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Constraint on net primary productivity of the global ocean by Argo oxygen measurements

Abstract

The biological transformation of dissolved inorganic carbon to organic carbon during photosynthesis in the ocean, marine primary production, is a fundamental driver of biogeochemical cycling, ocean health and Earth’s climate system. The organic matter created supports oceanic food webs, including fisheries, and is an essential control on atmospheric carbon dioxide levels. Marine primary productivity is sensitive to changes due to climate forcing, but observing the response at the global scale remains a major challenge. Sparsely distributed productivity measurements are made using samples collected and analysed on research vessels. However, there are never enough ships and scientists to enable direct observations at the global scale with seasonal to annual resolution. Today, global ocean productivity is estimated using remote-sensing ocean-colour observations or general circulation models with coupled biological models that are calibrated with the sparse shipboard measurements. Here we demonstrate the measurement of gross oxygen production by photosynthesis using the diel cycle of oxygen concentration detected with the array of Biogeochemical-Argo profiling floats. The global ocean net primary productivity computed from this data is 53 Pg C y−1, which will be an important constraint on satellite and general circulation model-based estimates of the ocean productivity.

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Fig. 1: Profile locations where primary production has been determined.
Fig. 2: Northern Hemisphere (60° N to 10° N) oxygen and GOP values.
Fig. 3: Oxygen anomalies and GOP from floats near the HOT and BATS time-series stations.

Data availability

The profiling float data used in this study were obtained in December 2020 by downloading all Argo Sprof files directly from the Argo Global Data Assembly Center (ftp://usgodae.org/pub/outgoing/argo or ftp://ftp.ifremer.fr/ifremer/argo). The corresponding monthly snapshot (December 2020) of the Argo database, which contains these Sprof files in addition to all floats that do not have biogeochemical sensors, is https://doi.org/10.17882/42182#79118. The Sprof files for floats with adjusted oxygen concentrations were then merged into netCDF files for the Northern and Southern Hemispheres and used for the analyses reported here. These files are available at https://doi.org/10.5281/zenodo.4989023. Monthly satellite data were downloaded from http://www.science.oregonstate.edu/ocean.productivity/.

Code availability

Analyses were performed in Matlab. Code used in this analysis is available at https://doi.org/10.5281/zenodo.4989023.

References

  1. 1.

    Field, C., Behrenfeld, M., Randerson, J. & Falkowski, P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998).

    Article  Google Scholar 

  2. 2.

    Falkowski, P. G., Laws, E. A., Barber, R. T., & Murray, J. W. in Ocean Biogeochemistry (ed. Fasham, M. J. R.) 99–121 (Springer, 2003).

  3. 3.

    Falkowski, P. G. The role of phytoplankton photosynthesis in global biogeochemical cycles. Photosynth. Res. 39, 235–258 (1994).

    Article  Google Scholar 

  4. 4.

    Chavez, F. P., Messié, M. & Pennington, J. T. Marine primary production in relation to climate variability and change. Ann. Rev. Mar. Sci. 3, 227–260 (2011).

    Article  Google Scholar 

  5. 5.

    Ducklow, H. W., Steinberg, D. K. & Buesseler, K. O. Upper ocean carbon export and the biological pump. Oceanography 14, 50–58 (2001).

    Article  Google Scholar 

  6. 6.

    Watson, A. J. & Orr, J. C. in Ocean Biogeochemistry (ed. Fasham, M. J. R.) 123–143 (Springer, 2003).

  7. 7.

    Steinacher, M. et al. Projected 21st century decrease in marine productivity: a multi-model analysis. Biogeosciences 7, 979–1005 (2010).

    Article  Google Scholar 

  8. 8.

    Bryndum-Buchholz, A. et al. Twenty-first-century climate change impacts on marine animal biomass and ecosystem structure across ocean basins. Glob. Change Biol. 25, 459–472 (2019).

    Article  Google Scholar 

  9. 9.

    Kavanaugh, M. T. et al. ALOHA from the edge: reconciling three decades of in situ Eulerian observations and geographic variability in the North Pacific Subtropical Gyre. Front. Mar. Sci. 5, 130 (2018).

    Article  Google Scholar 

  10. 10.

    Barber, R. T. & Hilting, A. K. in Phytoplankton Productivity: Carbon Assimilation in Marine and Freshwater Ecosystems (eds Williams, P. J. L. et al.) 16–43 (Blackwell, 2002).

  11. 11.

    Steeman Nielsen, E. The use of radioactive carbon (C14) for measuring organic production in the sea. ICES J. Mar. Sci. 18, 117–140 (1952).

    Article  Google Scholar 

  12. 12.

