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.

  • Review Article
  • Published:

The role of biota in the Southern Ocean carbon cycle

Nature Reviews Earth & Environment (2024)Cite this article

Subjects

Abstract

The Southern Ocean, although relatively understudied owing to its harsh environment and geographical isolation, has been shown to contribute substantially to processes that drive the global carbon cycle. For example, phytoplankton photosynthesis transforms carbon dioxide into new particles and dissolved organic carbon. The magnitude of these transformations depends on the unique oceanographic and biogeochemical properties of the Southern Ocean. In this Review, we synthesize observations of biologically mediated carbon flows derived from the expanded observational network provided by remote-sensing and autonomous platforms. These observations reveal patterns in the magnitude of net primary production, including under-ice blooms and subsurface chlorophyll maxima. Basin-scale annual estimates of the planktonic contribution to the Southern Ocean carbon cycle can also be calculated, indicating that the export of biogenic particles and dissolved organic carbon to depth accounts for 20–30% (around 3 Gt yr–1) of the global export flux. This flux partially compensates for carbon dioxide outgassing following upwelling, making the Southern Ocean a 0.4–0.7 Gt C yr–1 sink. This export flux is surprisingly large given that phytoplankton are iron-limited with low productivity in more than 80% of the Southern Ocean. Solving such enigmas will require the development of four-dimensional regional observatories and the use of data-assimilation and machine-learning techniques to integrate datasets.

Key points

  • Increasing coverage from a suite of observations from autonomous platforms will reduce uncertainties on estimates of key processes in the regional carbon cycle that determine the magnitude of the Southern Ocean carbon sink.

  • Episodic storms enhance chlorophyll stocks, presumably owing to enhanced iron supply from depth, but also drive concurrent carbon dioxide outgassing, with unknown cumulative effects on the regional carbon cycle.

  • The influence of climate change on the Southern Ocean and Antarctica is expected to alter the partitioning of basin-scale net primary production between open water, sea ice and under ice.

  • Observations from profiling robotic floats are providing important insights into how the fate of phytoplankton carbon drives regional patterns in export flux in the ocean’s interior over multiple annual cycles.

  • The inability to remotely measure dissolved iron or dissolved organic carbon concentrations makes it difficult to understand pivotal processes in the Southern Ocean carbon cycle.

  • Models using data assimilation are already providing promising guidelines on how to deploy autonomous platforms to address key questions around the regional carbon cycle.

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: The three eras of oceanographic investigation.
Fig. 2: Processes and timescale of iron supply in the Southern Ocean.
Fig. 3: Distribution of annual net primary production in the Southern Ocean.
Fig. 4: The transfer of Southern Ocean productivity to grazers.
Fig. 5: The influence of Southern Ocean productivity on dissolved organic carbon release and downward particle export flux.
Fig. 6: Southern Ocean circulation and biological processes driving the carbon cycle.
Fig. 7: Integrating measured and modelled biogeochemical properties.

Similar content being viewed by others

Data availability

The data for the FishMIP marine ecosystem models and the two Earth system models, IPSL-CM6A-LR and GFDL-ESM4, used to make Fig. 4c and d and Supplementary Figs. 1–4, are available through the ISIMIP repository (https://data.isimip.org/; https://doi.org/10.48364/ISIMIP.575744.4).

Code availability

The code used to produce Fig. 4, and Supplementary Figs. 1–4 is available at https://github.com/Fish-MIP/Extract_SouthernOcean.

References

  1. Talley, L. Closure of the global overturning circulation through the Indian, Pacific, and Southern oceans: schematics and transports. Oceanography 26, 80–97 (2013).

    Article  Google Scholar 

  2. Gruber, N. et al. Trends and variability in the ocean carbon sink. Nat. Rev. Earth Environ. 4, 119–134 (2023).

    Article  CAS  Google Scholar 

  3. Hauck, J. et al. The Southern Ocean Carbon Cycle 1985–2018: mean, seasonal cycle, trends, and storage. Glob. Biogeochem. Cycles 37, e2023GB007848 (2023).

    Article  CAS  Google Scholar 

  4. Schlitzer, R. Carbon export fluxes in the Southern Ocean: results from inverse modeling and comparison with satellite-based estimates. Deep. Sea Res. II 49, 1623–1644 (2002).

    Article  CAS  Google Scholar 

  5. DeVries, T. & Weber, T. The export and fate of organic matter in the ocean: new constraints from combining satellite and oceanographic tracer observations. Glob. Biogeochem. Cycles 31, 535–555 (2017).

    Article  CAS  Google Scholar 

  6. Nissen, C. & Vogt, M. Factors controlling the competition between Phaeocystis and diatoms in the Southern Ocean and implications for carbon export fluxes. Biogeosciences 18, 251–283 (2021).

    Article  CAS  Google Scholar 

  7. Marinov, I., Gnanadesikan, A., Toggweiler, J. R. & Sarmiento, J. L. The Southern Ocean biogeochemical divide. Nature 441, 964–967 (2006).

    Article  CAS  Google Scholar 

  8. Landschützer, P. et al. The reinvigoration of the Southern Ocean carbon sink. Science 349, 1221–1224 (2015).

    Article  Google Scholar 

  9. Le Quéré, C. et al. Saturation of the Southern Ocean CO2 sink due to recent climate change. Science 316, 1735–1738 (2007).

    Article  Google Scholar 

  10. Sarmiento, J. L., Gruber, N., Brzezinski, M. A. & Dunne, J. P. High-latitude controls of thermocline nutrients and low latitude biological productivity. Nature 427, 56–60 (2004).

    Article  CAS  Google Scholar 

  11. El-Sayed, S. Z. Primary productivity and estimates of potential yields of the Southern Ocean. In Polar Research (Routledge, 1978).

  12. Holm-Hansen, O., EI-Sayed, S., Franchesini, G. A. & Cuhel, R. L. Primary production and the factors controlling phytoplankton growth in the Antarctic seas. In Proceedings of SCAR Symposium in Antarctic Biology (ed. Llano, G. A.) 11–50 (Wiley, 1977).

  13. Smith, W. O., Keene, N. K. & Comiso, J. C. Interannual variability in estimated primary productivity of the Antarctic marginal ice zone. In Antarctic Ocean and Resources Variability (ed. Sahrhage, D.) 131–139 (Springer, 1988).

  14. Smith, W. O. & Nelson, D. M. Importance of ice edge phytoplankton production in the Southern Ocean. BioScience 36, 251–257 (1986).

    Article  CAS  Google Scholar 

  15. Arrigo, K. R., Van Dijken, G. L. & Bushinsky, S. Primary production in the Southern Ocean, 1997–2006. J. Geophys. Res. 113, C08004 (2008).

    Google Scholar 

  16. Arrigo, K. R., Worthen, D., Schnell, A. & Lizotte, M. P. Primary production in Southern Ocean waters. J. Geophys. Res. Ocean. 103, 15587–15600 (1998).

    Article  Google Scholar 

  17. Moore, J. K. & Abbott, M. R. Phytoplankton chlorophyll distributions and primary production in the Southern Ocean. J. Geophys. Res. Ocean. 105, 28709–28722 (2000).

    Article  CAS  Google Scholar 

  18. Sarmiento, J. L. et al. The Southern Ocean carbon and climate observations and modeling (SOCCOM) project: a review. Prog. Oceanogr. 219, 103130 (2023).

    Article  Google Scholar 

  19. Gray, A. R. The four-dimensional carbon cycle of the Southern Ocean. Annu. Rev. Mar. Sci. 16, https://doi.org/10.1146/annurev-marine-041923-104057 (2024).

  20. Gray, A. R. et al. Autonomous biogeochemical floats detect significant carbon dioxide outgassing in the high‐latitude Southern Ocean. Geophys. Res. Lett. 45, 9049–9057 (2018).

    Article  Google Scholar 

  21. Sutton, A. J., Williams, N. L. & Tilbrook, B. Constraining Southern Ocean CO2 flux uncertainty using uncrewed surface vehicle observations. Geophys. Res. Lett. 48, https://doi.org/10.1029/2020GL091748 (2021).

  22. Ardyna, M. et al. Hydrothermal vents trigger massive phytoplankton blooms in the Southern Ocean. Nat. Commun. 10, 2451 (2019).

    Article  Google Scholar 

  23. Baldry, K., Strutton, P. G., Hill, N. A. & Boyd, P. W. Subsurface chlorophyll-a maxima in the Southern Ocean. Front. Mar. Sci. 7, 671 (2020).

