Skip to main content
Log in

Nitrogen fixation and nitrogen limitation of primary production along a natural marsh chronosequence

  • Ecosystems Ecology
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Nitrogen (N) limitation of primary production is common in temperate salt marshes, even though conservative N recycling can fulfill a large proportion of plant N demand. In nutrient poor young marshes, N limitation may be more severe and new N sources, such as N fixation, more important for plant growth. We measured N fixation and the response of salt marsh primary producers (Spartina alterniflora and benthic microalgae) to N fertilization in one mature (>150 year) and two young (7 and 15 year) naturally developing marshes at the Virginia Coast Reserve LTER site. S. alterniflora aboveground biomass in the mature marsh (1,700±273 g m−2) was 1.8 and 2.8 times higher than in the 15 year and 7 year old marshes, respectively. Fertilization significantly increased S. alterniflora biomass in the two young marshes (160–175%) and areal aboveground tissue N in the youngest marsh (260%). Microalgal chlorophyll a (Chl a) in the mature marsh was nearly 2-fold lower than in the 7-year-old marsh, and there was no evidence that this was due to light limitation. However, Chl a in fertilized plots was 30% higher than control plots at the youngest site. Daily N fixation decreased with increasing marsh age in summer, when rates were highest at all sites. Autotrophic N fixation (difference between rates in the light and dark) was most important in the summer, but we saw no indication of a shift in dominance between autotrophic and heterotrophic N fixers during marsh development. Estimated annual N fixation was 2- to 3-fold higher in the young marsh (18.3±1.5 g N m−2 year−1), than in the intermediate-aged (9.0±0.7) or mature marsh (6.1±0.5). In the young marshes, N fixation was sufficient to provide a substantial proportion of aboveground S. alterniflora N demand. Our results suggest that both benthic microalgae and S. alterniflora in young salt marshes are N limited, and that this limitation decreases as the marsh matures. The high rates of N fixation by autotrophic and heterotrophic bacteria in the sediment could provide an important source of N for primary producers during marsh development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2a–e.
Fig. 3.
Fig. 4.

Similar content being viewed by others

References

  • Anderson IC, Tobias CR, Neikirk BB, Wetzel RL (1997) Development of a process-based nitrogen mass balance for a Virginia (USA) salt marsh: implications for net DIN flux. Mar Ecol Prog Ser 159:13–27

    Google Scholar 

  • Aziz S, Nedwell DB (1986) The nitrogen cycle of an East Coast, UK salt marsh. II. Nitrogen fixation, nitrification, denitrification, tidal exchange. Estuar Coast Shelf Sci 22:689–704

    Google Scholar 

  • Bebout B, Paerl H, Crocker K, Prufert L (1987) Diel interactions of oxygenic photosynthesis and N2 fixation (acetylene reduction) in a marine microbial mat community. Appl Environ Microbiol 53:2353–2362

    CAS  Google Scholar 

  • Boyer KE, Zedler JB (1998) Effects of nitrogen additions on the vertical structure of a constructed cordgrass marsh. Ecol Appl 8:692–705

    Google Scholar 

  • Boyer KE, Calloway JC, Zedler JB (2000) Evaluating the progress of restored cordgrass (Spartina foliosa) marshes: belowground biomass and tissue nitrogen. Estuaries 23:711–721

    CAS  Google Scholar 

  • Boyle CD, Patriquin DG (1981) Carbon metabolism of Spartina alterniflora loisel in relation to that of associated nitrogen-fixing bacteria. New Phytol 89:275–283

    CAS  Google Scholar 

  • Bradley PM, Morris JT (1990) Influence of oxygen and sulfide concentration on nitrogen uptake kinetics in Spartina alterniflora. Ecology 71:282–287

    CAS  Google Scholar 

  • Capone DG (1988) In: Blackburn TH, Sorensen J (eds) Benthic nitrogen fixation. Wiley, New York, pp 85–123

  • Carpenter EJ, Van Raalte CD, Valiela I (1978) Nitrogen fixation by algae in a Massachusetts salt marsh. Limnol Oceanogr 23:318–327

    CAS  Google Scholar 

  • Chalmers AG (1979) The effects of fertilization on Nitrogen distribution in a Spartina alterniflora salt marsh. Estuar Coast Mar Sci 8:327–337

    CAS  Google Scholar 

  • Chapin FS III, Walker LR, Fastie CL, Sharman LC (1994) Mechanism of primary succession following deglaciation at Glacier Bay, Alaska. Ecol Monogr 64:149–175

    Google Scholar 

  • Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458

    CAS  Google Scholar 

  • Coles SM (1997) In: Jefferies RL, Davy AJ (eds) Benthic microalgal populations on intertidal sediments and their role as precursors to salt marsh development. Blackwell, Oxford, England, pp 25–42

  • Currin CA, Paerl HW (1998) Epiphytic nitrogen fixation associated with standing dead shoots of smooth cordgrass, Spartina alterniflora. Estuaries 21:108–117

