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Measuring carbon and nitrogen bioassimilation, burial, and denitrification contributions of oyster reefs in Gulf coast estuaries

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Abstract

The eastern oyster (Crassostrea virginica) and the reefs they create provide significant ecosystem services. This study measured their possible role in nutrient mitigation through bioassimilation, burial, and oyster-mediated sediment denitrification in near-shore shallow water (< 1 m water depth) and deep-water (> 1 m water depth) oyster reefs in Louisiana. Nitrogen (N) and carbon (C) in shell and tissue differed by oyster reproductive status, size, and habitat type. Changes in tissue percent N and C post-spawning combined with significant reductions in tissue dry weight from the release of gametes, resulted in 20 and 46% reductions in tissue N and C load (mg), respectively, for a 100-mm oyster. Oyster reefs did not enhance burial rates, with burial range rates estimated at 1.4–2.6 g N m−2 year−1, and 26.9–43.8 g C m−2 year−1. Closed-system ex situ incubations indicated net denitrification in all habitat types studied, with the highest rates exceeding 600 µmol N m−2 h−1 during the summer, but no enhancement attributable to oyster reefs specifically. Within the highly productive, organic-rich wetland complex systems of coastal Louisiana, oyster reefs were not associated with enhanced denitrification, likely due to the organic-rich setting, and redundant supplies of organic nitrogen and carbon from adjacent marshes. Context remains critical in determining ecosystem provision of habitats, and efforts to extrapolate and predict nitrogen removal across locations necessitates consideration of local conditions. Considering the large extent of reefs and oyster production across coastal Louisiana, oyster habitats may still contribute to N and C mitigation, but their unique contribution likely comes from bioassimilation, and removal of the oysters from the system.

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References

  • Ball DF (1964) Loss on ignition as an estimate of organic matter and organic carbon in noncalcareous soils. J Soil Sci 15:84–92

    Article  CAS  Google Scholar 

  • Beck S, La Peyre MK (2015) Effects of oyster harvest activities on Louisiana reef habitat and resident nekton communities. Fish Bull 113:327–340

    Article  Google Scholar 

  • Beck MW, Brumbaugh RD, Airoldi L, Carranza A, Coen LD, Crawford C, Defeo O, Edgar GJ, Hancock B, Kay MC, Lenihan HS, Luckenbach MW, Toropova CL, Zhang G, Guo X (2011) Oyster reefs at risk and recommendations for conservation, restoration, and management. Bioscience 61:107–116

    Article  Google Scholar 

  • Butzeck C, Eschenbach A, Grongroft A, Hansen K, Nolte S, Jensen K (2015) Sediment deposition and accretion rates in tidal marshes are highly variable along estuarine salinity and flooding gradients. Estuar Coasts 38:434–450

    Article  CAS  Google Scholar 

  • Caffrey JM, Hollibaugh JT, Mortazavi B (2016) Living oysters and their shells as sites of nitrification and denitrification. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2016.08.038

    Article  PubMed  Google Scholar 

  • Carmichael RH, Walton W, Clark H (2012) Bivalve-enhanced nitrogen removal from coastal estuaries. Can J Fish Aquat Sci 69:1131–1149

    Article  CAS  Google Scholar 

  • Casas SM, La Peyre J, La Peyre MK (2015) Restoration of oyster reefs in an estuarine lake: population dynamics and shell accretion. Mar Ecol Prog Ser 524:171–184

    Article  Google Scholar 

  • Coen LD, Brumbaugh RD, Bushek D, Grizzle R, Luckenbach MW, Posey MH, Powers SP, Tolley A (2007) Ecosystem services related to oyster restoration. Mar Ecol Prog Ser 341:303–307. https://doi.org/10.3354/meps341303

    Article  Google Scholar 

  • Dalrymple DJ, Carmichael RH (2015) Effects of age class on N removal capacity of oysters and implications for bioremediation. Mar Ecol Prog Ser 528:205–220

    Article  CAS  Google Scholar 

  • Dame R, Bushek D, Allen D, Lewitus A, Edwards D (2002) Ecosystem response to bivalve density reduction management implications. Aquat Ecol 36:51–65

    Article  Google Scholar 

  • Fertig B, Carruthers TJB, Dennsion WC, Fertig EJ, Altabet MA (2010) Eastern oyster (Crassostrea virginica) δ15N as a bioindicator of nitrogen sources: observations and modeling. Mar Pollut Bull 60:1288–1298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fodrie FJ, Rodriguez AB, Gitman RK, Grabowski JH, Lindquist NL, Peterson CH, Piehler MF, Ridge JT (2017) Oyster reefs as carbon sources and sinks. Proc R Soc B 284:20170891

    Article  PubMed  Google Scholar 

  • Freeman AM, Roberts HH (2013) Storm layer deposition on a coastal Louisiana lake bed. J Coast Res 29:31–42

    Google Scholar 

  • Fulweiler RW, Nixon SW (2012) Net sediment N2 fluxes in a southern New England estuary: variations in space and time. Biogeochemistry 111:111–124

    Article  Google Scholar 

  • Fulweiler RW, Nixon SW, Buckley BA, Granger SL (2008) Net sediment N2 fluxes in a coastal marine system: experiment manipulations and a conceptual model. Ecosystems 11:1168–1180

    Article  CAS  Google Scholar 

  • Haven D, Morales-Alamo R (1966) Aspects of biodeposition by oysters and other invertebrate filter feeders. Limnol Oceanogr 11:487–498

    Article  Google Scholar 

  • Heffner L (2013) Responses of nitrogen cycling to nutrient enrichment in New England salt marshes over an annual cycle. PhD, University of Rhode Island, USA

  • Henriksen K, Rasmussen MB, Jensen A (1983) Effect of bioturbation on microbial nitrogen transformations in the sediment and fluxes of ammonium and nitrate to the overlying water. Ecol Bull 35:193–205

    CAS  Google Scholar 

  • Henry KM (2012) Linking nitrogen biogeochemistry to different stages of wetland soil development in the Mississippi River delta, Louisiana. MS thesis, Department of Oceanography and Coastal Sciences, Louisiana State University, Baton Rouge, LA

  • Henry KM, Twilley RR (2014) Nutrient biogeochemistry during the early stages of delta development in the Mississippi River deltaic plain. Ecosystems 17:327–343

    Article  CAS  Google Scholar 

  • Higgins CB, Stephenson K, Brown BL (2011) Nutrient bioassimilation capacity of aquacultured oysters: quantification of an ecosystem service. J Environ Qual 40:271–277

    Article  CAS  PubMed  Google Scholar 

  • Higgins CB, Tobias C, Piehler MF, Smyth AR, Dame RF, Stephenson K, Brown BL (2013) Effect of aquacultured oyster biodeposition on sediment N2 production in Chesapeake Bay. Mar Ecol Prog Ser 473:7–27

    Article  CAS  Google Scholar 

  • Hoellein TJ, Zarnoch CB (2014) Effect of eastern oysters (Crassostrea virginica) on sediment carbon and nitrogen dynamics in an urban estuary. Ecol Appl 24:271–286

    Article  PubMed  Google Scholar 

  • Hoellein TJ, Zarnoch CB, Grizzle RE (2015) Eastern oyster (Crassostrea virginica) filtration, biodeposition, and sediment nitrogen cycling at two oyster reefs with contrasting water quality in Great Bay Estuary (New Hamshire, USA). Biogeochemistry 122:113–129

    Article  CAS  Google Scholar 

  • Howarth R, Anderson D, Cloern J, Elfring C, Hopkinson C, Lapointe B, Malone T, Marcus N, McGlathery K, Sharpley A, Walker D (2000) Nutrient pollution of coastal rivers, bays, and seas. Issues Ecol 7:1–16

    Google Scholar 

  • Humphries AT, Ayvazian SG, Carey JC, Hancock BT, Grabbert S, Cobb D, Strobel CJ, Fulweiler CJ (2016) Directly measured denitrification reveals oyster aquaculture and restored oyster reefs remove nitrogen at comparable high rates. Front Mar Sci 3:1–10

    Article  Google Scholar 

  • Joye SB, Hollibaugh JT (1995) Influence of sulfide inhibition of nitrification on nitrogen regeneration in sediments. Science 270:623–625

    Article  CAS  Google Scholar 

  • Kellogg ML, Cornwell JC, Owens MC, Paynter KT (2013) Denitrification and nutrient assimilation on a restored oyster reef. Mar Ecol Prog Ser 480:1–9

    Article  CAS  Google Scholar 

  • Kellogg ML, Smyth AR, Luckenbach MW, Carmichael RH, Brown BL, Cornwell JC, Piehler MF, Owens MS, Dalrymple DJ, Higgins CB (2014) Use of oysters to mitigate eutrophication in coastal waters. Estuar Coast Shelf Sci 151:156–168

    Article  CAS  Google Scholar 

  • La Peyre MK, Furlong J, Brown L, Brown KM, Piazza B (2014a) Oyster reef restoration in the northern Gulf of Mexico: extent, methods and outcomes. Ocean Coast Manag. https://doi.org/10.1016/j.ocecoman.2013.12.002

    Article  Google Scholar 

  • La Peyre MK, Humphries A, Casas S, La Peyre JF (2014b) Temporal variation in development of ecosystem services from oyster reef restoration. Ecol Eng 63:33–44

    Article  Google Scholar 

  • La Peyre MK, Serra K, Joyner TA, Humphries A (2015) Assessing shoreline exposure and oyster habitat suitability maximizes potential success for sustainable shoreline protection using restored oyster reefs. PeerJ 3:e1317. https://doi.org/10.7717/peerj.1317

    Article  PubMed  PubMed Central  Google Scholar 

  • LDWF. Louisiana Department of Wildlife and Fisheries. 2013. Oyster stock assessment report of the public oyster seed areas of Louisiana. Oyster data report series 19. Baton Rouge, LA

  • Lowe M, Sehlinger T, Soniat T, La Peyre MK (2017) Interactive effects of water temperature and salinity on growth and mortality of eastern oysters, Crassostrea virginica: a meta-analysis using 40 years of monitoring data. J Shellfish Res 36:1–15

    Article  Google Scholar 

  • Miller-Way T, Twilley R (1996) Theory and operation of continuous flow systems for the study of benthic-pelagic coupling. Mar Ecol Prog Ser 140:257–269

    Article  Google Scholar 

  • Mortazavi B, Ortmann AC, Wang L, Bernard RJ, Staudhammer CL, Dalrymple JD, Carmichael RH, Kleinhuizen AA (2015) Evaluating the impact of oyster (Crassostrea virginica) gardening on sediment nitrogen cycling in a subtropical estuary. Bull Mar Sci 91:323–341

    Article  Google Scholar 

  • Newell RIE, Jordan SJ (1983) Preferential ingestion of organic material by the American oyster Crassostrea virginica. Mar Ecol 13:47–53

    Article  Google Scholar 

  • Newell RIE, Cornwell JC, Owens MS (2002) Influence of simulated bivalve biodeposition and microphytobenthos on sediment nitrogen dynamics: a laboratory study. Limnol Oceanogr 47:1367–1379

    Article  Google Scholar 

  • Newell RIE, Fisher TR, Holyoke RR, Cornwell JC (2005) Influence of eastern oysters on nitrogen and phosphorus regeneration in Chesapeake Bay, USA. In: RiF D, Olenin S (eds) The comparative roles of suspension feeders in ecosystems, vol 47. NATO science series IV—earth and environmental sciences. Springer, Dordrecht, The Netherlands, pp 93–120

    Chapter  Google Scholar 

  • Nizzoli D, Welsh DT, Fano EA, Viaroli P (2006) Impact of clam and mussel farming on benthic metabolism and nitrogen cycling, with emphasis on nitrate reduction pathways. Mar Ecol Prog Ser 315:151–165

    Article  CAS  Google Scholar 

  • Piehler MF, Smyth AR (2011) Habitat-specific distinctions in estuarine denitrification affect both ecosystem function and services. Ecosphere 2:1–16

    Article  Google Scholar 

  • R Core Development Team (2015) R: a language and environment for statistical computing. R. Foundation for Statistical Computing, Vienna. https://www.R-project.org

  • Ren JS, Marsden ID, Ross AH, Schiel DR (2003) Seasonal variation in the reproductive activity and biochemical composition of the Pacific oyster (Crassostrea gigas) from the Marlborough Sounds, New Zealand. N Z J Mar Freshw Res 37:171–182

    Article  Google Scholar 

  • Rivera-Monroy VH, Lenaker P, Twilley RR, DeLaune RD, Lindau CW, Nuttle W, Habib E, Fulweiler RW, Castaneda-Moya E (2010) Denitrification in coastal Louisiana: a spatial assessment and research needs. J Sea Res 63:157–172

    Article  CAS  Google Scholar 

  • Rivera-Monroy VH, Branoff B, Meselhe E, McCorquodale A, Dortch Q, Steyer GD, Visser J, Wang H (2013) Landscape-level estimation of nitrogen removal in coastal Louisiana wetlands: potential sinks under different restoration scenarios. J Coast Res 67:75–87

    Article  CAS  Google Scholar 

  • Rodhouse PG, Roden CM, Hensey MP, Ryan TH (1984) Resource allocation in Mytilus edulis on the shore and in suspended culture. Mar Biol 84:27–34

    Article  Google Scholar 

  • Seitzinger SP (1988) Dentrification in freshwater and coastal marine ecosystems: ecological and geochemical significance. Limnol Oceanogr 33:702–724

    CAS  Google Scholar 

  • Smith RP (2009) Historic sediment accretion rates in a Louisiana coastal marsh and implications for sustainability. Department Environmental Sciences, University of Louisiana, Lafayette

    Google Scholar 

  • Smith CJ, DeLaune RD, Patrick WH Jr (1985) Fate of riverine nitrate entering an estuary: I. Denitrification and nitrogen burial. Estuaries 8:15–21

    Article  CAS  Google Scholar 

  • Smyth AR, Geraldi NR, Piehler MF (2013a) Oyster-mediated benthic-pelagic coupling modifies nitrogen pools and processes. Mar Ecol Prog Ser 493:23–30

    Article  CAS  Google Scholar 

  • Smyth AR, Thompson SP, Siporin KN, Gardner WS, McCarthy MJ, Piehler MF (2013b) Assessing nitrogen dynamics throughout the estuarine landscape. Estuar Coast 36:44–55

    Article  CAS  Google Scholar 

  • Smyth AR, Piehler MF, Grabowski JH (2015) Habitat context influences nitrogen removal by restored oyster reefs. J Appl Ecol 52:716–725

    Article  CAS  Google Scholar 

  • Soogsanjinda P, Matsudea O, Uamamoto T, Rajendran N, Maeda H (2000) The role of suspended oyster culture on nitrogen cycle in Hiroshima Bay. J Oceanogr 56:223–231. https://doi.org/10.1023/A:1011143414897

    Article  Google Scholar 

  • Valiela I, Foreman K, LaMontagne M, Hersh D, Costa J, Peckol P, DeMeo-Anderson B, D’Avanzo C, Babione M, Sham CH, Brawley J, Lajtha K (1992) Couplings of watersheds and coastal waters: sources and consequences of nutrient enrichment in Waquoit Bay, Massachusetts. Estuaries 15:443–457

    Article  CAS  Google Scholar 

  • Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilamn DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750

    Google Scholar 

  • Zu Ermgassen PSE, Spalding MD, Grizzle RE, Brumbaugh RD (2013) Quantifying the loss of a marine ecosystem service: filtration by the eastern oyster in US estuaries. Estaur Coasts 36:36–43

    Article  Google Scholar 

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Acknowledgements

This work was funded through the Coastal Science Assistantship Program, through Louisiana Sea Grant and the Coastal Protection and Restoration Authority of Louisiana, as well as the Louisiana Department of Wildlife and Fisheries through the U.S. Geological Survey Louisiana Fish and Wildlife Cooperative Research Unit. Thanks to Dr. Chris Swarzenski for comments on an earlier version of this manuscript. Early discussion with Drs. Bryan Piazza and Michael Piehler contributed to the development of this project. Input and discussion with Drs. Austin Humphries, S. Ayvazian and Boze Hancock informed this work. Many thanks to Robert Twilley, Edward Castañeda, Andy Nyman, Jerome La Peyre, John White, Mike Kaller, Brett Collier, Kristy Capelle, Romain Lavaud, Christian Flucke, Songjie He, Scott Harlamert, Steven Madere, Jay Curole, and Tommy Blanchard for their help and expertise. Data are available through MKL. Reviews from three anonymous reviewers significantly improved this manuscript. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Authors and Affiliations

  1. School of Renewable Natural Resources, Louisiana State University Agricultural Center, Baton Rouge, LA, 70803, USA

    Phillip Westbrook

  2. Western Alaska Landscape Conservation Cooperative, 1011 E. Tudor Rd. MS 281, Anchorage, AK, 99503, USA

    Leanna Heffner

  3. U.S. Geological Survey, Louisiana Fish and Wildlife Cooperative Research Unit, School of Renewable Natural Resources, Louisiana State University Agricultural Center, Baton Rouge, LA, 70803, USA

    Megan K. La Peyre

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  1. Phillip Westbrook
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Correspondence to Megan K. La Peyre.

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All applicable international, national and/or institutional guidelines for sampling, care and experimental use of organisms for the study have been followed.

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Responsible Editor: S. W. A. Naqvi.

Reviewed by S. Ayvazian, R. H. Carmichael and N. E. Ray.

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Westbrook, P., Heffner, L. & La Peyre, M.K. Measuring carbon and nitrogen bioassimilation, burial, and denitrification contributions of oyster reefs in Gulf coast estuaries. Mar Biol 166, 4 (2019). https://doi.org/10.1007/s00227-018-3449-1

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