Skip to main content


Log in

Assessing the Resiliency of Salt Marshes Under Increasing Nitrogen Loading

  • Special Issue: Concepts and Controversies in Tidal Marsh Ecology Revisited
  • Published:
Estuaries and Coasts Aims and scope Submit manuscript


Understanding the threat to ecosystems from excess nitrogen in coastal waters is a priority issue in scientific research and natural resource management. Previous field studies have demonstrated that high nitrogen loading can decrease the health and resiliency of salt marshes through shifting biomass allocation, increasing decomposition, and causing creek bank instability, all of which can lead to increased marsh loss with sea-level rise. However, other studies have shown relatively little impact of increasing nitrogen on the structure and function of these systems. Due to the long history of eutrophication in Long Island Sound, aggressive nitrogen reduction strategies have been enacted in this region, but detrimental nutrient inputs persist at variable levels throughout the watershed. Here, the extent of nitrogen-linked salt marsh change under varying levels of nutrient stress was measured, testing the hypothesis that salt marsh resilience (as measured by Spartina alterniflora belowground biomass and marsh edge stability) decreases with increasing nitrogen loading. S. alterniflora growth (stem height, stem density, and biomass) and within-marsh creek area were quantified in 10 salt marshes along a nitrogen-loading gradient. Increasing nitrogen loading showed a significant negative relationship with dead belowground biomass in S. alterniflora; the loss of this belowground biomass in higher nitrogen systems may decrease salt marshes’ ability to keep pace with sea-level rise. Neither shifts in live biomass allocation nor a positive relationship between aboveground biomass or stem height and increasing nitrogen was observed that might promote additional sediment capture, but higher stem density could play a role in promoting sedimentation on the marsh surface in more sediment-rich systems. Aerial photography analysis revealed marsh creek expansion since 1934 at 90% of the marshes studied, but unlike findings from prior experimental enrichment studies, the rate of marsh loss did not increase with increasing nitrogen loading. Given the importance of these ecosystems and the potential of nitrogen to decrease their resiliency, understanding the impacts of eutrophication on salt marshes is critical. However, these results show that the relative importance of nitrogen in driving salt marsh loss in Long Island Sound may be less than studies from other regions have suggested.

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. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others


  • Ammerman, James. 2020. LISS meets its nitrogen reduction target. Accessed May 3.

  • Anisfeld, Shimon C., and Troy D. Hill. 2012. Fertilization effects on elevation change and belowground carbon balance in a Long Island Sound tidal marsh. Estuaries and Coasts 35 (1): 201–211.

    Article  CAS  Google Scholar 

  • Barbier, Edward B., Sally D. Hacker, Chris Kennedy, Evamaria W. Koch, Adrian C. Stier, and Brian R. Silliman. 2011. The value of estuarine and coastal ecosystem services. Ecological Monographs 81 (2): 169–193.

    Article  Google Scholar 

  • Basso, Georgia, Kevin O’Brien, Melissa Albino Hegeman, and Victoria O’Neill. 2015. Status and trends of wetlands in the Long Island Sound Area: 130 year assessment.

  • Bertness Mark, and Steven Pennings. 2002. Spatial variation in process and pattern in salt marsh plant communities in Eastern North America. In , 39–57.

  • Blum, Michael J., K. Jun Bando, M. Katz, and Donald R. Strong. 2007. Geographic structure, genetic diversity and source tracking of Spartina alterniflora. Journal of Biogeography 34. Wiley (10.1111): 2055–2069.

    Article  Google Scholar 

  • Bortolus, Alejandro, Paul Adam, Janine B. Adams, Malika L. Ainouche, Debra Ayres, Mark D. Bertness, Tjeerd J. Bouma, et al. 2019. Supporting Spartina: Interdisciplinary perspective shows Spartina as a distinct solid genus. Ecology 0. Wiley: e02863.

    Article  Google Scholar 

  • Bromberg, Keryn D., and Mark D. Bertness. 2005. Reconstructing New England salt marsh losses using historical maps. Estuaries 28 (6): 823–832.

    Article  Google Scholar 

  • Charles, Heather, and Jeffrey S. Dukes. 2009. Effects of warming and altered precipitation on plant and nutrient dynamics of a New England salt marsh. Ecological Applications 19. Wiley: 1758–1773.

    Article  Google Scholar 

  • Cloern, James E. 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210: 223–253.

    Article  CAS  Google Scholar 

  • Collins, M., R. Knutti, J. Arblaster, J.-L. Dufresne, T. Fichefet, P. Friedlingstein, X. Gao, et al. 2013. Long-term climate change: Projections, commitments and irreversibility. In Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, ed. T.F. Stocker, D. Qin, G.K. Plattner, M. Tignor, S.K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, and P.M. Midgley. Cambridge, United Kingdom and New York, NY, USA: Cambridge University Press.

