine environment.Marine Ecology Progress Series 116:171–179.
Payne, W. J. 1981. Denitrification. Wiley Publishers, New York.
Pennings, S. C., L. E. Stanton, andJ. S. Brewer. 2002. Nutrient effects on the composition of salt marsh plant communities along the Southern Atlantic and Gulf Coasts of the United States.Estuaries 25:1164–1173.
Portnoy, J. W., B. L. Nowicki, C. T. Roman, andD. W. Urish. 1998. The discharge of nitrate-contaminated groundwater from developed shoreline to marsh-fringed estuary.Water Resources Research 34:3095–3104.
Prather M., R. Derwent, D. Ehhalt, P. Fraser, E. Sanhueza, andX. Zhou. 1995. Other trace gases and atmospheric chemistry, p. 73–126.In J. Houghton, L. G. Meira, E. Haites, N. Harris, and K. Maskell (eds.), Climate Change 1994: Radioactive Forcing of Climate Change and an Evaluation of the IPCC IS92 Emission Scenarios. Cambridge University Press, New York.
Schipper, L. andM. Vojvodic-Vukovic. 1998. Nitrate removal from groundwater using a denitrification wall amended with sawdust: Field trial.Journal of Environmental Quality 27:664–668.
Schultz, G. andC. Ruppel. 2002. Constraints on hydraulic parameters and implications for groundwater flux across the upland-estuary interface.Journal of Hydrology 260:255–269.
Seitzinger, S. P. 1988. Denitrification in freshwater and coastal marine ecosystems: Ecological and geochemical significance.Limnology and Oceanography 33:702–724.
Short, F. T. andD. M. Burdick. 1996. Quantifying eelgrass habitat loss in relation to housing development and nitrogen loading in Waquoit Bay, Massachusetts.Estuaries 19:730–739.
Simek, M. andJ. E. Cooper. 2002. The influence of soil pH on denitrification: Progress towards the understanding of this interaction over the last 50 years.European Journal of Soil Science 53:345–354.
Soil Survey Staff. 1999. Soil Taxonomy, 2nd edition. U.S. Department of Agriculture Handbook 436, U.S. Government Printing Office, Washington, D.C.
StatSoft. 2002. Statistica 6.0. StatSoft, Tulsa, Oklahoma.
Stolt, M. H. andM. C. Rabenhorst. 1991. Micromorphology of argillic horizons in an upland/tidal marsh catena.Soil Science Society of America Journal 55:443–450.
Talbot, J. M., K. D. Kroeger, A. Rago, M. C. Allen, andM. A. Charette. 2003. Nitrogen flux and speciation through the subterranean estuary of Waquoit Bay, Massachusetts.Biological Bulletin 205:244–245.
Thibodeau, P. M., L. R. Gardner, andH. W. Reeves. 1998. The role of groundwater flow in controlling the spatial distribution of soil salinity and rooted macrophytes in a southeastern salt marsh, USA.Mangroves and Salt Marshes 2:1–13.
Tiedje, J. M. 1982. Denitrification, p. 1011–1026.In A. L. Page, R. H. Miller, and D. R. Keeney (eds.), Methods of Soil Analysis, Part 2: Chemical and Microbiological Properties. Agronomy Monograph 9, 2nd edition. Agronomy Society of America, Madison, Wisconsin.
Tobias, C. R., I. C. Anderson, E. A. Canuel, andS. A. Macko. 2001a. Nitrogen cycling through a fringing marsh-aquifer ecotone.Marine Ecology Progress Series 210:25–39.
Tobias, C. R., J. W. Harvey, andI. C. Anderson. 2001b. Quantifying groundwater discharge through fringing wetlands to estuaries: Seasonal variability, methods comparisons, and implications for wetland-estuary exchange.Limnology and Oceanography 46:604–615.
Tobias, C. R., S. A. Macko, I. C. Anderson, E. A. Canuel, andJ. W. Harvey. 2001. Tracking the fate of a high concentration groundwater nitrate plume through a fringing marsh: A combined groundwater tracer and in situ isotope enrichment study.Limnology and Oceanography 46:1977–1989.
Turner, R. E., E. M. Swenson, C. S. Milan, J. M. Lee, andT. A. Oswald. 2004. Below-ground biomass in healthy and impaired salt marshes.Ecological Research 19:29–35.
Ueda, S., C. S. U. Go, M. Suzumura, andE. Sumi. 2003. Denitrification in a seashore sandy deposit influenced by groundwater discharge.Biogeochemistry 63:187–205.
Valiela, I., G. Collins, J. Kremer, K. Lajtha, M. Geist, B. Seely, J. Brawley, andC. H. Sham. 1997. Nitrogen loading from coastal watersheds to receiving estuaries: New method and application.Ecological Applications 7:358–380.
Valiela, I., J. Costa, K. Foreman, J. M. Teal, B. Howes, andD. Aubrey. 1990. Transport of groundwater-borne nutrients from watersheds and their effects on coastal waters.Biogeochemistry 10:177–197.
Valiela, I., K. Foreman, M. Lamontagne, D. Hersh, J. Costa, P. Peckol, B. Demeo-Andreson, C. D’Avanzo, M. Babione, C. Sham, J. Brawley, andK. Lajtha. 1992. Coupling of watersheds and coastal waters: Sources and consequences of nutrient enrichment in Waquoit Bay, Massachusetts.Estuaries 15: 443–457.
Valiela, I., M. Geist, J. McClelland, andG. Tomasky. 2000. Nitrogen loading from watersheds to estuaries: Verification of the Waquoit Bay nitrogen loading model.Biogeochemistry 49: 277–293.
Valiela, I. andJ. M. Teal. 1974. Nutrient limitation in salt marsh vegetation, p. 547–563.In R. J. Reimold and W. H. Queen (eds.), Ecology of Halophytes. Academic Press, San Diego, California.
Valiela, I. andJ. M. Teal. 1979. The nitrogen budget of a salt marsh ecosystem.Nature 280:652–656.
Wigand, C., R. A. McKinney, M. A. Charpentier, M. M. Chintala, andG. B. Thursby. 2003. Relationships of nitrogen loadings, residential development, and physical characteristics with plant structure in New England salt marshes.Estuaries 26:1494–1504.
Wigand, C., R. A. McKinney, M. M. Chintala, M. A. Charpentier, andP. M. Groffman. 2004. Denitrification enzyme activity of fringe salt marshes in New England (USA).Journal of Environmental Quality 33:1144–1151.
Windham, L. andJ. G. Ehrenfeld. 2003. Net impact of a plant invasion on nitrogen-cycling proceses within a brackish tidal marsh.Ecological Applications 13:883–896.
Winter, T. C., J. W. Harvey, O. L. Franke, andW. M. Alley. 1999. Ground Water and Surface Water: A Single Resource. U.S. Geological Survey Circular 1139. U.S. Geological Survey, Denver, Colorado.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Addy, K., Gold, A., Nowicki, B. et al. Denitrification capacity in a subterranean estuary below a Rhode Island fringing salt marsh. Estuaries 28, 896–908 (2005). https://doi.org/10.1007/BF02696018
Issue Date:
DOI: https://doi.org/10.1007/BF02696018