  24. Lacour, L., Llort, J., Briggs, N., Strutton, P. G. & Boyd, P. W. Seasonality of downward carbon export in the Pacific Southern Ocean revealed by multi-year robotic observations. Nat. Commun. 14, 1278 (2023).

    Article  CAS  Google Scholar 

  25. Bisson, K. M. & Cael, B. B. How are under ice phytoplankton related to sea ice in the Southern Ocean? Geophys. Res. Lett. 48, https://doi.org/10.1029/2021GL095051 (2021).

  26. Horvat, C., Bisson, K., Seabrook, S., Cristi, A. & Matthes, L. C. Evidence of phytoplankton blooms under Antarctic sea ice. Front. Mar. Sci. 9, https://doi.org/10.3389/fmars.2022.942799 (2022).

  27. Arteaga, L. A., Boss, E., Behrenfeld, M. J., Westberry, T. K. & Sarmiento, J. L. Seasonal modulation of phytoplankton biomass in the Southern Ocean. Nat. Commun. 11, 5364 (2020).

    Article  CAS  Google Scholar 

  28. Ardyna, M. et al. Delineating environmental control of phytoplankton biomass and phenology in the Southern Ocean: phytoplankton dynamics in the SO. Geophys. Res. Lett. 44, 5016–5024 (2017).

    Article  Google Scholar 

  29. Sallée, J.-B., Llort, J., Tagliabue, A. & Lévy, M. Characterization of distinct bloom phenology regimes in the Southern Ocean. ICES J. Mar. Sci. 72, 1985–1998 (2015).

    Article  Google Scholar 

  30. Prend, C. J. et al. Sub‐seasonal forcing drives year‐to‐year variations of southern ocean primary productivity. Glob. Biogeochem. Cycles 36, 2022GB007329 (2022).

    Article  Google Scholar 

  31. Nicholson, S.-A., Lévy, M., Llort, J., Swart, S. & Monteiro, P. M. S. Investigation into the impact of storms on sustaining summer primary productivity in the Sub-Antarctic Ocean: storms sustain summer primary production. Geophys. Res. Lett. 43, 9192–9199 (2016).

    Article  Google Scholar 

  32. Uchida, T. et al. Southern Ocean phytoplankton blooms observed by biogeochemical floats. J. Geophys. Res. Ocean. 124, 7328–7343 (2019).

    Article  Google Scholar 

  33. Hart, T. J. On the phytoplankton of the south-west Atlantic and the Bellingshausen Sea, 1929–31. Discovery Reports Vol. 8, 1–268 (Califrnia Univ. Press, 1934).

  34. Mitchell, B. G., Brody, E. A., Holm-Hansen, O., McClain, C. & Bishop, J. Light limitation of phytoplankton biomass and macronutrient utilization in the Southern Ocean. Limnol. Oceanogr. 36, 1662–1677 (1991).

    Article  Google Scholar 

  35. Banse, K. Does iron really limit phytoplankton production in the offshore subarctic Pacific? Limnol. Oceanogr. 35, 772–775 (1990).

    Article  CAS  Google Scholar 

  36. Martin, J. H. Glacial–interglacial CO2 change: the iron hypothesis. Paleoceanography 5, 1–13 (1990).

    Article  Google Scholar 

  37. Boyd, P. W. et al. Atmospheric iron supply and enhanced vertical carbon flux in the NE subarctic Pacific: is there a connection? Glob. Biogeochem. Cycles 12, 429–441 (1998).

    Article  CAS  Google Scholar 

  38. de Baar, H. J. W. et al. Importance of iron for plankton blooms and carbon dioxide drawdown in the Southern Ocean. Nature 373, 412–415 (1995).

    Article  Google Scholar 

  39. Boyd, P. W. & Ellwood, M. J. The biogeochemical cycle of iron in the ocean. Nat. Geosci. 3, 675–682 (2010).

    Article  CAS  Google Scholar 

  40. Tagliabue, A. et al. Surface-water iron supplies in the Southern Ocean sustained by deep winter mixing. Nat. Geosci. 7, 314–320 (2014).

    Article  CAS  Google Scholar 

  41. Meskhidze, N., Nenes, A., Chameides, W. L., Luo, C. & Mahowald, N. Atlantic Southern Ocean productivity: fertilization from above or below? Glob. Biogeochem. Cycles 21, GB2006 (2007).

    Article  Google Scholar 

  42. Wagener, T., Guieu, C., Losno, R., Bonnet, S. & Mahowald, N. Revisiting atmospheric dust export to the Southern Hemisphere ocean: biogeochemical implications. Glob. Biogeochem. Cycles 22, GB2006 (2008).

    Article  Google Scholar 

  43. de Jong, J. et al. Iron in land-fast sea ice of McMurdo Sound derived from sediment resuspension and wind-blown dust attributes to primary productivity in the Ross Sea, Antarctica. Mar. Chem. 157, 24–40 (2013).

    Article  Google Scholar 

  44. Duprat, L. et al. Enhanced iron flux to antarctic sea ice via dust deposition from ice‐free coastal areas. J. Geophys. Res. Ocean. 124, 8538–8557 (2019).

    Article  Google Scholar 

  45. Gassó, S. & Torres, O. Temporal characterization of dust activity in the central Patagonia Desert (years 1964–2017). J. Geophys. Res. Atmos. 124, 3417–3434 (2019).

    Article  Google Scholar 

  46. Tang, W. et al. Widespread phytoplankton blooms triggered by 2019-2020 Australian wildfires. Nature 597, 370–375 (2021).

    Article  CAS  Google Scholar 

  47. Weis, J. et al. Southern Ocean phytoplankton stimulated by wildfire emissions and sustained by iron recycling. Geophys. Res. Lett. 49, e2021GL097538 (2022).

    Article  Google Scholar 

  48. Perron, M. M. G., Proemse, B. C., Strzelec, M., Gault-Ringold, M. & Bowie, A. R. Atmospheric inputs of volcanic iron around Heard and McDonald Islands, Southern Ocean. Environ. Sci. Atmos. 1, 508–517 (2021).

    Article  CAS  Google Scholar 

  49. Alderkamp, A.-C. et al. Iron from melting glaciers fuels phytoplankton blooms in the Amundsen Sea (Southern Ocean): phytoplankton characteristics and productivity. Deep. Sea Res. II 71–76, 32–48 (2012).

    Article  Google Scholar 

  50. Hopwood, M. J. et al. Highly variable iron content modulates iceberg-ocean fertilisation and potential carbon export. Nat. Commun. 10, 5261 (2019).

    Article  Google Scholar 

  51. Moreau, S. et al. Sea ice meltwater and circumpolar deep water drive contrasting productivity in three Antarctic polynyas. J. Geophys. Res. Ocean. 124, 2943–2968 (2019).

    Article  Google Scholar 

  52. Sedwick, P. N. & DiTullio, G. R. Regulation of algal blooms in Antarctic shelf waters by the release of iron from melting sea ice. Geophys. Res. Lett. 24, 2515–2518 (1997).

    Article  CAS  Google Scholar 

  53. St‐Laurent, P., Yager, P. L., Sherrell, R. M., Stammerjohn, S. E. & Dinniman, M. S. Pathways and supply of dissolved iron in the Amundsen Sea (Antarctica). J. Geophys. Res. Ocean. 122, 7135–7162 (2017).

    Article  Google Scholar 

  54. Nicholson, S. A. et al. Iron supply pathways between the surface and subsurface waters of the Southern Ocean: from winter entrainment to summer storms. Geophys. Res. Lett. 46, 14567–14575 (2019).

    Article  Google Scholar 

  55. Nicholson, S.-A. et al. Storms drive outgassing of CO2 in the subpolar Southern Ocean. Nat. Commun. 13, 158 (2022).

    Article  CAS  Google Scholar 

  56. Lancelot, C. et al. Spatial distribution of the iron supply to phytoplankton in the Southern Ocean: a model study. Biogeosciences 6, 2861–2878 (2009).

    Article  CAS  Google Scholar 

  57. Lannuzel, D. et al. Iron in sea ice: review and new insights. Elem. Sci. Anthr. 4, 000130 (2016).

    Article  Google Scholar 

  58. Duprat, L. P. A. M., Bigg, G. R. & Wilton, D. J. Enhanced Southern Ocean marine productivity due to fertilization by giant icebergs. Nat. Geosci. 9, 219–221 (2016).

    Article  CAS  Google Scholar 

  59. Smith, K. L. Free-drifting icebergs in the Southern Ocean: an overview. Deep. Sea Res. II 58, 1277–1284 (2011).

    Article  Google Scholar 

  60. Boyd, P. W., Ibisanmi, E., Sander, S. G., Hunter, K. A. & Jackson, G. A. Remineralization of upper ocean particles: implications for iron biogeochemistry. Limnol. Oceanogr. 55, 1271–1288 (2010).

