Title: Southern Ocean carbon sink enhanced by sea-ice feedbacks at the
Antarctic Cold Reversal
Authors: C.J. Fogwill1,2, C.S.M. Turney2,3,4, L. Menviel2,5, A. Baker2, M. E. Weber6, B.
Ellis7, Z.A. Thomas2,3,4, N. R. Golledge8,9, D. Etheridge10, M. Rubino1,10,11, D.P. Thornton10,
T.D. van Ommen12,13, A.D. Moy12,13, M.A.J. Curran12,13, S. Davies14, M.I. Bird15,16, N.C.
Munksgaard15,17, C.M. Rootes18, H. Millman1,4, J. Vohra2, A. Rivera19,20, A. Mackintosh21, J.
Pike22, I.R. Hall22, E.A. Bagshaw22, E. Rainsley1, C. Bronk-Ramsey23, M, Montenari1, A.G.
Cage1, M.R.P. Harris1, R. Jones24†, A. Power24, J. Love24, J. Young25, L.S. Weyrich3,25, A.
Cooper26
Affiliations:
1School
of Geography, Geology and the Environment, Keele University, Staffordshire, UK
2Palaeontology,
Geobiology and Earth Archives Research Centre, School of Biological Earth
and Environmental Sciences, University of New South Wales, 2052, Australia
3ARC
Centre of Excellence in Australian Biodiversity and Heritage, School of Biological
Earth and Environmental Sciences, University of New South Wales, 2052, Australia
4Chronos 14Carbon-Cycle
5Climate
Facility, University of New South Wales, 2052, Australia
Change Research Centre, School of Biological Earth and Environmental Sciences,
University of New South Wales, 2052, Australia
6Department
of Geochemistry and Petrology, Institute of Geosciences, University of Bonn,
Bonn, 53115, Germany
7Research
8Antarctic
School of Earth Sciences, Australian National University, Canberra, Australia
Research Centre, Victoria University of Wellington, Wellington 6140, New
Zealand
9GNS
Science, Lower Hutt, 5001, New Zealand
10CSIRO
Oceans and Atmosphere, Aspendale, Victoria, 3195 Australia
11Dipartimento
di Matematica e Fisica, Università della Campania "Luigi Vanvitelli", viale
Lincoln, 5-81100 Caserta, Italy
12Department
of Agriculture, Water and the Environment, Australian Antarctic Division, 203
Channel Highway, Kingston, Tasmania 7050, Australia
13Antarctic
Climate & Ecosystems Cooperative Research Centre, University of Tasmania,
Private Bag 80, Hobart, Tasmania 7001, Australia
14Department
15Centre
of Geography, Swansea University, Swansea, United Kingdom
for Tropical Environmental and Sustainability Science, College of Science,
Technology and Engineering, James Cook University, Cairns, Australia
16ARC
Centre of Excellence in Australian Biodiversity and Heritage, James Cook University,
Cairns, Australia
17Research
Institute
for
the
Environment
and
Livelihoods,
Charles
Darwin
University, Australia
18Department
of Geography, University of Sheffield, United Kingdom
19
Instituto de Conservación, Biodiversidad y Territorio, Universidad Austral de Chile, Chile
20
Departamento de Geografia, Universidad de Chile, Portugal 84, Santiago 8331051, Chile
21School
of Earth, Atmosphere and Environment, Monash University, Melbourne, Australia
22School
of Earth and Ocean Sciences, University of Cardiff, Wales, UK
23Research
Laboratory for Archaeology and the History of Art, University of Oxford, Dyson
Perrins Building, South Parks Road, Oxford, OX1 3QY, UK
24BioEconomy
Centre, The Henry Wellcome building for Biocatalysis, Biosciences, Stocker
Road, Exeter University, Exeter, EX4 4QD, UK
25Australian
26South
Centre for Ancient DNA, University of Adelaide, 5005, Australia
Australian Museum, Adelaide, South Australia 5005, Australia
†Deceased
Contact Information: *Correspondence to c.j.fogwill@keele.ac.uk
The Southern Ocean occupies some 14% of the planet’s surface and plays a
fundamental role in the global carbon cycle and climate. It provides a direct connection
to the deep ocean carbon reservoir through biogeochemical processes that include
surface primary productivity, remineralisation at depth, and the upwelling of carbonrich water masses. However, the role of these different processes in modulating past and
future air-sea carbon flux remains poorly understood. A key period in this regard is the
Antarctic Cold Reversal (ACR, 14.6-12.7 kyr BP), when mid- to high-latitude Southern
Hemisphere cooling coincided with a sustained plateau in the global deglacial rise in
atmospheric CO2. Here we reconstruct high-latitude Southern Ocean surface
productivity from marine-derived aerosols captured in a highly-resolved horizontal ice
core. Our multiproxy reconstruction reveals a sustained signal of enhanced marine
productivity across the ACR. Transient climate modelling indicates this period
coincided with maximum seasonal variability in sea-ice extent, implying that sea-ice
biological feedbacks enhanced CO2 sequestration and created a significant regional
marine carbon sink, which contributed to the plateau in CO2 at the ACR. Our results
highlight the role Antarctic sea ice plays in controlling global CO2, and demonstrates
the need to incorporate such feedbacks into climate-carbon models.
The Last Glacial Transition (LGT; 18,000-11,000 years ago or 18-11 kyr BP) experienced
rapid and sustained changes in atmospheric CO2 (rising from approximately 190 parts per
million (ppm) to around 270 ppm; Figure 1), providing us with the potential to gain valuable
insights into climate-carbon dynamics1. Detailed analysis of the stable isotopic composition
of atmospheric carbon dioxide (δ13C-CO2)1,2 from Antarctic ice cores suggests terrestrial
carbon may have played a substantial role in rapid CO 2 rises, but variability across the LGT
may reflect a combination of sources, sinks and feedbacks. Parallel changes in Antarctic
temperature and atmospheric CO2 have been interpreted as the Southern Ocean playing a key
role in the global carbon budget3-5, but detailed mechanisms remain unresolved. Several
physical and biological mechanisms have been invoked to explain these observations,
including: changes in the strength and/or latitudinal migration of the mid-latitude jet stream
and prevailing surface westerly airflow influencing Southern Ocean overturning4,6-8;
variations in iron (dust) fertilisation of subantarctic phytoplankton impacting the biological
carbon pump efficiency9-11; sea-ice controlling CO2 exchange12,13 and carbon drawdown14;
and the potential impacts of a warming ocean on CO2 exchange1. The role of the Southern
Ocean as a source or sink of atmospheric carbon during the LGT remains highly contested,
with the above processes not fully accounting for the changes in CO2 recorded over this
period9, implying that one or more mechanisms are currently not captured in our
understanding15,16.
