# Increased nutrient supply to the Southern Ocean during the Holocene and its implications for the pre-industrial atmospheric CO2 rise

Anja Studer, Daniel Sigman, Alfredo Martínez-García, Lena Thöle, Elisabeth Michel, Samuel Jaccard, Jörg Lippold, Alain Mazaud, Xingchen Wang, Laura Robinson, et al.

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## To cite this version:

Anja Studer, Daniel Sigman, Alfredo Martínez-García, Lena Thöle, Elisabeth Michel, et al. Increased nutrient supply to the Southern Ocean during the Holocene and its implications for the pre-industrial atmospheric CO2 rise. Nature Geoscience, 2018, 11 (10), pp.756-760. 10.1038/s41561-018-0191-8. hal-02915987

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# Increased nutrient supply to the Southern Ocean during the Holocene and its implications for the pre-industrial atmospheric CO₂ rise

Anja S. Studer<sup>1,9*</sup>, Daniel M. Sigman<sup>2</sup>, Alfredo Martínez-García<sup>1</sup>, Lena M. Thöle<sup>1,3</sup>, Elisabeth Michel<sup>4</sup>, Samuel L. Jaccard<sup>1,3</sup>, Jörg A. Lippold<sup>5</sup>, Alain Mazaud<sup>4</sup>, Xingchen T. Wang<sup>1,2,6</sup>, Laura F. Robinson<sup>7</sup>, Jess F. Adkins<sup>6</sup> and Gerald H. Haug<sup>1,8</sup>

A rise in the atmospheric CO₂ concentration of ~20 parts per million over the course of the Holocene has long been recognized as exceptional among interglacials and is in need of explanation. Previous hypotheses involved natural or anthropogenic changes in terrestrial biomass, carbonate compensation in response to deglacial outgassing of oceanic CO₂, and enhanced shallow water carbonate deposition. Here, we compile new and previously published fossil-bound nitrogen isotope records from the Southern Ocean that indicate a rise in surface nitrate concentration through the Holocene. When coupled with increasing or constant export production, these data suggest an acceleration of nitrate supply to the Southern Ocean surface from underlying deep water. This change would have weakened the ocean's biological pump that stores CO₂ in the ocean interior, possibly explaining the Holocene atmospheric CO₂ rise. Over the Holocene, the circum-North Atlantic region cooled, and the formation of North Atlantic Deep Water appears to have slowed. Thus, the 'seesaw' in deep ocean ventilation between the North Atlantic and the Southern Ocean that has been invoked for millennial-scale events, deglaciations and the last interglacial period may have also operated, albeit in a more gradual form, over the Holocene.

There is growing evidence for ongoing changes in Southern Ocean overturning<fnref n="1" />, which may affect the rates at which anthropogenic CO₂ penetrates into the deep ocean and naturally stored deep ocean CO₂ is vented to the atmosphere. Unravelling these dynamics is central to predicting the trajectory of ocean CO₂ uptake and the atmospheric concentration of CO₂ in the coming decades and centuries. Palaeoceanographic reconstructions over the relatively climatically stable Holocene period have the potential to provide information on the variability of Southern Ocean circulation and biogeochemistry and their interaction with climate that is easier to interpret than over glacial cycles, when diverse aspects of the Earth system were changing markedly.

Recent work has shown that the Holocene, while stable in comparison to recent glacial cycles and most previous interglacials, did host significant changes in both physical climate and the global carbon cycle. Compilation of temperature records suggests a cooling of roughly 1°C since 8,000 years ago (8 ka), focused in the Northern Hemisphere². Ice core reconstructions indicate substantial changes in atmospheric CO₂: after an initial deglacial rise from 180 to 270 ppm between ~18 ka and 11 ka, CO₂ declined by 10 ppm from 11 ka to 8 ka before increasing from 260 ppm to a pre-industrial concentration of 280 ppm (ref. ³).