    Google Scholar 

  • Colombano, D.D., S.Y. Litvin, R.E. Turner, C.A. Currin, J. Cebrián, C.L. Martin, S.B. Alford, et al. 2021. Climate change implications for tidal marshes and food web linkages to estuarine and coastal nekton. Estuaries and Coasts.

  • Crosby, Sarah C., Dov F. Sax, Megan E. Palmer, Harriet S. Booth, Linda A. Deegan, Mark D. Bertness, and Heather M. Leslie. 2016. Salt marsh persistence is threatened by predicted sea-level rise. Estuarine, Coastal and Shelf Science 181. Elsevier Ltd: 93–99.

    Article  Google Scholar 

  • Crosby, Sarah C., Angus Angermeyer, Jennifer M. Adler, Mark D. Bertness, Linda A. Deegan, Nathaniel Sibinga, and Heather M. Leslie. 2017. Spartina alterniflora biomass allocation and temperature: Implications for salt marsh persistence with sea-level rise. Estuaries and Coasts 40 (1): 213–223.

    Article  CAS  Google Scholar 

  • Darby, F.A., and R.E. Turner. 2008. Effects of eutrophication on salt marsh root and rhizome biomass accumulation. Marine Ecology Progress Series 363: 63–70.

    Article  Google Scholar 

  • Deegan, Linda A, David Samuel Johnson, R Scott Warren, Bruce J Peterson, John W Fleeger, Sergio Fagherazzi, and Wilfred M Wollheim. 2012. Coastal eutrophication as a driver of salt marsh loss. Nature 490. Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.: 388.

  • Feagin, Rusty A, M Luisa Martinez, Gabriela Mendoza-Gonzalez, and Robert Costanza. 2010. Salt marsh zonal migration and ecosystem service change in response to global sea level rise. Ecology and Society 15. Resilience Alliance Inc.

  • Fox, John. 2005. The R Commander: A Basic-Statistics Graphical User Interface to R. Journal of Statistical Software 1 (9).

  • Fox, Liza, Ivan Valiela, and Erin L. Kinney. 2012. Vegetation cover and elevation in long-term experimental nutrient-enrichment plots in great Sippewissett Salt Marsh, Cape Cod, Massachusetts: Implications for eutrophication and sea level rise. Estuaries and Coasts 35 (2): 445–458.

    Article  CAS  Google Scholar 

  • Gedan, Keryn B., Matthew L. Kirwan, Eric Wolanski, Edward B. Barbier, and Brian R. Silliman. 2011. The present and future role of coastal wetland vegetation in protecting shorelines: Answering recent challenges to the paradigm. Climatic Change 106 (1): 7–29.

    Article  Google Scholar 

  • Gilby, B., M.P. Weinstein, S.B. Alford, R. Baker, J. Cebrián, A. Chelsky, D.D. Colombano, et al. 2020. Human actions alter tidal marsh seascapes and the provision of ecosystem services. Estuaries and Coasts.

  • Gleason, Mark L., Deborah A. Elmer, Natalie C. Pien, and John S. Fisher. 1979. Effects of stem density upon sediment retention by salt marsh cord grass, Spartina alterniflora loisel. Estuaries 2 (4): 271–273.

    Article  Google Scholar 

  • Greening, Holly S., Lindsay M. Cross, and Edward T. Sherwood. 2011. A multiscale approach to seagrass recovery in Tampa Bay, Florida. Ecological Restoration 29 (1-2): 82–93.

    Article  Google Scholar 

  • Hamilton, Stephen K. 2012. Biogeochemical time lags may delay responses of streams to ecological restoration. Freshwater Biology 57. Wiley: 43–57.

    Article  Google Scholar 

  • Hill, Troy D., and Shimon C. Anisfeld. 2015. Coastal wetland response to sea level rise in Connecticut and New York. Estuarine, Coastal and Shelf Science 163: 185–193.

    Article  CAS  Google Scholar 

  • Horton, Benjamin P., Ian Shennan, Sarah L. Bradley, Niamh Cahill, Matthew Kirwan, Robert E. Kopp, and Timothy A. Shaw. 2018. Predicting marsh vulnerability to sea-level rise using Holocene relative sea-level data. Nature Communications 9 (1): 2687.

    Article  CAS  Google Scholar 

  • Howarth, Robert W., Dennis P. Swaney, Thomas J. Butler, and Roxanne Marino. 2000. Rapid communication: Climatic control on eutrophication of the Hudson River estuary. Ecosystems 3 (2): 210–215.

    Article  Google Scholar 

  • Johnson, David Samuel, R. Scott Warren, Linda A. Deegan, and Thomas J. Mozdzer. 2016. Saltmarsh plant responses to eutrophication. Ecological Applications 26. Wiley: 2649–2661.

    Article  Google Scholar 

  • Jordan, Stephen J., Jonathan Stoffer, and Janet A. Nestlerode. 2011. Wetlands as sinks for reactive nitrogen at continental and global scales: A meta-analysis. Ecosystems 14 (1): 144–155.

    Article  CAS  Google Scholar 

  • Kirwan, Matthew L., and J. Patrick Megonigal. 2013. Tidal wetland stability in the face of human impacts and sea-level rise. Nature 504 (7478): 53–60.

    Article  CAS  Google Scholar 

  • Kirwan, Matthew L., Glenn R. Guntenspergen, Andrea D’Alpaos, James T. Morris, Simon M. Mudd, and Stijn Temmerman. 2010. Limits on the adaptability of coastal marshes to rising sea level. Geophysical Research Letters 37 (23) Wiley.

  • Kirwan, Matthew L., Stijn Temmerman, Emily E. Skeehan, Glenn R. Guntenspergen, and Sergio Fagherazzi. 2016. Overestimation of marsh vulnerability to sea level rise. Nature Climate Change 6 (3): 253–260.

    Article  Google Scholar 

  • Lefcheck, Jonathan S., Robert J. Orth, William C. Dennison, David J. Wilcox, Rebecca R. Murphy, Jennifer Keisman, Cassie Gurbisz, et al. 2018. Long-term nutrient reductions lead to the unprecedented recovery of a temperate coastal region. Proceedings of the National Academy of Sciences 115: 3658 LP–3653662.

    Article  CAS  Google Scholar 

  • Levine, Jonathan, Stephen Brewer, and Mark Bertness. 1998. Nutrients, competition and plant zonation in a New England salt marsh. Journal of Ecology 86 (2): 285–292.

    Article  Google Scholar 

  • Lloret, Javier, Arnaldo Marín, and Lázaro Marín-Guirao. 2008. Is coastal lagoon eutrophication likely to be aggravated by global climate change? Estuarine, Coastal and Shelf Science 78 (2): 403–412.

    Article  Google Scholar 

  • Long Island Sound Study. 2020a. LISS ecosystem targets and supporting indicators: Sea level trends. rates of sea-level,about 6.5 inches per century. Accessed Jun 11.

  • Long Island Sound Study. 2020b. LISS ecosystem targets and supporting indicators: Nitrogen loading. Accessed Feb 21.

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

    Article  Google Scholar 

  • Morris, James T., P.V. Sundareshwar, Christopher T. Nietch, Björn Kjerfve, and D.R. Cahoon. 2002. Responses of coastal wetlands to rising sea level. Ecology 83. Wiley: 2869–2877.[2869:ROCWTR]2.0.CO;2.

    Article  Google Scholar 

  • New York State Department of Environmental Conservation, and Connecticut Department of Environmental Protection. 2000. A total maximum daily load analysis to achieve water quality standards for dissolved oxygen in Long Island Sound.

  • Peteet, Dorothy M., Jonathan Nichols, Timothy Kenna, Clara Chang, James Browne, Mohammad Reza, Stephen Kovari, Louisa Liberman, and Stephanie Stern-Protz. 2018. Sediment starvation destroys New York City marshes’ resistance to sea level rise. Proceedings of the National Academy of Sciences 115: 10281 LP–10210286.

    Article  CAS  Google Scholar 

  • R Core Team. 2020. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

  • Rabalais, Nancy N., R. Eugene Turner, Robert J. Díaz, and Dubravko Justić. 2009. Global change and eutrophication of coastal waters. ICES Journal of Marine Science 66 (7): 1528–1537.

    Article  Google Scholar 

  • Rabalais, Nancy N., R.J. Díaz, L.A. Levin, R.E. Turner, D. Gilbert, and J. Zhang. 2010. Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences 7. Copernicus Publications: 585–619.

    Article  CAS  Google Scholar 

  • RStudio Team. 2015. RStudio: Integrated development for R. Boston: RStudio, Inc.

  • Save the Sound. 2019. 2019 unified water study data: Unified water study tier I water quality results.

  • Sherwood, Edward T., Holly S. Greening, Anthony J. Janicki, and David J. Karlen. 2016. Tampa Bay estuary: Monitoring long-term recovery through regional partnerships. Regional Studies in Marine Science 4: 1–11.

    Article  Google Scholar 

  • Silliman, Brian R, Qiang He, Christine Angelini, Carter S Smith, Matthew L Kirwan, Pedro Daleo, Julianna J Renzi, et al. 2019. Field experiments and meta-analysis reveal wetland vegetation as a crucial element in the coastal protection paradigm. Current Biology 29: 1800–1806.e3.

  • Smith, Val H. 2003. Eutrophication of freshwater and coastal marine ecosystems a global problem. Environmental Science and Pollution Research 10 (2): 126–139.

