Skip to main content

Marsh Plants Enhance Coastal Marsh Resilience by Changing Sediment Oxygen and Sulfide Concentrations in an Urban, Eutrophic Estuary

Abstract

Despite considerable efforts to restore coastal wetlands, the ecological mechanisms contributing to the success or failure of restoration are rarely assessed. Accumulation of hydrogen sulfide in sediments may accelerate rates of marsh loss in eutrophic estuaries and is likely driven by complex feedbacks between wetland plant growth and microbial redox reactions. We used a chronosequence of restored marshes in urbanized and eutrophic Jamaica Bay (New York City, USA) to assess how sediment redox conditions change among seasons and over the lifetime of restored marshes. We also compared a stable extant marsh to one that has deteriorated over the past 50 years. We collected seasonal sediment cores from each marsh, and used a motorized microprofiling system to measure the vertical distribution of oxygen and sulfide. We fit a logistic function to each profile to estimate (1) maximum concentrations, (2) rates of increase/decline, and (3) depths of maximum increase/decline. We quantified sediment density, porosity, organic content, and belowground plant biomass, and estimated differences in daily tidal inundation among sites using water-level loggers. We found that minimum oxygen and maximum sulfide concentrations occur during summer. Sulfide concentrations were highest in sites that experienced the longest daily tidal inundation, including the degraded extant marsh and the oldest restored marsh. Spatial patterns in oxygen and sulfide were related to belowground plant biomass, supporting our hypothesis that root growth increases sediment oxygen and partially alleviates sulfide stress. Our data support the growing body of evidence that belowground plant growth may enhance the resilience of marshes to sea-level rise by increasing marsh elevation and facilitating oxygen diffusion into marsh sediments.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Alldred, M., A. Liberti, and S.B. Baines. 2016. Impacts of nutrients and salinity on salt marsh stability. Ecosphere 8: e02010.

    Article  Google Scholar 

  • Alldred, M., J.J. Borrelli, T. Hoellein, et al. 2019. Sediment oxygen and sulfide microprofiles in extant and restored marshes of Jamaica Bay (New York, NY, USA). figshare. Dataset. https://doi.org/10.6084/m9.figshare.9175157.v2.

  • Anisfeld, S.C., T.D. Hill, and D.R. Cahoon. 2016. Elevation dynamics in a restored versus a submerging salt marsh in Long Island Sound. Estuarine, Coastal and Shelf Science 170: 145–154.

    Article  Google Scholar 

  • Arenovski, A.L., and B.L. Howes. 1992. Lacunal allocation and gas transport capacity in the salt marsh grass Spartina alterniflora. Oecologia 90 (3): 316–322.

    CAS  Article  Google Scholar 

  • Ashton, A.D., J.P. Donnelly, and R.L. Evans. 2008. A discussion of the potential impacts of climate change on the shorelines of the Northeastern USA. Mitigation and Adaptation Strategies for Global Change 13: 719–743.

    Article  Google Scholar 

  • Bradley, P.M., and J.T. Morris. 1990. Influence of oxygen and sulfide concentration on nitrogen uptake kinetics in Spartina alterniflora. Ecology 71: 282–287.

    CAS  Article  Google Scholar 

  • Bricker-Urso, S., S.W. Nixon, J.K. Cochran, et al. 1989. Accretion rates and sediment accumulation in Rhode Island salt marshes. Estuaries 12: 300–317.

    CAS  Article  Google Scholar 

  • Brin, L.D., I. Valiela, D. Goehringer, and B. Howes. 2010. Nitrogen interception and export by experimental salt marsh plots exposed to chronic nutrient addition. Marine Ecology Progress Series 400: 3–17.

    CAS  Article  Google Scholar 

  • Cahoon, D.R., J.C. Lynch, C.T. Roman, et al. 2019. Evaluating the relationship among wetland vertical development, elevation capital, sea-level rise, and tidal marsh sustainability. Estuaries and Coasts 42: 1–15.

