Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Analysis
  • Published:

Meta-analysis of oyster impacts on coastal biogeochemistry

Nature Sustainability volume 4, pages 261–269 (2021)Cite this article

Subjects

Abstract

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Location of studies used in this meta-analysis.
Fig. 2: Effect size of oysters on nutrient fluxes.
Fig. 3: Effect size of oysters on N2 flux.
Fig. 4: Transport of nitrogen through coastal ecosystems with oyster habitats.
Fig. 5: Effect size of oysters on GHG fluxes.

Similar content being viewed by others

Data availability

All data used in this study is available in the Figshare repository under the access number https://doi.org/10.6084/m9.figshare.12488753.

Code availability

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).

References

  1. Factsheet: People and Oceans (United Nations, 2017).

  2. Vitousek, P. M. et al. Human alteration of the global nitrogen cycle: sources and consequences. Ecol. Appl. 7, 737–750 (1997).

    Google Scholar 

  3. Galloway, J. N. et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892 (2008).

    CAS  Google Scholar 

  4. Canfield, D. E., Glazer, A. N. & Falkowski, P. G. The evolution and future of Earth’s nitrogen cycle. Science 330, 192–196 (2010).

    CAS  Google Scholar 

  5. Ryther, J. & Dunstan, W. Nitrogen, phosphorus, and eutrophication in the coastal marine environment. Science 171, 1008–1013 (1971).

    CAS  Google Scholar 

  6. Conley, D. J. et al. Controlling eutrophication: nitrogen and phosphorus. Science 323, 1014–1015 (2009).

    CAS  Google Scholar 

  7. 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).

    Google Scholar 

  8. Carey, J. C. & Fulweiler, R. W. Human activities directly alter watershed dissolved silica fluxes. Biogeochemistry 111, 125–138 (2012).

    Google Scholar 

  9. Turner, R. E. et al. Fluctuating silicate:nitrate ratios and coastal plankton food webs. Proc. Natl Acad. Sci. USA 95, 13048–13051 (1998).

    CAS  Google Scholar 

  10. Nixon, S. W. Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41, 199–219 (1995).

    Google Scholar 

  11. 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).

    CAS  Google Scholar 

  12. Mackenzie, C. L. Causes underlying the historical decline in eastern oyster (Crassostrea virginica Gmelin, 1791) landings. J. Shellfish Res. 26, 927–938 (2007).

    Google Scholar 

  13. 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).

    Google Scholar 

  14. Rick, T. et al. Millenial-scale sustainability of the Chesapeake Bay Native American oyster fishery. Proc. Natl Acad. Sci. USA 113, 6568–6573 (2016).

    CAS  Google Scholar 

  15. Beck, M. W. et al. Oyster reefs at risk and recommendations for conservation, restoration, and management. BioScience 61, 107–116 (2011).

    Google Scholar 

  16. 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).

    Google Scholar 

  17. Transforming Our World: The 2030 Agenda for Sustainable Development (United Nations, 2015).

  18. 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).

  19. Kellogg, M. L. et al. Use of oysters to mitigate eutrophication in coastal waters. Estuar. Coast. Shelf Sci. 151, 156–168 (2014).

    CAS  Google Scholar 

  20. 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).

    CAS  Google Scholar 

  21. 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).

    Google Scholar 

  22. 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).

    Google Scholar 

  23. 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).

    Google Scholar 

  24. Rowe, G., Clifford, C. & Smith, K. Jr Benthic nutrient regeneration and its coupling to primary productivity in coastal waters. Nature 255, 215–217 (1975).

    CAS  Google Scholar 

  25. Seitzinger, S. P. Denitrification in freshwater and coastal marine systems: ecological and geochemical significance. Limnol. Oceanogr. 334, 702–724 (1988).

    Google Scholar 

  26. 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).

    CAS  Google Scholar 

  27. Duarte, C. M. et al. Rebuilding marine life. Nature 580, 39–51 (2020).

    CAS  Google Scholar 

  28. The State of World Fisheries and Aquaculture 2018: Meeting the Sustainable Development Goals (FAO, 2018).

  29. Gentry, R. R. et al. Mapping the global potential for marine aquaculture. Nat. Ecol. Evol. 1, 1317–1324 (2017).

    Google Scholar 

  30. 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).