    Article  CAS  Google Scholar 

  61. Gerringa, L. J. A. et al. Iron from melting glaciers fuels the phytoplankton blooms in Amundsen Sea (Southern Ocean): iron biogeochemistry. Deep. Sea Res. II 71–76, 16–31 (2012).

    Article  Google Scholar 

  62. Ratnarajah, L., Nicol, S. & Bowie, A. R. Pelagic iron recycling in the Southern Ocean: exploring the contribution of marine animals. Front. Mar. Sci. 5, 109 (2018).

    Article  Google Scholar 

  63. Tovar-Sanchez, A., Duarte, C. M., Hernández-León, S. & Sañudo-Wilhelmy, S. A. Krill as a central node for iron cycling in the Southern Ocean. Geophys. Res. Lett. 32, L11601 (2007).

    Google Scholar 

  64. Moreau, S. et al. Wind-driven upwelling of iron sustains dense blooms and food webs in the eastern Weddell gyre. Nat. Commun. 14, 1303 (2023).

    Article  CAS  Google Scholar 

  65. Lovenduski, N. S. & Gruber, N. Impact of the southern annular mode on Southern Ocean circulation and biology. Geophys. Res. Lett. 32, L11603 (2005).

    Article  Google Scholar 

  66. Reygondeau, G. et al. Dynamic biogeochemical provinces in the global ocean. Glob. Biogeochem. Cycles 27, 1046–1058 (2013).

    Article  CAS  Google Scholar 

  67. Boyd, P. W., Arrigo, K. R., Strzepek, R. & Van Dijken, G. L. Mapping phytoplankton iron utilization: insights into Southern Ocean supply mechanisms: Southern Ocean Fe utilization and supply. J. Geophys. Res. Ocean. 117, C06009 (2012).

    Article  Google Scholar 

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

    Article  Google Scholar 

  69. Bowie, A. R. et al. Biogeochemical iron budgets of the Southern Ocean south of Australia: decoupling of iron and nutrient cycles in the subantarctic zone by the summertime supply. Glob. Biogeochem. Cycles 23, https://doi.org/10.1029/2009GB003500 (2009).

  70. Boyd, P. W. et al. FeCycle: attempting an iron biogeochemical budget from a mesoscale SF 6 tracer experiment in unperturbed low iron waters. Glob. Biogeochem. Cycles 19, GB4S20 (2005).

    Article  Google Scholar 

  71. Coale, K. H. et al. Southern Ocean iron enrichment experiment: carbon cycling in high- and low-Si waters. Science 304, 408–414 (2004).

    Article  CAS  Google Scholar 

  72. Hoppe, C. J. M. et al. Iron limitation modulates ocean acidification effects on Southern Ocean phytoplankton communities. PLoS One 8, e79890 (2013).

    Article  Google Scholar 

  73. Martin, J. H., Fitzwater, S. E. & Gordon, R. M. Iron deficiency limits phytoplankton growth in Antarctic waters. Glob. Biogeochem. Cycles 4, 5–12 (1990).

    Article  CAS  Google Scholar 

  74. Smetacek, V. et al. Deep carbon export from a Southern Ocean iron-fertilized diatom bloom. Nature 487, 313–319 (2012).

    Article  CAS  Google Scholar 

  75. Browning, T. J., Achterberg, E. P., Engel, A. & Mawji, E. Manganese co-limitation of phytoplankton growth and major nutrient drawdown in the Southern Ocean. Nat. Commun. 12, 884 (2021).

    Article  CAS  Google Scholar 

  76. Latour, P. et al. Manganese biogeochemistry in the Southern Ocean, from Tasmania to Antarctica. Limnol. Oceanogr. 66, 2547–2562 (2021).

    Article  CAS  Google Scholar 

  77. McCain, J. S. P. et al. Cellular costs underpin micronutrient limitation in phytoplankton. Sci. Adv. 7, eabg6501 (2021).

    Article  CAS  Google Scholar 

  78. Wu, M. et al. Manganese and iron deficiency in Southern Ocean Phaeocystis antarctica populations revealed through taxon-specific protein indicators. Nat. Commun. 10, 3582 (2019).

    Article  Google Scholar 

  79. Lee, P. A. et al. Influence of vitamin B12 availability on oceanic dimethylsulfide and dimethylsulfoniopropionate. Environ. Chem. 13, 293–301 (2015).

    Article  Google Scholar 

  80. Mikaloff Fletcher, S. E. et al. Inverse estimates of the oceanic sources and sinks of natural CO2 and the implied oceanic carbon transport. Glob. Biogeochem. Cycles 21, GB1010 (2007).

    Article  Google Scholar 

  81. Arrigo, K. R., Van Dijken, G. L. & Strong, A. L. Environmental controls of marine productivity hot spots around Antarctica. J. Geophys. Res. Ocean. 120, 5545–5565 (2015).

    Article  Google Scholar 

  82. Arrigo, K. R. & Van Dijken, G. Phytoplankton dynamics within 37 Antarctic coastal polynya systems. J. Geophys. Res. 108, 3271 (2003).

    Google Scholar 

  83. Smith, W. O. & Gordon, L. I. Hyperproductivity of the Ross Sea (Antarctica) polynya during austral spring. Geophys. Res. Lett. 24, 233–236 (1997).

    Article  Google Scholar 

  84. Cornec, M. et al. Deep chlorophyll maxima in the Global Ocean: occurrences, drivers and characteristics. Glob. Biogeochem. Cycles 35, e2020GB006759 (2021).

    Article  CAS  Google Scholar 

  85. Acuña, J., López-Alvarez, M., Nogueira, E. & González-Taboada, F. Diatom flotation at the onset of the spring phytoplankton bloom: an in situ experiment. Mar. Ecol. Prog. Ser. 400, 115–125 (2010).

    Article  Google Scholar 

  86. Llort, J. et al. Evaluating Southern Ocean carbon eddy‐pump from biogeochemical‐Argo floats. J. Geophys. Res. Ocean. 123, 971–984 (2018).

    Article  Google Scholar 

  87. Tripathy, S. C. et al. Deep chlorophyll maximum and primary productivity in Indian Ocean sector of the Southern Ocean: case study in the subtropical and polar front during austral summer 2011. Deep. Sea Res. II 118, 240–249 (2015).

    Article  CAS  Google Scholar 

  88. Carranza, M. M. et al. When mixed layers are not mixed. Storm‐driven mixing and bio‐optical vertical gradients in mixed layers of the Southern Ocean. J. Geophys. Res. Ocean 123, 7264–7289 (2018).

    Article  Google Scholar 

  89. Legendre, L. et al. Ecology of sea ice biota: 2. Global significance. Polar Biol. 12, 429–444 (1992).

    Article  Google Scholar 

  90. Saenz, B. T. & Arrigo, K. R. Annual primary production in Antarctic sea ice during 2005–2006 from a sea ice state estimate. J. Geophys. Res. Ocean. 119, 3645–3678 (2014).

    Article  Google Scholar 

  91. Horner, R. et al. Ecology of sea ice biota: 1. Habitat, terminology, and methodology. Polar Biol. 12, 417–427 (1992).

    Article  Google Scholar 

  92. Van Leeuwe, M. A. et al. Microalgal community structure and primary production in Arctic and Antarctic sea ice: a synthesis. Elem. Sci. Anthr. 6, 4 (2018).

    Article  Google Scholar 

  93. Garrison, D. L. & Buck, K. R. The biota of Antarctic pack ice in the Weddell Sea and Antarctic Peninsula regions. Polar Biol. 10, 211–219 (1989).

    Article  Google Scholar 

  94. Arrigo, K. R. Sea ice ecosystems. Annu. Rev. Mar. Sci. 6, 439–467 (2014).

    Article  Google Scholar 

  95. Jeffery, N. et al. Investigating controls on sea ice algal production using E3SMv1.1-BGC. Ann. Glaciol. 61, 51–72 (2020).

    Article  Google Scholar 

  96. Kostov, Y. et al. Fast and slow responses of Southern Ocean sea surface temperature to SAM in coupled climate models. Clim. Dyn. 48, 1595–1609 (2017).

    Article  Google Scholar 

  97. Thompson, D. W. J. & Solomon, S. Interpretation of recent southern hemisphere climate change. Science 296, 895–899 (2002).

