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CO2 storage and release in the deep Southern Ocean on millennial to centennial timescales


The cause of changes in atmospheric carbon dioxide (CO2) during the recent ice ages is yet to be fully explained. Most mechanisms for glacial–interglacial CO2 change have centred on carbon exchange with the deep ocean, owing to its large size and relatively rapid exchange with the atmosphere1. The Southern Ocean is thought to have a key role in this exchange, as much of the deep ocean is ventilated to the atmosphere in this region2. However, it is difficult to reconstruct changes in deep Southern Ocean carbon storage, so few direct tests of this hypothesis have been carried out. Here we present deep-sea coral boron isotope data that track the pH—and thus the CO2 chemistry—of the deep Southern Ocean over the past forty thousand years. At sites closest to the Antarctic continental margin, and most influenced by the deep southern waters that form the ocean’s lower overturning cell, we find a close relationship between ocean pH and atmospheric CO2: during intervals of low CO2, ocean pH is low, reflecting enhanced ocean carbon storage; and during intervals of rising CO2, ocean pH rises, reflecting loss of carbon from the ocean to the atmosphere. Correspondingly, at shallower sites we find rapid (millennial- to centennial-scale) decreases in pH during abrupt increases in CO2, reflecting the rapid transfer of carbon from the deep ocean to the upper ocean and atmosphere. Our findings confirm the importance of the deep Southern Ocean in ice-age CO2 change, and show that deep-ocean CO2 release can occur as a dynamic feedback to rapid climate change on centennial timescales.

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Fig. 1: Locations of deep-sea coral samples.
Fig. 2: Deep Southern Ocean CO2 chemistry, atmospheric CO2, and Antarctic climate records over the past 40,000 years.
Fig. 3: Deglacial records of deep Southern Ocean CO2 chemistry, atmospheric CO2, and climate over Antarctica and Greenland.
Fig. 4: Schematic of changes in sea ice, circulation, and deep ocean carbon storage.

Data availability

The data produced in this study are available in Extended Data Tables and will also be made available at the NOAA ( and Pangaea data repositories.


  1. Broecker, W. S. Glacial to interglacial changes in ocean chemistry. Prog. Oceanogr. 11, 151–197 (1982).

    ADS  Article  Google Scholar 

  2. Sarmiento, J. L. & Toggweiler, J. R. A new model for the role of the oceans in determining atmospheric pCO2. Nature 308, 621–624 (1984).

    CAS  ADS  Article  Google Scholar 

  3. Sigman, D. M., Hain, M. P. & Haug, G. H. The polar ocean and glacial cycles in atmospheric CO2 concentration. Nature 466, 47–55 (2010).

    CAS  ADS  Article  Google Scholar 

  4. Burke, A. & Robinson, L. F. The Southern Ocean’s role in carbon exchange during the last deglaciation. Science 335, 557–561 (2012).

    CAS  ADS  Article  Google Scholar 

  5. Roberts, J. et al. Evolution of South Atlantic density and chemical stratification across the last deglaciation. Proc. Natl Acad. Sci. USA 113, 514–519 (2016).

    CAS  ADS  Article  Google Scholar 

  6. Martinez-Garcia, A. et al. Iron fertilization of the Subantarctic Ocean during the last ice age. Science 343, 1347–1350 (2014).

    CAS  ADS  Article  Google Scholar 

  7. Yu, J. et al. Deep South Atlantic carbonate chemistry and increased interocean deep water exchange during last deglaciation. Quat. Sci. Rev. 90, 80–89 (2014).

    ADS  Article  Google Scholar 

  8. Rae, J. W. B. et al. Deep water formation in the North Pacific and deglacial CO2 rise. Paleoceanography 29, 645–667 (2014).

    ADS  Article  Google Scholar 

  9. Yu, J. et al. Responses of the deep ocean carbonate system to carbon reorganization during the last glacial–interglacial cycle. Quat. Sci. Rev. 76, 39–52 (2013).