The early Holocene atmospheric CO₂ decline from 11 ka to 8 ka has been suggested to result from regrowth of the terrestrial biosphere in the aftermath of glacial retreat³, while both terrestrial and oceanic processes have been proposed to explain the subsequent

20 ppm rise since 8 ka. A decline in terrestrial biomass has been proposed as the cause for the CO₂ rise and attributed to either natural climate change³ or deforestation by humans⁴. An alternative proposal is that ocean alkalinity decreased due to a pulse of deep sea calcium carbonate burial, itself a response to an increase in terrestrial biomass earlier in the Holocene⁵. Another ocean alkalinity-based hypothesis is that rising sea level led to enhanced deposition of coral reefs and other shallow water carbonates over the Holocene, lowering the ocean alkalinity and thus raising atmospheric CO₂ (ref. <fnref n="6" />).

The modern Southern Ocean is characterized by high surface nutrient (for example, nitrate) concentrations, which reflect the rapid circulation-driven exchange between surface waters and the nutrient-rich ocean interior. Phytoplankton are unable to consume the wealth of nutrients, as their growth in the region is limited by iron and/or light⁷. Thus, the nutrient excess of the Southern Ocean surface provides a potential indicator of overturning changes in the past. Moreover, the incomplete consumption of nutrients combines with the high overturning rate in the Southern Ocean to lower the efficiency of the global ocean's 'biological pump' of carbon, reducing the quantity of CO₂ that is sequestered in the deep ocean through the production and remineralization of sinking organic matter. As a result, the Southern Ocean, its biogeochemical conditions, and its relative importance in the ventilation of the ocean interior have long been recognized as a potential driver of atmospheric CO₂ change on timescales of hundreds and thousands of years⁸. Given the

<footnote n="1">¹Max Planck Institute for Chemistry, Climate Geochemistry Department, Mainz, Germany. ²Department of Geosciences, Princeton University, Princeton, NJ, USA. ³Institute of Geological Sciences and Oeschger Center for Climate Change Research, University of Bern, Bern, Switzerland. ⁴Laboratoire des Sciences du Climat et de l'Environnement (LSCE), Gif-sur-Yvette, France. ⁵Institute of Earth Sciences, Heidelberg University, Heidelberg, Germany.</footnote>

<footnote n="6">⁶Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, USA. ⁷Bristol Isotope Group, School of Earth Sciences, University of Bristol, Bristol, UK. ⁸Department of Earth Sciences, ETH Zurich, Zurich, Switzerland. ⁹Present address: Department of Environmental Sciences, University of Basel, Basel, Switzerland. *e-mail: anja.studer@unibas.ch</footnote>
<figure><img src="image_3.png" /><figcaption>**Fig. 1** | Sediment core and deep sea coral locations relative to austral summer surface nitrate concentrations and oceanic fronts. Core locations of the diatom-bound δ¹⁵N and opal flux records are shown in white with a black rim, locations of ODP Site 1090 foraminifera-bound δ¹⁵N record and of the coral-bound δ¹⁵N measurements are shown in white, and sediment core TN057-13, mentioned in the text, is shown in dark grey. APF, Antarctic Polar Front; SAF, Subantarctic Front; STF, Subtropical Front. Fronts are after ref. ⁵¹.</figcaption></figure>

importance of the Southern Ocean in setting atmospheric CO₂ and the hypothesis that Southern Hemisphere westerly wind strength is a critical climate-sensitive determinant of Southern Ocean overturning⁹, Moreno et al.¹⁰ used South American pollen assemblage changes to infer that westerly wind strengthening could have increased Southern Ocean CO₂ release over the Holocene, contributing to the Holocene atmospheric CO₂ rise. This hypothesis can be seen as an extension of the proposal that the Southern Hemisphere winds played a similar role in the rise of CO₂ during the last deglaciation⁹,¹¹,¹². However, so far, reconstructions of Holocene changes in westerly wind strength remain controversial¹⁰,¹³.

In high-nutrient regions such as the Southern Ocean, the N isotope composition of exported organic matter reflects the degree to which the gross nitrate supply is assimilated by phytoplankton growth. The consumption of surface nitrate causes its δ¹⁵N to rise as its concentration declines (δ¹⁵N = [(¹⁵N/¹⁴N)sample/ (¹⁵N/¹⁴N)atmN₂ - 1] × 1,000‰). This δ¹⁵N rise is recorded in the biomass of the phytoplankton such as diatoms that consume the nitrate. Thus, the δ¹⁵N of the organic matter bound and preserved within the siliceous frustules of diatoms (diatom-bound δ¹⁵N, δ¹⁵Ndb) provides a means for reconstructing past changes in the relative degree of nitrate consumption. In regions such as the Antarctic Zone (AZ) where the deep ocean is ventilated, a higher δ¹⁵Ndb would imply a rise in nitrate consumption and an increase in the efficiency of the global ocean's biological pump, and thus more deep ocean storage of CO₂.

