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Oxygen priming induced by elevated CO2 reduces carbon accumulation and methane emissions in coastal wetlands

Nature Geoscience volume 16, pages 63–68 (2023)Cite this article

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Abstract

Warming temperatures and elevated CO2 are inextricably linked global change phenomena, but they are rarely manipulated together in field experiments. As a result, ecosystem-level responses to these interacting facets of global change remain poorly understood. Here we report on a four-year field manipulation of warming and elevated CO2 in a coastal wetland. Contrary to our expectations, elevated CO2 combined with warming reduced the rate of carbon accumulation due to increases in plant-mediated oxygen flux that stimulated aerobic decomposition via oxygen priming. Evidence supporting this interpretation includes an increase in soil redox potential and a decrease in the nominal oxidation state of the dissolved organic carbon pool. While warming alone stimulated methane (CH4) emissions, we found that elevated CO2 combined with warming reduced net CH4 flux due to plant–microbe feedbacks. Together, these results demonstrate that ecosystem responses to interacting facets of global change are mediated by plant traits that regulate the redox state of the soil environment. Thus, plant responses are critical for predicting future ecosystem survival and climate feedbacks.

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Fig. 1: Fine-root productivity in ambient and warmed plots with and without elevated CO2.
Fig. 2: Automated redox data in warmed plots with and without elevated CO2 from April 2020 to December 2020.
Fig. 3: Root productivity versus mean NOSC for porewater DOC.
Fig. 4: Average rate of change in marsh surface elevation and carbon accumulation from January 2017 to August 2020.
Fig. 5: Summer CH4 emissions in ambient and warmed plots with and without elevated CO2.
Fig. 6: CO2-equivalent greenhouse gas emissions by treatment averaged across the four years of the fully crossed experiment.

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Data availability

The data that support the findings of this study are available from the corresponding authors upon request and in the Smithsonian Institution figshare repository (https://smithsonian.figshare.com) under https://doi.org/10.25573/serc.21263328.

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Acknowledgements

We thank G. Peresta for maintaining the field experiment and S. Kent, T. Messerschmidt, E. Herbert and D. Walters for assisting with field measurements. Funding for this project was provided by the US Department of Energy, Office of Science, Office of Biological and Environmental Research, Environmental System Science programme under award numbers DE-SC0014413 to J.P.M., M.L.K. and R.L.R. and DE-SC0019110 and DE-SC0021112 to J.P.M., G.L.N., M.L.K. and R.L.R.; the National Science Foundation Long-Term Research in Environmental Biology Program under award numbers DEB-0950080, DEB-1457100 and DEB-1557009 to J.P.M. and DEB-2051343 to J.P.M. and G.L.N.; and the Smithsonian Institution to J.P.M., G.L.N. and R.L.R. A portion of the research was performed using EMSL, a DOE Office of Science user facility sponsored by the Office of Biological and Environmental Research, under user project 50205 to G.L.N. and J.P.M.

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Authors and Affiliations

  1. Smithsonian Environmental Research Center, Edgewater, MD, USA

    Genevieve L. Noyce, Roy L. Rich & J. Patrick Megonigal

  2. Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, VA, USA

    Alexander J. Smith & Matthew L. Kirwan

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  1. Genevieve L. Noyce
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Contributions

J.P.M., R.L.R., G.L.N. and M.L.K. designed the original experiment, R.L.R. designed the feedback-controlled heating system and G.L.N. and R.L.R. designed the redox measurement system. G.L.N. collected and analysed all vegetation and biogeochemical data and wrote the initial manuscript. A.J.S. provided SET data and analysis. All authors contributed to interpreting results and editing the manuscript.

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Correspondence to Genevieve L. Noyce or J. Patrick Megonigal.

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Nature Geoscience thanks Jorge Villa and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Primary Handling Editor: Xujia Jiang, in collaboration with the Nature Geoscience team.

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Extended data

Extended Data Fig. 1 Annual Schoenoplectus americanus stem density in all treatments from 2017 to 2020.

Points are means of triplicate plots. Error bars are standard error across treatment replicates (n = 3). Temperature treatments are ambient (Amb) or +5.1 °C above ambient (+5.1 °C) either alone or crossed with elevated CO2 (+eCO2).

Extended Data Fig. 2 Mean redox potential measured at 5 cm depth in spring 2022 (Apr through Jun).

Error bars are standard error across treatment replicates (n = 3). Temperature treatments are ambient (Amb) or +5.1 °C above ambient (+5.1 °C) either alone or crossed with elevated CO2 (+eCO2).

Extended Data Fig. 3 Mean porewater CH4 (10–120 cm) from all treatments.

Samples were collected in May, Jun, and Sep. Brackets above the paired bars show the P values for the differences between treatments based on Tukey’s HSD test. Elevated CO2 significantly reduced porewater CH4 in both ambient and warmed treatments. Error bars are standard error across treatment replicates (n = 3). Temperature treatments are ambient (Amb) or +5.1 °C above ambient (+5.1 °C) either alone or crossed with elevated CO2 (+eCO2).

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Supplementary Information

Supplementary Table 1 and Figs. 1–3.

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Noyce, G.L., Smith, A.J., Kirwan, M.L. et al. Oxygen priming induced by elevated CO2 reduces carbon accumulation and methane emissions in coastal wetlands. Nat. Geosci. 16, 63–68 (2023). https://doi.org/10.1038/s41561-022-01070-6

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