    Google Scholar 

  31. 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).

    Google Scholar 

  32. 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).

    Google Scholar 

  33. 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).

    Google Scholar 

  34. 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).

    Google Scholar 

  35. 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).

    Google Scholar 

  36. Jackson, M. Characterization of Oyster-Associated Biogeochemical Processes in Oyster Restoration and Aquaculture. PhD dissertation, Univ. Maryland (2019).

  37. 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).

    CAS  Google Scholar 

  38. 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).

    CAS  Google Scholar 

  39. 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).

    CAS  Google Scholar 

  40. 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).

    CAS  Google Scholar 

  41. 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).

    Google Scholar 

  42. 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).

    Google Scholar 

  43. 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).

    Google Scholar 

  44. McCarthy, G., Ray, N. E. & Fulweiler, R. W. Greenhouse gas emissions from native and non-native oysters. Front. Environ. Sci. 7, 194 (2019).

    Google Scholar 

  45. 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).

    CAS  Google Scholar 

  46. 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).

    CAS  Google Scholar 

  47. 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).

    CAS  Google Scholar 

  48. 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).

    CAS  Google Scholar 

  49. 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).

    Google Scholar 

  50. 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).

    CAS  Google Scholar 

  51. 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).

    CAS  Google Scholar 

  52. 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).

    CAS  Google Scholar 

  53. 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).

    Google Scholar 

  54. 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).

    Google Scholar 

  55. 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).

    CAS  Google Scholar 

  56. 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).

    Google Scholar 

  57. 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).

    CAS  Google Scholar 

  58. 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).

    CAS  Google Scholar 

  59. Onorevole, K. M., Thompson, S. P. & Piehler, M. F. Living shorelines enhance nitrogen removal capacity over time. Ecol. Eng. 120, 238–248 (2018).

    Google Scholar 

  60. Lunstrum, A., McGlathery, K. & Smyth, A. Oyster (Crassostrea virginica) aquaculture shifts sediment nitrogen processes toward mineralization over denitrification. Estuaries Coast. 41, 1130–1146 (2018).

    CAS  Google Scholar 

  61. 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).

    CAS  Google Scholar 

  62. Ray, N. E., Al-Haj, A. & Fulweiler, R. W. Sediment biogeochemistry along an oyster aquaculture chronosequence. Mar. Ecol. Prog. Ser. 646, 13–27 (2020).

    CAS  Google Scholar 

  63. Hassett, M. The Influence of Eastern Oyster (Crassostrea virginica) Reef Restoration on Nitrogen Cycling in a Eutrophic Estuary. MSc thesis, Loyola Univ. Chicago (2015).

  64. Vieillard, A. M. Impacts of New England Oyster Aquaculture on Sediment Nitrogen Cycling: Implications for Nitrogen Removal and Retention. MSc thesis, Univ. Connecticut (2017).

  65. Boucher-Rodoni, R. & Boucher, G. In situ study of the effect of oyster biomass on benthic metabolic exchange rates. Hydrobiologia 206, 115–123 (1990).

    CAS  Google Scholar 

  66. 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).

    Google Scholar 

  67. 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).

    Google Scholar 

  68. Piehler, M. F. & Smyth, A. R. Habitat-specific distinctions in estuarine denitrification affect both ecosystem function and services. Ecosphere 2, 1–17 (2011).

    Google Scholar 

  69. Green, D. S., Boots, B. & Crowe, T. P. Effects of non-indigenous oysters on microbial diversity and ecosystem functioning. PLoS ONE 7, e48410 (2012).

    CAS  Google Scholar 

  70. 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).

    CAS  Google Scholar 

  71. Smyth, A. R. et al. Assessing nitrogen dynamics throughout the estuarine landscape. Estuaries Coast. 36, 44–55 (2013).

