, Volume 82, Issue 3, pp 251–264 | Cite as

Effect of nutrient loading on biogeochemical and microbial processes in a New England salt marsh

  • Jane M. Caffrey
  • Michael C. Murrell
  • Cathleen Wigand
  • Richard McKinney
Original Paper


Coastal marshes represent an important transitional zone between uplands and estuaries. One important function of marshes is to assimilate nutrient inputs from uplands, thus providing a buffer for anthropogenic nutrient loads. We examined the effects of nitrogen (N) and phosphorus (P) fertilization on biogeochemical and microbial processes during the summer growing season in a Spartina patens (Aiton (Muhl.)) marsh in the Narragansett Bay National Estuarine Research Reserve on Prudence Island (RI). Quadruplicate 1 m2 plots were fertilized with N and P additions, N-only, P-only, or no additions. N-only addition significantly stimulated bacterial production and increased pore water NH 4 + and NO 3 concentrations. Denitrification rates ranged from 0 to 8 mmol m−2 day−1. Fertilization had no apparent effect on soil oxygen consumption or denitrification measured in the summer in intact cores due to high core-to-core variation. P fertilization led to increased pore water dissolved inorganic phosphorus (DIP) concentrations and increased DIP release from soils. In contrast the control and N-only treatments had significant DIP uptake across the soil-water interface. The results suggest that in the summer fertilization has no apparent effect on denitrification rates, stimulates bacterial productivity, enhances pore water nutrient concentrations and alters some nutrient fluxes across the marsh surface.


Bacterial production Fertilization Denitrification Nitrogen Phosphorus Salt marsh 



We thank Nick Baldauf and John Searles for their invaluable assistance in the field and laboratory. We thank Kenny Raposa, Roger Green and Al Beck for facilitating the implementation of the manipulative field experiment on the National Estuarine Research Reserve on Prudence Island. We thank Saro Jayaraman and Marty Chintala for their assistance in running nutrient analyses and Jeff Cornwell and Todd Kana for the use of their MIMS mass spectrometer for denitrification measurements. Jeff Chanton and anonymous reviewers provided useful suggestions to improve this manuscript. This report was funded in part by the US EPA’s Office of Research and Development, National Health and Environmental Effects Research Laboratory, Atlantic Ecology Division. US EPA Funding does not signify that the contents necessarily reflect the views and policies of the US EPA. Mention of trade names or commercial products does not constitute endorsement by the US EPA. Contribution No. 1211 US EPA, Gulf Breeze, FL, USA.


  1. Abd. Aziz SA, Nedwell DB (1986) The nitrogen cycle of an east coast, UK saltmarsh: II Nitrogen fixation, nitrification, denitrification, tidal exchange. Estuar Coast Shelf Sci 22:689–704CrossRefGoogle Scholar
  2. Allen MF (1991) The ecology of mycorrhizae. Cambridge University Press, Cambridge, UKGoogle Scholar
  3. Anderson IC, Tobias CR, Neikirk BB, Wetzel RL (1997) Development of a process-based nitrogen mass balance model for a Virginia (USA) Spartina alterniflora salt marsh: implications for net DIN flux. Mar Ecol Prog Ser 159:13–27Google Scholar
  4. Austin HK, Findlay SEG (1989) Benthic bacterial biomass and production in the Hudson River estuary. Microb Ecol 18:105–116CrossRefGoogle Scholar
  5. Bott TL, Kaplan LA (1985) Bacterial biomass, metabolic state, and activity in stream sediments: relation to environmental variables and multiple assay comparisons. Appl Environ Microbiol 50:508–522Google Scholar
  6. Bottomley EZ, Bayley IL (1984) A sediment porewater sampler used in root zone studies of the submerged macrophyte, Myriophyllum spicatum. Limnol Oceanogr 29:671–673Google Scholar
  7. Bowden WB (1986) Nitrification, nitrate reduction and nitrogen immobilization in a tidal freshwater marsh sediment. Ecology 67:88–99CrossRefGoogle Scholar
  8. Boyer KE, Fong P, Vance RR, Ambrose RF (2001) Salicornia virginica in a southern California salt marsh: seasonal patterns and a nutrient-enrichment experiment. Wetlands 21:315–326CrossRefGoogle Scholar
  9. Buresh RJ, DeLaune RD, Patrick WH Jr (1980) Nitrogen and phosphorus distribution and utilization by Spartina alterniflora in a Louisiana Gulf Coast marsh. Estuaries 3:111–121CrossRefGoogle Scholar
  10. Burke DJ (2001) The interaction between the grass Spartina patens, N-fixing bacteria and vesicular arbuscular mycorrhizae in a Northeastern salt marsh. Ph.D. Dissertation, Rutgers UniversityGoogle Scholar
  11. Burke DJ, Hamerlynck EP, Hahn D (2002a) Effect of arbuscular mycorrhizae on soil microbial populations and associated plant performance of the salt marsh grass Spartina patens. Plant Soil 239:141–154CrossRefGoogle Scholar
  12. Burke DJ, Hamerlynck EP, Hahn D (2002b) Interactions among plant species and micoorganisms in salt marsh sediments. Appl Environ Microbiol 68:1157–1164CrossRefGoogle Scholar
  13. Buschbaum R, Valiela I, Swain T, Dzierzeski M, Allen S (1991) Available and refractory nitrogen in detritus of coastal vascular plants and macroalgae. Mar Ecol Prog Ser 72:131–143Google Scholar
  14. Caffrey JM, Kemp WM (1990) Nitrogen cycling in sediments with submerged macrophytes: microbial transformations and inorganic pools associated with estuarine populations of Potamogeton perfoliatus L. and Zostera marina. Mar Ecol Prog Ser 66:147–160Google Scholar
  15. Caffrey JM, Kemp WM (1992) Influence of the submersed plant, Potamogeton perfoliatus L., on nitrogen cycling in estuarine sediments. Limnol Oceanogr 37:1483–1495Google Scholar
  16. Chambers RM, Harvey JW, Odum WE (1992) Ammonium and phosphate dynamics in a Virginia salt marsh. Estuaries 15:349–359CrossRefGoogle Scholar
  17. Christensen RR, Hanson RB, Hall JR, Wiebe WJ (1981) Aerobic microbes and meiofauna. In: Pomeroy LR, Wiegert RG (eds) The ecology of a salt marsh. Springer, Berlin Heidelberg New York, NY, USA, pp 113–135Google Scholar
  18. Cooke JC, Butler R, Madole G (1993) Some observations on the vertical distribution of vesicular arbuscular mycorrhizae in the roots of salt marsh grasses growing in saturated soils. Mycologia 84:547–550Google Scholar
  19. Dacey JWH, Howes BL (1984) Water uptake by roots controls water table movement and sediment oxidation in short Spartina marsh. Science 224:487–489CrossRefGoogle Scholar
  20. Davis JL, Nowicki B, Wigand C (2004) Denitrification in Fringing salt marshes of Narragansett Bay, RI (USA). Wetlands 24:870–878CrossRefGoogle Scholar
  21. DeLaune RD, Patrick WH Jr (1980) Nitrogen and phosphorus cycling in a Gulf coast salt marsh. In: Kennedy VS (ed) Estuarine perspectives. Academic, New York, NY, USA, pp 143–151Google Scholar
  22. DeLaune RD, Patrick WH Jr (1990) Nitrogen cycling in Louisiana Gulf Coast brackish marshes. Hydrobiologia 199:73–79CrossRefGoogle Scholar
  23. Diamond DH (1997a) Determination of ammonia in brackish or seawater by flow injection analysis colorimetry. QuikChem Method 31-107-06-1-C for Lachat Instruments. Milwaukee, WIGoogle Scholar
  24. Diamond DH (1997b) Determination of nitrate in brackish or seawater by flow injection analysis. QuikChem Method 31-107-04-1-A for Lachat Instruments. Milwaukee, WIGoogle Scholar
  25. Dixon JL, Turley CM (2001) Measuring bacterial production in deep-sea sediments using 3H-thymidine incorporation: ecological significance. Microb Ecol 42:549–561CrossRefGoogle Scholar