We report two new δ¹⁵Ndb records from the Indian sector of the Southern Ocean and compile them with previously published Southern Ocean nitrogen isotope data¹⁴⁻¹⁶. Sediment core MD11-3353 is from the Indian sector of the AZ, and core MD12-3396CQ is from the Indian sector of the Polar Frontal Zone (PFZ), just to the North of the AZ (Fig. 1). The other records in the compilation are (1) a δ¹⁵Ndb record from core PS75/72-4 in the Pacific sector of the AZ¹⁵, (2) a foraminifera-bound δ¹⁵N (δ¹⁵Nfb) record from ODP Site 1090 in the Atlantic sector of the Subantarctic Zone (SAZ) to

the North of the PFZ¹⁴, and (3) Pacific sector compilations of deep sea coral-bound δ¹⁵N (δ¹⁵Ncb) in the AZ (Drake Passage) and SAZ (Drake Passage and south of Tasmania)¹⁶.

## Holocene decline in fossil-bound ¹⁵N/¹⁴N

Over the last 10 kyr, δ¹⁵Ndb declined in all AZ and PFZ records, by ~2‰, and AZ δ¹⁵Ncb appears consistent with this amplitude of decline (Fig. 2). The δ¹⁵Nfb record from the Atlantic SAZ and the δ¹⁵Ncb data from the Pacific SAZ suggest that the nitrate δ¹⁵N decline also extended into this region, although perhaps weakening towards its northern edge (for example, to a ~1‰ decrease at ODP Site 1090). Whereas the high rate of nitrate supply to the AZ surface is dominated by upwelling, the SAZ receives nitrate from both the AZ surface and underlying Circumpolar Deep water. Thus, a northward decline in the δ¹⁵N decrease is consistent with the AZ as the origin of the δ¹⁵N decrease.

Our observations derive from δ¹⁵N measurements in three fossil types (diatoms, foraminifera and corals), with records from each of the basins of the Southern Ocean. Nevertheless, previous work did not clearly show a Holocene δ¹⁵N decline. There is a range of plausible explanations for this disconnect between recent and earlier measurements. First, it is common for Southern Ocean sediment cores to lack a complete Holocene, and radiocarbon dates are often sparse or absent in Antarctic cores due to a lack of foraminiferal carbonate. For example, several of the first bulk sediment δ¹⁵N records extending back to the last ice age¹⁷ have subsequently been found to lack the latter half of the Holocene¹⁸. The second category of explanations relates to proxy characteristics and analytical methods. Bulk sedimentary δ¹⁵N can be affected by exogenous N inputs¹⁹,²⁰ and variable isotope fractionation associated with diagenesis¹⁴, interfering with its ability to robustly record the Holocene trend¹⁴. The accuracy of the earliest combustion-based δ¹⁵Ndb measurements²¹,²² was compromised by gaseous N absorption on the opal²³, and the precision of current methods has significantly improved over time²⁴, which is critical for recording modest changes. In addition, opal from non-diatom material can contaminate the δ¹⁵Ndb signal in intervals with low diatom flux²⁴, and diatom assemblage changes may lead to artefacts²⁵. Importantly, diatom assemblage separation was performed on all δ¹⁵Ndb records reported here, confirming that the Holocene trend is not an artefact of diatom species abundance changes or of non-diatom opal contamination (Supplementary Fig. 1).

It is also possible that the regional extent of the reconstructed Holocene nitrate δ¹⁵N decrease did not apply to all sectors and latitudes of the Southern Ocean. In particular, as discussed further below, the δ¹⁵Ndb record at core TN057-13 in the Atlantic AZ does not show a Holocene decline²⁵ (although δ¹⁵Nfb at ODP Site 1090 does; Fig. 2c).

All of our AZ records are located close to the Polar Front, so it is possible that the Holocene δ¹⁵N decline did not extend further southward into the more polar AZ, potentially explaining the lack of a clear Holocene decline in some other previous δ¹⁵Ndb records²⁶. Due to the convergence of Southern Ocean waters to flow through the Drake Passage, the δ¹⁵Ncb decline observed in the Drake Passage argues that the more polar AZ also experienced this δ¹⁵N change. However, the most polar sites in the Drake Passage do not have a high density of corals through the Holocene¹⁶, so this argument is preliminary.

The Holocene δ¹⁵N decline in the Southern Ocean might be suspected to derive from a decline in the δ¹⁵N or a rise in the concentration of the subsurface nitrate that is upwelled to the surface. Upper Circumpolar Deep Water (UCDW) upwells in the AZ near the Polar Front, while Lower Circumpolar Deep Water (LCDW) upwells further poleward in the AZ. The modern range in nitrate δ¹⁵N among pure North Atlantic Deep Water (NADW), LCDW and UCDW is less than 0.5‰ (ref. ²⁷), with Pacific Deep Water in the
low-latitude South Pacific expanding the deep nitrate $\delta^{15}N$ range to 1‰, at maximum²⁸. The nitrate $\delta^{15}N$ and concentration differences among these water masses are weakened further by circulation and remineralization in the Southern Ocean²⁹. With regard to nitrate concentration, even though NADW has a low nitrate concentration of ~17.5 µmol kg⁻¹ when measured in the low-latitude Atlantic²⁷, the nitrate concentration of LCDW that most directly derives from it is only slightly lower than that of UCDW (~32 versus 34 µmol kg⁻¹ in the Indian and Pacific oceans). Changing the nitrate concentration of LCDW or UCDW substantially (for example, by 10–20 µmol kg⁻¹) would require a comparable change in the global nitrate reservoir, which is unlikely²⁰,²⁷. What remains a greater concern is the assumption of a constant mean ocean nitrate $\delta^{15}N$ across the Holocene. Some non-Southern Ocean records show decreasing trends across the Holocene³⁰, and a decline in whole ocean nitrate $\delta^{15}N$ cannot be ruled out. However, previous studies do not provide evidence for a mean ocean decrease approaching 2‰ (refs ²⁰,³⁰).

## Increase in the supply rate of nitrate

The Holocene decline in Southern Ocean fossil-bound $\delta^{15}N$ is best interpreted as an increase in the proportion by which the nitrate supply to the surface ocean exceeded its demand by phytoplankton, resulting in a rise in surface nitrate concentration. Our records are located across the northward decline in surface nitrate concentration that characterizes the northern Southern Ocean (Fig. 1). This raises the possibility that the reconstructed rise in surface nitrate concentration represents a northward migration of oceanic fronts over the Holocene. However, this change should have been accompanied by Southern Hemisphere cooling, inconsistent with atmospheric temperature records (Supplementary Fig. 2). Moreover, $\delta^{15}N_{db}$ did not decline over the course of Marine Isotope stage 5e (128–115 ka), the previous interglacial, when atmospheric temperatures did decrease¹⁵.

If the decrease in nitrate consumption was driven by changing eolian iron supply, then the iron supply would have needed to decline over the late Holocene, yet there is no evidence for this³¹,³². Moreover, opal fluxes in the three cores with $\delta^{15}N_{db}$ records suggest constant or increasing export production over the Holocene (Fig. 2d; although the available Southern Ocean opal flux records appear heterogeneous, Supplementary Fig. 3). A decline in the degree of nitrate consumption coupled with stable or weakly rising export production points to a Holocene rise in the rate of gross nitrate supply into the Antarctic surface and thus an increase in water and CO₂ flux from the subsurface into the surface.

As noted above, sediment core TN057-13 from the Atlantic AZ has $\delta^{15}N_{db}$ and opal flux records that are inconsistent with those we report from the Indian and Pacific AZ¹¹,²⁵. With regard to opal flux, TN057-13 shows a decline since the last deglaciation¹¹, in contrast to our observations of stable or rising opal flux (Fig. 2d and Supplementary Fig. 3). We tentatively propose that the observed differences derive from the between-sector differences in (1) the sources of upwelled water and/or (2) basin-level constraints on the net upwelling rate. With regard to upwelling sources, the silicate concentration in the water to be upwelled in the Atlantic AZ—and thus the biogenic opal flux—is reduced by the inflow of low-silicate NADW, such that changes in opal flux may be affected by changes in NADW formation³³ (the nitrate concentration of the water upwelling in the AZ having much less potential to change, as described above). With regard to upwelling rate, net upwelling (the ‘residual circulation’³⁴) in the Atlantic sector AZ should be constrained by the north-south density structure in the region, which in turn may be sensitive to the rate of NADW formation³⁵. For example, an increase in northward wind-driven transport in the Southern Ocean, absent a parallel increase in NADW formation, would have led to a thickening of the low-latitude Atlantic thermocline and an associated steepening of isopycnals at the northern boundary of the

<figure><img src="image_4.png" /><figcaption>**Fig. 2** | Holocene records of fossil-bound $\delta^{15}N$ and biogenic opal flux from the Southern Ocean, compared with atmospheric CO₂ and with climate- and circulation-related records from the Northern Hemisphere.</figcaption></figure>

a, Atmospheric CO₂ concentration composite⁵². b, $\delta^{15}N$ records from the Antarctic and Polar Frontal Zones of the Southern Ocean. Diatom-bound $\delta^{15}N$ records are shown in green, from the Pacific Antarctic¹⁵ (circles, PS75/72-4), the Indian Antarctic (triangles, MD11-3353) and the Indian Polar Frontal Zone (diamonds, MD12-3396CQ). The compilation of coral-bound $\delta^{15}N$ data¹⁶ (Drake Passage) is shown in blue. c, Fossil-bound $\delta^{15}N$ records from the Subantarctic Zone of the Southern Ocean¹⁴,¹⁶. Red, foraminifera-bound $\delta^{15}N$ record from ODP Site 1090 in the Atlantic¹⁴; dark blue, coral-bound $\delta^{15}N$ compilation from the Drake Passage¹⁶; light blue, coral-bound $\delta^{15}N$ compilation from south of Tasmania¹⁶. d, Thorium-normalized opal flux records from cores PS75/72-4 (circles, ref. ¹⁵), MD12-3396CQ (diamonds) and MD11-3353 (triangles). e, Temperature anomaly from 30–90° N relative to the 1961–1990 instrumental mean². f, Mean grain size of the sorted silt fraction, a proxy for near-bottom flow speed, from core MD99-2251 from the Gardar Drift at 2,620 m water depth⁴⁶ (orange) and mean relative grain size from a stacked record from 13 sediment cores located south of Iceland⁴⁵ (grey), indicative of the relative strength of the Iceland-Scotland overflow and thus North Atlantic Deep Water formation. Data in **a** and **e** are shown for the period before 1900. Note that the right-hand axis in **c** (SAZ $\delta^{15}N$ coral-bound) has been scaled by two-thirds for plotting purposes.
Southern Ocean³⁶. This would have increased eddy transport operating counter to the winds, preventing a rise in the residual circulation³⁷. Because this North-Atlantic-driven feedback is more remote in the Indian and Pacific than in the Atlantic basin, upwelling in the Indian and Pacific Southern Ocean may have had more freedom to increase over the Holocene. In any case, the possibility of basin-to-basin variations in the Holocene nitrate evolution of the Southern Ocean should be pursued further.

## CO₂ leakage to the atmosphere

For almost all changes in circulation that would increase nitrate supply to and nitrate concentrations in the Southern Ocean surface, there would be increased leakage of biologically stored CO₂ from the Southern Ocean and a resulting increase in atmospheric CO₂ concentration³⁸. The Holocene change might be considered a gradual continuation of the AZ changes that have been proposed to contribute to the glacial-to-interglacial increases in atmospheric CO₂. A comparison with previous box model and ocean general circulation model results suggests that, for a range of scenarios, the reconstructed Holocene change could generate the observed 20 ppm rise in atmospheric CO₂ (see Supplementary Information). A more specific assessment awaits clarity as to whether the reconstructed increase in surface nitrate concentration applied to the more polar AZ.

Other carbon-cycle-related data do not as yet compellingly support or disprove our hypothesis. First, a release of biologically light carbon from the ocean adequate to explain the 20 ppm atmospheric CO₂ rise should cause the δ¹³C of atmospheric CO₂ to decline by 0.2‰, more than the observed ~0.05‰ decline over the last 7 kyr (ref. ³⁹) (Supplementary Fig. 4). However, there are other potential contributors to the history of atmospheric CO₂ δ¹³C, including changes in the terrestrial biosphere, ocean temperature and the isotopic characteristics of air/sea CO₂ exchange³⁹. Second, in terms of radiocarbon constraints, slow air/sea equilibration at the AZ surface probably explains the deep sea coral-based observation of a relatively weak Holocene difference in radiocarbon content between the upwelling UCDW and Antarctic Intermediate Water, the latter forming from AZ surface water near the Antarctic Polar Front⁴⁰. The existing data appear to suggest a weak decline in this difference through the Holocene, consistent with faster Southern Ocean overturning⁴⁰. Third, abyssal Indian Ocean carbonate ion concentration decreased over the Holocene⁴¹, whereas a weakening of the biological pump by itself would have transiently raised deep ocean carbonate ion⁴². However, deep ocean carbonate ion also depends on terrestrial biosphere size, shallow carbonate burial, and compensation of these by the deep ocean CaCO₃ burial rate⁵. Fourth, a weakening of the ocean's biological pump over the Holocene should have decreased the surface-to-deep-ocean dissolved inorganic carbon δ¹³C gradient, consistent with observations⁴³. Finally, weakening of the ocean's biological pump should have raised ocean interior oxygen concentrations. However, the existing redox-sensitive proxies may not record changes at the relatively high absolute oxygen concentrations that have characterized the deep ocean throughout the Holocene¹⁷.

A weakening of the biological pump was not the sole change affecting atmospheric CO₂ across the Holocene. However, when superimposed on terrestrial biosphere and ocean alkalinity changes³⁻⁶,⁴³, it can generate the net 20 ppm increase. This may explain why Earth system models, which do not hindcast a Holocene trend in Antarctic overturning, fail to produce the different trends in atmospheric CO₂ for the Holocene and previous interglacials⁴⁴. For example, during Marine Isotope Stage 5e, atmospheric CO₂ declined by roughly 10 ppm, and PS75/72-4 indicates no decrease in AZ δ¹⁵N<sub>db</sub> (ref. ¹⁵).

## Possible Northern Hemisphere driver

Data indicate a Northern Hemisphere cooling of 2°C since 7 ka (Fig. 2e) that was focused in the circum-North Atlantic². This cooling and North Atlantic sortable silt grain size and magnetic

susceptibility data suggest a decline in NADW formation into the later Holocene⁴⁵⁻⁴⁷ (Fig. 2f), to which the mid-Holocene increase in Antarctic overturning may have been a response. The same connection has been proposed for the Heinrich events of the last ice age and during deglaciation¹²,³³,⁴⁸.

One possible scenario connecting NADW reduction to Antarctic overturning enhancement involves the winds: at the deglaciations and during Northern Hemisphere stadials, reduction of NADW formation caused Southern Hemisphere warming and southward migration of the Southern Hemisphere westerly winds, which in turn drove an increase in Antarctic overturning⁹,¹¹,¹². Over the Holocene, Subantarctic surface water temperature appears to decline (Supplementary Fig. 2), consistent with an acceleration in wind-driven upwelling in the AZ and northward water transport. However, there is not yet clarity as to the sense of Southern Hemisphere atmospheric temperature change (Supplementary Fig. 2) or the strength and position of the westerly winds¹⁰,¹³. An alternative mechanism for a North Atlantic/Southern Ocean teleconnection is through the ocean interior. The apparent reduction in NADW formation over the Holocene may have impacted deep ocean density structure so as to accelerate Antarctic overturning³⁵.

The climate of the Holocene may have been more stable than that of most other late Pleistocene interglacials, with a weaker tendency for post-deglacial cooling⁴⁹, a characteristic that may have facilitated the development of complex human civilizations. Model simulations suggest that the rise in atmospheric CO₂ over the Holocene, which also appears to be a unique feature among interglacials, worked to counter the cooling trend that characterized most previous interglacials⁵⁰. Thus, the evidence reported here for Southern Ocean change, if it indeed explains the Holocene CO₂ rise, provides an oceanographic mechanism for the stability of the Holocene climate.

## Methods

Methods, including statements of data availability and any associated accession codes and references, are available at https://doi.org/10.1038/s41561-018-0191-8.