    CAS  Article  Google Scholar 

  • Carey, J.C., S.B. Moran, R.P. Kelly, et al. 2017. The declining role of organic matter in New England salt marshes. Estuaries and Coasts 40: 626–639.

    CAS  Article  Google Scholar 

  • Chambers, R.M., T.J. Mozdzer, and J.C. Ambrose. 1998. Effects of salinity and sulfide on the distribution of Phragmites australis and Spartina alterniflora in a tidal saltmarsh. Aquatic Botany 62: 161–169.

    CAS  Article  Google Scholar 

  • Darby, F.A., and R.E. Turner. 2008. Below- and aboveground biomass of Spartina alterniflora: Response to nutrient addition in a Louisiana salt marsh. Estuaries and Coasts 31: 326–334.

    CAS  Article  Google Scholar 

  • Davey, E., C. Wigand, R. Johnson, et al. 2011. Use of computed tomography imaging for quantifying coarse roots, rhizomes, peat, and particle densities in marsh soils. Ecological Applications 21: 2156–2171.

    Article  Google Scholar 

  • Deegan, L.A., D.S. Johnson, R.S. Warren, B.J. Peterson, J.W. Fleeger, S. Fagherazzi, and W.M. Wollheim. 2012. Coastal eutrophication as a driver of salt marsh loss. Nature 490 (7420): 388–392.

    CAS  Article  Google Scholar 

  • DeLaune, R.D., and S.R. Pezeshki. 2003. The role of soil organic carbon in maintaining surface elevation in rapidly subsiding U.S. Gulf of Mexico coastal marshes. Water, Air, and Soil Pollution: Focus 3: 167–179.

    CAS  Article  Google Scholar 

  • DeLaune, R.D., S.R. Pezeshki, J.H. Pardue, et al. 1990. Some influences of sediment addition to a deteriorating salt marsh in the Mississippi River Deltaic Plain: A pilot study. Journal of Coastal Research 6: 181–188.

    Google Scholar 

  • Donnelly, J.P. 1998. Evidence of late Holocene post-glacial isostatic adjustment in coastal wetland deposits of eastern North America. Georesearch Forum 3–4: 393–400.

    Google Scholar 

  • Fagherazzi, S., L. Carniello, L. D’Alpaos, and A. Defina. 2006. Critical bifurcation of shallow microtidal landforms in tidal flats and salt marshes. Proceedings of the National Academy of Sciences 103: 8337–8341.

    CAS  Article  Google Scholar 

  • Frame, G.W. 2006. Big egg marsh experimental restoration in Jamaica Bay, New York. In People, places, and parks: Proceedings of the 2005 George Wright Society Conference on Parks, Protected Areas, and Cultural Sites, ed. D. Harmon. Hancock, MI: The George Wright Society.

    Google Scholar 

  • Gedan, K.B., B.R. Silliman, and M.D. Bertness. 2009. Centuries of human-driven change in salt marsh ecosystems. Annual Review of Marine Science 1: 117–141.

    Article  Google Scholar 

  • Gedan, K.B., M.L. Kirwan, E. Wolanski, et al. 2011. The present and future role of coastal wetland vegetation in protecting shorelines: Answering recent challenges to the paradigm. Climatic Change 106: 7–29.

    Article  Google Scholar 

  • Hartig, E.K., V. Gornitz, A. Kolker, et al. 2002. Anthropogenic and climate-change impacts on salt marshes of Jamaica Bay, New York City. Wetlands 22: 71–89.

    Article  Google Scholar 

  • Henry, L., and H. Wickham. 2019. Functional programming tools. RStudio.

  • Howarth, R.W. 1984. The ecological significance of sulfur in the energy dynamics of salt marsh and coastal marine sediments. Biogeochemistry 1: 5–27.

    CAS  Article  Google Scholar 

  • Howes, B.L., and J.M. Teal. 1994. Oxygen loss from Spartina alterniflora and its relationship to salt-marsh oxygen balance. Oecologia 97 (4): 431–438.

    CAS  Article  Google Scholar 

  • Howes, B.L., R.W. Howarth, J.M. Teal, and I. Valiela. 1981. Oxidation-reduction potentials in a salt marsh: Spatial patterns and interactions with primary production. Limnology and Oceanography 26: 350–360.

    Article  Google Scholar 

  • IPCC. 2014. Climate change 2014: Synthesis report. In Core Writing Team, R. K. Pachauri and L. A. Meyer (Eds.), Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (p. 151). Geneva: IPCC.

  • Jeroschewski, P., C. Steuckart, and M. Kühl. 1996. An amperometric microsensor for the determination of H2S in aquatic environments. Analytical Chemistry 68: 4351–4357.

    CAS  Article  Google Scholar 

  • Kingsford, R.T., A. Basset, and L. Jackson. 2016. Wetlands: conservation’s poor cousins. Aquatic Conservation: Marine and Freshwater Ecosystems 26 (5): 892–916.

  • Kirwan, M.L., and G.R. Guntenspergen. 2012. Feedbacks between inundation, root production, and shoot growth in a rapidly submerging brackish marsh. Journal of Ecology 100: 1–7.

    Article  Google Scholar 

  • Koch, M.S., I.A. Mendelssohn, and K.L. McKee. 1990. Mechanism for the hydrogen sulfide-induced growth limitation in wetland macrophytes. Limnology and Oceanography 35: 399–408.

    CAS  Article  Google Scholar 

  • Kolker, A.S. 2005. The impacts of climate variability and anthropogenic activities on salt marsh accretion and loss on Long Island. Ph.D., State University of New York at Stony Brook.

  • Lee, R.W., D.W. Kraus, and J.E. Doeller. 1999. Oxidation of sulfide by Spartina alterniflora roots. Limnology and Oceanography 44: 1155–1159.

    CAS  Article  Google Scholar 

  • Leonard, L.A., and M.E. Luther. 1995. Flow hydrodynamics in tidal marsh canopies. Limnology and Oceanography 40: 1474–1484.

    Article  Google Scholar 

  • Marani, M., A. D’Alpaos, S. Lanzoni, et al. 2010. The importance of being coupled: Stable states and catastrophic shifts in tidal biomorphodynamics. Journal of Geophysical Research 115. https://doi.org/10.1029/2009JF001600.

  • Marani, M., C. Da Lio, and A. D’Alpaos. 2013. Vegetation engineers marsh morphology through multiple competing stable states. Proceedings of the National Academy of Sciences 110: 3259–3263.

    CAS  Article  Google Scholar 

  • Maximiliano-Cordova, C., K. Salgado, M.L. Martínez, et al. 2019. Does the functional richness of plants reduce wave erosion on embryo coastal dunes? Estuaries and Coasts 42: 1730–1741.

    Article  Google Scholar 

  • Messaros, R.C., P.S. Rafferty, and G.S. Woolley. 2010. Challenges and successes of tidal wetlands restoration in Jamaica Bay, New York. Watershed Management 2010, 343–363. Madison: American Society of Civil Engineers.

    Google Scholar 

  • Messaros, R.C., G.S. Woolley, M.J. Morgan, and P.S. Rafferty. 2012. Tidal wetlands restoration. In M. Ali (Ed.), The functioning of ecosystems (pp. 149–170). IntechOpen. https://doi.org/10.5772/35965.

  • Morris, J.T., P.V. Sundareshwar, C.T. Nietch, et al. 2002. Responses of coastal wetlands to rising sea level. Ecology 83: 2869–2877.

    Article  Google Scholar 

  • Morris, J.T., D.C. Barber, J.C. Callaway, R. Chambers, S.C. Hagen, C.S. Hopkinson, B.J. Johnson, P. Megonigal, S.C. Neubauer, T. Troxler, and C. Wigand. 2016. Contributions of organic and inorganic matter to sediment volume and accretion in tidal wetlands at steady state. Earth’s Future 4 (4): 110–121.

