Estuaries and Coasts

, Volume 41, Issue 3, pp 784–799 | Cite as

How Well Do Restored Intertidal Oyster Reefs Support Key Biogeochemical Properties in a Coastal Lagoon?

  • Lisa G. ChambersEmail author
  • Stephanie A. Gaspar
  • Christian J. Pilato
  • Havalend E. Steinmuller
  • Kevin J. McCarthy
  • Paul E. Sacks
  • Linda J. Walters


The restoration of dead/degraded oyster reefs is increasingly pursued worldwide to reestablish harvestable populations or renew ecosystem services. Evidence suggests that oysters can improve water quality, but less is known about the role of associated benthic sediments in promoting biogeochemical processes, such as nutrient cycling and burial. There is also limited understanding of if, or how long postrestoration, a site functions like a natural reef. This study investigated key biogeochemical properties (e.g., physiochemical properties, nutrient pools, microbial community size and activity) in the sediments of dead reefs; 1-, 4-, and 7-year-old restored reefs; and natural reference reefs of the eastern oyster, Crassostrea virginica, in Mosquito Lagoon (FL, USA). Results indicated that most of the measured biogeochemical properties (dissolved organic carbon (C), NH4 +, total C, total nitrogen (N), and the activity of major extracellular enzymes involved in C, N, and phosphorus (P) cycling) increased significantly by 1-year postrestoration, relative to dead reefs, and then remained fairly constant as the reefs continued to age. Few differences were observed in biogeochemical properties between restored reefs of any age (1 to 7 years) and natural reference reefs. Variability among reefs of the same treatment category was often correlated with differences in the number of live oysters, reef thickness, and/or the availability of C and N in the sediments. Overall, this study demonstrates the role of live intertidal oyster reefs as biogeochemical hot spots for nutrient cycling and burial and the rapidity (within 1 year) with which biogeochemical properties can be reestablished following successful restoration.


Crassostrea virginica Shellfish Restoration Biogeochemistry Carbon Nitrogen Phosphorus 



The authors would like to thank Lacie Anderson, Phyllis Klarmann, Meagan Mindalie, Jaice Metherall, John Heiland, and Janet Ho for assistance with field sampling, as well as the cooperation of Canaveral National Seashore and the St. Johns Water Management District in the completion of this study. This work was supported by the Indian River Lagoon National Estuarine Program and the National Science Foundation, under the Coupled Natural-Human Systems program, award #1617374.


  1. Andersen, J.M. 1976. An ignition method for determination of total phosphorus in lake sediments. Water Research 10: 329–331.CrossRefGoogle Scholar
  2. Asmus, R.M., and H. Asmus. 1991. Mussel beds: Limiting or promoting phytoplankton? Journal of Experimental Marine Biology and Ecology 148: 215–232.CrossRefGoogle Scholar
  3. Beck, Michael W., Robert D. Brumbaugh, Laura Airoldi, Alvar Carranza, Loren D. Coen, Christine Crawford, Omar Defeo, et al. 2011. Oyster reefs at risk and recommendations for conservation, restoration, and management. Bioscience 61: 107–116. Scholar
  4. Bell, Colin W., Barbara E. Fricks, Jennifer D. Rocca, Jessica M. Steinweg, Shawna K. McMahon, and Matthew D. Wallenstein. 2013. High-throughput fluorometric measurement of potential soil extracellular enzyme activities. Journal of Visualized Experiments.
  5. Birch, A., and L. Walters. 2012. Restoring intertidal oyster reefs in Mosquito Lagoon: the evolution of a successful model. TNC/NOAA Community-Based Restoration Partnership Program. 70 pp.Google Scholar
  6. Campbell, D. 2015. Quantifying the effects of boat wakes on intertidal oyster reefs in a shallow estuary. Orlando: University of Central Florida.Google Scholar
  7. Chambers, L.G., T.Z. Osborne, and K.R. Reddy. 2013. Effect of salinity pulsing events on soil organic carbon loss across an intertidal wetland gradient: A laboratory experiment. Biogeochemistry 115: 363–383. Scholar
  8. Chrost, R.J. 1991. Environmental control of the synthesis and activity of aquatic microbial ectoenzymes. In Microbial enzymes in aquatic environments, ed. R.J. Chrost, 29–59. New York: Springer.CrossRefGoogle Scholar
  9. Chrost, R.J., and H.J. Krambeck. 1986. Fluorescence correction for measurements of enzyme-activity in natural-waters using methylumbelliferyl substrates. Archiv Fur Hydrobiologie 106: 79–90.Google Scholar
  10. Coen, Loren D., Robert D. Brumbaugh, David Bushek, Ray Grizzle, Mark W. Luckenbach, Martin H. Posey, Sean P. Powers, and S. Gregory Tolley. 2007. Ecosystem services related to oyster restoration. Marine Ecology Progress Series 341: 303–307. Scholar
  11. Cressman, K.A., M.H. Posey, M.A. Mallin, L.A. Leonard, and T.D. Alphin. 2003. Effects of oyster reefs on water quality in a tidal creek estuary. Journal of Shellfish Research 22: 753–762.Google Scholar
  12. Dalrymple, D. Joseph, and Ruth H. Carmichael. 2015. Effects of age class on N removal capacity of oysters and implications for bioremediation. Marine Ecology Progress Series 528: 205–220. Scholar
  13. Dame, Richard F. 1999. Oyster reefs as components of estuarine nutrient cycling: inceidental or controlling? In Oyster reef habitat restoration: a synopsis and synthesis of approaches, ed. Mark W. Luckenbach, Roger Mann, and James A. Wesson, 267–280. Williamsburg: W&M Publish.
  14. Dame, Richard F., Richard G. Zingmark, and Elizabeth Haskin. 1984. Oyster reefs as processors of estuarine materials. Journal of Experimental Marine Biology and Ecology 83: 239–247.CrossRefGoogle Scholar
  15. Dame, Richard F., T.G. Wolaver, and S.M. Libes. 1985. The summer uptake and release of nitrogen by an intertidal oyster reef. Netherlands Journal of Sea Research 19: 265–268. Scholar
  16. Dame, Richard F., Norbert Dankers, Theo Prins, Henk Jongsma, and Aad Smaal. 1991. The influence of mussel beds on nutrients in the western Wadden Sea and eastern Scheldt estuaries. Estuaries 14: 130–138. Scholar
  17. Dame, Richard F., John D. Spurrier, and Richard G. Zingmark. 1992. In situ metabolism of an oyster reef. Journal of Experimental Marine Biology and Ecology 164: 147–159. Scholar
  18. DeBusk, W.F., and K.R. Reddy. 1998. Turnover of detrital organic carbon in a nutrient-impacted Everglades marsh. Soil Science Society of America Journal 62: 1460–1468. Scholar
  19. DeForest, Jared L. 2009. The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and l-DOPA. Soil Biology and Biochemistry 41: 1180–1186. Scholar
  20. Dybas, C.L. 2002. Florida’s Indian River lagoon: An estuary in transition. Bioscience 52: 554–559.CrossRefGoogle Scholar
  21. Frankignoulle, M, M. Pichon, and J-P. Gattuso. 1995. Aquatic calcification as a source of carbon dioxide. In Carbon sequestration in the biosphere, ed. Max A. Beran, 265–271. Berlin Heidelberg: Springer-Verlag.Google Scholar
  22. Gardner, L.M., and J.R. White. 2010. Denitrification enzyme activity as an indicator of nitrate movement through a diversion wetland. Soil Science Society of America Journal 74: 1037–1047. Scholar
  23. Garvis, Stephanie K., Paul E. Sacks, and Linda J. Walters. 2015. Formation, movement, and restoration of dead intertidal oyster reefs in Canaveral National Seashore and Mosquito Lagoon, Florida. Journal of Shellfish Research 34: 251–258. Scholar
  24. German, Donovan P., Michael N. Weintraub, A. Stuart Grandy, Christian L. Lauber, Zachary L. Rinkes, and Steven D. Allison. 2011. Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biology and Biochemistry 43: 1387–1397.
  25. Grabowski, Jonathan H., Robert D. Brumbaugh, Robert F. Conrad, Andrew G. Keeler, J. Opaluch, Charles H. Peterson, Michael F. Piehler, Sean P. Powers, and Ashley R. Smyth. 2012. Economic valuation of ecosystem services provided by oyster reefs. Bioscience 62: 900–909. Scholar
  26. Grizzle, R.E., J.R. Adams, and L.J. Walters. 2002. Historical changes in intertidal oyster (Crassostrea virginica) reefs in a Florida lagoon potentially related to boating activities. Journal of Shellfish Research 21: 749–756.Google Scholar
  27. Groffman, Peter M., and James M. Tiedje. 1989. Denitrification in north temperate forest soils: Relationships between denitrification and environmental factors at the landscape scale. Soil Biology and Biochemistry 21: 621–626. Scholar
  28. Guo, Lin, Fei Xu, Zhigang Feng, and Guofan Zhang. 2016. A bibliometric analysis of oyster research from 1991 to 2014. Aquaculture International 24: 327–344. Scholar
  29. Hale, R.L., and P.M. Groffman. 2006. Chloride effects on nitrogen dynamics in forested and suburban stream debris dams. Journal of Environmental Quality 35: 2425–2432. Scholar
  30. Higgins, Colleen B., Kurt Stephenson, and Bonnie L. Brown. 2011. Nutrient bioassimilation capacity of aquacultured oysters: Quantification of an ecosystem service. Journal of Environment Quality 40: 271. Scholar
  31. Higgins, Colleen B., Craig Tobias, Michael F. Piehler, Ashley R. Smyth, Richard F. Dame, Kurt Stephenson, and Bonnie L. Brown. 2013. Effect of aquacultured oyster biodeposition on sediment N2 production in Chesapeake Bay. Marine Ecology Progress Series 473: 7–27. Scholar
  32. Hoellein, Timothy J., Chester B. Zarnoch, and Raymond E. Grizzle. 2015. Eastern oyster (Crassostrea virginica) filtration, biodeposition, and sediment nitrogen cycling at two oyster reefs with contrasting water quality in Great Bay Estuary (New Hampshire, USA). Biogeochemistry 122: 113–129. Scholar
  33. Hoppe, Hans-Georg. 1993. Use of fluorogenic model substrates for extracellular enzyme activity (EEA) measurement of bacteria. In Handbook of methods in aquatic microbial ecology, eds. Paul F. Kemp, Barry F. Sherr, Evelyn B. Sherr, and Jonathan J. Cole, 423–431. Boca Raton: CRC Press LLC.Google Scholar
  34. Huang, Qinghui, Zijian Wang, Chunxia Wang, Shengrui Wang, and Xiangcan Jin. 2005. Phosphorus release in response to pH variation in the lake sediments with different ratios of iron-bound P to calcium-bound P. Chemical Speciation and Bioavailability 17: 55–61. Scholar
  35. Kellogg, M. Lisa, Jeffrey C. Cornwell, Michael S. Owens, and Kennedy T. Paynter. 2013. Denitrification and nutrient assimilation on a restored oyster reef. Marine Ecology Progress Series 480: 1–19. Scholar
  36. Kellogg, M. Lisa, Ashley R. Smyth, Mark W. Luckenbach, Ruth H. Carmichael, Bonnie L. Brown, Jeffrey C. Cornwell, Michael F. Piehler, Michael S. Owens, D. Joseph Dalrymple, and Colleen B. Higgins. 2014. Use of oysters to mitigate eutrophication in coastal waters. Estuarine, Coastal and Shelf Science 151: 156–168. Scholar
  37. Krom, M.D., and R.A. Berner. 1981. The diagenesis of phosphorus in a nearshore marine sediment. Geochimica et Cosmochimica Acta 45: 207–216.CrossRefGoogle Scholar
  38. Laing, I., P. Walker, and F. Areal. 2006. Return of the native - is European oyster (Ostrea edulis) stock restoration in the UK feasible? Aquatic Living Resources 19: 283–287. Scholar
  39. Leffler, Merrill and Pauli Hayes. 2004. Oyster research and restoration in U.S. coastal waters: research priorities and strategies. Accessed 23 Aug 2017.
  40. Lenihan, Hunter S. 1999. Physical-biological coupling on oyster reefs: How habitat structure influences individual performance. Ecological Monographs 69: 251–275.Google Scholar
  41. Leschine, S.B. 1995. Cellulose degradation in anaerobic environments. Annual Review of Microbiology 49: 399–426. Scholar
  42. Lindemann, Samantha, Chester B. Zarnoch, Domenic Castignetti, and Timothy J. Hoellein. 2016. Effect of eastern oysters (Crassostrea virginica) and seasonality on nitrite reductase gene abundance (nirS, nirK, nrfA) in an urban estuary. Estuaries and Coasts 39: 218–232. Scholar
  43. Makoi, Jhjr, and P.A. Ndakidemi. 2008. Selected soil enzymes: Examples of their potential roles in the ecosystem. African Journal of Biotechnology 7: 181–191.Google Scholar
  44. McClain, Michael E., Elizabeth W. Boyer, C. Lisa Dent, Sarah E. Gergel, Nancy B. Grimm, Peter M. Groffman, Stephen C. Hart, et al. 2003. Biogeochemical hot spots and hot moments at the interface of terrestrial and aquatic ecosystems. Ecosystems 6: 301–312. Scholar
  45. Meyer, David L., Edward C. Townsend, and Gordon W. Thayer. 1997. Stabilization and erosion control value of oyster cultch for intertidal marsh. Restoration Ecology 5: 93–99. Scholar
  46. Mortazavi, Behzad, Alice C. Ortmann, Lei Wang, Rebecca J. Bernard, Christina L. Staudhammer, J. Donald Dalrymple, Ruth H. Carmichael, and Alice A. Kleinhuizen. 2015. Evaluating the impact of oyster (Crassostrea virginica) gardening on sediment nitrogen cycling in a subtropical estuary. Bulletin of Marine Science 91: 323–341. Scholar
  47. Murphy, Anna E., Iris C. Anderson, and Mark W. Luckenbach. 2015. Enhanced nutrient regeneration at commercial hard clam (Mercenaria mercenaria) beds and the role of macroalgae. Marine Ecology Progress Series 530: 135–151. Scholar
  48. Nannipieri, P., J. Ascher, M.T. Ceccherini, L. Landi, G. Pietramellara, and G. Renella. 2003. Microbial diversity and soil functions. European Journal of Soil Science 54: 655–670. Scholar
  49. Newell, R.I.E., Jeffrey C. Cornwell, and Michael S. Owens. 2002. Influence of simulated bivalve biodeposition and microphytobenthos on sediment nitrogen dynamics: A laboratory study. Limnology and Oceanography 47: 1367–1379. Scholar
  50. Newell, R.I.E, T.R. Fisher, R.R. Holyoke, and J.C. Cornwell. 2005. Influence of eastern oysters on nitrogen and phosphorus regeneration in Chesapeake Bay, USA. In The comparative roles of suspension feeders in ecosystems, ed. R. Dame and S. Olenin, 93–120. Dordrecht: Springer pp. 93–120.Google Scholar
  51. Nizzoli, Daniele, David T. Welsh, Marco Bartoli, and Pierluigi Viaroli. 2005. Impacts of mussel (Mytilus galloprovincialis) farming on oxygen consumption and nutrient recycling in a eutrophic coastal lagoon. Hydrobiologia 550: 183–198. Scholar
  52. Peterson, Charles H., Jonathan H. Grabowski, and Sean P. Powers. 2003. Estimated enhancement of fish production resulting from restoring oyster reef habitat: Quantitative valuation. Marine Ecology Progress Series 264: 249–264. Scholar
  53. La Peyre, Megan, Jessica Furlong, Laura A. Brown, Bryan P. Piazza, and Ken Brown. 2014. Oyster reef restoration in the northern Gulf of Mexico: Extent, methods and outcomes. Ocean and Coastal Management 89: 20–28. Scholar
  54. Piehler, M.F., and A.R. Smyth. 2011. Habitat-specific distinctions in estuarine denitrification affect both ecosystem function and services. Ecosphere.
  55. Plutchak, Rochelle, Kelly Major, Cebrian Just, C. Drew Foster, Mary Elizabeth C. Miller, Andrea Anton, Kate L. Sheehan, Kenneth L. Heck, and Sean P. Powers. 2010. Impacts of oyster reef restoration on primary productivity and nutrient dynamics in tidal creeks of the north Central Gulf of Mexico. Estuaries and Coasts 33: 1355–1364. Scholar
  56. Pollack, Jennifer, David Yoskowitz, Hae Cheol Kim, and Paul A. Montagna. 2013. Role and value of nitrogen regulation provided by oysters (Crassostrea virginica) in the Mission-Aransas Estuary, Texas, USA. PloS One 8: 6–13. Scholar
  57. Reddy, K.R., and R. DeLaune. 2008. Biogeochemistry of wetlands: Science and applications. New York: CRC.CrossRefGoogle Scholar
  58. Smyth, Ashley R., Suzanne P. Thompson, Kaylyn N. Siporin, Wayne S. Gardner, Mark J. McCarthy, and Michael F. Piehler. 2013. Assessing nitrogen dynamics throughout the estuarine landscape. Estuaries and Coasts 36: 44–55. Scholar
  59. St. Johns River Water Management District. 2016. The Indian River Lagoon: An estuary of national significance. Accessed 26 Oct 2016.
  60. Stenberg, B., M. Johansson, M. Pell, K. Sjodahl-Svensson, J. Stenstrom, and L. Torstensson. 1998. Microbial biomass and activities in soil as affected by frozen and cold storage. Soil Biology & Biochemistry 30: 393–402. Scholar
  61. Styles, Richard. 2015. Flow and turbulence over an oyster reef. Journal of Coastal Research 31: 978–985. Scholar
  62. Tiedje, J.M. 1982. Denitrification. In Methods of soil analysis. Part 2, ed. A.L. Page, 1011–1026. Madison: ASA-SSSA.Google Scholar
  63. USEPA. 1993. Methods for the determination of inorganic substances in environmental samples, EPA/600/R-93/100. Washington: U.S. Environmental Protection Agency.Google Scholar
  64. Vance, E.D.D., P.C.C. Brookes, and D.S.S. Jenkinson. 1987. An extraction method for measuring soil microbial biomass-C. Soil Biology & Biochemistry 19: 703–707. Scholar
  65. Waldbusser, George G., Ryan A. Steenson, and Mark A. Green. 2011. Oyster shell dissolution rates in estuarine waters: Effects of pH and shell legacy. Journal of Shellfish Research 30: 659–669. Scholar
  66. Waldbusser, George G., Eric N. Powell, and Roger Mann. 2013. Ecosystem effects of shell aggregations and cycling in coastal waters: An example of Chesapeake Bay oyster reefs. Ecology 94: 895–903. Scholar
  67. Wall, L.M., Linda J. Walters, R.E. Grizzle, and P.E. Sacks. 2005. Recreational boating activity and its impact on the recruitment and survival of the oyster Crassostrea virginica on intertidal reefs in Mosquito Lagoon, Florida. Journal of Shellfish Research 24: 965–973. Scholar
  68. Walters, Linda J. 2016. Oyster reef deployment and monitoring: Final technical report. Indian River Lagoon National Estuary Program, 25 pp.Google Scholar
  69. White, J.R., and K.R. Reddy. 1999. Influence of nitrate and phosphorus loading on denitrifying enzyme activity in Everglades wetland soils. Soil Science Society of America Journal 63: 1945. Scholar
  70. White, J.R., and K.R.R. Reddy. 2000. Influence of phosphorus loading on organic nitrogen mineralization of Everglades soils. Soil Science Society of America Journal 64: 1525. Scholar
  71. Wilberg, Michael J., Maude E. Livings, Jennifer S. Barkman, Brian T. Morris, and Jason M. Robinson. 2011. Overfishing, disease, habitat loss, and potential extirpation of oysters in upper Chesapeake Bay. Marine Ecology Progress Series 436: 131–144. Scholar
  72. Wildish, D.J., and D.D. Kristmanson. 1997. Benthic suspension feeders and flow. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  73. Yoshinari, Tadashi, and Roger Knowles. 1976. Acetylene inhibition of nitrous oxide reduction by denitrifying bacteria. Biochemical and Biophysical Research Communications 69: 705–710. Scholar

Copyright information

© Coastal and Estuarine Research Federation 2017

Authors and Affiliations

  • Lisa G. Chambers
    • 1
    Email author
  • Stephanie A. Gaspar
    • 1
  • Christian J. Pilato
    • 2
  • Havalend E. Steinmuller
    • 1
  • Kevin J. McCarthy
    • 1
  • Paul E. Sacks
    • 2
    • 3
  • Linda J. Walters
    • 2
  1. 1.Aquatic Biogeochemistry Lab, Department of BiologyUniversity of Central FloridaOrlandoUSA
  2. 2.Coastal and Estuarine Ecology Lab, Department of BiologyUniversity of Central FloridaOrlandoUSA
  3. 3.Winter Springs High SchoolWinter SpringsUSA

Personalised recommendations