Received: 23 January 2017; Accepted: 26 June 2018;
Published online: 30 July 2018

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## Acknowledgements

This study was supported by Swiss NSF grant PBEZP2_145695 to A.S.S., US NSF grants 1401489 and 1234664 to D.M.S., Swiss NSF grant PZ00P2_142424 to A.M.-G., grants PP00P2-144811 and PP00P2_172915 to S.L.J., by the Deutsche Forschungsgemeinschaft through grant Li1815/4 to J.A.L., by funding from the Swedish Research Council VR-349-2012-6278 to E.M., from the Natural Environment Research Council NE/N003861/1 to L.F.R., and from the French INSU/LEFE Indien Sud to A.M. This research was also supported by ExxonMobil through the Andlinger Center for Energy and the Environment at Princeton University and by the Grand Challenges Program of Princeton University. Cores MD11-3353 and MD12-3396CQ were retrieved during Indien Sud oceanographic cruises (A.M.) and we express our thanks to the crew of the R/V Marion Dufresne as well as the French Polar Institute (IPEV). The authors thank K. Hendry, M. Palmer and B. Heinz for their valuable input, and X. Crosta for his help with diatom species identification.

## Author contributions

A.S.S., D.M.S., A.M.-G. and G.H.H. designed the study. A.S.S. performed the δ¹⁵Nₐ₆ analyses and wrote the first draft of the manuscript with D.M.S., A.M.-G. and G.H.H. L.M.T., S.L.J. and J.A.L. contributed the ²³⁰Th-normalized opal flux data. E.M. and A.M. provided access to the sediment cores and measured the radiocarbon ages for the construction of the age model. L.F.R. and J.F.A. recovered the corals, and X.T.W. generated the coral-bound δ¹⁵N data. All authors contributed to the interpretation of the data and provided input to the final manuscript.

## Competing interests

The authors declare no competing interests.

## Additional information

*Supplementary information* is available for this paper at https://doi.org/10.1038/s41561-018-01918-8.

Reprints and permissions information is available at www.nature.com/reprints.

Correspondence and requests for materials should be addressed to A.S.S.

**Publisher's note:** Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
**Methods**

**δ¹⁵N<sub>ab</sub> analysis.** The N isotopic composition of the diatom fraction was measured at Princeton University with the persulfate-denitrifier technique<sup>15,24,53,54</sup>. The diatom separation and cleaning protocol is described in detail in the Supplementary Information.

**Biogenic opal concentration and opal fluxes.** Opal concentrations were measured using the wet digestion technique<sup>55</sup>, and opal fluxes were evaluated by correcting for sediment focusing with <sup>230</sup>Th normalization<sup>56</sup>.

**Age models and radiocarbon dating.** Sediment core PS75/72-4 was recovered in the AZ of the Pacific sector of the Southern Ocean (57° 33.51′ S, 151° 13.17′ W, 3,099 m water depth). The Holocene portion of the age model was constrained by four accelerator mass spectrometry (AMS) radiocarbon ages on *Neogloboquadrina pachyderma* (sin.) for the past 11 kyr<sup>15</sup>. Sediment core MD12-3396CQ is located in the Polar Frontal Zone of the Indian sector of the Southern Ocean (47° 43.88′ S, 86° 41.71′ E, 3,615 m water depth). The stratigraphy of the sediment core was based on 16 AMS radiocarbon dates on monospecific planktonic samples chosen within the abundance peak of the species, with four replicates on different species (Supplementary Table 1). The calendar age model was obtained using a deposition model with OxCal<sup>27,58</sup>, using calibration curve SH2013 and a marine reservoir age for the core location during the Holocene of 900 ± 100 yr following GLODAP<sup>59</sup>. Sediment core MD11-3353 was retrieved in the AZ of the Indian sector of the Southern Ocean (50° 34.02′ S, 68° 23.13′ E, 1,568 m), south of Kerguelen Island. The age model was constructed by correlating distinctive features in the potassium (K) X-ray

fluorescence scanning record of MD11-3353 to those observed in core MD12-3396CQ (Supplementary Fig. 5).

**Data availability.** Data supporting the findings of this study are available within the Article and its Supplementary Information files. Data are also available on Pangaea at https://doi.pangaea.de/10.1594/PANGAEA.891436.

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