  26. Dollhopf SL, Hyun J-H, Smith AC, Adams HJ, O’Brien S, Kostka JE (2005) Quantification of ammonia-oxidizing bacteria and factors controlling nitrification in salt marsh sediments. Appl Environ Microbiol 71:240–246CrossRefGoogle Scholar
  27. Eriksson PG, Svensson JM, Carrer GM (2003) Temporal changes and spatial variation of soil oxygen consumption, nitrification and denitrification rates in a tidal salt marsh of the Lagoon of Venice, Italy. Estuar Coast Shelf Sci 58:861–871CrossRefGoogle Scholar
  28. Furtado ALS, Casper P (1999) Bacterial production and abundance in sediment of an oligo- and a eutrophic German Lake. German Society of Limnology (DGL), Annual Meeting 1998, Klagenfurt, Austria, Extended abstracts vol 2. Eigenverlag der DGL Tutzing (ISBN 3-9805678-2-6) pp 554–558Google Scholar
  29. Gleason ML, Zieman JC (1981) Influence of tidal inundation on internal oxygen supply of Spartina alterniflora and Spartina patens. Estuar Coast Shelf Sci 13:47–57Google Scholar
  30. Haines EB, Chalmers A, Hanson R, Sherr B (1977) Nitrogen pools and fluxes on a Georgia salt marsh. In: Wiley M (ed) Estuarine processes, vol 2. Academic, New York, NY, USA, pp 241–254Google Scholar
  31. Hamersley MR, Howes BL (2005) Coupled nitrification-denitrification measured in situ in a Spartina alterniflora marsh with 15NH4+ tracer. Mar Ecol Prog Ser 299:123–135Google Scholar
  32. Hesslein RH (1976) An in situ sampler for close interval porewater studies. Limnol Oceanogr 21:912–914Google Scholar
  33. Hogan ME, Ward BB (1998) Response of a sediment microbial community exposed to 2,4-Dichlorophenoxyacetic acid. Microb Ecol 35:72–82CrossRefGoogle Scholar
  34. Howes BL, Goehringer DD (1994) Porewater drainage and dissolved organic carbon and nutrient losses through the intertidal creekbanks of a New England salt marsh. Mar Ecol Prog Ser 114:289–301Google Scholar
  35. Howes BL, Teal JM (1994) Oxygen loss from spartina alterniflora and its relationship to salt marsh oxygen balance. Oecologia 97:431–438CrossRefGoogle Scholar
  36. Huberty A, Diamond D (1998) Determination of phosphorus by flow injection analysis colorimetry. QuikChem Method 31-115-01-3-A for Lachat Instruments. Milwaukee, WIGoogle Scholar
  37. Johnson R, LaMontagne M, Valiela I (1994) Rate of denitrification in submerged salt marsh sediments. Biol Bull 187:289–290CrossRefGoogle Scholar
  38. Joye SB, Paerl HW (1994) Nitrogen cycling in microbial mats: rates and patterns of denitrification and nitrogen fixation. Mar Biol 119:285–296CrossRefGoogle Scholar
  39. Kana TM, Darkangelo C, Hunt MD, Oldham JB, Bennett GE, Cornwell JC (1994) Membrane inlet mass spectrometer for rapid high-precision determination of N2, O2 and Ar in environmental water samples. Anal Chem 66:4166–4170CrossRefGoogle Scholar
  40. Kaplan W (1977) Denitrification in a Massachusetts salt marsh. Ph.D. Dissertation, Boston UniversityGoogle Scholar
  41. Kaplan W, Valiela I, Teal JM (1979) Denitrification in a salt marsh ecosystem. Limnol Oceanogr 24:726–734Google Scholar
  42. Kirschner AKT, Velimirov B (1999) Benthic bacterial secondary production measured via simultaneous 3H-thymidine and 14C-leucine incorporation, and its implication for the carbon cycle of a shallow macrophyte-dominated backwater system. Limnol Oceanogr 44:1871–1881Google Scholar
  43. Koch MS, Maltby E, Oliver GA, Bakker SA (1992) Factors controlling denitrification rates of tidal mudflats and fringing salt marshes in South-west England. Estuar Coast Shelf Sci 34:471–485CrossRefGoogle Scholar
  44. Langis RM, Zalejko M, Zedler JB (1991) Nitrogen assessments in a constructed and a natural salt marsh of San Diego Bay. Ecol Appl 1:40–51CrossRefGoogle Scholar
  45. Lindau CW, DeLaune RD (1991) Dinitrogen and nitrous oxide emission and entrapment in Spartina alterniflora saltmarsh soils following addition of N-15 labeled ammonium and nitrate. Estuar Coast Shelf Sci 32:161–172CrossRefGoogle Scholar