    Article  CAS  Google Scholar 

  98. Stuecker, M. F., Bitz, C. M. & Armour, K. C. Conditions leading to the unprecedented low Antarctic sea ice extent during the 2016 austral spring season. Geophys. Res. Lett. 44, 9008–9019 (2017).

    Article  Google Scholar 

  99. Ardyna, M. et al. Under-ice phytoplankton blooms: shedding light on the “invisible” part of Arctic primary production. Front. Mar. Sci. 7, 608032 (2020).

    Article  Google Scholar 

  100. Arrigo, K. R. et al. Massive phytoplankton blooms under Arctic Sea ice. Science 336, 1408–1408 (2012).

    Article  CAS  Google Scholar 

  101. Hague, M. & Vichi, M. Southern Ocean biogeochemical argo detect under-ice phytoplankton growth before sea ice retreat. Biogeosciences 18, 25–38 (2021).

    Article  CAS  Google Scholar 

  102. Balch, W. M. et al. Factors regulating the Great Calcite Belt in the Southern Ocean and its biogeochemical significance. Glob. Biogeochem. Cycles 30, 1124–1144 (2016).

    Article  CAS  Google Scholar 

  103. Holligan, P. M., Charalampopoulou, A. & Hutson, R. Seasonal distributions of the coccolithophore, Emiliania huxleyi, and of particulate inorganic carbon in surface waters of the Scotia Sea. J. Mar. Syst. 82, 195–205 (2010).

    Article  Google Scholar 

  104. Balch, W. M. Calcium carbonate measurements in the surface global ocean based on moderate-resolution imaging spectroradiometer data. J. Geophys. Res. 110, C07001 (2005).

    Google Scholar 

  105. Chen, H., Haumann, F. A., Talley, L. D., Johnson, K. S. & Sarmiento, J. L. The deep ocean’s carbon exhaust. Glob. Biogeochem. Cycles 36, e2021GB007156 (2022).

    Article  CAS  Google Scholar 

  106. Kaufman, D. E. et al. Climate change impacts on southern Ross Sea phytoplankton composition, productivity, and export. J. Geophys. Res. Ocean. 122, 2339–2359 (2017).

    Article  Google Scholar 

  107. Arrigo, K. R. et al. Phytoplankton community structure and the drawdown of nutrients and CO2 in the Southern Ocean. Science 283, 365–367 (1999).

    Article  CAS  Google Scholar 

  108. Delmont, T. O., Hammar, K. M., Ducklow, H. W., Yager, P. L. & Post, A. F. Phaeocystis antarctica blooms strongly influence bacterial community structures in the Amundsen Sea polynya. Front. Microbiol. 5, 646 (2014).

    Article  Google Scholar 

  109. Oliver, H., St‐Laurent, P., Sherrell, R. M. & Yager, P. L. Modeling iron and light controls on the summer Phaeocystis antarctica bloom in the Amundsen Sea polynya. Glob. Biogeochem. Cycles 33, 570–596 (2019).

    Article  CAS  Google Scholar 

  110. Yager, P. et al. A carbon budget for the Amundsen Sea polynya, Antarctica: estimating net community production and export in a highly productive polar ecosystem. Elem. Sci. Anthr. 4, 000140 (2016).

    Article  Google Scholar 

  111. Schine, C. M. S. et al. Massive Southern Ocean phytoplankton bloom fed by iron of possible hydrothermal origin. Nat. Commun. 12, 1211 (2021).

    Article  CAS  Google Scholar 

  112. Schoemann, V., Becquevort, S., Stefels, J., Rousseau, V. & Lancelot, C. Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J. Sea Res. 53, 43–66 (2005).

    Article  CAS  Google Scholar 

  113. Smith, H. E. K. et al. The influence of environmental variability on the biogeography of coccolithophores and diatoms in the Great Calcite Belt. Biogeosciences 14, 4905–4925 (2017).

    Article  CAS  Google Scholar 

  114. Vogt, M. et al. Global marine plankton functional type biomass distributions: Phaeocystis spp. Earth Syst. Sci. Data 4, 107–120 (2012).

    Article  Google Scholar 

  115. Arrigo, K. R. et al. Early spring phytoplankton dynamics in the western Antarctic Peninsula. J. Geophys. Res. Ocean. 122, 9350–9369 (2017).

    Article  Google Scholar 

  116. Biggs, T. E. G. et al. Antarctic phytoplankton community composition and size structure: importance of ice type and temperature as regulatory factors. Polar Biol. 42, 1997–2015 (2019).

    Article  Google Scholar 

  117. Kropuenske, L. R. et al. Photophysiology in two major Southern Ocean phytoplankton taxa: photoprotection in Phaeocystis antarctica and Fragilariopsis cylindrus. Limnol. Oceanogr. 54, 1176–1196 (2009).

    Article  CAS  Google Scholar 

  118. Trimborn, S. et al. Two Southern Ocean diatoms are more sensitive to ocean acidification and changes in irradiance than the prymnesiophyte Phaeocystis antarctica. Physiol. Plant. 160, 155–170 (2017).

    Article  CAS  Google Scholar 

  119. Fisher, B. J. et al. Biogeochemistry of climate driven shifts in Southern Ocean primary producers. Biogeosciences Discuss. https://doi.org/10.5194/bg-2023-10 (2023).

  120. Lewis, K. M., van Dijken, G. L. & Arrigo, K. R. Changes in phytoplankton concentration now drive increased Arctic Ocean primary production. Science 369, 198–202 (2020).

    Article  CAS  Google Scholar 

  121. Stammerjohn, S., Massom, R., Rind, D. & Martinson, D. Regions of rapid sea ice change: an inter-hemispheric seasonal comparison. Geophys. Res. Lett. 39, L06501 (2012).

    Article  Google Scholar 

  122. Schine, C. M. S., Van Dijken, G. & Arrigo, K. R. Spatial analysis of trends in primary production and relationship with large‐scale climate variability in the Ross Sea, Antarctica (1997–2013). J. Geophys. Res. Ocean. 121, 368–386 (2016).

    Article  Google Scholar 

  123. Del Castillo, C. E., Signorini, S. R., Karaköylü, E. M. & Rivero‐Calle, S. Is the Southern Ocean getting greener? Geophys. Res. Lett. 46, 6034–6040 (2019).

    Article  Google Scholar 

  124. Thomalla, S. J., Fauchereau, N., Swart, S. & Monteiro, P. M. S. Regional scale characteristics of the seasonal cycle of chlorophyll in the Southern Ocean. Biogeosciences 8, 2849–2866 (2011).

    Article  CAS  Google Scholar 

  125. Eppley, R. W., Stewart, E., Abbott, M. R. & Heyman, U. Estimating ocean primary production from satellite chlorophyll. Introduction to regional differences and statistics for the Southern California Bight. J. Plankton Res. 7, 57–70 (1985).

    Article  Google Scholar 

  126. Monteiro, T., Kerr, R., Orselli, I. B. M. & Lencina-Avila, J. M. Towards an intensified summer CO2 sink behaviour in the Southern Ocean coastal regions. Prog. Oceanogr. 183, 102267 (2020).

    Article  Google Scholar 

  127. Li, Y., Ji, R., Jenouvrier, S., Jin, M. & Stroeve, J. Synchronicity between ice retreat and phytoplankton bloom in circum‐Antarctic polynyas. Geophys. Res. Lett. 43, 2086–2093 (2016).

    Article  Google Scholar 

  128. Liniger, G., Strutton, P. G., Lannuzel, D. & Moreau, S. Calving event led to changes in phytoplankton bloom phenology in the mertz polynya, Antarctica. J. Geophys. Res. Ocean. 125, e2020JC016387 (2020).

    Article  Google Scholar 

  129. Greaves, B. L. et al. The Southern Annular Mode (SAM) influences phytoplankton communities in the seasonal ice zone of the Southern Ocean. Biogeosciences 17, 3815–3835 (2020).

    Article  CAS  Google Scholar 

  130. Noh, K. M., Lim, H.-G. & Kug, J.-S. Zonally asymmetric phytoplankton response to the Southern annular mode in the marginal sea of the Southern Ocean. Sci. Rep. 11, 10266 (2021).

    Article  CAS  Google Scholar 

  131. Fu, W., Randerson, J. T. & Moore, J. K. Climate change impacts on net primary production (NPP) and export production (EP) regulated by increasing stratification and phytoplankton community structure in the CMIP5 models. Biogeosciences 13, 5151–5170 (2016).

    Article  Google Scholar 

  132. Leung, S., Cabré, A. & Marinov, I. A latitudinally banded phytoplankton response to 21st century climate change in the Southern Ocean across the CMIP5 model suite. Biogeosciences 12, 5715–5734 (2015).

    Article  Google Scholar 

  133. Kwiatkowski, L. et al. Twenty-first century ocean warming, acidification, deoxygenation, and upper-ocean nutrient and primary production decline from CMIP6 model projections. Biogeosciences 17, 3439–3470 (2020).

    Article  CAS  Google Scholar 

  134. Krishnamurthy, A. et al. Impacts of increasing anthropogenic soluble iron and nitrogen deposition on ocean biogeochemistry. Glob. Biogeochem. Cycles 23, GB3016 (2009).

    Article  Google Scholar 

  135. Sallée, J.-B. et al. Summertime increases in upper-ocean stratification and mixed-layer depth. Nature 591, 592–598 (2021).

    Article  Google Scholar 

  136. Moreau, S. et al. Climate change enhances primary production in the western Antarctic Peninsula. Glob. Change Biol. 21, 2191–2205 (2015).

    Article  Google Scholar 

  137. Schofield, O. et al. Changes in the upper ocean mixed layer and phytoplankton productivity along the west Antarctic Peninsula. Phil. Trans. R. Soc. Math. Phys. Eng. Sci. 376, 20170173 (2018).

    Google Scholar 

  138. Hauck, J., Lenton, A., Langlais, C. & Matear, R. The fate of carbon and nutrients exported out of the Southern Ocean. Glob. Biogeochem. Cycles 32, 1556–1573 (2018).

    Article  CAS  Google Scholar 

  139. Moore, J. K. et al. Sustained climate warming drives declining marine biological productivity. Science 359, 1139–1143 (2018).

    Article  CAS  Google Scholar 

  140. Henson, S. A. et al. Uncertain response of ocean biological carbon export in a changing world. Nat. Geosci. 15, 248–254 (2022).

    Article  CAS  Google Scholar 

  141. Hauck, J. et al. Sparse observations induce large biases in estimates of the global ocean CO2 sink: an ocean model subsampling experiment. Phil. Trans. R. Soc. Math. Phys. Eng. Sci. 381, 20220063 (2023).

    CAS  Google Scholar 

  142. Moreau, S., Boyd, P. W. & Strutton, P. G. Remote assessment of the fate of phytoplankton in the Southern Ocean sea-ice zone. Nat. Commun. 11, 3108 (2020).

    Article  CAS  Google Scholar 

  143. Rohr, T., Richardson, A. J., Lenton, A., Chamberlain, M. A. & Shadwick, E. H. Zooplankton grazing is the largest source of uncertainty for marine carbon cycling in CMIP6 models. Commun. Earth Env. 4, 212 (2023).

    Article  Google Scholar 

  144. Yang, G., Atkinson, A., Pakhomov, E. A., Hill, S. L. & Racault, M. Massive circumpolar biomass of Southern Ocean zooplankton: implications for food web structure, carbon export, and marine spatial planning. Limnol. Oceanogr. 67, 2516–2530 (2022).

    Article  CAS  Google Scholar 

  145. Atkinson, A. et al. KRILLBASE: a circumpolar database of Antarctic krill and salp numerical densities, 1926–2016. Earth Syst. Sci. Data 9, 193–210 (2017).

    Article  Google Scholar 

  146. Trebilco, R., Baum, J. K., Salomon, A. K. & Dulvy, N. K. Ecosystem ecology: size-based constraints on the pyramids of life. Trends Ecol. Evol. 28, 423–431 (2013).

    Article  Google Scholar 

  147. Tittensor, D. P. et al. A protocol for the intercomparison of marine fishery and ecosystem models: fish-MIP v1.0. Geosci. Model. Dev. 11, 1421–1442 (2018).

    Article  Google Scholar 

  148. Dornan, T., Fielding, S., Saunders, R. A. & Genner, M. J. Large mesopelagic fish biomass in the Southern Ocean resolved by acoustic properties. Proc. R. Soc. B 289, 20211781 (2022).

    Article  CAS  Google Scholar 

  149. Hindell, M. A. et al. Tracking of marine predators to protect Southern Ocean ecosystems. Nature 580, 87–92 (2020).

    Article  CAS  Google Scholar 

  150. Chawarski, J., Klevjer, T. A., Coté, D. & Geoffroy, M. Evidence of temperature control on mesopelagic fish and zooplankton communities at high latitudes. Front. Mar. Sci. 9, 917985 (2022).

    Article  Google Scholar 

  151. Block, B. A. et al. Toward a national animal telemetry network for aquatic observations in the United States. Anim. Biotelem. 4, 6 (2016).

    Article  Google Scholar 

  152. Le Ster, L. et al. Improved accuracy and spatial resolution for bio-logging-derived chlorophyll a fluorescence measurements in the Southern Ocean. Front. Mar. Sci. 10, 1122822 (2023).

    Article  Google Scholar 

  153. Naito, Y. New steps in bio-logging science. Mem. Natl. Inst. Polar Res. 58, 50–57 (2004).

    Google Scholar 

  154. Block, B. A. et al. Tracking apex marine predator movements in a dynamic ocean. Nature 475, 86–90 (2011).

    Article  CAS  Google Scholar 

  155. Labrousse, S. et al. Coastal polynyas: winter oases for subadult southern elephant seals in East Antarctica. Sci. Rep. 8, 3183 (2018).

    Article  Google Scholar 

  156. McMahon, C. R. et al. Animal borne ocean sensors — AniBOS — an essential component of the Global Ocean observing system. Front. Mar. Sci. 8, 751840 (2021).

    Article  Google Scholar 

  157. DuVivier, A. K. et al. Projections of winter polynyas and their biophysical impacts in the Ross Sea Antarctica. Clim. Dyn. 62, 989–1012 (2023).

    Article  Google Scholar 

  158. Hansell, D. A. & Carlson, C. A. (eds) Biogeochemistry of Marine Dissolved Organic Matter 2nd edn (Elsevier, 2015).

  159. Eich, C. et al. Ecological importance of viral lysis as a loss factor of phytoplankton in the Amundsen Sea. Microorganisms 10, 1967 (2022).

    Article  Google Scholar 

  160. Hansell, D. A. & Orellana, M. V. Dissolved organic matter in the global ocean: a primer. Gels 7, 128 (2021).

    Article  CAS  Google Scholar 

  161. Bercovici, S. K. & Hansell, D. A. Dissolved organic carbon in the deep Southern Ocean: local versus distant controls: Southern Ocean DOC: local versus distant controls. Glob. Biogeochem. Cycles 30, 350–360 (2016).

    Article  CAS  Google Scholar 

  162. Boyd, P. W., Claustre, H., Levy, M., Siegel, D. A. & Weber, T. Multi-faceted particle pumps drive carbon sequestration in the ocean. Nature 568, 327–335 (2019).

    Article  CAS  Google Scholar 

  163. Lopez, C. N. & Hansell, D. A. Anomalous DOC signatures reveal iron control on export dynamics in the Pacific Southern Ocean. Front. Mar. Sci. 10, 1070458 (2023).

    Article  Google Scholar 

  164. Yu, J. et al. Sea ice melting drives substantial change in dissolved organic matter in surface water off Prydz Bay, East Antarctic. J. Geophys. Res. Biogeosci. 128, e2023JG007415 (2023).

    Article  CAS  Google Scholar 

  165. Genovese, C. et al. Influence of organic complexation on dissolved iron distribution in East Antarctic pack ice. Mar. Chem. 203, 28–37 (2018).

    Article  CAS  Google Scholar 

  166. Lannuzel, D., Grotti, M., Abelmoschi, M. L. & Van Der Merwe, P. Organic ligands control the concentrations of dissolved iron in Antarctic sea ice. Mar. Chem. 174, 120–130 (2015).

    Article  CAS  Google Scholar 

  167. Smith, A. J. R. et al. Identifying potential sources of iron-binding ligands in coastal Antarctic environments and the wider Southern Ocean. Front. Mar. Sci. 9, 948772 (2022).

    Article  Google Scholar 

  168. Norman, L. et al. The characteristics of dissolved organic matter (DOM) and chromophoric dissolved organic matter (CDOM) in Antarctic sea ice. Deep. Sea Res. II 58, 1075–1091 (2011).

    Article  CAS  Google Scholar 

  169. Biggs, T. E. G., Huisman, J. & Brussaard, C. P. D. Viral lysis modifies seasonal phytoplankton dynamics and carbon flow in the Southern Ocean. ISME J. 15, 3615–3622 (2021).

    Article  CAS  Google Scholar 

  170. Henson, S. A. et al. A seasonal transition in biological carbon pump efficiency in the northern Scotia Sea, Southern Ocean. Deep. Sea Res. II 208, 105274 (2023).

    Article  CAS  Google Scholar 

  171. Terrats, L. et al. BioGeoChemical-Argo floats reveal stark latitudinal gradient in the Southern Ocean deep carbon flux driven by phytoplankton community composition. Glob. Biogeochem. Cycles 37, e2022GB007624 (2023).

    Article  CAS  Google Scholar 

  172. Ratnarajah, L. et al. Distribution and export of particulate organic carbon in East Antarctic coastal polynyas. Deep. Sea Res. I 190, 103899 (2022).

    Article  CAS  Google Scholar 

  173. Omand, M. M. et al. Eddy-driven subduction exports particulate organic carbon from the spring bloom. Science 348, 222–225 (2015).

    Article  CAS  Google Scholar 

  174. Belcher, A. et al. Krill faecal pellets drive hidden pulses of particulate organic carbon in the marginal ice zone. Nat. Commun. 10, 889 (2019).

    Article  CAS  Google Scholar 

  175. Pinti, J., Jónasdóttir, S. H., Record, N. R. & Visser, A. W. The global contribution of seasonally migrating copepods to the biological carbon pump. Limnol. Oceanogr. https://doi.org/10.1002/lno.12335 (2023).

  176. Takahashi, T. et al. Global sea–air CO2 flux based on climatological surface ocean pCO2, and seasonal biological and temperature effects. Deep. Sea Res. II 49, 1601–1622 (2002).

    Article  CAS  Google Scholar 

  177. Gruber, N. et al. The oceanic sink for anthropogenic CO2 from 1994 to 2007. Science 363, 1193–1199 (2019).

    Article  CAS  Google Scholar 

  178. Huang, Y., Fassbender, A. J. & Bushinsky, S. M. Biogenic carbon pool production maintains the Southern Ocean carbon sink. Proc. Natl Acad. Sci. USA 120, e2217909120 (2023).

    Article  CAS  Google Scholar 

  179. Gregor, L., Kok, S. & Monteiro, P. M. S. Empirical methods for the estimation of Southern Ocean CO2 support vector and random forest regression. Biogeosciences 14, 5551–5569 (2017).

    Article  Google Scholar 

  180. Le Quéré, C. & Saltzman, E. S. Introduction to surface ocean–lower atmosphere processes. In Geophysical Monograph Series Vol. 187 (eds Le Quéré, C. & Saltzman, E. S.) 1–5 (American Geophysical Union, 2009).

  181. Pasquer, B., Metzl, N., Goosse, H. & Lancelot, C. What drives the seasonality of air–sea CO2 fluxes in the ice-free zone of the Southern Ocean: a 1D coupled physical–biogeochemical model approach. Mar. Chem. 177, 554–565 (2015).

    Article  CAS  Google Scholar 

  182. Shadwick, E. H. et al. Sea ice suppression of CO2 outgassing in the west Antarctic Peninsula: implications for the evolving Southern Ocean carbon sink. Geophys. Res. Lett. 48, e2020GL091835 (2021).

    Article  CAS  Google Scholar 

  183. Arrigo, K. R., Van Dijken, G. & Long, M. Coastal Southern Ocean: a strong anthropogenic CO2 sink. Geophys. Res. Lett. 35, L21602 (2008).

    Article  Google Scholar 

  184. Keppler, L. & Landschützer, P. Regional wind variability modulates the Southern Ocean carbon sink. Sci. Rep. 9, 7384 (2019).

    Article  Google Scholar 

  185. Matear, R. J., Hirst, A. C. & McNeil, B. I. Changes in dissolved oxygen in the Southern Ocean with climate change. Geochem. Geophys. Geosyst. https://doi.org/10.1029/2000GC000086 (2000).

  186. Sarmiento, J. L. & Le Quéré, C. Oceanic carbon dioxide uptake in a model of century-scale global warming. Science 274, 1346–1350 (1996).

    Article  CAS  Google Scholar 

  187. Uchida, T. et al. Vertical eddy iron fluxes support primary production in the open Southern Ocean. Nat. Commun. 11, 1125 (2020).

    Article  CAS  Google Scholar 

  188. Du Plessis, M. D. et al. The daily‐resolved Southern Ocean mixed layer: regional contrasts assessed using glider observations. J. Geophys. Res. Ocean. 127, e2021JC017760 (2022).

    Article  Google Scholar 

  189. Boyd, P. W. et al. Mesoscale iron enrichment experiments 1993–2005: synthesis and future directions. Science 315, 612–617 (2007).

    Article  CAS  Google Scholar 

  190. Su, J., Schallenberg, C., Rohr, T., Strutton, P. G. & Phillips, H. E. New estimates of Southern Ocean annual net community production revealed by BGC‐Argo floats. Geophys. Res. Lett. 49, e2021GL097372 (2022).

    Article  Google Scholar 

  191. Liniger, G., Moreau, S. Lannuzel, D. & Strutton P. Large contribution of the sea-ice zone to Southern Ocean carbon export revealed by BGC-Argo floats. Preprint at https://www.researchsquare.com/article/rs-3937570/v1 (2024).

  192. Dinauer, A., Laufkötter, C., Doney, S. C. & Joos, F. What controls the large‐scale efficiency of carbon transfer through the ocean’s mesopelagic zone? Insights from a new, mechanistic model (MSPACMAM). Glob. Biogeochem. Cycles 36, e2021GB007131 (2022).

    Article  CAS  Google Scholar 

  193. Jaccard, S. L., Galbraith, E. D., Martínez-García, A. & Anderson, R. F. Covariation of deep Southern Ocean oxygenation and atmospheric CO2 through the last ice age. Nature 530, 207–210 (2016).

    Article  CAS  Google Scholar 

  194. Ingrosso, G. et al. Physical and biological controls on anthropogenic CO2 sink of the Ross Sea. Front. Mar. Sci. 9, 954059 (2022).

    Article  Google Scholar 

  195. Nissen, C., Timmermann, R., Hoppema, M., Gürses, Ö. & Hauck, J. Abruptly attenuated carbon sequestration with Weddell Sea dense waters by 2100. Nat. Commun. 13, 3402 (2022).

    Article  CAS  Google Scholar 

  196. Silvano, A. et al. Freshening by glacial meltwater enhances melting of ice shelves and reduces formation of Antarctic Bottom Water. Sci. Adv. 4, eaap9467 (2018).

    Article  Google Scholar 

  197. Rickard, G. J., Behrens, E., Bahamondes Dominguez, A. A. & Pinkerton, M. H. An assessment of the oceanic physical and biogeochemical components of CMIP5 and CMIP6 models for the Ross Sea region. J. Geophys. Res. Ocean. 128, e2022JC018880 (2023).

    Article  CAS  Google Scholar 

  198. Brown, M. S. et al. Enhanced oceanic CO2 uptake along the rapidly changing west Antarctic Peninsula. Nat. Clim. Change 9, 678–683 (2019).

    Article  CAS  Google Scholar 

  199. Shadwick, E. H. et al. Glacier tongue calving reduced dense water formation and enhanced carbon uptake. Geophys. Res. Lett. 40, 904–909 (2013).

    Article  Google Scholar 

  200. Herraiz‐Borreguero, L., Lannuzel, D., Van Der Merwe, P., Treverrow, A. & Pedro, J. B. Large flux of iron from the Amery Ice Shelf marine ice to Prydz Bay, East Antarctica. J. Geophys. Res. Ocean. 121, 6009–6020 (2016).

    Article  Google Scholar 

  201. Arroyo, M. C., Shadwick, E. H., Tilbrook, B., Rintoul, S. R. & Kusahara, K. A continental shelf pump for CO2 on the Adélie land coast, East Antarctica. J. Geophys. Res. Ocean. 125, e2020JC016302 (2020).

    Article  CAS  Google Scholar 

  202. Krumhardt, K. M. et al. Potential predictability of net primary production in the Ocean. Glob. Biogeochem. Cycles 34, e2020GB006531 (2020).

    Article  CAS  Google Scholar 

  203. Freeman, N. M. & Lovenduski, N. S. Decreased calcification in the Southern Ocean over the satellite record. Geophys. Res. Lett. 42, 1834–1840 (2015).

    Article  CAS  Google Scholar 

  204. Volk, T. & Hoffert, M. I. Ocean carbon pumps: analysis of relative strengths and efficiencies in ocean-driven atmospheric CO2 changes. In The Carbon Cycle and Atmospheric CO2: Natural Variations Archean to Present. Chapman Conference Papers, 1984. Geophysical Monograph 32 (eds Sundquist, E. T. & Broecker, W. S.) 99–110 (American Geophysical Union, 1985).