    ADS  Article  Google Scholar 

  10. Rickaby, R. E. M., Elderfield, H., Roberts, N., Hillenbrand, C. D. & Mackensen, A. Evidence for elevated alkalinity in the glacial Southern Ocean. Paleoceanography 25, PA1209 (2010).

    ADS  Google Scholar 

  11. Ferrari, R. et al. Antarctic sea ice control on ocean circulation in present and glacial climates. Proc. Natl Acad. Sci. USA 111, 8753–8758 (2014).

    CAS  ADS  Article  Google Scholar 

  12. Marcott, S. A. et al. Centennial-scale changes in the global carbon cycle during the last deglaciation. Nature 514, 616–619 (2014).

    CAS  ADS  Article  Google Scholar 

  13. Adkins, J. F., McIntyre, K. & Schrag, D. P. The salinity, temperature, and δ18O of the glacial deep ocean. Science 298, 1769–1773 (2002).

    CAS  ADS  Article  Google Scholar 

  14. Burke, A., Stewart, A. L., Adkins, J. F. & Ferrari, R. The glacial mid-depth radiocarbon bulge and its implications for the overturning circulation. Paleoceanography 30, 1021–1039 (2015).

    ADS  Article  Google Scholar 

  15. Charles, C. D. et al. Millennial scale evolution of the Southern Ocean chemical divide. Quat. Sci. Rev. 29, 399–409 (2010).

    ADS  Article  Google Scholar 

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

    CAS  ADS  Article  Google Scholar 

  17. Stephens, B. B. & Keeling, R. F. The influence of Antarctic sea ice on glacial-interglacial CO2 variations. Nature 404, 171–174 (2000).

    CAS  ADS  Article  Google Scholar 

  18. Wolff, E. W. et al. Southern Ocean sea-ice extent, productivity and iron flux over the past eight glacial cycles. Nature 440, 491–496 (2006).

    CAS  ADS  Article  Google Scholar 

  19. Abram, N. J., Wolff, E. W. & Curran, M. A. J. A review of sea ice proxy information from polar ice cores. Quat. Sci. Rev. 79, 168–183 (2013).

    ADS  Article  Google Scholar 

  20. Galbraith, E. & de Lavergne, C. Response of a comprehensive climate model to a broad range of external forcings: relevance for deep ocean ventilation and the development of late Cenozoic ice ages. Clim. Dyn. (2018).

  21. Ahn, J. & Brook, E. J. Atmospheric CO2 and climate on millennial time scales during the last glacial period. Science 322, 83–85 (2008).

    CAS  ADS  Article  Google Scholar 

  22. Stocker, T. F. The seesaw effect. Science 282, 61–62 (1998).

    CAS  Article  Google Scholar 

  23. Anderson, R. F. et al. Wind-driven upwelling in the Southern Ocean and the deglacial rise in atmospheric CO2. Science 323, 1443–1448 (2009).

    CAS  ADS  Article  Google Scholar 

  24. Abernathey, R. & Ferreira, D. Southern Ocean isopycnal mixing and ventilation changes driven by winds. Geophys. Res. Lett. 42, 10,357–10,365 (2015).

    Article  Google Scholar 

  25. Chen, T. et al. Synchronous centennial abrupt events in the ocean and atmosphere during the last deglaciation. Science 349, 1537–1541 (2015).

    CAS  ADS  Article  Google Scholar 

  26. Martínez-Botí, M. A. et al. Boron isotope evidence for oceanic carbon dioxide leakage during the last deglaciation. Nature 518, 219–222 (2015).

    ADS  Article  Google Scholar 

  27. Broecker, W. S., Bond, G., Klas, M., Bonani, G. & Wolfli, W. A salt oscillator in the glacial Atlantic? 1. The concept. Paleoceanography 5, 469–477 (1990).

    ADS  Article  Google Scholar 

  28. Members, W. D. P. et al. Precise interpolar phasing of abrupt climate change during the last ice age. Nature 520, 661–665 (2015).