    Marra, J. A. in Phytoplankton Productivity: Carbon Assimilation in Marine and Freshwater Ecosystems (eds Williams, P. J. L. et al.) 78–108 (Blackwell, 2002).

  13. 13.

    Marra, J. Net and gross productivity: weighing in with 14C. Aquatic Microb. Ecol. 56, 123–131 (2009).

    Article  Google Scholar 

  14. 14.

    Fitzwater, S. E., Knauer, G. A. & Martin, J. H. Metal contamination and its effect on primary production measurements. Limnol. Oceanogr. 27, 544–551 (1982).

    Article  Google Scholar 

  15. 15.

    Koblentz-Mischke, O. J., Volkovinsky, V. V. & Kabanova, J. G. in Scientific Exploration of the South Pacific (ed. Wooster, W.) 183–192 (National Academies Press, 1970).

  16. 16.

    Luz, B. & Barkan, E. Assessment of oceanic productivity with the triple-isotope composition of dissolved oxygen. Science 288, 2028–2031 (2000).

    Article  Google Scholar 

  17. 17.

    Juranek, L. W. & Quay, P. D. Using triple isotopes of dissolved oxygen to evaluate global marine productivity. Annu. Rev. Mar. Sci. 5, 503–524 (2013).

    Article  Google Scholar 

  18. 18.

    Carr, M. E. et al. A comparison of global estimates of marine primary production from ocean color. Deep-Sea Res. 2 53, 741–770 (2006).

    Google Scholar 

  19. 19.

    Lee, Z., Marra, J., Perry, M. J. & Kahru, M. Estimating oceanic primary productivity from ocean color remote sensing: a strategic assessment. J. Mar. Syst. 149, 50–59 (2015).

    Article  Google Scholar 

  20. 20.

    Antoine, D., André, J.-M. & Morel, A. Oceanic primary production: 2. Estimation at global scale from satellite (coastal zone color scanner) chlorophyll. Glob. Biogeochem. Cycles 10, 57–69 (1996).

    Article  Google Scholar 

  21. 21.

    Behrenfeld, M. J. & Falkowski, P. G. Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol. Oceanogr. 42, 1–20 (1997).

    Article  Google Scholar 

  22. 22.

    Buitenhuis, E. T., Hashioka, T. & Quéré, C. L. Combined constraints on global ocean primary production using observations and models. Glob. Biogeochem. Cycles 27, 847–858 (2013).

    Article  Google Scholar 

  23. 23.

    Gregg, W. W. & Rousseaux, C. S. Global ocean primary production trends in the modern ocean color satellite record (1998−2015). Environ. Res. Lett. 14, 124011 (2019).

    Article  Google Scholar 

  24. 24.

    Westberry, T. K., Behrenfeld, M. J., Siegel, D. A. & Boss, E. Carbon-based primary productivity modeling with vertically resolved photoacclimation. Glob. Biogeochem. Cycles 22, GB2024 (2008).

    Article  Google Scholar 

  25. 25.

    Saba, V. S. et al. The challenges of modeling depth-integrated marine primary productivity over multiple decades: a case study at BATS and HOT. Glob. Biogeochem. Cycles 24, GB3020 (2010).

    Article  Google Scholar 

  26. 26.

    Behrenfeld, M. J. et al. Revaluating ocean warming impacts on global phytoplankton. Nat. Clim. Change 6, 323–330 (2016).

    Article  Google Scholar 

  27. 27.

    Johnson, K. S. Simultaneous measurements of nitrate, oxygen, and carbon dioxide on oceanographic moorings: observing the Redfield ratio in real time. Limnol. Oceanogr. 55, 615–627 (2010).

    Article  Google Scholar 

  28. 28.

    Nicholson, D. P., Wilson, S. T., Doney, S. C. & Karl, D. M. Quantifying subtropical North Pacific gyre mixed layer primary productivity from Seaglider observations of diel oxygen cycles. Geophys. Res. Lett. 42, 4032–4039 (2015).

    Article  Google Scholar 

  29. 29.

    Barone, B., Nicholson, D., Ferrón, S., Firing, E. & Karl, D. The estimation of gross oxygen production and community respiration from autonomous time-series measurements in the oligotrophic ocean. Limnol. Oceanogr. Methods 17, 650–664 (2019).

    Article  Google Scholar 

  30. 30.

    Henderikx Freitas, F., White, A. E. & Quay, P. D. Diel measurements of oxygen- and carbon-based ocean metabolism across a trophic gradient in the North Pacific. Glob. Biogeochem. Cycles 34, e2019GB006518 (2020).

    Article  Google Scholar 

  31. 31.

    Gordon, C., Fennel, K., Richards, C., Shay, L. K. & Brewster, J. K. Can ocean community production and respiration be determined by measuring high-frequency oxygen profiles from autonomous floats? Biogeosciences 17, 4119–4134 (2020).

    Article  Google Scholar 

  32. 32.

    Claustre, H., Johnson, K. S. & Takeshita, Y. Observing the global ocean with Biogeochemical-Argo. Annu. Rev. Mar. Sci. 12, 23–48 (2020).

    Article  Google Scholar 

  33. 33.

    Gille, S. T. Diurnal variability of upper ocean temperatures from microwave satellite measurements and Argo profiles. J. Geophys. Res. 117, C11027 (2012).

    Google Scholar 

  34. 34.

    Juranek, L. W. & Quay, P. D. In vitro and in situ gross primary and net community production in the North Pacific subtropical gyre using labeled and natural abundance isotopes of dissolved O2. Glob. Biogeochem. Cycles 19, GB3009 (2005).

    Article  Google Scholar 

  35. 35.

    Quay, P. D., Peacock, C., Bjorkman, K. & Karl, D. M. Measuring primary production rates in the ocean: enigmatic results between incubation and non-incubation methods at station ALOHA. Glob. Biogeochem. Cycles 24, GB3014 (2010).

    Article  Google Scholar 

  36. 36.

    Ferrón, S., Barone, B., Church, M. J., White, A. E. & Karl, D. M. Euphotic zone metabolism in the North Pacific subtropical gyre based on oxygen dynamics. Global Biogeochem. Cycles 35, e2020GB00674 (2021).

    Article  Google Scholar 

  37. 37.

    Church, M. J., Lomas, M. W. & Muller-Karger, F. Sea change: charting the course for biogeochemical time-series research in a new millennium. Deep Sea Res. 2 93, 2–15 (2013).

    Article  Google Scholar 

  38. 38.

    Fawcett, S. E., Johnson, K. S., Riser, S. C., Van Oostende, N. & Sigman, D. M. Low-nutrient organic matter in the Sargasso Sea thermocline: a hypothesis for its role, identity, and carbon cycle implications. Mar. Chem. 20, 108–123 (2018).

    Article  Google Scholar 

  39. 39.

    Huang, Y., Nicholson, D., Huang, B. & Cassar, N. Global estimates of marine gross primary production based on machine-learning upscaling of field observations. Glob. Biogeochem. Cycles 35, GB006718 (2021).

  40. 40.

    Silsbe, G. M., Behrenfeld, M. J., Halsey, K. H., Milligan, A. J. & Westberry, T. K. The CAFE model: a net production model for global ocean phytoplankton. Glob. Biogeochem. Cycles 30, 1756–1777 (2016).

    Article  Google Scholar 

  41. 41.

    Johnson, K. S. & Claustre, H. The Scientific Rationale, Design and Implementation Plan for a Biogeochemical-Argo Float Array (Ifremer, 2016); https://doi.org/10.13155/46601

  42. 42.

    Kahru, M. Ocean productivity from space: commentary. Glob. Biogeochem. Cycles 31, 214–216 (2017).

    Article  Google Scholar 

  43. 43.

    Bittig, H., Wong, A. & Plant, J. BGC-Argo Synthetic Profile File Processing and Format On Coriolis GDAC Version 1.21 (Ifremer, 2021); https://doi.org/10.13155/55637

  44. 44.

    Takeshita, Y. et al. A climatology-based quality control procedure for profiling float oxygen data. J. Geophys. Res. Oceans 118, 5640–5650 (2013).

    Article  Google Scholar 

  45. 45.

    Johnson, K. S., Plant, J. N., Riser, S. C. & Gilbert, D. Air oxygen calibration of oxygen optodes on a profiling float array. J. Atmos. Ocean. Technol. 32, 2160–2172 (2015).

    Article  Google Scholar 

  46. 46.

    Bittig, H. C. et al. Oxygen optode sensors: principle, characterization, calibration, and application in the ocean. Front. Mar. Sci. 4, 429 (2018).

    Article  Google Scholar 

  47. 47.

    Johnson, K. S. et al. Biogeochemical sensor performance in the SOCCOM profiling float array. J. Geophys. Res. 122, 6416–6436 (2017).

    Article  Google Scholar 

  48. 48.

    Wanninkhof, R. Relationship between wind speed and gas exchange over the ocean revisited. Limnol. Oceanogr. Methods 12, 351–362 (2014).

    Article  Google Scholar 

  49. 49.

    Riser, S. C. & Johnson, K. S. Net production of oxygen in the subtropical ocean. Nature 451, 323–325 (2008).

    Article  Google Scholar 

  50. 50.

    Emerson, S. Annual net community production and the biological carbon flux in the ocean. Global Biogeochem. Cycles 28, 14–28 (2014).

    Article  Google Scholar 

  51. 51.

    Schmechtig, C., Poteau, A., Claustre, H., D’Ortenzio, F. & Boss, E. Processing Bio-Argo Chlorophyll-a Concentration at the DAC Level (Ifremer, 2015); https://doi.org/10.13155/39468

  52. 52.

    Roesler, C. et al. Recommendations for obtaining unbiased chlorophyll estimates from in situ chlorophyll fluorometers: a global analysis of WET Labs ECO sensors. Limnol. Oceanogr. Methods 15, 572–585 (2017).

    Article  Google Scholar 

  53. 53.

    Briggs, N., Dall’Olmo, G. & Claustre, H. Major role of particle fragmentation in regulating biological sequestration of CO2 by the oceans. Science 367, 791–793 (2020).

    Article  Google Scholar 

  54. 54.

    Buesseler, K. O., Boyd, P. W., Black, E. E. & Siegel, D. A. Metrics that matter for assessing the ocean biological carbon pump. Proc. Natl Acad. Sci. USA 117, 9679–9687 (2020).

    Article  Google Scholar 

  55. 55.

    Morel, A. et al. Examining the consistency of products derived from various ocean color sensors in open ocean (Case 1) waters in the perspective of a multi-sensor approach. Remote Sens. Environ. 111, 69–88 (2007).

    Article  Google Scholar 

  56. 56.

    Oregon State University Ocean Productivity (Ocean Productivity, 2021); http://www.science.oregonstate.edu/ocean.productivity/

  57. 57.

    National Geophysical Data Center ETOPO5: Data Announcement 88-MGG-02, Digital Relief of the Surface of the Earth (NOAA, 1988); https://doi.org/10.7289/V5C8276M

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Acknowledgements

This work was supported by the Global Ocean Biogeochemical Array project (NSF OCE-1946578; publication no. 1), the Southern Ocean Carbon and Climate Observations and Modeling project (NSF PLR-1425989 and OPP-1936222) and the David and Lucile Packard Foundation. Profiling floats in the equatorial Pacific were supported by NOAA under grant NA16OAR4310161 to the University of Washington. We thank J. Long for assistance with the satellite data, and T. Maurer and J. Plant for processing data and assistance with coding. S. Riser and D. Swift prepared many of the profiling floats whose data were used in this analysis. We thank the Hawaii Ocean Time-series and Bermuda Atlantic Time-series Station programmes for making their data easily accessible. The float data were collected and made freely available by the International Argo Program and the national programmes that contribute to it (https://argo.ucsd.edu, https://www.ocean-ops.org). The Argo Program is part of the Global Ocean Observing System.

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Authors

Contributions

K.S.J. conceived the study, performed final data analysis and drafted the initial manuscript. M.B.B. developed analytical methods and performed exploratory data analyses and contributed to the interpretation of results and writing of the manuscript.

Corresponding author

Correspondence to Kenneth S. Johnson.

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The authors declare no competing interests.

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Peer review information Nature Geoscience thanks Benedetto Barone and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Primary Handling Editor: Xujia Jiang.

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

Extended data

Extended Data Fig. 1 Profiling float oxygen data at surface versus time.

Extended Data Figure 1. Profiling float oxygen data at surface versus time. a, Dissolved oxygen and b, Oxygen Anomaly = Oxygen – Oxygen Saturation in the upper 10 m for all adjusted oxygen data with quality flag = 1 (good data) in the Argo Global Data Assembly Center, except for 9 floats listed in Extended Data Table 1.

Extended Data Fig. 2 Global (60°N to 60°S) oxygen and GOP values for the years 2016 through 2020.

Global (60°N to 60°S) oxygen and GOP values for the years 2016 through 2020. a, Mean oxygen anomaly in the upper 20 m from each profile with acceptable cycle timing versus local hour of the day. b, Mean oxygen anomaly in each hourly interval and the least squares fit of equation 2 to the data shown in a) with GOP = 2.1 ± 0.4 (1 Std Error) mmol O2 m−3 d−1.

Extended Data Fig. 3 Annual mean NPP rates from 2010 through 2020 in each 10° latitude band from 50°N to 50°S.

Annual mean NPP rates from 2010 through 2020 in each 10° latitude band from 50°N to 50°S. a, Float and satellite NPP rates versus latitude. b, Satellite NPP rates in each 10° latitude band for each model versus float NPP rates. Satellite NPP models include VGPM21, CBPM24, and CAFE40. All values from Table 1.

Extended Data Table 1 WMO numbers of floats with inconsistent oxygen concentrations and not used in this analysis

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Johnson, K.S., Bif, M.B. Constraint on net primary productivity of the global ocean by Argo oxygen measurements. Nat. Geosci. 14, 769–774 (2021). https://doi.org/10.1038/s41561-021-00807-z

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