  205. Manno, C. et al. Threatened species drive the strength of the carbonate pump in the northern Scotia Sea. Nat. Commun. 9, 4592 (2018).

    Article  CAS  Google Scholar 

  206. Salter, I. et al. Carbonate counter pump stimulated by natural iron fertilization in the Polar Frontal Zone. Nat. Geosci. 7, 885–889 (2014).

    Article  CAS  Google Scholar 

  207. Rembauville, M. et al. Planktic foraminifer and coccolith contribution to carbonate export fluxes over the central Kerguelen Plateau. Deep. Sea Res. I 111, 91–101 (2016).

    Article  CAS  Google Scholar 

  208. Wynn-Edwards, C. A. et al. Particle fluxes at the Australian Southern Ocean Time Series (SOTS) achieve organic carbon sequestration at rates close to the global median, are dominated by biogenic carbonates, and show no temporal trends over 20-years. Front. Earth Sci. 8, 329 (2020).

    Article  Google Scholar 

  209. Neukermans, G. et al. Quantitative and mechanistic understanding of the open ocean carbonate pump — perspectives for remote sensing and autonomous in situ observation. Earth Sci. Rev. 239, 104359 (2023).

    Article  CAS  Google Scholar 

  210. Ryan-Keogh, T. J., Thomalla, S. J., Monteiro, P. M. S. & Tagliabue, A. Multidecadal trend of increasing iron stress in Southern Ocean phytoplankton. Science 379, 834–840 (2023).

    Article  CAS  Google Scholar 

  211. Henley, S. F. et al. Changing biogeochemistry of the Southern Ocean and its ecosystem implications. Front. Mar. Sci. 7, 581 (2020).

    Article  Google Scholar 

  212. Hutchins, D. A. & Boyd, P. W. Marine phytoplankton and the changing ocean iron cycle. Nat. Clim. Change 6, 1072–1079 (2016).

    Article  CAS  Google Scholar 

  213. van der Merwe, P., Trull, T. W., Goodwin, T., Jansen, P. & Bowie, A. The autonomous clean environmental (ACE) sampler: a trace‐metal clean seawater sampler suitable for open‐ocean time‐series applications. Limnol. Oceanogr. Meth. 17, 490–504 (2019).

    Article  Google Scholar 

  214. Mitchell, G. B. & Holm-Hansen, O. Bio-optical properties of Antarctic Peninsula waters: differentiation from temperate ocean models. Deep. Sea Res. I 38, 1009–1028 (1991).

    Article  Google Scholar 

  215. Strzepek, R. F., Boyd, P. W. & Sunda, W. G. Photosynthetic adaptation to low iron, light, and temperature in Southern Ocean phytoplankton. Proc. Natl Acad. Sci. USA 116, 4388–4393 (2019).

    Article  CAS  Google Scholar 

  216. Andrew, S. M. et al. Widespread use of proton-pumping rhodopsin in Antarctic phytoplankton. Proc. Natl Acad. Sci. USA 120, e2307638120 (2023).

    Article  CAS  Google Scholar 

  217. Verdy, A. & Mazloff, M. R. A data assimilating model for estimating Southern Ocean biogeochemistry. J. Geophys. Res. Ocean. 122, 6968–6988 (2017).

    Article  CAS  Google Scholar 

  218. Gloege, L. et al. Quantifying errors in observationally based estimates of ocean carbon sink variability. Glob. Biogeochem. Cycles 35, e2020GB006788 (2021).

    Article  CAS  Google Scholar 

  219. Bushinsky, S. M. et al. Reassessing Southern Ocean air–sea CO2 flux estimates with the addition of biogeochemical float observations. Glob. Biogeochem. Cycles 33, 1370–1388 (2019).

    Article  CAS  Google Scholar 

  220. Boyd, P. W. et al. Controls on polar Southern Ocean deep chlorophyll maxima: viewpoints from multiple observational platforms. Glob. Biogeochem. Cycles https://doi.org/10.1029/2023GB008033 (2023).

  221. Mallet, M. D., Alexander, S. P., Protat, A. & Fiddes, S. L. Reducing Southern Ocean shortwave radiation errors in the ERA5 reanalysis with machine learning and 25 years of surface observations. Artif. Intell. Earth Syst. https://doi.org/10.1175/AIES-D-22-0044.1 (2023).

  222. Rosso, I. et al. Water mass and biogeochemical variability in the kerguelen sector of the Southern Ocean: a machine learning approach for a mixing hot spot. J. Geophys. Res. Ocean. 125, e2019JC015877 (2020).

    Article  CAS  Google Scholar 

  223. Landschützer, P., Laruelle, G. G., Roobaert, A. & Regnier, P. A uniform pCO2 climatology combining open and coastal oceans. Earth Syst. Sci. Data 12, 2537–2553 (2020).

    Article  Google Scholar 

  224. Kidston, M., Matear, R. & Baird, M. E. Phytoplankton growth in the Australian sector of the Southern Ocean, examined by optimising ecosystem model parameters. J. Mar. Syst. 128, 123–137 (2013).

    Article  Google Scholar 

  225. Schartau, M. et al. Reviews and syntheses: parameter identification in marine planktonic ecosystem modelling. Biogeosciences 14, 1647–1701 (2017).

    Article  Google Scholar 

  226. Kriest, I. et al. One size fits all? Calibrating an ocean biogeochemistry model for different circulations. Biogeosciences 17, 3057–3082 (2020).

    Article  CAS  Google Scholar 

  227. Melbourne-Thomas, J. et al. Optimal control and system limitation in a Southern Ocean ecosystem model. Deep. Sea Res. II 114, 64–73 (2015).

    Article  Google Scholar 

  228. Ward, B. A. et al. When is a biogeochemical model too complex? Objective model reduction and selection for North Atlantic time-series sites. Prog. Oceanogr. 116, 49–65 (2013).

    Article  Google Scholar 

  229. Losa, S. N., Kivman, G. A. & Ryabchenko, V. A. Weak constraint parameter estimation for a simple ocean ecosystem model: what can we learn about the model and data? J. Mar. Syst. 45, https://doi.org/10.1016/j.jmarsys.2003.08.005 (2004).

  230. Buitenhuis, E. T., Rivkin, R. B., Sailley, S. & Le Quéré, C. Biogeochemical fluxes through microzooplankton. Glob. Biogeochem. Cycles 24, GB4015 (2010).

    Article  Google Scholar 

  231. Buitenhuis, E. et al. Biogeochemical fluxes through mesozooplankton. Glob. Biogeochem. Cycles 20, GB2003 (2006).

    Article  Google Scholar 

  232. Le Quéré, C. et al. Role of zooplankton dynamics for Southern Ocean phytoplankton biomass and global biogeochemical cycles. Biogeosciences 13, 4111–4133 (2016).

    Article  Google Scholar 

  233. Strzepek, R. F. et al. Spinning the “ferrous wheel”: the importance of the microbial community in an iron budget during the FeCycle experiment. Glob. Biogeochem. Cycles 19, 2005GB002490 (2005).

    Article  Google Scholar 

  234. Raiswell, R., Benning, L. G., Tranter, M. & Tulaczyk, S. Bioavailable iron in the Southern Ocean: the significance of the iceberg conveyor belt. Geochem. Trans. 9, 7 (2008).

    Article  Google Scholar 

  235. Laufkötter, C., Stern, A. A., John, J. G., Stock, C. A. & Dunne, J. P. Glacial iron sources stimulate the Southern Ocean carbon cycle. Geophys. Res. Lett. 45, 13377–13385 (2018).

    Article  Google Scholar 

  236. Ito, A., Ye, Y., Baldo, C. & Shi, Z. Ocean fertilization by pyrogenic aerosol iron. npj Clim. Atmos. Sci. 4, 30 (2021).

    Article  Google Scholar 

  237. Bowie, A. R. et al. The fate of added iron during a mesoscale fertilisation experiment in the Southern Ocean. Deep. Sea Res. II 48, 2703–2743 (2001).

    Article  CAS  Google Scholar 

  238. Law, C. S., Abraham, E. R., Watson, A. J. & Liddicoat, M. I. Vertical eddy diffusion and nutrient supply to the surface mixed layer of the Antarctic Circumpolar Current. J. Geophys. Res. Ocean. 108, 2002JC001604 (2003).

    Article  Google Scholar 

  239. Blain, S. et al. Effect of natural iron fertilization on carbon sequestration in the Southern Ocean. Nature 446, 1070–1074 (2007).

    Article  CAS  Google Scholar 

  240. Watson, A. J. et al. Minimal effect of iron fertilization on sea-surface carbon dioxide concentrations. Nature 371, 143–145 (1994).

    Article  CAS  Google Scholar 

  241. De Jong, J. et al. Natural iron fertilization of the Atlantic sector of the Southern Ocean by continental shelf sources of the Antarctic Peninsula: iron fertilization from Antarctic continental shelf. J. Geophys. Res. Biogeosci. 117, G01029 (2012).

    Google Scholar 

  242. Tagliabue, A. et al. Constraining the contribution of hydrothermal iron to Southern Ocean export production using deep ocean iron observations. Front. Mar. Sci. 9, 754517 (2022).

    Article  Google Scholar 

  243. Wu, S.-Y. & Hou, S. Impact of icebergs on net primary productivity in the Southern Ocean. Cryosphere 11, 707–722 (2017).

    Article  Google Scholar 

  244. Büchner, M. ISIMIP3b ocean input data (v1.4) (ISIMIP Repository); https://data.isimip.org/10.48364/ISIMIP.575744.4.

  245. MacCready, P. & Quay, P. Biological export flux in the Southern Ocean estimated from a climatological nitrate budget. Deep. Sea Res. II 48, 4299–4322 (2001).

    Article  CAS  Google Scholar 

  246. Louanchi, F. & Najjar, R. G. Annual cycles of nutrients and oxygen in the upper layers of the North Atlantic Ocean. Deep. Sea Res. II 48, 2155–2171 (2001).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the Fisheries and Marine Ecosystem Model Intercomparison Project coordinators and modellers for providing the model projections used in Fig. 4 and in Supplementary Figs. 1–4 of this paper. C.N. and D.L. were supported by the Australian Research Council (ARC) FT210100798 and FT190100688 respectively. P.W.B. was funded by an ARC Laureate (FL160100131). A.M.K. acknowledges funding from SOCCOM (OPP-1936222). S.J.T. was supported through the CSIR’s Southern Ocean Carbon — Climate Observatory (SOCCO) Programme (http://socco.org.za/) funded by the Department of Science and Innovation (DSI/CON C3184/2023), the CSIR’s Parliamentary Grant (0000005278) and the National Research Foundation (MCR210429598142). G.N. has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant 853516 CarbOcean). S.S. was funded by a Wallenberg Academy Fellowship (WAF 2015.0186) and the Swedish Research Council (VR 2019–04400) and supported by the European Unions Horizon 2020 research and innovation programme under grant 821001 (SO-CHIC). E.H.S., P.W.B. and D.L. received grant funding from the Australian Government as part of the Antarctic Science Collaboration Initiative programme. This research was also supported by the Australian Research Council Special Research Initiative, Australian Centre for Excellence in Antarctic Science (project number SR200100008).

Author information

Authors and Affiliations

  1. Australian Centre for Excellence in Antarctic Science, University of Tasmania, Hobart, Tasmania, Australia

    Philip W. Boyd & Delphine Lannuzel

  2. Australian Antarctic Program Partnership, Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, Australia

    Philip W. Boyd, Delphine Lannuzel & Elizabeth H. Shadwick

  3. Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, Australia

    Philip W. Boyd, Delphine Lannuzel & Camilla Novaglio

  4. Department of Earth System Science, Stanford University, Stanford, CA, USA

    Kevin R. Arrigo

  5. Takuvik Joint International Laboratory, Laval University (Canada) — CNRS (France), Département de biologie et Québec-Océan, Université Laval, Québec, QC, Canada

    Mathieu Ardyna

  6. National Institute of Water and Atmospheric Research, Hataitai, Wellington, New Zealand

    Svenja Halfter

  7. Centre for Ecology and Conservation, College of Life & Environmental Sciences, University of Exeter, Penryn Campus, Cornwall, United Kingdom

    Luis Huckstadt

  8. Scripps Institution of Oceanography, UC San Diego, La Jolla, CA, USA

    Angela M. Kuhn

  9. Ghent University, Biology Department, MarSens Research Group, Ghent, Belgium

    Griet Neukermans

  10. Flanders Marine Institute (VLIZ), Ostend, Belgium

    Griet Neukermans

  11. CSIRO Environment, Hobart, Tasmania, Australia

    Elizabeth H. Shadwick

  12. Department of Marine Sciences, University of Gothenburg, Gothenburg, Sweden

    Sebastien Swart

  13. Department of Oceanography, University of Cape Town, Rondebosch, South Africa

    Sebastien Swart

  14. Southern Ocean Carbon — Climate Observatory, CSIR, Cape Town, South Africa

    Sandy J. Thomalla

  15. Marine and Antarctic Research Centre for Innovation and Sustainability, University of Cape Town, Cape Town, South Africa

    Sandy J. Thomalla

Authors
  1. Philip W. Boyd
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kevin R. Arrigo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mathieu Ardyna
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Svenja Halfter
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Luis Huckstadt
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Angela M. Kuhn
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Delphine Lannuzel
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Griet Neukermans
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Camilla Novaglio
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Elizabeth H. Shadwick
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Sebastien Swart
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Sandy J. Thomalla
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors researched data for the article. P.W.B., K.R.A., M.A., A.M.K., L.H., D.L., G.N., C.N., E.H.S., S.S. and S.J.T. contributed substantially to discussion of the content. P.W.B., K.R.A., D.L., G.N., C.N., E.H.S. and S.S. wrote the article. P.W.B., K.R.A., M.A., A.M.K., L.H., D.L., G.N., E.H.S., S.S. and S.J.T. reviewed and/or edited the manuscript before submission.

Corresponding author

Correspondence to Philip W. Boyd.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Reviews Earth & Environment thanks Channing Prend, Lydia Keppler, Cara Nissen and the other, anonymous, reviewer for their contribution to the peer review of this work.

Additional information

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

Related links

BGC-Argo: https://biogeochemical-argo.org/index.php

B-SOSE: https://soccom.princeton.edu/content/biogeochemical-sose-solution-now-available

Coupled Model Intercomparison Project: https://www.wcrp-climate.org/wgcm-cmip

FishMIP: www.fishmip.org

KRILLBASE: https://www.bas.ac.uk/project/krillbase/

NASA PACE: https://pace.oceansciences.org/home.htm

National Snow and Ice Data Centre: https://nsidc.org/arcticseaicenews/2023/09/antarctic-sets-a-record-low-maximum-by-wide-margin/

OC-CCI: https://www.oceancolour.org/

SOCLIM: http://soclim.com/

Supplementary information

Glossary

Biogeochemical Argo

(BGC-Argo). An international study using floats to measure oxygen, nitrate, pH, fluorescence, suspended particles and downwelling irradiance in addition to standard oceanographic variables such as temperature, salinity, and pressure measured by Argo floats.

Biogeochemical Southern Ocean State Estimate

(B-SOSE). A model estimate of circulation and biogeochemistry that assimilates output from Argo floats, hydrographic cruises and satellites.

Biological carbon pump

(BCP). The transport of a small but substantial proportion of photosynthetically fixed carbon through the gravitational settling of particles or the injection of particles by physical or biological processes to the ocean’s interior.

Biological gravitational pump

(BGP). A component of the biological carbon pump that focuses on passively sinking material.

Fisheries and Marine Ecosystem Model Intercomparison Project

(FishMIP). A project that aims to understand and project long-term effects of climate change on fisheries and marine ecosystems and inform policy.

Great Calcite Belt

(GCB). A circumpolar band of high calcite concentrations in the water column between the circumpolar subtropical and polar fronts caused by a dominance of coccolithophores.

NASA Plankton, Aerosol, Cloud, ocean Ecosystems project

(NASA PACE). A project that aims to improve NASA’s satellite records of global ocean biology, aerosols and clouds through hyperspectral measurements (5 nm resolution). PACE launched in February 2024.

Net primary production

(NPP). The difference between the energy fixed by autotrophs such as phytoplankton and their respiration. NPP drives phytoplankton growth and increases in phytoplankton stocks, that is, high NPP leads to high chlorophyll concentrations.

Underwater Vision Profiler version 6

(UVP6). A miniaturized and low-price version of the UVP5, which was designed to be attached to floats and acquire float profiles of plankton and particle images.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Boyd, P.W., Arrigo, K.R., Ardyna, M. et al. The role of biota in the Southern Ocean carbon cycle. Nat Rev Earth Environ (2024). https://doi.org/10.1038/s43017-024-00531-3

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s43017-024-00531-3

Search

Advanced search

Quick links

Nature Briefing Anthropocene

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

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