    ADS  Article  Google Scholar 

  29. Markle, B. R. et al. Global atmospheric teleconnections during Dansgaard-Oeschger events. Nat. Geosci. 10, 36–40 (2017).

    CAS  ADS  Article  Google Scholar 

  30. Köhler, P., Knorr, G. & Bard, E. Permafrost thawing as a possible source of abrupt carbon release at the onset of the Bølling/Allerød. Nat. Commun. 5, 5520 (2014).

    ADS  Article  Google Scholar 

  31. Galbraith, E. D. & Eggleston, S. A lower limit to atmospheric CO2 concentrations over the past 800,000 years. Nat. Geosci. 10, 295–298 (2017).

    CAS  ADS  Article  Google Scholar 

  32. Bereiter, B., Shackleton, S., Baggenstos, D., Kawamura, K. & Severinghaus, J. Mean global ocean temperatures during the last glacial transition. Nature 553, 39–44 (2018).

    CAS  ADS  Article  Google Scholar 

  33. Keeling, R. F. & Stephens, B. B. Antarctic sea ice and the control of Pleistocene climate instability. Paleoceanography 16, 112–131 (2001).

    ADS  Article  Google Scholar 

  34. Key, R. M. et al. Global Ocean Data Analysis Project, Version 2 (GLODAPv2). (2015).

  35. Olsen, A. et al. The Global Ocean Data Analysis Project version 2 (GLODAPv2)—an internally consistent data product for the world ocean. Earth Syst. Sci. Data 8, 297–323 (2016).

    ADS  Article  Google Scholar 

  36. Bereiter, B. et al. Revision of the EPICA Dome C CO2 record from 800 to 600 kyr before present. Geophys. Res. Lett. 42, 542–549 (2015).

    ADS  Article  Google Scholar 

  37. Burke, A. et al. Reconnaissance dating: A new radiocarbon method applied to assessing the temporal distribution of Southern Ocean deep-sea corals. Deep Sea Res. Part I Oceanogr. Res. Pap. 57, 1510–1520 (2010).

    CAS  ADS  Article  Google Scholar 

  38. Margolin, A. R. et al. Temporal and spatial distributions of cold-water corals in the Drake Passage: Insights from the last 35,000 years. Deep Sea Res. Part II Top. Stud. Oceanogr. 99, 237–248 (2014).

    ADS  Article  Google Scholar 

  39. Spooner, P. T., Chen, T., Robinson, L. F. & Coath, C. Rapid uranium-series age screening of carbonates by laser ablation mass spectrometry. Quat. Geochronol. 31, 28–39 (2016).

    Article  Google Scholar 

  40. Sinclair, D. J., Kinsley, L. P. & McCulloch, M. T. High resolution analysis of trace elements in corals by laser ablation ICP-MS. Geochim. Cosmochim. Acta 62, 1889–1901 (1998).

    CAS  ADS  Article  Google Scholar 

  41. Robinson, L. F. et al. Primary U distribution in scleractinian corals and its implications for U series dating. Geochem. Geophys. Geosyst. 7, Q05022 (2006).

    ADS  Article  Google Scholar 

  42. Gagnon, A. C., Adkins, J. F., Fernandez, D. P. & Robinson, L. F. Sr/Ca and Mg/Ca vital effects correlated with skeletal architecture in a scleractinian deep-sea coral and the role of Rayleigh fractionation. Earth Planet. Sci. Lett. 261, 280–295 (2007).

    CAS  ADS  Article  Google Scholar 

  43. Rollion-Bard, C., Chaussidon, M. & France-Lanord, C. Biological control of internal pH in scleractinian corals: Implications on paleo-pH and paleo-temperature reconstructions. C. R. Geosci. 343, 397–405 (2011).

    CAS  Article  Google Scholar 

  44. Stewart, J. A., Anagnostou, E. & Foster, G. L. An improved boron isotope pH proxy calibration for the deep-sea coral Desmophyllum dianthus through sub-sampling of fibrous aragonite. Chem. Geol. 447, 148–160 (2016).

    CAS  ADS  Article  Google Scholar 

  45. Boyle, E. A. Cadmium, zinc, copper, and barium in foraminifera tests. Earth Planet. Sci. Lett. 53, 11–35 (1981).

    CAS  ADS  Article  Google Scholar 

  46. Barker, S., Greaves, M. & Elderfield, H. A study of cleaning procedures used for foraminiferal Mg/Ca paleothermometry. Geochem. Geophys. Geosyst. 4, 8407 (2003).

    ADS  Article  Google Scholar 

  47. Rae, J. W. B., Foster, G. L., Schmidt, D. N. & Elliott, T. Boron isotopes and B/Ca in benthic foraminifera: Proxies for the deep ocean carbonate system. Earth Planet. Sci. Lett. 302, 403–413 (2011).

    CAS  ADS  Article  Google Scholar 

  48. Foster, G. L. et al. Interlaboratory comparison of boron isotope analyses of boric acid, seawater and marine CaCO3 by MC-ICPMS and NTIMS. Chem. Geol. 358, 1–14 (2013).

    CAS  ADS  Article  Google Scholar 

  49. Kiss, E. Ion-exchange separation and spectrophotometric determination of boron in geological materials. Anal. Chim. Acta 211, 243–256 (1988).

    CAS  Article  Google Scholar 

  50. Lemarchand, D., Gaillardet, J., Göpel, C. & Manhès, G. An optimized procedure for boron separation and mass spectrometry analysis for river samples. Chem. Geol. 182, 323–334 (2002).

    CAS  ADS  Article  Google Scholar 

  51. Foster, G. L. Seawater pH, pCO2 and [CO3 =] variations in the Caribbean Sea over the last 130 kyr: A boron isotope and B/Ca study of planktic foraminifera. Earth Planet. Sci. Lett. 271, 254–266 (2008).

    CAS  ADS  Article  Google Scholar 

  52. Al-Ammar, A. S., Gupta, R. K. & Barnes, R. M. Elimination of boron memory effect in inductively coupled plasma-mass spectrometry by ammonia gas injection into the spray chamber during analysis. Spectrochim. Acta B At. Spectrosc. 55, 629–635 (2000).

    ADS  Article  Google Scholar 

  53. Misra, S., Owen, R., Kerr, J. & Greaves, M. Determination of δ11B by HR-ICP-MS from mass limited samples: application to natural carbonates and water samples. Geochim. Cosmochim. Acta 140, 531–552 (2014).

    CAS  ADS  Article  Google Scholar 

  54. Rae, J. W. B. in Boron Isotopes 107–143 (Springer, 2018).

  55. McCulloch, M. T. et al. in Boron Isotopes 145–162 (Springer, 2018).

  56. Anagnostou, E., Huang, K. F., You, C. F., Sikes, E. L. & Sherrell, R. M. Evaluation of boron isotope ratio as a pH proxy in the deep sea coral Desmophyllum dianthus: evidence of physiological pH adjustment. Earth Planet. Sci. Lett. 349-350, 251–260 (2012).

    CAS  ADS  Article  Google Scholar 

  57. Trotter, J. et al. Quantifying the pH ‘vital effect’ in the temperate zooxanthellate coral Cladocora caespitosa: validation of the boron seawater pH proxy. Earth Planet. Sci. Lett. 303, 163–173 (2011).

    CAS  ADS  Article  Google Scholar 

  58. Venn, A. A. et al. Impact of seawater acidification on pH at the tissue-skeleton interface and calcification in reef corals. Proc. Natl Acad. Sci. USA 110, 1634–1639 (2013).

    CAS  ADS  Article  Google Scholar 

  59. Allison, N., Cohen, I., Finch, A. A., Erez, J. & Tudhope, A. W. Corals concentrate dissolved inorganic carbon to facilitate calcification. Nat. Commun. 5, 5741 (2014).

    CAS  ADS  Article  Google Scholar 

  60. McCulloch, M. et al. Resilience of cold-water scleractinian corals to ocean acidification: Boron isotopic systematics of pH and saturation state up-regulation. Geochim. Cosmochim. Acta 87, 21–34 (2012).

    CAS  ADS  Article  Google Scholar 

  61. Gagnon, A. C., Adkins, J. F., Erez, J. & Eiler, J. M. Sr/Ca sensitivity to aragonite saturation state in cultured subsamples from a single colony of coral: mechanism of biomineralization during ocean acidification. Geochim. Cosmochim. Acta 105, 240–254 (2013).

    CAS  ADS  Article  Google Scholar 

  62. Wang, X. T. et al. Deep-sea coral evidence for lower Southern Ocean surface nitrate concentrations during the last ice age. Proc. Natl Acad. Sci. USA 114, 3352–3357 (2017).

    CAS  ADS  Article  Google Scholar 

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This work was supported by NERC Standard Grant NE/N003861/1 to J.W.B.R. and L.F.R., an NOAA Climate and Global Change VSP Fellowship to J.W.B.R, NERC Standard Grant NE/M004619/1 to A.B. and J.W.B.R., a NERC Strategic Environmental Science Capital Grant to A.B. and J.W.B.R., Marie Curie Career Integration Grant CIG14-631752 to A.B., an ERC consolidator grant to L.F.R., NSF grant OCE-1503129 to J.F.A., and NERC studentships to B.T. and E.L.

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Nature thanks C. Buizert and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Authors and Affiliations



J.W.B.R., A.B., and L.F.R. designed the study. A.B., L.F.R., T.C., and T.L. collected and uranium–thorium dated the coral samples. J.W.B.R., B.T., E.L., C.C., R.G., J.A.S., and D.C.N. made boron isotope analyses. J.W.B.R., A.B., L.F.R., and J.F.A. developed the interpretation and all authors contributed to the preparation of the manuscript.

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Correspondence to J. W. B. Rae.

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Extended data figures and tables

Extended Data Fig. 1 Deep Southern Ocean CO2 chemistry and atmospheric CO2 over the last 40,000 years.

Green triangles and blue diamonds show lower and upper cell deep-sea coral δ11B data, respectively. Individual subsamples are shown as small open symbols and mean values as larger filled symbols. Error bars on individual subsamples are equivalent to 2 s.d. analytical reproducibility and error bars on mean coral values represent 2 s.e. uncertainty on the mean of replicate subsamples (see Methods). Approximate pH values are given based on coral δ11B using the calibration in Extended Data Fig. 5, but uncertainty on this calibration is large (inset error bar), given the paucity of modern deep-sea coral data from low pH waters. Instead we focus on the δ11B values themselves, which provide a proxy of carbonate chemistry in their own right54. Synchronized ice core CO2 data36 are shown in grey symbols: circles from Dome C, dots from WAIS, stars from Taylor Dome, triangles from TALDICE, pluses from EDML, diamonds from Byrd, and squares from Siple Dome. Grey bands highlight intervals of CO2 rise.

Extended Data Fig. 2 Deep Southern Ocean CO2 chemistry and atmospheric CO2 over the last 40,000 years, highlighting the depths of upper cell corals.

Symbols and data are as plotted in Extended Data Fig. 1, but with the addition of the lower panel and annotations showing the depth in metres of each upper cell coral sample. No systematic offset is seen between samples from different depths. The only signal that occurs simultaneous with a change in depth is the decrease at ~11.5 kyr ago, but the jump back up to higher δ11B values following this event occurs without a change in depth, giving confidence that the excursion is not a depth-related signal. Furthermore the large excursion at ~14.7 kyr ago occurs without a significant change in depth. Note that all of the lower cell corals come from within 17 m water depth of each other.

Extended Data Fig. 3 Records of Southern Ocean biogeochemistry and CO2 over the last 40,000 years.

Data are plotted as in Fig. 2, but with opal flux23, a proxy for upwelling, deep sea coral δ15N62, a proxy for surface ocean nitrate consumption, and authigenic uranium concentrations16, a proxy for bottom water redox. The opal flux and authigenic uranium records combine two sediment cores: TN057-13-4PC in the younger part of the record (pluses) and TN057-14PC in the older part of the record (crosses). The opal flux records from each core are shown on separate scales. The coral δ15N data are grouped into samples from the Antarctic zone (AZ, blue) and Subantarctic zone (SAZ, red); smoothed fits to the data are shown, as provided in the original study62. Intervals of low CO2 during the last ice age are associated with low upwelling, an efficient biological pump, low oxygen water rich in respired carbon, and low-pH carbon-rich water in the deep Southern Ocean.

Extended Data Fig. 4 Deglacial records of Southern Ocean CO2 chemistry and opal fluxes, and climate over Antarctica and Greenland.

Data are plotted as in Figs. 2, 3, but with opal flux23, a proxy for upwelling, surface ocean-atmosphere CO2 difference, based on δ11B in planktic foraminifera26, and radiocarbon data4,25 from corals within these sample groupings, shown as 14C age offsets compared to the contemporaneous atmosphere. Intervals of rising CO2 in the atmosphere are associated with input of waters rich in CO2 and nutrients to the upper reaches of the Southern Ocean. Radiocarbon ages reflect the competing influences of upwelling of 14C-depleted waters and improved ventilation over the deglaciation.

Extended Data Fig. 5 Boron isotope calibration for modern D. dianthus.

Data are from open ocean sites44,56,60, with two additional recent (<1,650 years ago) samples from the Southern Ocean from this study. Water column δ11B of borate (B(OH)4) values are as previously published or are calculated from carbonate chemistry data from nearby GLODAPv2 sites for the new samples, as described47,54. Note that the sensitivity of δ11B in carbonates to pH is based on the pH sensitivity of δ11B of borate. pH itself is not easily shown on a plot like this, as the relationship between δ11B of borate and pH is also somewhat influenced by water temperature, salinity, and depth54. A power law function was fitted to the data using Matlab’s curve fitting toolbox (solid line: δ11BCoral = −1.8214 × δ11BB(OH)4−−12.22 + 27.03; R2 = 0.57). Dashed lines show the 95% confidence intervals and give a measure of calibration uncertainty as shown in the error bar in Extended Data Fig. 1, although data from a given site may be able to record relative changes in pH more sensitively, as seen in many paleo-proxies.

Extended Data Fig. 6 Replicate subsamples from a D. dianthus septum.

To test for the potential influence of microstructural variability in composition, a coral septum was divided into four areas, which were then split into chunks of approximately 0.2, 0.8, 3.2 and 11 mg. These were then individually crushed, cleaned, and analysed. This sample treatment was designed to preserve heterogeneity between subsamples, although note that the clustering of subsamples of a given size from a certain area of the coral may lead to that group recording a slightly different signal (as seen in the 3.2 mg group). The lines in the middle panel show the mean and 2 s.d., excluding one outlier in the 11 mg group. δ11B is correlated with Mg/Ca and U/Ca, showing the influence of internal variability in coral composition.

Extended Data Table 1 δ11B data for all fossil D. dianthus coral samples and subsamples (open symbols in Figures)
Extended Data Table 2 Averaged δ11B data from each D. dianthus coral specimen (filled symbols in figures)
Extended Data Table 3 D. dianthus δ11B calibration data (as shown in Extended Data Fig. 5)

Supplementary information

Supplementary Data

This file contains a zip folder which includes source data as used in Extended Data Tables 1-3 in txt format and an Excel workbook with all source data files combined.

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Rae, J.W.B., Burke, A., Robinson, L.F. et al. CO2 storage and release in the deep Southern Ocean on millennial to centennial timescales. Nature 562, 569–573 (2018).

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  • Deep Southern Ocean
  • Centennial Timescales
  • Boron Isotope
  • Oceanic Carbonate System
  • Atlantic Meridional Overturning Circulation (AMOC)

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