Skip to main content
SpringerLink
Log in

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)

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

Benthic deposition of carbon (C) and nitrogen (N)-rich oyster biodeposits may increase denitrification, or anaerobic respiration of nitrate (NO3 −) to di-nitrogen gas (N2). However, environmental drivers of C and N dynamics in oyster biodeposits and reef-adjacent sediments require clarification. In July 2012, we collected intact sediment cores adjacent to and 15–20 m away from two oyster reefs (Crassostrea virginica) in Great Bay, New Hampshire, USA: one reference site and one site with cultural eutrophication. We also measured seston, chlorophyll a, and in situ oyster feeding and biodeposition. Cores were incubated in continuous-flow chambers where inflow water received 15N-ammonium (NH4 +), 15NO3 −, or no isotopes (control). We quantified fluxes of dissolved nutrients and gasses (oxygen, 28N2, 29N2, 30N2, and argon) after 24 h. Finally, we measured size-fractionated sediment organic matter. At the eutrophic site, abundant phytoplankton in the 5–28 µm size range was correlated with enhanced oyster feeding rates and biodeposit quality (lower C:N). This site had greater denitrification rates in reef-adjacent cores relative to distal cores. Low production of 29,30N2 in 15NH4 + amended cores suggested water column or biodeposit NH4 + were unlikely to be converted to N2. At both sites, reef-adjacent cores had more shell and higher 29,30N2 production with 15NO3 − addition relative to distal cores, suggesting direct denitrification enhancement near reefs. Oysters likely increased sediment N2 production via high quality biodeposits (eutrophic site), and NO3 − diffusion via structural complexity of reef-adjacent sediment (both sites). Overall, results suggest oyster-mediated ecosystems services may be expected to vary with environmental conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • An S, Gardner WS, Kana T (2001) Simultaneous measurement of denitrification and nitrogen fixation using isotope pairing with membrane inlet mass spectrometry analysis. Appl Environ Microbiol 67(3):1171–1178

    Article  Google Scholar 

  • APHA (1998) Standard methods for the examination of water and wastewater, 20th edn. United Book Press Inc, Baltimore

    Google Scholar 

  • Atkinson CL, Kelly JF, Vaughn CC (2014) Tracing consumer-derived nitrogen in riverine food webs. Ecosystems 17(3):485–496

    Article  Google Scholar 

  • Barber BJ, Langan R, Howell TL (1997) Haplosporidium nelsoni (MSX) epizootic in the Piscataqua River Estuary (Maine/New Hampshire, USA). J Parasitol 83(1):148–150

    Article  Google Scholar 

  • Bayne BL (2002) A physiological comparison between Pacific oysters Crassostrea gigas and Sydney Rock oysters Saccostrea glomerata: food, feeding and growth in a shared habitat. Mar Ecol Prog Ser 232:163–178

    Article  Google Scholar 

  • Bayne BL, Newell RC (1983) Physiological energetics of marine molluscs. In: Wilber KM, Saleuddin AS (eds) The Mollusca. Academic Press, New York, pp 407–515

    Google Scholar 

  • Bayne BL, Hedgecock D, McGoldrick D, Rees R (1999) Feeding behaviour and metabolic efficiency contribute to growth heterosis in Pacific oysters Crassostrea gigas (Thunberg). J Exp Mar Biol Ecol 233(1):115–130

    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(2):107–116

    Article  Google Scholar 

  • Beseres Pollack J, Yoskowitz D, Kim HC, Montagna PA (2013) Role and value of nitrogen regulation provided by oysters (Crassostrea virginica) in the Mission-Aransas Estuary, Texas, USA. Plos One 8(6):e65314

    Article  Google Scholar 

  • Bruesewitz DA, Tank JL, Bernot MJ (2008) Delineating the effects of zebra mussels (Dreissena polymorpha) on N transformation rates using laboratory mesocosms. J N Am Benthol Soc 27(2):236–251

    Article  Google Scholar 

  • Bruesewitz DA, Tank JL, Hamilton SK (2009) Seasonal effects of zebra mussels on littoral nitrogen transformation rates in Gull Lake, Michigan, USA. Freshwater Biol 54(7):1427–1443

    Article  Google Scholar 

  • Bruesewitz DA, Gardner WS, Mooney RF, Pollard L, Buskey EJ (2013) Estuarine ecosystem function response to flood and drought in a shallow, semiarid estuary: nitrogen cycling and ecosystem metabolism. Limnol Oceanogr 58(6):2293–2309

    Article  Google Scholar 

  • Brumbaugh RD, Coen LD (2009) Contemporary approaches for small-scale oyster restoration to address substrate versus recruitment limitation: a review and comments relevant for the Olympia oyster, Ostrea lurida (Carpenter, 1964). J Shellfish Res 28:147–161

    Article  Google Scholar 

  • Cerco CF, Noel MR (2007) Can oyster restoration reverse cultural eutrophication in Chesapeake Bay? Estuar Coasts 30(2):331–343

    Article  Google Scholar 

  • Cloern JE (2001) Our evolving conceptual model of the coastal eutrophication problem. Mar Ecol Prog Ser 210:223–253

    Article  Google Scholar 

  • Coen LD, Luckenbach MW, Breitburg DL (1999) The role of oyster reefs as essential fish habitat: a review of current knowledge and some new perspectives. Am Fish Soc Symp 22:438–454

    Google Scholar 

  • Coen LD, Brumbaugh RD, Bushek D, Grizzle R, Luckenbach MW, Posey MH, Powers SP, Tolley G (2007) A broader view of ecosystem services related to oyster restoration. Mar Ecol Prog Ser 341:303–307

    Article  Google Scholar 

  • Cranford PJ, Evans DA, Shumway SE (2011) Bivalve filter feeding: of variability and limits the aquaculture biofilter. In: Shumway SE (ed) Shellfish aquaculture and the environment. John Wiley & Sons, West Sussex, pp 157–228

    Google Scholar 

  • Dame R (2012) Ecology of marine bivalves: an ecosystem approach. CRC Marine Science Series, Boca Raton

    Google Scholar 

  • Dang HY, Wang CY, Li J, Li TG, Tian F, Jin W, Ding YS, Zhang ZN (2009) Diversity and distribution of sediment nirS-encoding bacterial assemblages in response to environmental gradients in the eutrophied Jiaozhou Bay, China. Microb Ecol 58(1):161–169

    Article  Google Scholar 

  • Engström P, Dalsgaard T, Hulth S, Aller RC (2005) Anaerobic ammonium oxidation by nitrite (anammox): implications for N-2 production in coastal marine sediments. Geochim Cosmochim Acta 69(8):2057–2065

    Article  Google Scholar 

  • Eyre BD, Ferguson AJP (2005) Benthic metabolism and nitrogen cycling in a subtropical east Australian Estuary (Brunswick): temporal variability and controlling factors. Limnol Oceanogr 50(1):81–96

    Article  Google Scholar 

  • Eyre BD, Rysgaard S, Dalsgaard T, Christensen PB (2002) Comparison of isotope pairing and N2:Ar methods for measuring sediment denitrification—assumption, modifications, and implications. Estuaries 25(6):1077–1087

    Article  Google Scholar 

  • Eyre BD, Santos IR, Maher DT (2013) Seasonal, daily and diel N2 effluxes in permeable carbonate sediments. Biogeosci Disc 10:2601–2615

    Article  Google Scholar 

  • Fulweiler RW, Brown SM, Nixon SW, Jenkins BD (2013) Evidence and a conceptual model for the co-occurrence of nitrogen fixation and denitrification in heterotrophic marine sediments. Mar Ecol Prog Ser 482:57–68

    Article  Google Scholar 

  • Galimany E, Rose JM, Dixon MS, Wikfors GH (2013) Quantifying feeding behaviors of ribbed mussels, Geukensia demissa, in two urban sites (Long Island Sound, USA) with different seston conditions. Estuar Coasts 36:1265–1273

    Article  Google Scholar 

  • Gardner WS, McCarthy MJ (2009) Nitrogen dynamics at the sediment-water interface in shallow, sub-tropical Florida Bay: why denitrification efficiency may decrease with increased eutrophication. Biogeochemistry 95(2–3):185–198

    Article  Google Scholar 

  • Gardner WS, McCarthy MJ, An S, Sobolev D, Sell KS, Brock D (2006) Nitrogen fixation and dissimilatory nitrate reduction to ammonium (DNRA) support nitrogen dynamics in Texas estuaries. Limnol Oceanogr 51(1):558–568

    Article  Google Scholar 

  • Gobler CJ, Renaghan MJ, Buck NJ (2002) Impacts of nutrients and grazing mortality on the abundance of Aureococcus anophagefferens during and New York brown tide bloom. Limnol Oceanogr 47:129–141

    Article  Google Scholar 

  • Grabowski JH, Peterson CH (2007) Restoring oyster reefs to recover ecosystem services. In: Cuddington K, Byers JE, Wilson WG, Hastings A (eds) Ecosystem engineers: plants to protists. Academic Press, Amsterdam, pp 281–298

    Chapter  Google Scholar 

  • Grizzle R, Ward K (2013) Oyster bed mapping in the Great Bay Estuary, 2012-2013. Piscataqua Region Estuaries Partnership and the New Hampshire Department of Environmental Services, Concord

    Google Scholar 

  • Grizzle RE, Brodeur MA, Abeels HA, Greene JK (2008a) Bottom habitat mapping using towed underwater videography: subtidal oyster reefs as an example application. J Coast Res 24(1):103–109

    Article  Google Scholar 

  • Grizzle RE, Greene JK, Coen LD (2008b) Seston removal by natural and constructed intertidal eastern oyster (Crassostrea virginica) reefs: a comparison with previous laboratory studies, and the value of in situ methods. Estuar Coasts 31(6):1208–1220

    Article  Google Scholar 

  • Heisterkamp IM, Schramm A, de Beer D, Stief P (2010) Nitrous oxide production associated with coastal marine invertebrates. Mar Ecol Prog Ser 415:1–9

    Article  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  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(2):271–286

    Article  Google Scholar 

  • Iglesias JIP, Urrutia MB, Navarro E, Ibarrola I (1998) Measuring feeding and absorption in suspension-feeding bivalves: an appraisal of the biodeposition method. J Exp Mar Biol Ecol 219(1–2):71–86

    Article  Google Scholar 

  • Jones HFE, Pilditch CA, Bruesewitz DA, Lohrer AM (2011) Sedimentary environment influences the effect of an infaunal suspension feeding bivalve on estuarine ecosystem function. Plos One 6(10):e27065

    Article  Google Scholar 

  • Kana TM, Weiss DL (2004) Comment on “Comparison of isotope pairing and N2:Ar methods for measuring sediment denitrification” by B. D. Eyre, S. Rysgaard, T. Dalsgaard, and P. Bondo Christensen. 2002. Estuaries 25:1077–1087 Estuaries 27(1): 173-176

    Google Scholar 

  • Kana TM, Sullivan MB, Cornwell JC, Groszkowski KM (1998) Denitrification in estuarine sediments determined by membrane inlet mass spectrometry. Limnol Oceanogr 43(2):334–339

    Article  Google Scholar 

  • Kellogg LM, Cornwell JC, Owens MS, Paynter KT (2013) Denitrification and nutrient assimilation on a restored oyster reef. Mar Ecol Prog Ser 480:1–19

    Article  Google Scholar 

  • Koop-Jakobsen K, Giblin AE (2009) Anammox in tidal marsh sediments: The role of salinity, nitrogen loading, and marsh vegetation. Estuar Coasts 32(2):238–245

    Article  Google Scholar 

  • Langdon CJ, Newell RIE (1996) Digestion and nutrition in larvae and adults. In: Kennedy VS, Newell RIE, Eble AF (eds) The Eastern oyster Crassostrea virginica. Maryland Sea Grant, College Park, pp 231–269

    Google Scholar 

  • Luckenbach MW, Mann R, Wesson J (eds) (1999) Oyster reef habitat restoration: a synopsis and synthesis of approaches. Virginia Institute of Marine Science, Gloucester Point

    Google Scholar 

  • Malone TC (1992) Effects of water column processes on dissolved oxygen, nutrients, phytoplankton, and zooplankton. In: Smith DE, Leffler M, Mackiernan G (eds) Oxygen dynamics in the Chesapeake Bay. Maryland Sea Grant Publications, College Park, pp 61–112

    Google Scholar 

  • McCarthy MJ, Gardner WS (2003) An application of membrane inlet mass spectrometry to measure denitrification in a recirculating mariculture system. Aquaculture 218(1–4):341–355

    Article  Google Scholar 

  • McCarthy M, Lavrentyev P, Yang L, Zhang L, Chen Y, Qin B, Gardner W (2007a) Nitrogen dynamics and microbial food web structure during a summer cyanobacterial bloom in a subtropical, shallow, well-mixed, eutrophic lake (Lake Taihu, China). In: Qin B, Liu Z, Havens K (eds) Eutrophication of Shallow Lakes with Special Reference to Lake Taihu, China. Developments in Hydrobiology. Springer, Netherlands, pp 195–207

    Chapter  Google Scholar 

  • McCarthy MJ, Gardner WS, Lavrentyev PJ, Moats KM, Joehem FJ, Klarer DM (2007b) Effects of hydrological flow regime on sediment-water interface and water column nitrogen dynamics in a great lakes coastal wetland (Old Woman Creek, Lake Erie). J Great Lakes Res 33(1):219–231

    Article  Google Scholar 

  • McCarthy M, McNeal K, Morse J, Gardner W (2008) Bottom-water hypoxia effects on sediment–water interface nitrogen transformations in a seasonally hypoxic, shallow bay (Corpus Christi Bay, TX, USA). Estuar Coasts 31(3):521–531

    Article  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for determination of phosphate in natural waters. Anal Chim Acta 26(1):31–36

    Article  Google Scholar 

  • Newell RIE (2004) Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J Shellfish Res 23(1):51–61

    Google Scholar 

  • Newell RIE, Langdon CJ (1996) Mechanisms and physiology of larval and adult feeding. In: Kennedy VS, Newell RIE, Eble AF (eds) The Eastern oyster Crassostrea virginica. Maryland Sea Grant, College Park, pp 185–229

    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: Dame R, Olenin S (eds) The comparative roles of suspension feeders in ecosystems. Nato science series IV: earth and environmental sciences. NATO science series: IV: earth and environmental sciences. Springer, Netherlands, pp 93–120

    Google Scholar 

  • Nixon SW (1995) Coastal marine eutruophication: a definition, social causes, and future concerns. Ophelia 41:199–219

    Article  Google Scholar 

  • Odell J, Eberhardt A, Burdick D, Ingraham P (2006) Great Bay Estuary restoration compendium. The Nature Conservancy, New Hampshire Estuaries Project. University of New Hampshire, Dunham

    Google Scholar 

  • Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, New York

    Google Scholar 

  • Petersen JK, Bougrier S, Smaal AC, Garen P, Robert S, Larsen JEN, Brummelhuis E (2004) Intercalibration of mussel Mytilus edulis clearance rate measurements. Mar Ecol Prog Ser 267:187–194

    Article  Google Scholar 

  • Piehler MF, Smyth AR (2011) Habitat-specific distinctions in estuarine denitrification affect both ecosystem function and services. Ecosphere 2(1): art12

  • Piscataqua Region Estuaries Partnership (2013) State of our estuaries, 2013. University of New Hampshire, Durham

    Google Scholar 

  • Plutchak R, Major K, Cebrian J, Foster CD, Miller MEC, Anton A, Sheehan KL, Heck KL, Powers SP (2010) Impacts of oyster reef restoration on primary productivity and nutrient dynamics in tidal creeks of the North Central Gulf of Mexico. Estuar Coasts 33(6):1355–1364

    Article  Google Scholar 

  • Riisgård HU (1988) Efficiency of particle retention and filtration rate in 6 species of Northeast American bivalves. Mar Ecol Prog Ser 45:217–223

    Article  Google Scholar 

  • Risgaard-Petersen N (2003) Coupled nitrification-denitrification in autotrophic and heterotrophic estuarine sediments: on the influence of benthic microalgae. Limnol Oceanogr 48(1):93–105

    Article  Google Scholar 

  • Ryther JH (1954) The ecology of phytoplankton blooms in Moriches Bay and Great South Bay, Long Island, New York. Biol Bull 106:198–209

    Article  Google Scholar 

  • Seitzinger S, Harrison JA, Bohlke JK, Bouwman AF, Lowrance R, Peterson B, Tobias C, Drecht GV (2006) Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl 16:2064–2090

    Article  Google Scholar 

  • Shumway SE (1996) Natural Environmental Factors. In: Kennedy VS, Newell RIE, Eble AF (eds) The Eastern oyster, Crassostrea virginica. Maryland Sea Grant, College Park, pp 467–514

    Google Scholar 

  • Smyth AR, Thompson SP, Siporin KN, Gardner WS, McCarthy MJ, Piehler MF (2013) Assessing nitrogen dynamics throughout an estuarine landscape. Estuar Coasts 36(1):44–55

    Article  Google Scholar 

  • Solorzano L (1969) Determination of ammonium in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799–801

    Article  Google Scholar 

  • Thamdrup B, Dalsgaard T (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 68(3):1312–1318

    Article  Google Scholar 

  • Wall CC, Gobler CJ, Peterson BJ, Ward EJ (2013) Contrasting growth patterns of suspension-feeding molluscs (Mercenaria mercenaria, Crassostrea virginica, Argopecten irradians, and Crepidula fornicata) across a eutrophication gradient in the Peconic Estuary, NY, USA. Estuar Coasts 36:1274–1291

    Article  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. Estuar Coasts 36(1):36–43

    Article  Google Scholar 

Download references

Acknowledgments

Funding was provided by the Hudson River Foundation. For field assistance we thank Krystin Ward and Deb Lamson. For assistance in the lab we thank Michael Hassett, Matthew Girard, and Ashley Cook from Loyola University Chicago and Doris Law, Andrew Liang, and Erika Fusco from Baruch College. Thanks to Denise Bruesewitz for comments on an early version of this manuscript. The manuscript was also greatly improved by insightful comments from 3 anonymous reviewers and Associate Editor Leila J. Hamdan.

Author information

Authors and Affiliations

  1. Department of Biology, Loyola University Chicago, 1032 W Sheridan Rd, Chicago, IL, 60660, USA

    Timothy J. Hoellein

  2. Department of Natural Sciences, Baruch College, City University of New York, Box A-0506, 17 Lexington Ave, New York, NY, 10010, USA

    Chester B. Zarnoch

  3. Jackson Estuarine Laboratory and Department of Biological Sciences, University of New Hampshire, 85 Adams Point Road, Durham, NH, 03824, USA

    Raymond E. Grizzle

Authors
  1. Timothy J. Hoellein
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chester B. Zarnoch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Raymond E. Grizzle
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Timothy J. Hoellein.

Additional information

Responsible Editor: Leila J. Hamdan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hoellein, T.J., Zarnoch, C.B. & Grizzle, R.E. 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 (2015). https://doi.org/10.1007/s10533-014-0034-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-014-0034-7

Keywords

Search

Navigation