  46. Merrill JZ, Cornwell JC (2000) The role of oligohaline marshes in estuarine nutrient cycling. In: Weinstein MP, Kreeger DA (eds) Concepts and controversies in tidal marsh ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 425–442Google Scholar
  47. Moran MA, Hodson RE (1992) Contributions of three subsystems of a freshwater marsh to total bacterial secondary productivity. Microb Ecol 24:161–170CrossRefGoogle Scholar
  48. Moriarty DJW, Pollard PC (1981) DNA synthesis as a measure of bacterial productivity in seagrass sediments. Mar Ecol Prog Ser 5:151–156Google Scholar
  49. Morris JT, Bradley PM (1999) Effects of nutrient loading on the carbon balance of coastal wetland sediments. Limnol Oceanogr 44:699–702CrossRefGoogle Scholar
  50. National Research Council (2000) Clean coastal waters: understanding and reducing the effects of nutrient pollution. National Academy Press, Washington, DC, USAGoogle Scholar
  51. Page HM (1995) Variation in the natural abundance of 15N in the halophyte, Salicornia virginica, associated with groundwater subsidies of nitrogen in a southern California salt-marsh. Oecologia 104:181–188CrossRefGoogle Scholar
  52. Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis Pergamon Press, Oxford, UKGoogle Scholar
  53. Porter KG, Feig YK (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948Google Scholar
  54. Rublee PA (1982) Seasonal distribution of bacteria in salt marsh sediments in North Carolina. Estuar Coast Shelf Sci 15:67–74CrossRefGoogle Scholar
  55. Rublee P, Dornseif BE (1978) Direct counts of bacteria in the sediments of a North Carolina salt marsh. Estuaries 1:188–191CrossRefGoogle Scholar
  56. Schroeder S (1997) Determination of nitrite in brackish or seawater by flow injection analysis. QuikChem Method 31-107-05-1-A for Lachat Instruments. Milwaukee, WIGoogle Scholar
  57. Scudlark JR, Church TM (1989) The sedimentary flux of nutrients at a Delaware salt marsh site: a geochemical perspective. Biogeochemistry 7:55–75CrossRefGoogle Scholar
  58. Seitzinger SP (1988) Denitrification in freshwater and coastal marine ecosystems: ecological and geochemical significance. Limnol Oceanogr 33:702–724Google Scholar
  59. Seitzinger SP (1994) Linkages between organic matter mineralization and denitrification in eight riparian wetlands. Biogeochemistry 28:19–39Google Scholar
  60. Seitzinger SP, Nixon SW (1985) Eutrophication and the rate of denitrification and N2O production in coastal marine sediments. Limnol Oceanogr 30:1332–1339Google Scholar
  61. Sherr BF, Payne WJ (1981) The effect of sewage sludge on salt-marsh denitrifying bacteria. Estuaries 4:146–149CrossRefGoogle Scholar
  62. Simon M, Azam F (1989) Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser 51:201–213Google Scholar
  63. Smith DC, Azam F (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microbial Food Webs 6:107–114Google Scholar
  64. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San Diego, CA, USAGoogle Scholar
  65. Sullivan MJ, Daiber FC (1974) Response in production of cord grass, Spartina alterniflora, to inorganic nitrogen and phosphorus fertilizer. Chesapeake Sci 15:121–123CrossRefGoogle Scholar
  66. Sundareshwar PV, Morris JT, Koepfler EK, Fornwalt B (2003) Phosphorus limitation of coastal ecosystem processes. Science 299:563–565CrossRefGoogle Scholar
  67. Teal JM, Howes BL (2000) Salt marsh values: retrospection from the end of the century. In: Weinstein MP, Kreeger DA (eds) Concepts and controversies in tidal marsh ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 9–19Google Scholar