A striking feature of the LGT record is a 1,900 year-long plateau in CO2 concentration, when
the ongoing rise in CO2 paused at a near-constant 240 ppm during the Antarctic Cold
Reversal (ACR)17, a period characterised by surface cooling across the mid- to high-latitudes
of the Southern Hemisphere18-20. The ACR was coincident with sustained warming across the
Northern Hemisphere (the North Atlantic Bølling-Allerød interstadial)9,17 and abrupt global
sea level rise21,22, as well as major disruptions to atmospheric and ocean circulation8,22 and
the carbon cycle (Figure 1)9,10,23. Whilst the global sequence of events during the ACR is
reasonably well known19, a clear understanding of the drivers and impacts of contrasting
polar climate changes on global CO2 trends has proved elusive, owing to the challenges in
precisely aligning ice and marine records across this period9. This reflects the lack of wellresolved, high-accumulation marine sedimentary records from the high-latitude Southern
Ocean.
One crucial record in this regard comes from marine sediment core TN057-13 (~53°S 5°E)4,9
(Figure 2), which suggests the ACR was characterised by reduced carbon sequestration in the
mid to high-latitudes (measured by decreased biological productivity or export production 4,5;
Figure 1E). This was possibly the result of enhanced stratification, which decreased the
vertical supply of nutrients across the high-nutrient, low-chlorophyll (HNLC) sectors of the
Southern Ocean during cooling4. However, such a hypothesis is difficult to test in the absence
of a network of well-resolved records of productivity from the high latitudes of the Southern
Ocean.
Southern Ocean productivity polewards of TN057-13 has been previously recorded in the
Scotia Sea from marine core MD07-3134, (~59°S 42°W; Figures 1F and 2; see
Supplementary Information)21. In common with core TN057-13, this sequence is
exceptionally well-resolved (with sedimentation rates of 20 to 200 cm/kyr21) and, given the
location, records changes south of the Polar Front, even during glacial terminations24. After
accounting for sediment focussing with
230 Th
normalisation (see Supplementary
Information)25, MD07-3134 opal burial rates provide estimated changes in biological
productivity (export production) (Figure 1F). This suggests that export production in the
high-latitude Southern Ocean increased from ~17 ka, in line with that shown to the north in
core TN057-13; however, subsequently, export production in the high-latitude Southern
Ocean (MD07-3134) continued to increase through the ACR, in antiphase to the trend
recorded further north (TN057-13)4 (Figures 1 and 2). This indicates that different driver(s)
of marine biological activity may have operated across the high latitudes, contributing to the
sustained ACR CO2 plateau.
In the absence of a network of highly-resolved marine records from the high-latitude
Southern Ocean (that are normalised through
230Th)24,
we present a new reconstruction of
high-latitude surface ocean productivity from aerosol derived marine biomarkers captured in
a highly-resolved horizontal ice core from the Weddell Sea, Antarctica22 that record regionalscale environmental processes operating across the south Atlantic sector of the Southern
Ocean during the LGT (Figure 2)22,26.
The Patriot Hills blue ice record
A new ‘horizontal’ ice core record was developed from the exposed blue ice area (BIA) at the
Patriot Hills in Horseshoe Valley, Ellsworth Mountains (Figure 2) 22, where ancient ice has
been drawn up to the surface of the ice sheet. With a well-constrained chronology,
uninterrupted sequence of ice through the LGT (Figure 3; Methods), and contemporary
precipitation and aerosol delivery from the South Atlantic sector of the Southern Ocean
(Figure 2; Supplementary Information)27, the Patriot Hills is ideally placed to record
environmental changes across the high-latitude South Atlantic. The record provides
unrestricted volumes of ice of known age, offering a unique opportunity to develop
innovative multiproxy biomarker reconstructions22,28. In contrast to many other BIAs, the site
has not been mixed through ice flow, providing a coherent stratigraphic succession across the
LGT (Figure 3, Methods and Supplementary Information)22,29.
Identifying marine biomarkers in ancient ice
To examine regional environmental responses through the LGT, fluorescent organic matter
(fOM) analysis and liquid chromatography organic carbon detection (LC-OCD)30 was
undertaken across the Patriot Hills record, to identify biomarker signals and quantify changes
in dissolved organic carbon (DOC) before and after the ACR (see Figure 4, Methods and
Supplementary Information)30. Detailed analysis (using an Aqualog®) of fOM emission
spectra from samples taken at depth identified two protein-like components in ice across the
profile, TRYLIS and TYLIS: tryptophan and tyrosine-like substances31 (see Methods and
Supplementary Information). Whilst there are limited studies of such biomarkers in ancient
Antarctic ice32, past work has unambiguously demonstrated that a strong TRYLIS microbial
signal is found in contemporary Antarctic snow and ice derived from precipitation and
aerosols from the marine environment33-35. Previous work on the West Antarctic Ice Sheet
Divide ice core (WAIS Divide) using similar fOM approaches, epifluorescence microscopy
and flow cytometry, has identified chlorophyll and tryptophan in ancient ice, demonstrating
that these are primarily derived from marine aerosol sources, rather than being solely
geomicrobial (in situ) in origin34,35 (Methods and Supplementary Information). These studies
have also identified inter-annual variability in the fOM signal, concluding that in situ
secondary production or post-depositional alteration of fOM in ice are unlikely to be primary
factors in interpreting marine fOM signals in Antarctic ice cores (see Methods and
Supplementary Information)34,35.
To examine the source of the fOM signal in the Patriot Hills BIA, and test our hypothesis of a
marine origin35 we applied imaging flow cytometry (IFC; ImageStream®) and Scanning
Electron Microscopy (SEM) to the Patriot Hills samples to identify microscopic populations
within the ice (Figure 4, see Methods and Supplementary Information). IFC on samples
across the record reveals four significant non in-situ microbial populations (Figure 4C) based
on the autofluorescence and morphology of particulates: nanoplankton36; eukaryotic
picoplankton37; chitin37; and crypto-tephra and/or wind-blown dust22. SEM analysis on
unvortexed samples demonstrates that the eukaryotic picoplankton and the chitin populations
are related (Figure 4D). These marine populations are represented in all samples analysed
throughout the profile, and whilst IFC is not quantitative it provides valuable independent
support for the fOM signal being marine in origin. Together, the fOM, LC-OCD and IFC
analysis indicate that marine biomarkers are present throughout the profile, in agreement with
other Antarctic ice core studies34,35.
Intercomparison of biomarkers from the Patriot Hills BIA
In comparing the records of fOM across the LGT we observe a pronounced intensity peak
related to autofluorescence of marine biomarkers across the ACR section of the Patriot Hills
BIA (Figure 4A and 5F). This change in fOM signal could reflect marked changes in
precipitation source over the LGT; however, we discount this through regime shift analysis38
on the deuterium-excess profile, which reveals no significant variability across the ACR or
the LGT, at either 99% or 95% confidence, indicating that the precipitation source remained
constant over the LGT (Figure 3B). This implies that the intensity of the fOM signal reflects
an increase in the autofluorescent marine biomarkers in the precipitation and aerosol source
regions, associated with nanoplankton, picoplankton and picoeukaryotes as identified through
IFC. We focus on the variation in the TRYLIS fOM component, which represents 83.33% of
the variance in fOM signal (Methods and Supplementary Information). The TRYLIS
component is highly variable across the BIA record, but has a sustained high concentration
across the period defined by the ACR (Figures 4 and 5). This pattern is mirrored in samples
taken from a parallel transect from the Patriot Hills BIA, demonstrating the robustness of the
fOM signal (Extended Data).
To further investigate the detail of the marine biomarker signals, large-volume ice samples
were taken across key transitions of the Patriot Hills BIA to extract ancient bacterial DNA in
situ by directly melting and filtering ice from specific time-horizons –maximising the signal
and minimising contamination (Figure 4B, Methods and Supplementary Information) –
allowing the identification of picoplankton, picoeukaryotes and nanoplankton at a taxa level.
16S rRNA indexing reveals that a marked ecological switch – characterised by the
appearance of an exceptionally diverse range of halotolerant microorganisms commonly
found in seawater – was observed during the ACR, coincident with the increase in fOM
TRYLIS signal (Figure 4B). Specifically, we found that the marine-associated taxa
Salinibacterium,
(f)
Erythrobacteraceae,
Rhodobacteraceae,
Marinobacter
and
Pseudidiomarina are statistically associated with the ACR period (p<0.038). The increase in
species diversity (predominantly marine taxa) compared to that observed during either the
mid-Holocene or Last Glacial Maximum is marked (Figures 4 and 5). Whilst the source of
this signal could have been from brine pools associated with sea-ice build-up, the signal
likely reflects an enhanced diversity and productivity from an open marine, or marginal seaice zone, an interpretation that agrees with the WAIS divide ice core analysis34,35.
With four independent approaches (LC-OCD, IFC analysis, fOM and DNA) providing a
record of marine biological productivity in the high-latitude South Atlantic sector of the
Southern Ocean, our results strongly suggest that the ACR was a period of enhanced marine
biological productivity and diversity. With the enhanced picoplankton and picoeukaryotes
signals derived from the surface precipitation and aerosol source waters of the HNLC
Southern Ocean during the ACR, we suggest that there was sustained strengthening of the
biological pump, similar to the effects of contemporary iron fertilisation experiments16, a
finding that supports the enhanced export production recorded in marine sediments from the
Scotia Sea (Figure 1F)21.
Comparison between marine and terrestrial records
To reconcile the apparent conflict between the increase in marine productivity across the
ACR recorded in marine cores from the Scotia Sea (MD07-3134) and the Patriot Hills BIA
with the decrease reported further north in the South Atlantic (TN057-13)4,9 (Figure 1), we
compare our record of marine biomarkers (fOM) captured in the Patriot Hills ice with
potential drivers of Southern Ocean productivity: iceberg rafted debris (IBRD; a proxy for
Antarctic iceberg discharge)21, sea salt sodium (ssNa+) from the EDML ice core (a proxy for
sea-ice extent)39, and proxy sea-ice reconstructions40,41. We further compare these records to
published independent transient modelling experiments using LOVECLIM, which include
fresh water hosing in the Ross and Weddell Seas42 (Figure 5; Supplementary Information).
During the LGT, these comparisons indicate weak relationships between inferred marine
biological productivity, sea-ice expansion, atmospheric CO2 variability and the peak in
marine derived biomarkers (fOM) between ~24 and ~14.6 kyr BP, agreeing with previous
studies (Figure 5)43. This contrasts with the period defined by the ACR, where we observe a
strong relationship between marine fOM in the Patriot Hills BIA, increased production of
biogenic opal in the Scotia Sea, and the extended atmospheric CO 2 plateau (Figures 1 and 5).
Given that this increase in marine productivity seen in the Scotia Sea during the ACR is not
apparent in mid-latitude marine records (Figure 2)4,9, we focus on possible high-latitude
drivers of CO2 exchange: iron fertilisation from enhanced IBRD flux44; a reduction in
Antarctic Bottom Water (AABW) formation due to enhanced freshwater flux 45-47; and sea-ice
feedbacks40.
IBRD contains high concentrations of bioavailable iron, making iceberg melt a potential
source for increased primary productivity and carbon sequestration through fertilisation
across the HNLC regions of the high-latitude Southern Ocean44. However, despite significant
evidence for potential enhanced iron fertilisation of the Southern Ocean through increased
delivery of IBRD at around 20-19 kyr BP and 17-16 kyr BP21, there does not appear to be a
strong biological response in the Patriot Hills fOM or Scotia Sea opal flux records (Figures 2
and 5), suggesting enhanced IRBD influx did not lead to increased high-latitude marine
export production. Another possibility is ice-sheet drawdown across the Weddell Sea
Embayment21,22, with associated meltwater influx that may have triggered stratification and
substantial circulation changes across the broader Southern Ocean, magnified by associated
shifts in the intensity and/or location of surface westerly air flow4,9,22,48; this is supported by
independent ice-sheet and Earth system modelling experiments21,42. However, the disparity in
the opal flux records between marine cores from the mid-latitude South Atlantic4 and Scotia
Sea argues that the enhanced ACR export production was focussed on the high-latitude South
Atlantic across the Scotia Sea (Figure 1).