    Article  Google Scholar 

  • Morton, R.A., N.A. Buster, and M.D. Krohn. 2002. Subsurface controls on historical subsidence rates and associated wetland loss in southcentral Louisiana. Gulf Coast Association of Geological Societies Transactions 52: 767–778.

    Google Scholar 

  • Morton, R.A., J.C. Bernier, J.A. Barras, and N.F. Ferina. 2005. Historical subsidence and wetland loss in the Mississippi Delta Plain. Gulf Coast Association of Geological Societies Transactions 55: 555–571.

    Google Scholar 

  • Mudd, S.M. 2011. The life and death of salt marshes in response to anthropogenic disturbance of sediment supply. Geology 39: 511–512.

    Article  Google Scholar 

  • Nicholls, R.J., and A. Cazenave. 2010. Sea-level rise and its impact on coastal zones. Science 328 (5985): 1517–1520.

    CAS  Article  Google Scholar 

  • Nieuwenhuize, J., Y.E.M. Maas, and J.J. Middelburg. 1994. Rapid analysis of organic carbon and nitrogen in particulate materials. Marine Chemistry 45: 217–224.

    CAS  Article  Google Scholar 

  • NOAA. 2019. National coastal population report: Population trends from 1970 to 2020. NOAA Office for Coastal Management. https://coast.noaa.gov/digitalcoast/training/population-report.html. Accessed 1 Aug 2018.

  • Nyman, J.A., R.D. DeLaune, S.R. Pezeshki, and W.H. Patrick. 1995. Organic matter fluxes and marsh stability in a rapidly submerging estuarine marsh. Estuaries 18: 207–218.

    Article  Google Scholar 

  • Nyman, J.A., R.J. Walters, R.D. Delaune, and W.H. Patrick Jr. 2006. Marsh vertical accretion via vegetative growth. Estuarine, Coastal and Shelf Science 69: 370–380.

    Article  Google Scholar 

  • Padfield, D., and G. Matheson.  2018. Robust non-linear regression using AIC scores. RStudio.

  • Peteet, D.M., J. Nichols, T. Kenna, et al. 2018. Sediment starvation destroys New York City marshes’ resistance to sea level rise. Proceedings of the National Academy of Sciences 115: 10281.

    CAS  Article  Google Scholar 

  • R Core Team. 2012. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

  • Rafferty, P., J. Castagna, and D. Adamo. 2011. Building partnerships to restore an urban marsh ecosystem at Gateway National Recreation Area. Park Science 27: 34–41.

    Google Scholar 

  • Redfield, A.C. 1972. Development of a New England salt marsh. Ecological Monographs 42: 201–237.

    Article  Google Scholar 

  • Revsbech, N.P. 1989. An oxygen microsensor with a guard cathode. Limnology and Oceanography 34: 474–478.

    CAS  Article  Google Scholar 

  • Roman, C.T., N. Jaworski, F.T. Short, et al. 2000. Estuaries of the Northeastern United States: Habitat and land use signatures. Estuaries 23: 743.

    CAS  Article  Google Scholar 

  • Rooth, J.E., J.C. Stevenson, and J.C. Cornwell. 2003. Increased sediment accretion rates following invasion by Phragmites australis: The role of litter. Estuaries 26: 475–483.

    Article  Google Scholar 

  • Silliman, B.R., Q. He, C. Angelini, 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.

    CAS  Article  Google Scholar 

  • Stagg, C.L., and I.A. Mendelssohn. 2011. Controls on resilience and stability in a sediment-subsidized salt marsh. Ecological Applications 21 (5): 1731–1744.

    Article  Google Scholar 

  • Swanson, L., M. Dorsch, M. Giampieri, et al. 2016. Dynamics of the biophysical systems of Jamaica Bay. In Prospects for resilience: Insights from New York City’s Jamaica Bay, ed. E.W. Sanderson, W.D. Solecki, J.R. Waldman, and A.S. Parris, 65–89. Washington, DC: Island Press/Center for Resource Economics.

    Chapter  Google Scholar 

  • Teal, J.M., and J.W. Kanwisher. 1966. Gas transport in the marsh grass, Spartina alterniflora. Journal of Experimental Botany 17: 355–361.

    CAS  Article  Google Scholar 

  • Törnqvist, T.E., D.J. Wallace, J.E.A. Storms, et al. 2008. Mississippi Delta subsidence primarily caused by compaction of Holocene strata. Nature Geoscience 1: 173–176.

    Article  CAS  Google Scholar 

  • Turner, R.E. 2011. Beneath the salt marsh canopy: Loss of soil strength with increasing nutrient loads. Estuaries and Coasts 34: 1084–1093.

    CAS  Article  Google Scholar 

  • Warren, R.S., and W.A. Niering. 1993. Vegetation change on a northeast tidal marsh - interaction of sea-level rise and marsh accretion. Ecology 74: 96–103.

    Article  Google Scholar 

  • Watson, E.B., C. Wigand, E.W. Davey, H.M. Andrews, J. Bishop, and K.B. Raposa. 2017. Wetland loss patterns and inundation-productivity relationships prognosticate widespread salt marsh loss for Southern New England. Estuaries and Coasts 40 (3): 662–681.

    CAS  Article  Google Scholar 

  • Watson, E.B., E. Powell, N.P. Maher, et al. 2018. Indicators of nutrient pollution in Long Island, New York, estuarine environments. Marine Environmental Research 134: 109–120.

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  • Wickham, H., and Henry L. 2019. Easily tidy data with “spread()” and “gather()” functions. RStudio.

  • Wickham, H., R. François, L. Henry, and K. Müller. 2019. A grammar of data manipulation. R Studio.

  • Wigand, C., P. Brennan, M. Stolt, et al. 2009. Soil respiration rates in coastal marshes subject to increasing watershed nitrogen loads in southern New England, USA. Wetlands 29: 952–963.

    Article  Google Scholar 

  • Wigand, C., C.T. Roman, E. Davey, M. Stolt, R. Johnson, A. Hanson, E.B. Watson, S.B. Moran, D.R. Cahoon, J.C. Lynch, and P. Rafferty. 2014. Below the disappearing marshes of an urban estuary: Historic nitrogen trends and soil structure. Ecological Applications 24 (4): 633–649.

    Article  Google Scholar 

  • Zedler, J.B. 2003. Wetlands at your service: Reducing impacts of agriculture at the watershed scale. Frontiers in Ecology and the Environment 1: 65–72.

    Article  Google Scholar 

  • Zedler, J.B., and S. Kercher. 2005. Wetland resources: Status, trends, ecosystem services, and restorability. Annual Review of Environment and Resources 30: 39–74.

    Article  Google Scholar 

Download references

Acknowledgements

This research was supported by the Hudson River Foundation (Grant 013-15A). We would like to extend special thanks to Patricia Rafferty, Jolene Willis, and George Frame of the National Park Service for site access and information. We thank the editor, as well as Associate Editor R. Scott Warren and two anonymous reviewers for their feedback, which improved the quality of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mary Alldred.

Additional information

Communicated by R Scott Warren

Electronic supplementary material

Online Resource 1

Annotated R code used to fit logistic functions to sediment microprofiles, analyze sediment parameters, and generate figures (PDF 2083 kb)

Online Resource 2

Interactive app available to view all logistic fits to microprofile data (PDF 89 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Alldred, M., Borrelli, J.J., Hoellein, T. et al. Marsh Plants Enhance Coastal Marsh Resilience by Changing Sediment Oxygen and Sulfide Concentrations in an Urban, Eutrophic Estuary. Estuaries and Coasts 43, 801–813 (2020). https://doi.org/10.1007/s12237-020-00700-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-020-00700-9

Keywords

  • Spartina alterniflora
  • Hydrogen sulfide
  • Redox
  • Marsh stability
  • Rhizosphere
  • Restoration