  68. Thompson SP, Paerl HW, Go MC (1995) Seasonal patterns of nitrification and denitrification in a natural and restored salt marsh. Estuaries 18:399–408CrossRefGoogle Scholar
  69. Tibbles BJ, Davis CL, Harris JM, Lucas MI (1992) Estimates of bacterial productivity in marine sediments and water from a temperate saltmarsh lagoon. Microb Ecol 23:195–209CrossRefGoogle Scholar
  70. Tobias CR, Macko SA, Anderson IC, Canuel EA (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. Limnol Oceanogr 46:1977–1989CrossRefGoogle Scholar
  71. Tuominen L (1995) Comparison of leucine uptake methods and a thymidine incorporation method for measuring bacterial activity in sediment. J Microbiol Methods 24:125–137CrossRefGoogle Scholar
  72. Valiela I, Teal JM (1974) Nutrient limitation in salt marsh vegetation. In: Reimold RJ, Queen WH (eds) Ecology of halophytes. Academic, New York, NY, USA, pp 547–563Google Scholar
  73. Valiela I, Teal JM, Sass WJ (1975) Production and dynamics of salt marsh vegetation and the effects of experimental treatment with sewage sludge. J Appl Ecol 12:973–981CrossRefGoogle Scholar
  74. Valiela I, Teal JM, Persson NY (1976) Production and dynamics of experimentally enriched salt marsh vegetation: belowground biomass. Limnol Oceanogr 21:245–252CrossRefGoogle Scholar
  75. Valiela I, Cole ML, McClelland J, Hauxwell J, Cebrian J, Joye SB (2000) Role of salt marshes as part of coastal landscapes. In: Weinstein MP, Kreeger DA (eds) Concepts and controversies in tidal marsh ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 23–38Google Scholar
  76. van Duyl FC, Kop AJ (1994) Bacterial production in North Sea sediments: clues to seasonal and spatial variations. Mar Biol 120:323–337CrossRefGoogle Scholar
  77. Van Raalte CD, Valiela I, Carpenter EJ, Teal JM (1974) Inhibition of nitrogen fixation in salt marshes measured by acetylene reduction. Estuar Coast Mar Sci 2:301–305CrossRefGoogle Scholar
  78. van Wijnen HJ, Bakker JP (1999) Nitrogen and phosphorus limitation in a coastal barrier salt marsh: the implications for vegetation succession. J Ecol 87:265–272CrossRefGoogle Scholar
  79. White DS, Howes BL (1994) Long term 15N-nitrogen retention in the vegetated sediments of a New England salt marsh. Limnol Oceanogr 39:1878–1892CrossRefGoogle Scholar
  80. Whitney DM, Chalmers AG, Haines EB, Hanson RB, Pomeroy LR, Sherr B (1981) The cycles of nitrogen and phosphorus. In: Pomeroy LR, Wiegert RG (eds) The ecology of a salt marsh. Springer, Berlin Heidelberg New York, NY, USA, pp 163–181Google Scholar
  81. Wigand C, Stevenson JC, JC Stevenson (1997) Effects of different submersed macrophytes on sediment biogeochemistry. Aquat Bot 56:233–244CrossRefGoogle Scholar
  82. Wigand C, Thursby GB, McKinney RA, Santos AF (2004a) Response of Spartina patens to dissolved inorganic nutrient additions. J Coastal Res 20 Special Issue 45:134–149Google Scholar
  83. Wigand C, McKinney R, Chintala M, Charpentier M, Groffman P (2004b) Denitrification enzyme activity of fringe salt marshes in New England (USA). J Environ Qual 33:1144–1151Google Scholar
  84. Zelenke-Merrill J (1999) Tidal freshwater marshes as nutrient sinks: particulate nutrient burial and denitrification. Ph.D. Dissertation, University of MarylandGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  • Jane M. Caffrey
    • 1
  • Michael C. Murrell
    • 2
  • Cathleen Wigand
    • 3
  • Richard McKinney
    • 3
  1. 1.Center for Environmental Diagnostics and BioremediationUniversity of West FloridaPensacolaUSA
  2. 2.Office of Research and Development, National Health and Environmental Effects Research Laboratory, Gulf Ecology DivisionUS EPAGulf BreezeUSA
  3. 3.Office of Research and Development, National Health and Environmental Effects Research Laboratory, Atlantic Ecology DivisionUS EPANarragansettUSA

Personalised recommendations