    Article  CAS  Google Scholar 

  • Smith, Val H., and David W. Schindler. 2009. Eutrophication science: Where do we go from here? Trends in Ecology & Evolution 24 (4): 201–207.

    Article  Google Scholar 

  • Turner, R. Eugene, Brian L. Howes, John M. Teal, Charles S. Milan, Erick M. Swenson, and Dale D. Goehringer-Tonerb. 2009. Salt marshes and eutrophication: An unsustainable outcome. Limnology and Oceanography 54. Wiley: 1634–1642.

    Article  CAS  Google Scholar 

  • Valiela, Ivan, John M. Teal, and Warren J. Sass. 1975. Production and dynamics of salt marsh vegetation and the effects of experimental treatment with sewage sludge. Biomass, production and speies composition. Journal of Applied Ecology 12. [British Ecological Society, Wiley]: 973–981.

    Article  CAS  Google Scholar 

  • Valiela, Ivan, John M. Teal, and Norma Y. Persson. 1976. Production and dynamics of experimentally enriched salt marsh vegetation: Belowground biomass. Limnology and Oceanography 21. Wiley: 245–252.

    Article  Google Scholar 

  • Van Meter, K.J., and N.B. Basu. 2017. Time lags in watershed-scale nutrient transport: An exploration of dominant controls. Environmental Research Letters 12. IOP Publishing: 84017.

    Article  CAS  Google Scholar 

  • Vaudrey, J.M.P., James N. Kremer, Brett F. Branco, and Frederick T. Short. 2010. Eelgrass recovery after nutrient enrichment reversal. Aquatic Botany 93 (4): 237–243.

    Article  Google Scholar 

  • Vaudrey, J.M.P., C. Yarish, J.K. Kim, C.H. Pickerell, L. Brousseau, J. Eddings, and M. Sautkulis. 2016. Long Island Sound nitrogen loading model, v. 2017. Groton, CT.

  • Vinent, O.D., E. Herbert, and M.L. Kirwan. 2019. Lower threshold for marsh drowning suggests loss of microtidal marshes regardless of sediment supply. Preprint.

  • Wallace, Ryan B., Hannes Baumann, Jason S. Grear, Robert C. Aller, and Christopher J. Gobler. 2014. Coastal ocean acidification: The other eutrophication problem. Estuarine, Coastal and Shelf Science 148: 1–13.

    Article  CAS  Google Scholar 

  • Watson, E.B., A.J. Oczkowski, C. Wigand, A.R. Hanson, E.W. Davey, S.C. Crosby, R.L. Johnson, and H.M. Andrews. 2014. Nutrient enrichment and precipitation changes do not enhance resiliency of salt marshes to sea level rise in the Northeastern U.S. Climatic Change 125 (3-4): 501–509.

    Article  CAS  Google Scholar 

  • Weston, Nathaniel B. 2014. Declining sediments and rising seas: An unfortunate convergence for tidal wetlands. Estuaries and Coasts 37 (1): 1–23.

    Article  Google Scholar 

  • Wigand, Cathleen, Richard A. McKinney, Michael A. Charpentier, Marnita M. Chintala, and Glen B. Thursby. 2003. Relationships of nitrogen loadings, residential development, and physical characteristics with plant structure in New England salt marshes. Estuaries 26 (6): 1494–1504.

    Article  CAS  Google Scholar 

  • Wigand, Cathleen, Patricia Brennan, Mark Stolt, Matt Holt, and Stephan Ryba. 2009. Soil respiration rates in coastal marshes subject to increasing watershed nitrogen loads in southern New England, USA. Wetlands 29 (3): 952–963.

    Article  Google Scholar 

  • zu Ermgassen, P.S.E., R. Baker, M.W. Beck, K. Dodds, D. Mallick, M.D. Taylor, and R.E. Turner. Ecosystem services: Delivering for salt marshes. Estuaries and Coasts.

Download references


We thank Josh Cooper and Megan Roughan for assistance in the lab and field. We thank Mary Donato as well as two anonymous reviewers for their thoughtful comments on the draft manuscript. We thank Sherwood Island State Park, Darien Land Trust, Norwalk Land Trust, Milford Land Conservation Trust, Farm River State Park, Quinnipiac University, Branford Land Trust, Hammonasset Beach State Park, and Madison Land Conservation Trust for access to the study sites. We thank Connecticut Environmental Conditions Online and the Connecticut State Library for providing the aerial photographs and orthoimagery.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Sarah C. Crosby.

Additional information

Communicated by Carolyn A. Currin

Supplementary Information


(PDF 228 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Crosby, S.C., Spiller, N.C., Healy, D.S. et al. Assessing the Resiliency of Salt Marshes Under Increasing Nitrogen Loading. Estuaries and Coasts 44, 1658–1670 (2021).

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: