Overfishing, nutrient-fuelled hypoxia and habitat destruction have reduced oyster populations to a fraction of their former abundance. Over the past two decades there has been a widespread effort to restore oyster reefs and develop oyster aquaculture. Yet it remains unclear how re-introduction of large oyster populations will change coastal biogeochemistry. Of particular interest is whether oysters may help offset excess nitrogen loading, which is responsible for widespread coastal water quality degradation, low oxygen conditions and biodiversity declines. Here we used a meta-analysis approach to assess how oysters alter inorganic nutrient cycling, with a focus on nitrogen removal. Additionally, we examined how oysters alter greenhouse gas emissions. We demonstrate that oysters enhance removal of excess nitrogen by stimulating denitrification, promote efficient nutrient recycling and may have a negligible greenhouse gas footprint. Further, oyster reefs and oyster aquaculture appear to have similar biogeochemical function, suggesting the potential for sustainable production of animal protein alongside environmental restoration.
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All data used in this study is available in the Figshare repository under the access number https://doi.org/10.6084/m9.figshare.12488753.
The R script used in this meta-analysis is available in the GitHub community repository (https://github.com/nray17/Meta-analysis-oyster-impacts-on-biogeochemistry).
Factsheet: People and Oceans (United Nations, 2017).
Vitousek, P. M. et al. Human alteration of the global nitrogen cycle: sources and consequences. Ecol. Appl. 7, 737–750 (1997).
Galloway, J. N. et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892 (2008).
Canfield, D. E., Glazer, A. N. & Falkowski, P. G. The evolution and future of Earth’s nitrogen cycle. Science 330, 192–196 (2010).
Ryther, J. & Dunstan, W. Nitrogen, phosphorus, and eutrophication in the coastal marine environment. Science 171, 1008–1013 (1971).
Conley, D. J. et al. Controlling eutrophication: nitrogen and phosphorus. Science 323, 1014–1015 (2009).
Downing, J. A., Cherrier, C. T. & Fulweiler, R. W. Low ratios of silica to dissolved nitrogen supplied to rivers arise from agriculture not reservoirs. Ecol. Lett. 19, 1414–1418 (2016).
Carey, J. C. & Fulweiler, R. W. Human activities directly alter watershed dissolved silica fluxes. Biogeochemistry 111, 125–138 (2012).
Turner, R. E. et al. Fluctuating silicate:nitrate ratios and coastal plankton food webs. Proc. Natl Acad. Sci. USA 95, 13048–13051 (1998).
Nixon, S. W. Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41, 199–219 (1995).
Kirby, M. X. Fishing down the coast: historical expansion and collapse of oyster fisheries along continental margins. Proc. Natl Acad. Sci. USA 101, 13096–13099 (2004).
Mackenzie, C. L. Causes underlying the historical decline in eastern oyster (Crassostrea virginica Gmelin, 1791) landings. J. Shellfish Res. 26, 927–938 (2007).
Powell, E., Ashton-Alcox, K., Kraeuter, J., Ford, S. & Bushek, D. Long-term trends in oyster population dynamics in Delaware Bay: regime shifts and response to disease. J. Shellfish Res. 27, 729–755 (2008).
Rick, T. et al. Millenial-scale sustainability of the Chesapeake Bay Native American oyster fishery. Proc. Natl Acad. Sci. USA 113, 6568–6573 (2016).
Beck, M. W. et al. Oyster reefs at risk and recommendations for conservation, restoration, and management. BioScience 61, 107–116 (2011).
Zu Ermgassen, P. S. E. et al. Historical ecology with real numbers: past and present extent and biomass of an imperilled estuarine habitat. Proc. R. Soc. Lond. B 279, 3393–3400 (2012).
Transforming Our World: The 2030 Agenda for Sustainable Development (United Nations, 2015).
Newell, R., Fisher, T., Holyoke, R. & Cornwell, J. in The Comparative Roles of Suspension-Feeders in Ecosystems Vol. 47 (eds Dame, R. F. & Olenin, S.) 93–120 (Springer, 2005).
Kellogg, M. L. et al. Use of oysters to mitigate eutrophication in coastal waters. Estuar. Coast. Shelf Sci. 151, 156–168 (2014).
Ray, N. E., Maguire, T. J., Al-Haj, A., Henning, M. & Fulweiler, R. W. Low greenhouse gas emissions from oyster aquaculture. Environ. Sci. Technol. 53, 9118–9127 (2019).
Carman, M. R., Morris, J. A., Karney, R. C. & Grunden, D. W. An initial assessment of native and invasive tunicates in shellfish aquaculture of the North American east coast. J. Appl. Ichthyol. 26, 8–11 (2010).
Guy-Haim, T. et al. Diverse effects of invasive ecosystem engineers on marine biodiversity and ecosystem functions: a global review and meta-analysis. Glob. Change Biol. 24, 906–924 (2018).
Murray, A. G., Munro, L. A. & Matejusova, I. The network of farmed Pacific oyster movements in Scotland and routes for introduction and spread of invasive species and pathogens. Aquaculture 520, 734747 (2020).
Rowe, G., Clifford, C. & Smith, K. Jr Benthic nutrient regeneration and its coupling to primary productivity in coastal waters. Nature 255, 215–217 (1975).
Seitzinger, S. P. Denitrification in freshwater and coastal marine systems: ecological and geochemical significance. Limnol. Oceanogr. 334, 702–724 (1988).
Ray, N. E., Henning, M. C. & Fulweiler, R. W. Nitrogen and phosphorus cycling in the digestive system and shell biofilm of the eastern oyster (Crassostrea virginica). Mar. Ecol. Prog. Ser. 621, 95–105 (2019).
Duarte, C. M. et al. Rebuilding marine life. Nature 580, 39–51 (2020).
The State of World Fisheries and Aquaculture 2018: Meeting the Sustainable Development Goals (FAO, 2018).
Gentry, R. R. et al. Mapping the global potential for marine aquaculture. Nat. Ecol. Evol. 1, 1317–1324 (2017).
Lacoste, E., Gueguen, Y., Moullac, G. L. E., Koua, M. S. & Gaertner-Mazouni, N. Influence of farmed pearl oysters and associated biofouling communities on nutrient regeneration in lagoons of French Polynesia. Aquac. Environ. Interact. 5, 209–219 (2014).
Buzin, F., Dupuy, B., Lefebvre, S., Barillé, L. & Haure, J. Storage of Pacific oysters Crassostrea gigas in recirculating tank: Ammonia excretion and potential nitrification rates. Aquac. Eng. 64, 8–14 (2015).
Han, T. et al. Interactive effects of oyster and seaweed on seawater dissolved inorganic carbon systems: Implications for integrated multi-trophic aquaculture. Aquac. Environ. Interact. 9, 469–478 (2017).
Kesarcodi-Watson, A., Klumpp, D. W. & Lucas, J. S. Comparative feeding and physiological energetics of diploid and triploid Sydney rock oysters, Saccostrea commercialis I. Effects of oyster size. Aquaculture 203, 195–216 (2001).
Winter, J., Acevedo, M. & Navarro, J. Quempillen estuary, an experimental oyster cultivation station in southern Chile. Energy balance in Ostrea chilensis. Mar. Ecol. Prog. Ser. 20, 151–164 (1984).
Sma, R. F. & Baggaley, A. Rate of excretion of ammonia by the hard clam Mercenaria mercenaria and the American oyster Crassostrea virginica. Mar. Biol. 36, 251–258 (1976).
Jackson, M. Characterization of Oyster-Associated Biogeochemical Processes in Oyster Restoration and Aquaculture. PhD dissertation, Univ. Maryland (2019).
Mao, Y., Zhou, Y., Yang, H. & Wang, R. Seasonal variation in metabolism of cultured Pacific oyster, Crassostrea gigas, in Sanggou Bay, China. Aquaculture 253, 322–333 (2006).
Smyth, A. R., Geraldi, N. R. & Piehler, M. F. Oyster-mediated benthic–pelagic coupling modifies nitrogen pools and processes. Mar. Ecol. Prog. Ser. 493, 23–30 (2013).
Caffrey, J. M., Hollibaugh, J. T. & Mortazavi, B. Living oysters and their shells as sites of nitrification and denitrification. Mar. Pollut. Bull. 112, 86–90 (2016).
Erler, D. V. et al. The impact of suspended oyster farming on nitrogen cycling and nitrous oxide production in a sub-tropical Australian estuary. Estuar. Coast. Shelf Sci. 192, 117–127 (2017).
Arfken, A., Song, B., Bowman, J. S. & Piehler, M. Denitrification potential of the eastern oyster microbiome using a 16S rRNA gene based metabolic inference approach. PLoS ONE 12, e0185071 (2017).
Jackson, M., Owens, M. S., Cornwell, J. C. & Kellogg, M. L. Comparison of methods for determining biogeochemical fluxes from a restored oyster reef. PLoS ONE 13, e0209799 (2018).
Gárate, M., Moseman-Valtierra, S. & Moen, A. Potential nitrous oxide production by marine shellfish in response to warming and nutrient enrichment. Mar. Pollut. Bull. 146, 236–246 (2019).
McCarthy, G., Ray, N. E. & Fulweiler, R. W. Greenhouse gas emissions from native and non-native oysters. Front. Environ. Sci. 7, 194 (2019).
Kellogg, M. L., Cornwell, J. C., Owens, M. S. & Paynter, K. T. Denitrification and nutrient assimilation on a restored oyster reef. Mar. Ecol. Prog. Ser. 480, 1–19 (2013).
Higgins, C. B. et al. Effect of aquacultured oyster biodeposition on sediment N2 production in Chesapeake Bay. Mar. Ecol. Prog. Ser. 473, 7–27 (2013).
Green, D. S., Rocha, C. & Crowe, T. P. Effects of non-indigenous oysters on ecosystem processes vary with abundance and context. Ecosystems 16, 881–893 (2013).
Hyun, J. et al. Impacts of long-line aquaculture of Pacific oysters (Crassostrea gigas) on sulfate reduction and diffusive nutrient flux in the coastal sediments of Jinhae–Tongyeong, Korea. Mar. Pollut. Bull. 74, 187–198 (2013).
Hoellein, T. J. & Zarnoch, C. B. Effect of eastern oysters (Crassostrea virginica) on sediment carbon and nitrogen dynamics in an urban estuary. Ecol. Appl. 24, 271–286 (2014).
Andrieux-Loyer, F. et al. Impact of oyster farming on diagenetic processes and the phosphorus cycle in two estuaries (Brittany, France). Aquat. Geochem. 20, 573–611 (2014).
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).
Smyth, A. R., Piehler, M. F. & Grabowski, J. H. Habitat context influences nitrogen removal by restored oyster reefs. J. Appl. Ecol. 52, 716–725 (2015).
Mortazavi, B. et al. Evaluating the impact of oyster (Crassostrea virginica) gardening on sediment nitrogen cycling in a subtropical estuary. Bull. Mar. Sci. 91, 323–341 (2015).
Testa, J. M. et al. Modeling the impact of floating oyster (Crassostrea virginica) aquaculture on sediment–water nutrient and oxygen fluxes. Aquac. Environ. Interact. 7, 205–222 (2015).
Smyth, A. R., Geraldi, N. R., Thompson, S. P. & Piehler, M. F. Biological activity exceeds biogenic structure in influencing sediment nitrogen cycling in experimental oyster reefs. Mar. Ecol. Prog. Ser. 560, 173–183 (2016).
Humphries, A. T. et al. Directly measured denitrification reveals oyster aquaculture and restored oyster reefs remove nitrogen at comparable high rates. Front. Mar. Sci. 3, 74 (2016).
Lacoste, E. & Gaertner-Mazouni, N. Nutrient regeneration in the water column and at the sediment–water interface in pearl oyster culture (Pinctada margaritifera) in a deep atoll lagoon (Ahe, French Polynesia). Estuar. Coast. Shelf Sci. 182, 304–309 (2016).
Smyth, A. R., Murphy, A. E., Anderson, I. C. & Song, B. Differential effects of bivalves on sediment nitrogen cycling in a shallow coastal bay. Estuaries Coasts 41, 1147–1163 (2018).
Onorevole, K. M., Thompson, S. P. & Piehler, M. F. Living shorelines enhance nitrogen removal capacity over time. Ecol. Eng. 120, 238–248 (2018).
Lunstrum, A., McGlathery, K. & Smyth, A. Oyster (Crassostrea virginica) aquaculture shifts sediment nitrogen processes toward mineralization over denitrification. Estuaries Coast. 41, 1130–1146 (2018).
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, 1–14 (2019).
Ray, N. E., Al-Haj, A. & Fulweiler, R. W. Sediment biogeochemistry along an oyster aquaculture chronosequence. Mar. Ecol. Prog. Ser. 646, 13–27 (2020).
Hassett, M. The Influence of Eastern Oyster (Crassostrea virginica) Reef Restoration on Nitrogen Cycling in a Eutrophic Estuary. MSc thesis, Loyola Univ. Chicago (2015).
Vieillard, A. M. Impacts of New England Oyster Aquaculture on Sediment Nitrogen Cycling: Implications for Nitrogen Removal and Retention. MSc thesis, Univ. Connecticut (2017).
Boucher-Rodoni, R. & Boucher, G. In situ study of the effect of oyster biomass on benthic metabolic exchange rates. Hydrobiologia 206, 115–123 (1990).
Mazouni, N., Gaertner, J., Deslous-Paoli, J., Landrein, S. & D’Oedenberg, M. Nutrient and oxygen exchanges at the water–sediment interface in a shellfish farming lagoon (Thau, France). J. Exp. Mar. Biol. Ecol. 205, 91–113 (1996).
Porter, E. T., Cornwell, J. C., Sanford, L. P. & Newell, R. I. E. Effect of oysters Crassostrea virginica and bottom shear velocity on benthic-pelagic coupling and estuarine water quality. Mar. Ecol. Prog. Ser. 271, 61–75 (2004).
Piehler, M. F. & Smyth, A. R. Habitat-specific distinctions in estuarine denitrification affect both ecosystem function and services. Ecosphere 2, 1–17 (2011).
Green, D. S., Boots, B. & Crowe, T. P. Effects of non-indigenous oysters on microbial diversity and ecosystem functioning. PLoS ONE 7, e48410 (2012).
Gaertner-Mazouni, N. et al. Nutrient fluxes between water column and sediments: potential influence of the pearl oyster culture. Mar. Pollut. Bull. 65, 500–505 (2012).
Smyth, A. R. et al. Assessing nitrogen dynamics throughout the estuarine landscape. Estuaries Coast. 36, 44–55 (2013).
Borenstein, M., Hedges, L. V., Higgins, J. P. T. & Rothstein, H. R. Introduction to Meta-Analysis (Wiley, 2009).
Egge, J. & Aksnes, D. Silicate as a regulating nutrient in phytoplankton competition. Mar. Ecol. Prog. Ser. 83, 281–289 (1992).
Glibert, P. M. et al. Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition, with emphasis on nitrogen-enriched conditions. Limnol. Oceanogr. 61, 165–197 (2016).
Doering, P. H. et al. Structure and function in a model coastal ecosystem: silicon, the benthos and eutrophication. Mar. Ecol. Prog. Ser. 52, 287–299 (1989).
Vandevenne, F. I. et al. Grazers: biocatalysts of terrestrial silica cycling. Proc. R. Soc. Lond. B 280, 20132083 (2013).
Newell, R. I. E. Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J. Shellfish Res. 23, 51–61 (2004).
Kana, T. M. et al. Membrane inlet mass spectrometer for rapid high-precision determination of N2, O2, and Ar in environmental water samples. Anal. Chem. 66, 4166–4170 (1994).
Nielsen, L. Denitrification in sediment determined from nitrogen isotope pairing technique. FEMS Microbiol. Lett. 86, 357–362 (1992).
Eyre, B. D., Rysgaard, S. S., Dalsgaard, T. & Christensen, P. B. Comparison of isotope pairing and N2:Ar methods for measuring sediment denitrification—assumptions, modifications, and implications. Estuaries 25, 1077–1087 (2002).
Ferguson, A. J. P. & Eyre, B. D. Seasonal discrepancies in denitrification measured by isotope pairing and N2:Ar techniques. Mar. Ecol. Prog. Ser. 350, 19–27 (2007).
Cornwell, J. C., Kemp, W. M. & Kana, T. M. Denitrification in coastal ecosystems: methods, environmental controls, and ecosystem level controls, a review. Aquat. Ecol. 33, 41–54 (1999).
Eyre, B. D. & Ferguson, A. J. P. Comparison of carbon production and decomposition, benthic nutrient fluxes and denitrification in seagrass, phytoplankton, benthic microalgae- and macroalgae-dominated warm-temperate Australian lagoons. Mar. Ecol. Prog. Ser. 229, 43–59 (2002).
Fulweiler, R. W., Nixon, S. W., Buckley, B. A. & Granger, S. L. Net sediment N2 fluxes in a coastal marine system—experimental manipulations and a conceptual model. Ecosystems 11, 1168–1180 (2008).
PAS 2050:2011 Specification for the Assessment of the Life Cycle Greenhouse Gas Emissions of Goods and Services (BSI, 2011).
PAS 2050-2:2012 Assessment of Life Cycle Greenhouse Gas Emissions - Supplementary Requirements for the Application of PAS 2050:2011 to Seafood and Other Aquatic Products (BSI, 2012).
Fodrie, F. J. et al. Oyster reefs as carbon sources and sinks. Proc. R. Soc. Lond. 284, 20170891 (2017).
Ray, N. E., O’Meara, T., Wiliamson, T., Izursa, J.-L. L. & Kangas, P. C. Consideration of carbon dioxide release during shell production in LCA of bivalves. Int. J. Life Cycle Assess. 23, 1042–1048 (2018).
Filgueira, R. et al. An integrated ecosystem approach for assessing the potential role of cultivated bivalve shells as part of the carbon trading system. Mar. Ecol. Prog. Ser. 518, 281–287 (2015).
Troost, K. Causes and effects of a highly successful marine invasion: case-study of the introduced Pacific oyster Crassostrea gigas in continental NW European estuaries. J. Sea Res. 64, 145–165 (2010).
Scanes, E. et al. Quantifying abundance and distribution of native and invasive oysters in an urbanised estuary. Aquat. Invasions 11, 425–436 (2016).
Laugen, A. T., Hollander, J., Obst, M. & Strand, Å. in Biological Invasions in Changing Ecosystems: Vectors, Ecological Impacts, Management and Predictions (ed. Canning-Clode, J.) 230–246 (De Gruyter Open, 2015).
Erbland, P. J. & Ozbay, G. A comparison of the macrofaunal communities inhabiting a Crassostrea virginica oyster reef and oyster aquaculture gear in Indian River Bay, Delaware. J. Shellfish Res. 27, 757–768 (2008).
Marenghi, F., Ozbay, G., Erbland, P. J. & Rossi-Snook, K. A comparison of the habitat value of sub-tidal and floating oyster (Crassostrea virginica) aquaculture gear with a created reef in Delaware’s Inland Bays, USA. Aquac. Int. 18, 69–81 (2010).
Tallman, J. & Forrester, G. Oyster grow-out cages function as artificial reefs for temperate fishes. Trans. Am. Fish. Soc. 136, 790–799 (2007).
Hossain, M. et al. Oyster aquaculture for coastal defense with food production in Bangladesh. Aquac. Asia 18, 15–24 (2013).
Piazza, B. P., Banks, P. D. & La Peyre, M. K. The potential for created oyster shell reefs as a sustainable shoreline protection strategy in Louisiana. Restor. Ecol. 13, 499–506 (2005).
Fisheries of the United States, 2017 (NOAA Fisheries, 2018).
Delgado, C. L. Rising consumption of meat and milk in developing countries has created a new food revolution. J. Nutr. 133, 3907–3910 (2003).
Sans, P. & Combris, P. World meat consumption patterns: an overview of the last fifty years (1961–2011). Meat Sci. 109, 106–111 (2015).
Viechtbauer, W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1–48 (2010).
Harrer, M., Cuijpers, P., Furukawa, T. & Ebert, D. Doing Meta-Analysis in R: A Hands-On Guide (2019).
Anton, A. et al. Global ecological impacts of marine exotic species. Nat. Ecol. Evol. 3, 787–800 (2019).
Harrer, M., Cuijpers, P., Furukawa, T. & Ebert, D. dmetar: companion R package for the guide ‘Doing Meta-Analysis in R’, version 0.0.9 (2019).
Rudolph, J., Frenzel, P. & Pfennig, N. Acetylene inhibition technique underestimates in situ denitrification rates in intact cores of freshwater sediment. FEMS Microbiol. Lett. 85, 101–106 (1991).
Fulweiler, R. W. et al. Examining the impact of acetylene on N-fixation and the active sediment microbial community. Front. Microbiol. 6, 418 (2015).
This work was supported by fellowship funding to N.E.R. and R.W.F. from the Frederick S. Pardee Center for the Study of the Longer Range Future at Boston University. N.E.R. also received support from the Biology Department at Boston University and R.W.F. was supported by a grant from Rhode Island Sea Grant. We thank E. Moothart and T. Condon for assistance with creating the map of study sites.
The authors declare no competing interests.
Peer review information Nature Sustainability thanks Tamar Guy-Haim and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
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Ray, N.E., Fulweiler, R.W. Meta-analysis of oyster impacts on coastal biogeochemistry. Nat Sustain 4, 261–269 (2021). https://doi.org/10.1038/s41893-020-00644-9
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