An alternative mechanism involves sea-ice feedbacks, which have been implicated in
amplifying climate and ice sheet feedbacks across the ACR 19,46. Recent studies of full glacial
conditions suggest that reduced surface–deep ocean exchange and enhanced micro nutrient
consumption by phytoplankton in the Southern Ocean may have lowered atmospheric
CO240,43. During the austral winter, sea-ice expansion allowed the mixed layer to deepen,
‘refuelling’ the surface ocean with micro nutrients from the deep ocean reservoir, and
enhancing near-surface productivity and export production during the breakup of sea ice in
the subsequent summer. This was likely amplified by the addition of iron from sea-ice melt
and breakup in the post-glacial HNLC ocean, and possibly also by seasonal temperature
changes and CaCO3 dissolution13. Proxy records and the LOVECLIM transient Earth system
modelling42 suggest the highest seasonal variability in sea-ice extent across the LGT took
place during the ACR (with greatest extent during winter and spring) (Figure 5), implying
that sea-ice feedbacks were amplified across this period (Figure 6). These conditions contrast
markedly with the periods immediately prior to (Figure 6A) and following (Figure 6D) the
ACR, when the seasonal sea ice zone was relatively less variable (Figure 5), the high-latitude
Southern Ocean less stratified21,42,46, and the locations of the Intertropical Convergence Zone
(ITCZ) and mid-latitude Southern Hemisphere Westerlies were relatively south (Figure 2).
Set against a backdrop of a warming ocean during the LGT, these conditions likely created
ideal conditions for enhanced Southern Ocean productivity in the high-latitude Southern
Ocean, especially in sectors of the South Atlantic such as the Weddell and Scotia Seas.
Comparison between our continuous Scotia Sea opal flux record 21 and the Patriot Hills BIA
fOM record indicates the high-latitude signal of enhanced surface marine primary
productivity was related to marked seasonal sea-ice variability during the ACR, a period
characterised by a sustained atmospheric CO 2 plateau9,17,23. During the ACR, most marine
records across the mid-latitudes suggest the biological pump in the Southern Ocean
weakened, in apparent contradiction of the plateau in atmospheric CO 2 at that time (Figure
1). Our results indicate that despite low dust input (Figure 1) and surface cooling across
subantarctic waters during the ACR, marked variability in sea-ice extent resulted in increased
seasonal surface productivity in the HNLC waters of the high-latitude South Atlantic sector
of the Southern Ocean, in comparison to periods prior to and following this event (Figure 5).
We suggest that increased seasonal marine primary productivity in fact enhanced the
Southern Ocean organic carbon pump, increasing carbon drawdown and leading to enhanced
export production (Figure 6). Whilst other mechanisms may have played a part in the ACR
CO2 plateau – including iron fertilisation, cool Southern Ocean surface temperatures and
possibly reductions in the rate of AABW formation8 – our observation that seasonal Southern
Ocean sea-ice feedbacks in the South Atlantic sector of the high-latitude Southern Ocean may
have contributed to a slowdown in the rate of CO 2 rise during the ACR has significant
implications for our understanding of the role of the Southern Ocean in global carbon
dynamics. Our results imply that during periods of Southern Ocean sea-ice expansion, high
variability in winter and summer sea-ice extent may result in enhanced carbon sequestration –
as seen recently with significant sea ice variability enhancing benthic carbon drawdown14 –
providing a negative feedback during periods of rising CO2. This finding has ramifications
for our understanding of contemporary ice-ocean-carbon feedbacks, and confirms the
dynamic role Antarctic sea ice plays in providing a negative feedback during periods of rising
CO2. This mechanism requires detailed modelling assessment with high-resolution tracer
enabled models that capture such processes 49, particularly given recent Antarctic sea ice
changes50, which may impact the efficiency of the Southern Ocean as carbon sink in the
future14.
Figure Captions
Figure 1. Intercomparison of Antarctic ice core with marine proxy records from independent
referenced studies. a. WAIS divide core (WDC51) δ18O isotopic record. b. CO2 concentration
from WDC (WD2014 chronology)17 c. Cariaco Basin grey scale (measure of latitudinal
changes in the trade winds related to the Intertropical Convergence Zone (ITCZ)48). d. nonsea salt Ca2+ (nssCa2+) from EPICA Dronning Maud Land (EDML)52. E. South Atlantic opal
flux from TN057-13 (blue)4. F. Scotia Sea opal flux core MD07-3134 (red)21. Vertical boxes
indicate the periods defined by the Antarctic Cold Reversal (ACR) (blue), the Younger Dryas
(YD) chronozone (pink; 11.7-12.7 kyr BP).
Figure 2. The South Atlantic sector of the Southern Ocean with the locations of Patriot Hills
in the Ellsworth Mountains, the EPICA Dronning Maud Land (EDML) ice core52, and marine
cores MD07-313421 and TN057-134. Positions of the southern limb of the Antarctic
Circumpolar Current (purple line), the polar front (red), subantarctic front (green) and the
subtropical front (yellow)53. Inset. Monthly grouped 72-hour atmospheric back trajectories
for the Patriot Hills (November 2009), from the NOAA HySPLIT54, with WAIS Divide
(WDC) and EDML ice cores. South Pole Stereographic basemap produced in Generic
Mapping Tools v5.4.5 (ref55) with the NOAA ETOPO1 Ice Surface dataset.
Figure 3. Stratigraphic and chronological details of the Patriot Hill Blue ice area (BIA). a.
Schematic stratigraphic succession from Ground Penetrating Radar (GPR), across the Patriot
Hills BIA, indicating ice accumulation punctuated by two periods of erosion (D1 and D2;
thick black lines), and the position of known tephras (red lines)22. b. d-excess across profile;
solid horizontal black lines denote potential regime shifts at 99% confidence, dashed black
lines denote potential regime shifts at 95% confidence38. c. Age-depth model between D1
~21 ka (21,000 years) and D2 ~10 ka (10,000 years) with volcanic ‘tephra’ horizons (TD822a
and WCM-93-25) marked (see Supplementary Information22).