    CAS  Google Scholar 

  • Currin CA, Joye SB, Paerl HW (1996) Diel rates of N2 fixation and denitrification in a transplanted Spartina alterniflora marsh: Implications for N-flux dynamics. Estuar Coast Shelf Sci 42:597–616

    Article  CAS  Google Scholar 

  • Dai T, Wiegert RG (1997) A field study of photosynthetic capacity and its response to nitrogen fertilization in Spartina alterniflora. Estuar Coast Shelf Sci 45:273–283

    Article  Google Scholar 

  • De Souza MP, Yoch DC (1997) Spartina alterniflora dieback recovery correlates with increased acetylene reduction activity in saltmarsh sediments. Estuar Coast Shelf Sci 45:547–555

    Article  Google Scholar 

  • Dicker H, Smith D (1980) Acetylene reduction (nitrogen fixation) in a Delaware, USA salt marsh. Mar Biol 57:241–250

    CAS  Google Scholar 

  • Fitch GM (1991) The role of overwash on Hog Island. M.S. thesis. University of Virginia, Charlottesville, Va.

  • Gallagher JL (1975) Effect of an ammonium pulse on the growth and elemental composition of natural stands of Spartina alternifloraand Juncus roemerianus. Am J Bot 62:644–648

    CAS  Google Scholar 

  • Gallagher JL, Daiber FC (1974) Primary production of edaphic algal communities in a Delaware salt marsh. Limnol Oceanogr 19:390–395

    Google Scholar 

  • Haines E, Chalmers A, Hanson R, Sherr B (1976) In: Wiley M (ed) Nitrogen pools and fluxes in a Georgia salt marsh. Academic Press, New York, pp 241–254

  • Hobbie E, Macko S, Shugart H (1998) Patterns in N dynamics and N isotopes during primary succession in Glacier Bay, Alaska. Chem Geol 152:3–11

    Article  CAS  Google Scholar 

  • Langis R, Zalejko M, Zedler JB (1991) Nitrogen assessments in a constructed and a natural salt marsh of San Diego Bay. Ecol Appl 1:40–51

    Google Scholar 

  • McGlathery KJ, Rysgaard-Petersen N, Christiansen PB (1998) Temporal and spatial variation in nitrogen fixation activity in the eelgrass Zostera marina rhizosphere. Mar Ecol Prog Ser 168:245–258

    CAS  Google Scholar 

  • Mendelssohn IA (1979) The influence of nitrogen level, form, and application method on the growth response of Spartina alterniflora in North Carolina. Estuaries 2:106–112

    Google Scholar 

  • Morris JT, Dacey JWH (1984) Effects of O2 on ammonium uptake and root respiration by Spartina alterniflora. Am J Bot 71:979–985

    CAS  Google Scholar 

  • Odum EP (1969) The strategy of ecosystem development. Science 164:262–270

    CAS  PubMed  Google Scholar 

  • Osgood DT, Zieman JC (1993a) Factors controlling aboveground Spartina alterniflora (smooth cordgrass) tissue element composition and production in different-age barrier island marshes. Estuaries 16:815–826

    CAS  Google Scholar 

  • Osgood DT, Zieman JC (1993b) Spatial and temporal patterns of substrate physico-chemical parameters in different-aged barrier island marshes. Estuar Coast Shelf Sci 37:421–436

    Article  CAS  Google Scholar 

  • Paerl H, Bebout B, Prufert L (1989) In: Cohen Y, Rosenberg E (eds) Naturally occurring patterns of oxygenic photosynthesis and N2 fixation in a marine microbial mat: physiological and ecological ramifications. American Society of Microbiology, Washington, D.C., pp 326–341

  • Patriquin D, Knowles R (1972) Nitrogen fixation in the rhizosphere of marine angiosperms. Mar Biol 16:49–58

    CAS  Google Scholar 

  • Pickett STA (1991) Space-for-time substitution as an alternative to long-term studies. In: Likens GE (ed) Long-term studies in ecology: approaches and alternatives. Springer, Berlin Heidelberg New York, pp 110–135

  • Piehler MF, Currin CA, Cassanova R, Paerl HW (1998) Development and N2-fixing activity of the benthic microbial community in transplanted Spartina alterniflora marshes in North Carolina. Restor Ecol 6:290–296

    Article  Google Scholar 

  • Pinckney JL, Zingmark RG (1993) Modeling the annual production of intertidal benthic microalgae in estuarine ecosystems. J Phycol 29:396–407

    Google Scholar 

  • Pringle CM (1987) Effects of water and substratum nutrient supplies on lotic periphyton growth—an integrated bioassay. Can J Fish Aquat Sci 44:619–629

    CAS  Google Scholar 

  • Rastetter E, Vitousek P, Field C, Shaver G, Herbert D, Agren G (2001) Resource optimization and symbiotic nitrogen fixation. Ecosystems 4:369–388