    CAS  Google Scholar 

  72. Borenstein, M., Hedges, L. V., Higgins, J. P. T. & Rothstein, H. R. Introduction to Meta-Analysis (Wiley, 2009).

  73. Egge, J. & Aksnes, D. Silicate as a regulating nutrient in phytoplankton competition. Mar. Ecol. Prog. Ser. 83, 281–289 (1992).

    CAS  Google Scholar 

  74. 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).

    Google Scholar 

  75. 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).

    Google Scholar 

  76. Vandevenne, F. I. et al. Grazers: biocatalysts of terrestrial silica cycling. Proc. R. Soc. Lond. B 280, 20132083 (2013).

    Google Scholar 

  77. 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).

    Google Scholar 

  78. 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).

    CAS  Google Scholar 

  79. Nielsen, L. Denitrification in sediment determined from nitrogen isotope pairing technique. FEMS Microbiol. Lett. 86, 357–362 (1992).

    CAS  Google Scholar 

  80. 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).

    CAS  Google Scholar 

  81. 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).

    CAS  Google Scholar 

  82. 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).

    CAS  Google Scholar 

  83. 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).

    CAS  Google Scholar 

  84. 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).

    CAS  Google Scholar 

  85. PAS 2050:2011 Specification for the Assessment of the Life Cycle Greenhouse Gas Emissions of Goods and Services (BSI, 2011).

  86. 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).

  87. Fodrie, F. J. et al. Oyster reefs as carbon sources and sinks. Proc. R. Soc. Lond. 284, 20170891 (2017).

    Google Scholar 

  88. 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).

    CAS  Google Scholar 

  89. 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).

    Google Scholar 

  90. 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).

    Google Scholar 

  91. Scanes, E. et al. Quantifying abundance and distribution of native and invasive oysters in an urbanised estuary. Aquat. Invasions 11, 425–436 (2016).

    Google Scholar 

  92. 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).

  93. 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).

    Google Scholar 

  94. 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).

    Google Scholar 

  95. Tallman, J. & Forrester, G. Oyster grow-out cages function as artificial reefs for temperate fishes. Trans. Am. Fish. Soc. 136, 790–799 (2007).

    Google Scholar 

  96. Hossain, M. et al. Oyster aquaculture for coastal defense with food production in Bangladesh. Aquac. Asia 18, 15–24 (2013).

    Google Scholar 

  97. 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).

    Google Scholar 

  98. Fisheries of the United States, 2017 (NOAA Fisheries, 2018).

  99. Delgado, C. L. Rising consumption of meat and milk in developing countries has created a new food revolution. J. Nutr. 133, 3907–3910 (2003).

    Google Scholar 

  100. Sans, P. & Combris, P. World meat consumption patterns: an overview of the last fifty years (1961–2011). Meat Sci. 109, 106–111 (2015).

    CAS  Google Scholar 

  101. Viechtbauer, W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1–48 (2010).

    Google Scholar 

  102. Harrer, M., Cuijpers, P., Furukawa, T. & Ebert, D. Doing Meta-Analysis in R: A Hands-On Guide (2019).

  103. Anton, A. et al. Global ecological impacts of marine exotic species. Nat. Ecol. Evol. 3, 787–800 (2019).

    Google Scholar 

  104. 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).

  105. 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).

    CAS  Google Scholar 

  106. Fulweiler, R. W. et al. Examining the impact of acetylene on N-fixation and the active sediment microbial community. Front. Microbiol. 6, 418 (2015).

    Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Department of Biology, Boston University, Boston, MA, USA

    Nicholas E. Ray & Robinson W. Fulweiler

  2. Department of Earth and Environment, Boston University, Boston, MA, USA

    Robinson W. Fulweiler

Authors
  1. Nicholas E. Ray
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robinson W. Fulweiler
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

N.E.R. and R.W.F. conceived and designed the study. N.E.R. constructed the dataset and performed statistical analyses. Both authors interpreted the results. N.E.R. wrote the manuscript with significant contribution from R.W.F. N.E.R. and R.W.F. edited the manuscript. Both authors take full responsibility for the contents of the manuscript.

Corresponding author

Correspondence to Nicholas E. Ray.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Fig. 1, list of studies included in meta-analysis, and Supplementary Tables 1–12.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41893-020-00644-9

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology