Living on the Edge: Increasing Patch Size Enhances the Resilience and Community Development of a Restored Salt Marsh

  • Rachel K. Gittman
  • F. Joel Fodrie
  • Christopher J. Baillie
  • Michelle C. Brodeur
  • Carolyn A. Currin
  • Danielle A. Keller
  • Matthew D. Kenworthy
  • Joseph P. Morton
  • Justin T. Ridge
  • Y. Stacy Zhang
Article

Abstract

Foundation species regulate communities by reducing environmental stress and providing habitat for other species. Successful restoration of biogenic habitats often depends on restoring foundation species at appropriate spatial scales within a suitable range of environmental conditions. An improved understanding of the relationship between restoration scale and environmental conditions has the potential to improve restoration outcomes for many biogenic habitats. Here, we identified and tested whether inundation/exposure stress and spatial scale (patch size) can interactively determine (1) survival and growth of a foundation species, Spartina alterniflora and (2) recruitment of supported fauna. We planted S. alterniflora and artificial mimics in large and small patches at elevations above and below local mean sea level (LMSL) and monitored plant survivorship and production, as well as faunal recruitment. In the first growing season, S. alterniflora plant survivorship and stem densities were greater above LMSL than below LMSL regardless of patch size, while stem height was greatest in small patches below LMSL. By the third growing season, S. alterniflora patch expansion was greater above LMSL than below LMSL, while stem densities were higher in large patches than small patches, regardless of location relative to LMSL. Unlike S. alterniflora, which was more productive above LMSL, sessile marine biota recruitment to mimic plants was higher in patches below LMSL than above LMSL. Our results highlight an ecological tradeoff at ~LMSL between foundation species restoration and faunal recruitment. Increasing patch size as inundation increases may offset this tradeoff and enhance resilience of restored marshes to sea-level rise.

Keywords

Biogenic habitat Exposure Foundation species Recruitment Spartina alterniflora 

Supplementary material

12237_2017_302_MOESM1_ESM.docx (114 kb)
ESM 1(DOCX 113 kb)

References

  1. Adams, D.A. 1963. Factors influencing vascular plant zonation in North Carolina salt marshes. Ecology 44: 445–456.CrossRefGoogle Scholar
  2. Altieri, A., and J.D. Witman. 2006. Local extinction of a foundation species in a hypoxic estuary: integrating individuals to ecosystem. Ecology 87: 717–730.CrossRefGoogle Scholar
  3. Angelini, C., and B.R. Silliman. 2012. Patch size-dependent community recovery after massive disturbance. Ecology 93: 101–110.CrossRefGoogle Scholar
  4. Bertness, M.D., and E. Grosholz. 1985. Population dynamics of the ribbed mussel, Geukensia demissa: the costs and benefits of an aggregated distribution. Oecologia 67: 192–204.CrossRefGoogle Scholar
  5. Broome, S.W., E.D. Seneca, and W.W. Woodhouse. 1983. The effects of source, rate and placement of nitrogen and phosphorus fertilizers on growth of Spartina alterniflora transplants in North Carolina. Estuaries 6: 212–226.CrossRefGoogle Scholar
  6. Broome, S.W., E.D. Seneca, and W.W. Woodhouse Jr. 1988. Tidal salt marsh restoration. Aquatic Botany 32: 1–22.CrossRefGoogle Scholar
  7. Bruno, J.F. 2000. Facilitation of cobble beach plant communities through habitat modification by Spartina alterniflora. Ecology 8: 1179–1192.CrossRefGoogle Scholar
  8. Bruno, J.F., J.J. Stachowicz, and M.D. Bertness. 2003. Inclusion of facilitation into ecological theory. Trends in Ecology & Evolution 18: 119–125.CrossRefGoogle Scholar
  9. Coiffait-Gombault, C., E. Buisson, and T. Dutoit. 2012. Using a two-phase sowing approach in restoration: sowing foundation species to restore, and subordinate species to evaluate restoration success. Applied Vegetation Science 15: 277–289.CrossRefGoogle Scholar
  10. Craft, C., J. Reader, J.N. Sacco, and S.W. Broome. 1999. Twenty-five years of ecosystem development of constructed Spartina alterniflora (Loisel) marshes. Ecological Applications 9: 1405–1419.CrossRefGoogle Scholar
  11. Craft, C., J. Clough, J. Ehman, S. Joye, R. Park, S. Pennings, H. Guo, and M. Machmuller. 2009. Forecasting the effects of accelerated sea-level rise on tidal marsh ecosystem services. Frontiers in Ecology and the Environment 7: 73–78.CrossRefGoogle Scholar
  12. Currin, C., S. Newell, and H. Paerl. 1995. The role of standing dead Spartina alterniflora and benthic microalgae in salt marsh food webs: considerations based on multiple stable isotope analysis. Marine Ecology Progress Series 121: 99–116.CrossRefGoogle Scholar
  13. Currin, Carolyn A., Priscilla C. Delano, and Lexia M. Valdes-Weaver. 2008. Utilization of a citizen monitoring protocol to assess the structure and function of natural and stabilized fringing salt marshes in North Carolina. Wetlands Ecology and Management 16(2): 97–118.Google Scholar
  14. Dayton, P.K. 1972. Toward an understanding of community resilience and the potential effects of enrichment to the benthos of McMurdo Sound, Antarctica. In Proceedings of the colloquium on conservation problems in Antarctica, ed. B.C. Parker, 81–96. Lawrence: Allen Press.Google Scholar
  15. Davis, J.L., C.A. Currin, C. O’Brien, C. Raffenburg, and A. Davis. 2015. Living shorelines: coastal resilience with a blue carbon benefit. PloS One 10: e0142595.CrossRefGoogle Scholar
  16. Ellison, A., M. Bank, B. Clinton, E. Colburn, K. Elliott, C. Ford, D. Foster, B. Kloeppel, J. Knoepp, G. Lovett, J. Mohan, D. Orwig, N. Rodenhouse, W. Sobczak, K. Stinson, J. Stone, C. Swan, J. Thompson, B. von Holle, and J. Webster. 2005. Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment 3: 479–486.CrossRefGoogle Scholar
  17. Ellison, A. M., and E. J. Farnsworth. 2001. Mangrove Communities. In: Marine Community Ecology, 1st edn. pp 423–442.Google Scholar
  18. Fodrie, F.J., A.B. Rodriguez, C.J. Baillie, M.C. Brodeur, S.E. Coleman, R.K. Gittman, M.D. Kenworthy, A.K. Poray, J.T. Ridge, E.J. Theuerkauf, and N.L. Lindquist. 2014. Classic paradigms in a novel environment: inserting food web and productivity lessons from rocky shores and saltmarshes into biogenic reef restoration. Journal of Applied Ecology 51: 1314–1325.CrossRefGoogle Scholar
  19. Gedan, K.B., L. Kellogg, and D.L. Breitburg. 2014. Accounting for multiple foundation species in oyster reef restoration benefits. Restoration Ecology 22: 517–524.CrossRefGoogle Scholar
  20. Gittman, R.K., and D.A. Keller. 2013. Fiddler crabs facilitate Spartina alterniflora growth, mitigating periwinkle overgrazing of marsh habitat. Ecology 94: 2709–2718.CrossRefGoogle Scholar
  21. Gittman, R.K., A.M. Popowich, J.F. Bruno, and C.H. Peterson. 2014. Marshes with and without sills protect estuarine shorelines from erosion better than bulkheads during a category 1 hurricane. Ocean & Coastal Management 102: 94–102.CrossRefGoogle Scholar
  22. Gittman, R.K., C.H. Peterson, C.A. Currin, F. Joel Fodrie, M.F. Piehler, and J.F. Bruno. 2016. Living shorelines can enhance the nursery role of threatened estuarine habitats. Ecological Applications 26: 249–263.CrossRefGoogle Scholar
  23. Halpern, B.S., B.R. Silliman, and J.D. Olden. 2007. Incorporating positive interactions in aquatic restoration and conservation. Frontiers in Ecology and Environment 5: 153–160.CrossRefGoogle Scholar
  24. Hansen, M.C., P.V. Potapov, R. Moore, M. Hancher, S.A. Turubanova, A. Tyukavina, D. Thau, S.V. Stehman, S.J. Goetz, T.R. Loveland, A. Kommareddy, A. Egorov, L. Chini, C.O. Justice, and J.R.G. Townshend. 2013. High-resolution global maps of 21st-century forest cover change. Science 342: 850–853.CrossRefGoogle Scholar
  25. Hewitt, J.E., S.F. Thrush, J. Halliday, and C. Duffy. 2008. The importance of small-scale habitat structure for maintaining beta diversity. Ecology 86: 1619–1626.CrossRefGoogle Scholar
  26. Hilderbrand, R.H., A.C. Watts, and A.M. Randle. 2005. The myths of restoration ecology. Ecology and Society 10: 19.CrossRefGoogle Scholar
  27. Holmgren, M., and M. Scheffer. 2010. Strong facilitation in mild environments: the stress gradient hypothesis revisited. Journal of Ecology 98: 1269–1275.CrossRefGoogle Scholar
  28. Hovel, K.A., and R.N. Lipcius. 2001. Habitat fragmentation in a seagrass landscape: patch size and complexity control blue crab survival. Ecology 82: 1814–1829.CrossRefGoogle Scholar
  29. Hughes, A.R., S.L. Williams, C.M. Duarte, K.L. Heck Jr., and M. Waycott. 2009. Associations of concern: declining seagrasses and threatened dependent species. Frontiers in Ecology and the Environment 7: 242–246.CrossRefGoogle Scholar
  30. Jones, R.C. 1980. Productivity of algal epiphytes in a Georgia salt marsh: effect of inundation frequency and implications for total marsh productivity. Estuaries 3: 315.CrossRefGoogle Scholar
  31. Kemp, A.C., B.P. Horton, J.P. Donnelly, M.E. Mann, M. Vermeer, and S. Rahmstorf. 2011. Climate related sea-level variations over the past two millennia. Proceedings of the National Academy of Sciences 108: 11017e11022.CrossRefGoogle Scholar
  32. Kennish, M. 2001. Coastal salt marsh systems in the US: a review of anthropogenic impacts. Journal of Coastal Research 17: 731–748.Google Scholar
  33. 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.Google Scholar
  34. Kneib, R.T. 1997. The role of tidal marshes in the ecology of estuarine nekton. Oceanography and Marine Biology 35: 163–220.Google Scholar
  35. Kneib, R. T. 2000. Salt marsh ecoscapes and production transfers by estuarine nekton in the Southeastern United States. In Concepts and controversies in tidal marsh ecology, ed. Daniel A. Kreeger, 267–291. Dordrecht: Kluwer Academic Publishers.Google Scholar
  36. Kremen, C., and L.K. M'Gonigle. 2015. Small-scale restoration in intensive agricultural landscapes supports more specialized and less mobile pollinator species. Journal of Applied Ecology 52: 602–610.CrossRefGoogle Scholar
  37. Lamb, D. 1998. Large-scale ecological restoration of degraded tropical forest lands: the potential role of timber plantations. Restoration Ecology 6: 271–279.CrossRefGoogle Scholar
  38. Levin, L.A., D. Talley, and G. Thayer. 1996. Succession of macrobenthos in a created salt marsh. Marine Ecology Progress Series 141: 67–82.CrossRefGoogle Scholar
  39. Lewis, D.B., and L.A. Eby. 2002. Spatially heterogeneous refugia and predation risk in intertidal salt marshes. Oikos 96: 119–129.CrossRefGoogle Scholar
  40. Lirman, D. 1999. Reef fish communities associated with Acropora palmata: relationships to benthic attributes. Bulletin of Marine Science 65: 235–252.Google Scholar
  41. Manning, A.D., D.B. Lindenmayer, and J. Fischer. 2006. Stretch goals and backcasting: approaches for overcoming barriers to large-scale ecological restoration. Restoration Ecology 14: 487–492.CrossRefGoogle Scholar
  42. Marinucci, A.C. 1982. Trophic importance of Spartina alterniflora production and decomposition to the marsh-estuarine ecosystem. Biological Conservation 22: 35–58.CrossRefGoogle Scholar
  43. McDougall, K.D. 1943. Sessile marine invertebrates of Beaufort, North Carolina: a study of settlement, growth, and seasonal fluctuations among pile-dwelling organisms. Ecological Monographs 13: 321.CrossRefGoogle Scholar
  44. Mendelssohn, I.A., and E.D. Seneca. 1980. The influence of soil drainage on the growth of salt marsh cordgrass Spartina alterniflora in North Carolina. Estuarine and Coastal Marine Science 11: 27–40.CrossRefGoogle Scholar
  45. Minello, T.J., K.W. Able, M.P. Weinstein, and C. Hays. 2003. Salt marshes as nurseries for nekton: testing hypotheses on density, growth and survival through meta-analysis. Marine Ecology Progress Series 246: 39–59.CrossRefGoogle Scholar
  46. Möller, I., M. Kudella, F. Rupprecht, T. Spencer, M. Paul, B.K. van Wesenbeeck, G. Wolters, K. Jensen, T.J. Bouma, M. Miranda-Lange, and S. Schimmels. 2014. Wave attenuation over coastal salt marshes under storm surge conditions. Nature Geoscience 7: 727–731.CrossRefGoogle Scholar
  47. Morris, J.T., and B. Haskin. 1990. A 5-yr record of aerial primary production and stand characteristics of Spartina alterniflora. Ecology 71: 2209–2217.CrossRefGoogle Scholar
  48. Morris, J., P. Sundareshwar, C. Nietch, B. Kjerfve, and D. Cahoon. 2002. Responses of coastal wetlands to rising sea level. Ecology 83: 2869–2877.CrossRefGoogle Scholar
  49. National Oceanographic and Atmospheric Administration (NOAA). 2011–2014. Cape Lookout, NC, Station CLKN7.Google Scholar
  50. NOAA. 2013. Wave Exposure Model (WEMo). Version 3.1. https://products.coastalscience.noaa.gov/wemo/download.aspx
  51. NOAA. 2015a. Tides and currents http://tidesandcurrents.noaa.gov.
  52. NOAA. 2015b. VDATUM v3.4. http://vdatum.noaa.gov.
  53. Parsons, T.R., Y. Maita, and C.M. Lalli. 1984. A manual of chemical and biological methods for seawater analysis. New York: Pergamon Press.Google Scholar
  54. Pastorok, R.A., A. MacDonald, J.R. Sampson, P. Wilber, D.J. Yozzo, and J.P. Titre. 1997. An ecological decision framework for environmental restoration projects. Ecological Engineering 9: 89–107.CrossRefGoogle Scholar
  55. Pennings, S.C., and R.M. Callaway. 1992. Salt marsh plant zonation: the relative importance of competition and physical factors. Ecology 73: 681–690.CrossRefGoogle Scholar
  56. Pennings, S.C., B. Grant, and M.D. Bertness. 2005. Plant zonation in low-latitude salt marshes: disentangling the roles of flooding, salinity and competition. Journal of Ecology 93: 159–167.CrossRefGoogle Scholar
  57. Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar, and R Core Team. 2015. nlme: linear and nonlinear mixed effects models. R package version 3.1–120.Google Scholar
  58. Prach, K., and R.J. Hobbs. 2008. Spontaneous succession versus technical reclamation in the restoration of disturbed sites. Restoration Ecology 16: 363–366.CrossRefGoogle Scholar
  59. Prevéy, J.S., M.J. Germino, and N.J. Huntly. 2010. Loss of foundation species increases population growth of exotic forbs in sagebrush steppe. Ecological Applications 20: 1890–1902.CrossRefGoogle Scholar
  60. R Core Development Team. 2015. R 3. R version 3.2.1. The R Foundation for Statistical Computing Platform.Google Scholar
  61. Redfield, A.C. 1972. Development of a new England salt marsh. Ecological Monographs: 201–237.Google Scholar
  62. Ridge, J.T., A.B. Rodriguez, F.J. Fodrie, N.L. Lindquist, M.C. Brodeur, S.E. Coleman, J.H. Grabowski, and E.J. Theuerkauf. 2015. Maximizing oyster-reef growth supports green infrastructure with accelerating sea-level rise. Scientific Reports 5: 1–8.CrossRefGoogle Scholar
  63. Rodriguez, A.B., F.J. Fodrie, J.T. Ridge, N.L. Lindquist, E.J. Theuerkauf, S.E. Coleman, J.H. Grabowski, M.C. Brodeur, R.K. Gittman, D.A. Keller, and M.D. Kenworthy. 2014. Oyster reefs can outpace sea-level rise. Nature Climate Change 4: 493–497.CrossRefGoogle Scholar
  64. Rogers, Kerrylee, Neil Saintilan, and Craig Copeland. 2012. Modelling wetland surface elevation dynamics and its application to forecasting the effects of sea-level rise on estuarine wetlands. Ecological Modelling 244: 148–157.Google Scholar
  65. Roth, B.M., K.A. Rose, and L.P. Rozas. 2008. Relative influence of habitat fragmentation and inundation on brown shrimp Farfantepenaeus aztecus production in northern Gulf of Mexico salt marshes. Marine Ecology 359: 185–202.CrossRefGoogle Scholar
  66. Scheffer, M., J. Bascompte, W.A. Brock, V. Brovkin, S.R. Carpenter, V. Dakos, H. Held, E.H. van Nes, M. Rietkerk, and G. Sugihara. 2009. Early-warning signals for critical transitions. Nature 461: 53–59.CrossRefGoogle Scholar
  67. Schile, Lisa M., John C. Callaway, James T. Morris, Diana Stralberg, V. Thomas Parker, Maggi Kelly, and Just Cebrian. 2014. Modeling Tidal Marsh Distribution with Sea-Level Rise: Evaluating the Role of Vegetation, Sediment, and Upland Habitat in Marsh Resiliency. PLoS ONE 9(2): e88760.Google Scholar
  68. Silliman, B. R., E. Schrack, Q. He, R. Cope, A. Santoni, T. van der Heide, R. Jacobi, M. Jacobi, and J. van de Koppel. 2015. Facilitation shifts paradigms and can amplify coastal restoration efforts. Proceedings of the National Academy of Sciences of the United States of America: 1–6.Google Scholar
  69. Stiven, A.E., and S.A. Gardner. 1992. Population processes in the ribbed mussel Geukensia demissa (Dillwyn) in a North Carolina salt marsh tidal gradient: spatial pattern, predation, growth and mortality. Journal of Experimental Marine Biology and Ecology 160: 81–102.CrossRefGoogle Scholar
  70. Suding, K.N. 2011. Toward an era of restoration in ecology: successes, failures, and opportunities ahead. Annual Review of Ecology 42: 465–487.CrossRefGoogle Scholar
  71. Suding, K.N., and R.J. Hobbs. 2009. Threshold models in restoration and conservation: a developing framework. Trends in Ecology and Evolution 24: 271–279.CrossRefGoogle Scholar
  72. Sueiro, M.C., A. Bortolus, and E. Schwindt. 2011. Habitat complexity and community composition: relationships between different ecosystem engineers and the associated macroinvertebrate assemblages. Helgoland Marine Research 65: 467–477.CrossRefGoogle Scholar
  73. Teal, J.M. 1962. Energy flow in the salt marsh ecosystem of Georgia. Ecology 43: 614–624.CrossRefGoogle Scholar
  74. Theuerkauf, E.J., J.D. Stephens, J.T. Ridge, F.J. Fodrie, and A.B. Rodriguez. 2015. Carbon export from fringing saltmarsh shoreline erosion overwhelms carbon storage across a critical width threshold. Estuarine, Coastal and Shelf Science 164: 367–378.CrossRefGoogle Scholar
  75. Vaughn, C.C., and F.M. Fisher. 1988. Vertical migration as a refuge from predation in intertidal marsh snails: a field test. Journal of Experimental Marine Biology and Ecology 123: 163–176.CrossRefGoogle Scholar
  76. Waycott, M., C.M. Duarte, T.J.B. Carruthers, R.J. Orth, W.C. Dennison, S. Olyarnik, A. Calladine, J.W. Fourqurean, K.L. Heck Jr., A.R. Hughes, G.A. Kendrick, W.J. Kenworthy, F.T. Short, and S.L. Williams. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences of the United States of America 106: 12377–12381.CrossRefGoogle Scholar
  77. Wilson, E.O. 1992. The diversity of life. New York: Norton.Google Scholar
  78. Zedler, Joy B. 2000. Progress in wetland restoration ecology. Trends in Ecology & Evolution 15(10): 402–407.Google Scholar
  79. Zu Ermgassen, P.S.E., M.D. Spalding, B. Blake, L.D. Coen, B. Dumbauld, S. Geiger, J.H. Grabowski, R. Grizzle, M. Luckenbach, K. McGraw, W. Rodney, J.L. Ruesink, S.P. Powers, and R. Brumbaugh. 2012. Historical ecology with real numbers: past and present extent and biomass of an imperilled estuarine habitat. Proceedings of the Royal Society of London B: Biological Sciences 279: 3393–3400.CrossRefGoogle Scholar
  80. Zuur, A.F., E.N. Ieno, N. Walker, A.A. Saveliev, and G.M. Smith. 2009. Mixed effects models and extensions in ecology with R. New York, NY: Springer New York.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2017

Authors and Affiliations

  • Rachel K. Gittman
    • 1
  • F. Joel Fodrie
    • 2
  • Christopher J. Baillie
    • 1
  • Michelle C. Brodeur
    • 2
  • Carolyn A. Currin
    • 3
  • Danielle A. Keller
    • 2
  • Matthew D. Kenworthy
    • 2
  • Joseph P. Morton
    • 4
  • Justin T. Ridge
    • 4
  • Y. Stacy Zhang
    • 4
  1. 1.Marine Science CenterNortheastern UniversityNahantUSA
  2. 2.University of North Carolina at Chapel Hill Institute of Marine SciencesMorehead CityUSA
  3. 3.Center for Coastal Fisheries and Habitat Research, National Oceanographic and Atmospheric AdministrationBeaufortUSA
  4. 4.Division of Marine Science and Conservation, Nicholas School of the EnvironmentDuke UniversityBeaufortUSA

Personalised recommendations