Figure 4. Marine biomarkers from Patriot Hills blue ice area (BIA). a. 5m resolved fOM
intensity. b. Percentage marine taxa from 16S rRNA extractions (top Powerlyzer, middle
CTAB), and (Lower) LC-OCD component analysis with dissolved organic carbon (DOC;
ppb). LGT and ACR periods highlighted in grey and blue respectfully. c. Marine populations
from IFC (ImageSteam®) (sample 380 m), i) Nanoplankton, ii) Eukaryotic picoplankton, iii)
Chitin, and iv) non-fluorescent dust (left to right: brightfield (Ch01), autofluorescence (Ch02)
and side scatter (Ch06)). Sub-populations differentiated based on Intensity vs Aspect ratio
(central plot). d. SEM of picoeukaryotes with chitin (tails) at 7,000 and 16,000 magnification.
Figure 5. Regional climate proxy and model intercomparisons with the Patriot Hills record.
a. Diatom transfer function-based winter sea-ice concentration41. b. Sea salt (ssNa+) from
EPICA Dronning Maud Land (EDML)52. c. Iceberg-rafted debris flux (IBRD) from MD07313421 (normalised 100-year, relative to Holocene). d. Modelled seasonal difference in
Antarctic sea-ice area (LOVECLIM42). e. Percentage marine microorganisms from 16S
rRNA CTAB extraction (upper), and Powerlyzer (Lower). f. fOM concentration (Component
1; TRYLIS). Vertical boxes indicate the Antarctic Cold Reversal (ACR) (blue), and Younger
Dryas (YD) chronozones (11.7-12.7 ka). Black triangles represent the age tie points.
Figure 6. Schematic depicting events across mid to high-latitude Southern Ocean during the
Last Glacial Transition. a. Post-Last Glacial Maximum (LGM). Displacement of the Southern
Hemisphere Westerlies (SHW), enhances overturning of mid-latitude Southern Ocean
between ~17 ka- 14.7 ka evidenced by opal flux4. b. Antarctic Cold Reversal (ACR).
Enhanced intrusion of Circumpolar Deepwater (CDW) and winter sea-ice (WSI) expansion
(winter / spring winter). Increased stratification, mixed layer deepening and reduction in
Antarctic Bottom Water (AABW)40. c. ACR (summer/autumn), WSI break up enhances CO2
drawdown at high latitudes. d. Younger Dryas chronozone, reinvigorated mid-latitude
overturning and degassing of old CO2 enhancing opal flux.
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Acknowledgments: CJF, CSMT, LM, NRG, LSW and AC are supported by their respective
Australian Research Council (ARC) and Royal Society of NZ fellowships, and CJF and AC
thank Keele University for a Research Development Award that underpinned this research at
Keele University Ice Lab and Exeter University. Fieldwork was undertaken under ARC
Linkage Project (LP120200724), supported by Linkage Partner Antarctic Logistics and
Expeditions whose enduring support we gratefully acknowledge. CSIRO’s contribution was
supported in part by the Australian Climate Change Science Program (ACCSP), an
Australian Government Initiative. SMD acknowledges financial support from Coleg
Cymraeg Cenedlaethol and the European Research Council (ERC grant agreement no.
25923). MEW acknowledges support from the Deutsche Forschungsgemeinschaft (grant
We2039/8-1). Finally, we thank Dr Helen Glanville for comments on the final draft of the
manuscript.
Author contribution: CJF, CSMT, AB and AC conceived this research. CJF, CSMT, AB,
MEW, DE, MR DPT, TDvO, ADM, MAJC, SD, MB, NCM, JV, AR, LM, HM, CM, JY,
MM, AC, MH, AP, JL, LSW and AC undertook analysis and sampling. CJF, CSMT, AB,
MEW, MH and AC wrote the manuscript with input from all the authors.
Data availability: The data supporting this study is available at National Oceanic and
Atmospheric Administration Paleoclimatology Database
(https://www.ncdc.noaa.gov/paleo/study/29415), the data from core MD07-3134 are
available on the PANGEA Database http://dx.doi.org/10.1594/PANGAEA.819646.
Competing interests: The authors declare no competing interests.
Additional information: Extended data and supplementary information accompanies the online version of this paper at www.xxxxxxx.
Corresponding author: Correspondence and requests for materials should be addressed to
Professor Christopher Fogwill at c.j.fogwill@keele.ac.uk
Methods
Patriot Hills site description and chronology
The Patriot Hills BIA (Horseshoe Valley, Ellsworth Mountains; 80°18′S, 81°21′W) is a slow
flowing (<12 m yr-1), locally-sourced compound glacier system situated within an overdeepened catchment that is buttressed by, but ultimately coalesces with, the Institute Ice
Stream close to the contemporary grounding line of the AIS22. The Patriot Hills BIA record is
chronologically constrained by multiple greenhouse gas species (CO 2, CH4 and N2O)
supported by geochemically identified volcanic (tephra) horizons (Figure 3 and
Supplementary Information); here we build on the chronology of previous studies 22 with
increased sampling and the identification of more tephras, to provide tighter age control
through the LGT. The age model demonstrates that this part of the BIA sequence spans from
~2.5 to 50 kyr BP, with two unconformities (Discontinuities D1 and D2), that mark the buildup to (D1), and deglaciation from (D2), the last glacial cycle (Figure 3)22. High-resolution
ground penetrating radar and detailed analysis of trace gases and volcanic tephra horizons 22
demonstrate that the conformable BIA layers (or ‘isochrons’) between these two
unconformities span the period between ~11 to ~23 kyr BP (Figure 3C). Thus, the horizontal
ice core captures a unique highly-resolved record of ice-sheet dynamics22, in an area of
exceptionally slow moving ice29, with no chronological breaks or unconformities across the
LGT (see Figure 3A). Source areas for delivery of air masses to the Patriot Hills were
investigated using the NOAA HySPLIT Lagrangian single-particle model54; interfacing and
model parameterization was performed with ëSplitRí and ëopenairí packages for Rv3.6.0.
Back-trajectories were forced with GDAS 1∞ meteorological data and generated at 6-hour
intervals,
resulting
in
112-124
(https://ready.arl.noaa.gov/HYSPLIT.php.).
trajectories
per
month
Climate reanalysis27 and HySplit particle
trajectory analysis demonstrate that contemporary snow and marine aerosol delivery at the
site is associated with low-pressure systems that have either tracked across the Weddell Sea
from the southern Atlantic Ocean, or that relate to blocking by the Antarctic Peninsula
(Figure 2; see Supplementary Information)26,27,56,57. As such, the Patriot Hills BIA profile
provides an opportunity to obtain large volume ice samples of known ages for innovative
multiproxy biomarker reconstruction, making it the ideal site to build up a record of
environmental and ice sheet change in this sector of Antarctica22.
Sampling strategy
Sterile discrete samples were extracted from depth across the 800 m Patriot Hills BIA profile.
For the fOM analysis samples were taken across the full profile at ~5m resolution (Figure 4).
To remove surface contaminants, the team first drilled down to 10 cm with a Jiffy ice drill to
expose a fresh ice surface. Using a cleaned hand drill, a ~50 mm long x ~25 mm wide ice
plug was extracted from the fresh surface and transferred into a gamma-sterilised 50 ml
centrifuge tube that was sealed and double bagged. Samples were kept frozen until analysis,
then thawed naturally in a refrigerator and analysed within 48 hours before measurement
against water and quinine sulfate blanks with no sample manipulation or pre-treatment on an
Aqualog® at UNSW Icelab (see supplementary information).
Fluorescence organic matter analysis (fOM)
Detailed analysis of the fOM fluorescence emission spectra (using an Aqualog®) from
samples taken at depth identified two protein-like components in ice across the profile and in
contemporary snow (see Supplementary Information). Due to their excitation-emission
wavelengths, we can unambiguously identify these fOM biomarker components as those
widely reported in precipitation as TRYLIS and TYLIS: tryptophan and tyrosine-like
substances31, with TRYLIS making up over 83% of the total fOM signal in all samples
analysed (see Supplementary Information). Whilst there are limited studies of such
biomarkers in ancient Antarctic ice32, past work has unambiguously demonstrated that a
strong TRYLIS microbial signal is found in Antarctic snow and ice derived from
precipitation and aerosols from the marine environment33-35. Indeed, previous work on the
WAIS Divide ice core using similar fOM approaches, epifloresence microscopy and flow
cytometry, has identified chlorophyll and tryptophan in ancient ice, and demonstrated that
these are derived from a marine aerosol source as opposed to being geomicrobial (in situ) in
origin34,35. Furthermore, results from the WAIS Divide core also highlight that there is
seasonal variability in the marine biomarker signal, with an estimated ~25% inter-annual
variability at this inland site, and crucially that alteration of fOM in ice is unlikely to be a
factor in interpreting the fOM signal in Antarctic ice core studies 35.
To test for reproducibility of fOM available a selection of samples from a second parallel
transect were run at UNSW Icelab in 2015, and subsequently at Keele Icelab on a different
Aqualog® in 2019 (see Supplementary Information). Despite storage, the reproducibility
between the transects and repeated analysis was robust and coherent (Figure S2).
Identification of marine biomarker populations in ancient ice
IFC analysis identified four populations in ancient and contemporary ice samples (Figure 4
and Supplementary Information). The first population is composed of dark angular particles
~5-12m in length, that have a high autofluorescence (Ch02), and a 3-D structure evidenced
from a strong side scatter (Ch06) signal, which we classify as nanoplankton 36. The second
population is characterised by spheroidal forms ranging in diameter from ~2-5 m, that again
have a high autofluorescence (Ch02), and a 3-D structure evidenced from a strong side scatter
(Ch06) signal, which we identify as eukaryotic picoplankton and picoeukaryotes 37. The third
population is characterised by elongate spicules or rods between 2-10 m, that have a high
autofluorescence, and a 3-D structure evidenced from a side scatter (Ch06) signal, which we
identify as chitin, most likely related to the second population of eukaryotic picoplankton and
picoeukaryotes37, an interpretation confirmed through SEM (Figure 4D). Finally, a fourth
population comprising an inorganic fraction ranging from ~2-10m in length, characterised
by a flaky flat structure and no autofluorescence, which we interpret as a mixture of crypto-
tephra, and / or wind-blown dust22. Beyond these four populations few other events were
recorded; these were identified as broken diatom frustules, characterised by a high
autofluorescence and a side scatter signal (see Supplementary Information). These
populations represent far travelled ‘aerosol’ transported marine detritus, which is not in situ
derived or geomicrobial in origin35. Those with high autofluorescence (the eukaryotic
picoplankton and picoeukaryotes and chitin) clearly impact the fOM signal, but do not
apparently significantly alter the DOC content of the sample; we suggest this reflects the fact
that such planktonic forms represent an important dissolved inorganic carbon component of
ancient ice from the Patriot Hills BIA record.
Of the populations identified through IFC, the nanoplankton, eukaryotic picoplankton and
picoeukaryotes and chitin populations made up ~46% of the total, with the non-fluorescent
signal comprising ~12%. Finally ~43% of the signal is unclassified at present and includes
particulate less than 2µm, which is difficult to identify due to its small size. However, ~20 %
of events within this fraction are characteristic of smaller picoeukaryotes, displaying similar
properties to eukaryotic picoplankton identified in the > 2 µm fraction 37. The remaining
particulate is comprised of ‘elongate fluorescent rods’ (likely chitin), and unclassified angular
and round particulate matter again with high autofluorescence (Figure 4 and Supplementary
Information).
The fact that the picoplankton, picoeukaryotes and chitin populations (>2µm) were not
recorded as one population in the IFC analysis was interesting, and likely reflects the process
of the flow cytometry, where sheath fluids run through the machine at the same time as the
sample – this focuses the sample in a steady stream, so that each ‘event’ can be analysed
individually. This effect, or possibly vortexing prior to analysis, may have disaggregated the
picoplankton and picoeukaryotes, separating the tails (chitin) from the spheroidal ‘body’ (see
Supplementary Information). To test this, Scanning Electron Microscopy (SEM) analysis was
undertaken on samples that had not been previously unfrozen or analysed. SEM imaging
demonstrated unambiguously that whole picoplankton and picoeukaryotes were present in the
water samples from ancient ice, complete with chitin (Figure 4D)37.
Defining exotic aerosol derived marine biomarker populations from in situ geomicrobial
biomakers
fOM analysis across the Patriot Hills BIA profile indicates that the TRYLIS intensity is a
persistent signal, highly variable across centennial and millennial timescales. The relationship
between in-situ microbial (geomicrobial) production within a given medium and the resulting
TRYLIS signal is complex, with microbes capable of producing TRYLIS fluctuations prior to
population growth, and creating secondary fluorophores as a result of metabolic activity 58.
Given the absence of a relationship between any LC-OCD dissolved organic carbon (DOC)
components and the TRYLIS signal, and the IFC analysis identifying the microbial fraction
as being predominantly planktonic in nature, we assert that secondary in-situ metabolic
activity is an unlikely explanation for the observed fluctuations in the TRYLIS fluorescence
signal at Patriot Hills (Figure 4B). It is possible, or even likely, that the presence and/or
metabolic activity of microbial populations existing in-situ accounts for a portion of the low
‘baseline’ fluorescence exhibited across many portions of the profile (Figure 4A).
It is also possible that external ‘fertilisation’ by the observed marine inputs could constitute a
nutrient source for in-situ production, thereby contributing to the TRYLIS intensity signal.
However, IFC analysis demonstrates that the significant changes in the fOM signal across the
profile relate to the presence of microscopic marine plankton, principally picoplankton and
picoeukaryotes, but also with nanoplankton populations up to ~8m in size.
The distinct planktonic populations identified from IFC are particularly interesting, and as
recorded in contemporary mesoscale experiments16, picoplankton and picoeukaryotes form
the basis of the pelagic community’s response to iron fertilisation in the high-latitude HLNC
Southern Ocean, and are potentially key to CO 2 drawdown in the polar Southern Ocean15.
The origin of these organisms can only be explained by precipitation or aerosols derived
marine detritus from the high-latitude Southern Ocean26,34,35,56,57. With the TRYLIS
component also being identified in the WAIS Divide core34 and in the fOM signal in
contemporary snow cores from the Patriot Hills site that record the past decade (see Methods
and Supplementary Information), fOM provides a rapid, reproducible measure of highlatitude surface marine productivity that may be directly linked to export production in this
sector of the Southern Ocean16,34,35. This premise is testable through comparison with
analyses of marine sediments from sites such as the Scotia Sea (Figure 1F).
Analysis of ancient DNA in the Patriot Hills BIA
To analyse the DNA content of the ancient ice across the Patriot Hills profile, a new protocol
for extracting DNA from large (~5-7 L) discrete ice core samples was devised (see
Supplementary Information). The novel ability to process very large volume samples of
ancient Antarctic ice in the field (i.e. ~7 kg per temporal sample) under sealed sterile
conditions creates a powerful new opportunity to generate sufficient concentration to permit
detailed genetic biodiversity surveys. Samples were extracted across the profile to extract 16S
ribosomal RNA (rRNA) for analysis at 7.5 kyr BP, 13.7 kyr BP, 16.0 kyr BP, 24 kyr BP and
35 kyr BP to compare taxa across the profile to better understand the diversity of the
biomarkers captured in the record. Whilst a limited sample set, the samples covered the full
range of glacial to interglacial conditions from the profile, and crucially the LGT (Figure 4).
Strict ancient DNA methodologies designed to assess low-biomass microbial samples were
applied at all times. Within ACAD, all work was conducted within a UV-treated hood in a
still-air room. Each 0.45-micron nitrocellulose filter was cut in half using a sterile scalpel
blade. Using sterilised tweezers, one half of the filter was extracted using the PowerLyzer
Soil DNA Isolation kit (MOBIO, Carlsbad, CA, USA), following the manufacturer’s
instructions, and the second was extracted using the CTAB method59. Both extraction
methods were employed to examine microorganisms with different cellular wall structures.
Extraction blank controls (EBCs), i.e. extractions containing no sample, control samples from
the field (e.g. swabs of coring and filtering equipment), and blank filters were processed in
parallel to monitor background DNA levels from laboratory reagents.
Following strict ancient DNA techniques60, all DNA extracts and EBCs were amplified using
published, universal bacterial 16S rRNA primers that are modified to include Illumina
sequencing adapters and a unique sample specific 12 bp Golay barcode61; forward
primer515F
(AATGATACGGCGACCACCGAGATCTACACTATGGTAATTGTGTGCCAGCMGCCG
CGGTAA)
and
barcoded
reverse
primer
806R
(CAAGCAGAAGACGGCATACGAGATnnnnnnnnnnnnAGTCAGTCAGCCGGACTAC
HVGTWTCTAAT). PCR amplifications of the 291 target region were performed in a 25 μL
reaction mix containing: 2.5 mM MgCl2, 0.24 mM dNTPs, 0.24 μm of each primer,
Invitrogen Platinum HiFi Taq polymerase in 10x reaction buffer (Applied Biosystems,
Melbourne Australia), and 2 μL DNA extract. The PCR protocol included the following
parameters: 6 mins at 95oC, followed by 35 cycles of 95oC for 30 sec, 50oC for 30 sec, and
72oC for 30 sec, and a final extension at 60oC for 10 mins. PCR amplifications were
performed in triplicate and pooled to minimise PCR bias, and a no-template PCR
amplification control was included to monitor background DNA levels in PCR reagents.
Pooled PCR products were purified using an Agencourt AMPure XP PCR Purification kit
(Beckman Coulter Genomics, NSW), and quantified using the HS dsDNA Qubit Assay on a
Qubit 2.0 Fluorometer (Life Technologies, Carlsbad, CA, USA). Purified PCR products from
all samples were pooled at equimolar concentrations, and diluted to 2nM for sequencing
using a 300 cycle, 2x150bp Illumina MiSeq kit.
Following DNA sequencing, all individually indexed 16S rRNA libraries were demultiplexed from raw bcl files using CASAVA version 1.8.2 (Illumina), allowing for one
mismatch. Sequencing adapters were removed from reads using Cutadapt v.1.1, and
sequences were quality filtered (i.e. reads >100 bp and >Q20 for 90% of each sequence)
using
fastx
toolkit
v.0.0.14
(https://github.com/agordon/fastx_toolkit.git).
Processed
sequences were then formatted for use with QIIME v.1.8.062, and sequences with greater than
97% similarity to the Geengenes v13 reference database63 were binned into Operational
Taxonomic Units (OTUs) using closed reference clustering in UCLUST. Representative
sequences of each OTU were chosen by selecting the most abundant sequence from collapsed
sequences. To assess the levels of contamination from laboratory reagents, OTUs detected in
the EBCs, known laboratory contaminants64, and genera identified in the Human Oral
Microbiome Database (HOMD)65 were filtered from the experimental samples. After
filtering, an average of 1.417 sequences per sample remained (minimum of 4 and maximum
7,174 sequences per sample). Extraction methods for each location were pooled, and alpha
diversity (diversity within the sample) was compared using Simpson’s, Chao 1, and observed
species indexes in QIIME with the following parameters (min: 20; max: 200; step: 10); no
statistically significant differences in diversity were detected. Specific taxa were summarized
by collapsing OTUs at the genus level (Figure 4). Marine taxa were identified by
comparisons to Tara Oceans66, or by performing literature searches for the ‘taxa name;
marine’ and determining if a marine source for the taxa was present within the first ten
publications (see Supplementary Information).
Methods References
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348 (2015).
12
14
kyr BP
16
18
20
22
24
34
38
240
220
40
YD ACR
ITCZ
North
200
210
200
190
ITCZ
South
42
Cariacao Basin
Grey scale
WAIS CO2 (ppm)
260
180
170
+
c
Dust Fux
200
–
Export Production
6
4
2
0
0
+
f
Scotia Sea Opal Flux
(g cm–2 kyr–1)
South Atlantic Opal Flux
(g cm–2 kyr–1)
100
1.0
–
0.5
12
14
16
18
kyr BP
20
d
EDML nssCa2+
e
WDC δ18O (‰)
b
36
a
22
24
0
m
8000
˚W
0˚
10˚W
20˚W
10˚E
20˚E
30
˚E
30
30
˚S
W
0˚
4
˚W
0
40
50
˚S
60
˚
W
TN057-13
50
˚S
−8000
70˚
W
Dust Delivery
˚S
ry
cto
Patriot
Hills
EDML
˚S
60°S
0°
65°S
60°S
70
70°S
Patriot Hills
EDML
WDC
75°S
70°S
80°S
75°S
80
˚S
90°E
90°W
80˚S
70˚S
60˚S
50˚S
40˚S
Pre
val
ent
Ae
ros
ol
Tra
je
80˚W
IBRD
WSE
30˚S
60
MD07-3134
75°S
65°S
70°S
75°S
180°
Patriot Hills Profile (m)
a
700
800
600
500
400
300
D2
760
Elevation (m)
200
100
0
D1
750
740
730
720
710
700
b
Towards centre of Horseshoe Valley
D2
8
Proximal to Patriot Hills
D1
d-excess
6
4
2
0
-2
700
800
20
600
500
400
300
200
100
0
D1
D2
18
16
TD822a
14
12
WCM-93-25
Kyr BP
c
10
360
350
340
330
320
310
300
Patriot Hills Profile (m)
290
280
270
260
Key
800
16S rRNA Taxa
700
600
Salinibacterium
Arthrobacters nasiphocae
Nocardioides
(f) Erythrobacteraceae
(f) Sphingomonadaceae
Sphingobium
Marinobacter
Pseudidiomarina
(o) Alteromonadales (f) OM60
Shewanella
(f) Halomonadaceae
Halomonas
Aurantimonas
Synechococcus
Balneola
Sphingobacterium
Arenibacter
Sulfurospirillum
No marine taxa
+
500
400
300
200
ACR
100
–
0
b
16S rRNA and LC-OCD
Analysis for key periods
16S rRNA Powerlyzer
16S rRNA Powerlyzer
16S rRNA CTAB
LC-OCD analysis
DOC 1,831 ppb
LC-OCD analysis
DOC 1,704 ppb
~7.5 kyr BP
380
c
16S rRNA CTAB
340
16S rRNA Powerlyzer
16S rRNA Powerlyzer
16S rRNA Powerlyzer
16S rRNA CTAB
16S rRNA CTAB
320
~24.0 kyr BP
~16.0 kyr BP
300
280
260
Populations from
ImageStream® analysis
240
~35.0 kyr BP
220
200
ii) Eukaryotic picoplankton
d. SEM: Eukaryotic picoplankton
C.
iii) Chitin from picoplankton
16S rRNA CTAB
Distance across Patriot Hills BIA Profile (m)
i) Nanoplankton
7 µm
Humics
Building Blocks
LMW Acids
LMW Neutrals
LC-OCD analysis
DOC 1,495 ppb
~13.7 kyr BP
360
% compoent
from Liquid chromatography:
organic carbon detection
LC:OCD
Component 1 TRYLIS
fOM sample
16S rRNA sample with age (kyr BP)
fOM TRYLIS
Signal Intensity
a
Patriot Hills BIA
fOM (component 1, TRYLIS)
LGT section of Patriot Hills BIA Profile (m)
i)
7 µm
iv) Crypto-tephra or dust
(Non Fluorescent)
10 µm
ii)
5 µm
7 µm
7 µm
Kyr BP
a
30
20
10
18
20
22
24
+
sea ice %
40
16
YD ACR
60
50
14
100
80
–
60
0
40
b
EDML % ssNa+
Diatom based winter sea ice
concentration %
12
c
0
1.0
d
0.5
18
17
0
Δ seasonal sea ice
16
e
15
14
16S rRNA Taxa
13
Salinibacterium
Arthrobacters nasiphocae
Nocardioides
(f) Erythrobacteraceae
(f) Sphingomonadaceae
Sphingobium
Marinobacter
Pseudidiomarina
(o) Alteromonadales (f) OM60
Shewanella
(f) Halomonadaceae
Halomonas
Aurantimonas
Synechococcus
Balneola
Sphingobacterium
Arenibacter
Sulfurospirillum
No marine taxa
16S rRNA CTAB
–
16S rRNA Powerlyzer
800
Patriot Hills BIA
fOM (component 1, TRYLIS)
f
+
600
400
200
12
0
12
14
16
18
Kyr BP
20
22
24
LOVECLIM seasonal difference
in sea ice area (10*12 km2)
Scotia Sea IBRD
20
70oS
A
50oS
CO2
SHW
fOM
Transport
CO2
WSI
Enhanced
productivity
CDW
AABW
17-14.7 ka
Post LGM configuration
enhanced
opal flux
SHW
fOM
Transport
B
Iron accumulation
WSI
Enhanced
basal melt
Nutrient accumulation
CDW
14.7-12.7 ka
ACR (Winter / Spring)
C
AABW
fOM
Transport
SHW
CO2
CO2
Enhanced
basal melt
CDW
CO2
Enhanced
productivity
and diversity
AABW
14.7-12.7 ka
ACR (Summer / Autumn)
D
low opal
flux
enhanced
opal flux
fOM
Transport
SHW
CO2
CO2
CO2
WSI
CDW
12.6-11.3 ka
Younger Dryas Chronozone
AABW
enhanced
opal flux
CO2