    CAS  Google Scholar 

  • Redfield AC (1972) Development of a New England salt marsh. Ecol Monogr 42:201–237

    Google Scholar 

  • Sacco JN, Seneca ED, Wentworth TR (1994) Infaunal community development of artificially established salt marshes in North Carolina. Estuaries 17:489–500

    Google Scholar 

  • Silliman BR, Zieman JC (2001) Top-down control of Spartina alterniflora production by periwinkle grazing in a Virginia salt marsh. Ecology 82:2830–2845

    Google Scholar 

  • Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799–801

    CAS  Google Scholar 

  • Stewart JQ (1962) The great Atlantic coast tides of 5–8 March 1962. Weatherwise June 1962:117–120

    Google Scholar 

  • Stewart W, Fitzgerald G, Burris R (1967) In situ studies on N2 fixation using the acetylene reduction technique. Proc Nat Acad Sci USA 58:2071–2078

    CAS  PubMed  Google Scholar 

  • Sullivan MJ, Daiber FC (1974) Response in production of cordgrass, Spartina alterniflora, to inorganic nitrogen and phosphorus fertilizer. Chesape Sci 15:121–123

    Google Scholar 

  • Teal JM, Valiela I, Berlo D (1979) Nitrogen fixation by rhizosphere and free-living bacteria in salt marsh sediments. Limnol Oceanogr 24:126–132

    CAS  Google Scholar 

  • Thompson SP, Paerl HW, Go MC (1995) Seasonal patterns of nitrification and denitrification in a natural and a restored salt marsh. Estuaries 18:399–408

    CAS  Google Scholar 

  • Tyler AC, Zieman JC (1999) Patterns of development in the creekbank region of a barrier island Spartina alterniflora marsh. Mar Ecol Prog Ser 180:161–177

    Google Scholar 

  • Underwood GJC (1997) Microalgal colonization in a saltmarsh restoration scheme. Estuar Coast Shelf Sci 44:471–481

    Article  CAS  Google Scholar 

  • Van Raalte CD, Valiela I, Teal JM (1976) Production of epibenthic salt marsh algae: light and nutrient limitation. Limnol Oceanogr 21:862–872

    Google Scholar 

  • Vitousek PM, Reiners WA (1975) Ecosystem succession and nutrient retention: a hypothesis. BioScience 25:376–381

    CAS  Google Scholar 

  • Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57/58:1–45

    Google Scholar 

  • Walsh JP (1998) Low marsh succession along an over-wash salt marsh chronosequence. Ph.D. dissertation. University of Virginia, Charlottesville, Va.

  • Welsh DT, Bourgues S, Wit RD, Herbert RA (1996) Seasonal variation in rates of heterotrophic nitrogen fixation (acetylene reduction) in Zostera noltii meadows and uncolonised sediments of the Bassin d'Arcachon, south-west France. Hydrobiology 329:161–174

    CAS  Google Scholar 

  • White DS, Howes BL (1994) Long-term 15N-nitrogen retention in the vegetated sediments of a New England salt marsh. Limnol Oceanogr 39:1878–1892

    Google Scholar 

  • Whiting GJ, Gandy EL, Yoch DC (1986) Tight coupling of root-associated nitrogen fixation and plant photosynthesis in the salt marsh grass Spartina alterniflora and carbon dioxide enhancement of nitrogenase activity. Appl Environ Microbiol 52:108–113

    CAS  PubMed  Google Scholar 

  • Wijnholds AE, Young DR (2000) Interdependence of Myrica cerifera seedlings and the nodule forming actinomycete, Frankia, in a coastal environment. J Coast Res 16:139–144

    Google Scholar 

  • Yoch D, Whiting G (1986) Evidence for NH4 + switch-off regulation of nitrogenase activity by bacteria in salt marsh sediments and roots of the grass Spartina alterniflora. Appl Environ Microbiol 51:143–149

    CAS  PubMed  Google Scholar 

  • Zedler JB (2000) Progress in wetland restoration ecology. Trends Ecol Evol 15:402–407

    Article  Google Scholar 

Download references

Acknowledgements

Funding for this work came from The Virginia Coast Reserve LTER Project (National Science Foundation award numbers DEB-9411974), a U.S. Environmental Protection Agency STAR Fellowship to C.T. (U-915532) and an undergraduate research grant from the University of Virginia to T.M. We are grateful to Jimmy Spitler for field assistance, Iris Anderson for the use of her laboratory, and Brian Silliman and Ted Grosholz for their comments on the manuscript. We also thank the anonymous reviewers for their comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anna Christina Tyler.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tyler, A.C., Mastronicola, T.A. & McGlathery, K.J. Nitrogen fixation and nitrogen limitation of primary production along a natural marsh chronosequence. Oecologia 136, 431–438 (2003). https://doi.org/10.1007/s00442-003-1277-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-003-1277-5

Keywords

Navigation