Deep-Sea Coral Evidence for Lower Southern Ocean Surface Nitrate Concentrations During the Last Ice Age
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Deep-sea coral evidence for lower Southern Ocean surface nitrate concentrations during the last ice age Xingchen Tony Wanga,b,1,2, Daniel M. Sigmana, Maria G. Prokopenkoc, Jess F. Adkinsd, Laura F. Robinsone, Sophia K. Hinesd, Junyi Chaif, Anja S. Studerb, Alfredo Martínez-Garcíab, Tianyu Chene, and Gerald H. Haugb,g aDepartment of Geosciences, Princeton University, Princeton, NJ 08544; bClimate Geochemistry Department, Max Planck Institute for Chemistry, 55128 Mainz, Germany; cDepartment of Geology, Pomona College, Claremont, CA 91711; dDivision of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA 91125; eBristol Isotope Group, School of Earth Sciences, University of Bristol, Bristol BS8 1RJ, United Kingdom; fAtmospheric and Oceanic Sciences Program, Princeton University, NJ 08544; and gGeological Institute, ETH Zürich, 8092 Zurich, Switzerland Edited by Mark H. Thiemens, University of California, San Diego, La Jolla, CA, and approved February 15, 2017 (received for review September 20, 2016) The Southern Ocean regulates the ocean’s biological sequestration which speaks more directly to air–sea CO2 exchange, is how the of CO2 and is widely suspected to underpin much of the ice age de- degree of nutrient consumption varied in each of these two zones of cline in atmospheric CO2 concentration, but the specific changes in the the Southern Ocean. region are debated. Although more complete drawdown of surface The nitrogen isotopic composition of organic matter has the − nutrients by phytoplankton during the ice ages is supported by some potential to record the degree of nitrate (NO3 ) consumption in sediment core-based measurements, the use of different proxies Southern Ocean surface waters in the past. During nitrate uptake, in different regions has precluded a unified view of Southern phytoplankton preferentially consume 14Nrelativeto15N, resulting Ocean biogeochemical change. Here, we report measurements in a correlation between the δ15N of sinking organic matter and the of the 15N/14N of fossil-bound organic matter in the stony deep- fraction of the nitrate supply that is consumed in the surface ocean, Desmophyllum dianthus 15 15 14 15 14 sea coral , a tool for reconstructing surface where δ N = [( N/ N)sample/( N/ N)air] − 1. The early applica- ocean nutrient conditions. The central robust observation is of higher tion of this correlation was with bulk sedimentary N (10). However, 15N/14N across the Southern Ocean during the Last Glacial Maximum bulk sedimentary δ15N can be biased due to diagenetic alteration (LGM), 18–25 thousand years ago. These data suggest a reduced sum- and contamination by foreign N input, with evidence for major mer surface nitrate concentration in both the Antarctic and Subant- artifacts from these processes in sediment records from both low- arctic Zones during the LGM, with little surface nitrate transport and high-latitude sites (11, 12). The δ15N of organic matter bound between them. After the ice age, the increase in Antarctic surface within diatom and foraminifera microfossils avoids these issues and nitrate occurred through the deglaciation and continued in the Holo- has been applied to reconstruct the nitrate consumption in the AZ cene. The rise in Subantarctic surface nitrate appears to have had and SAZ of the Southern Ocean, respectively (12, 13). both early deglacial and late deglacial/Holocene components, prelim- To complement isotopic studies of planktonic microfossil-bound inarily attributed to the end of Subantarctic iron fertilization and in- N, we have pursued the N isotopic composition of organic matter creasing nitrate input from the surface Antarctic Zone, respectively. bound within the carbonate skeleton of deep-sea scleractinian corals (14). Relative to the sedimentary microfossil-based δ15Nre- Southern Ocean | nutrient consumption | atmospheric CO2 | ice ages cords, deep-sea corals have the advantages that (i) they feed on organic matter that derives from the sinking flux out of the surface hytoplankton grow in the sunlit surface waters of the ocean, ocean, the δ15N of which is forced by mass balance to covary with ii Ptransforming carbon dioxide (CO2) into organic carbon, and the degree of nitrate consumption in surface waters (14); ( )they the portion of this organic carbon that sinks out of the surface ocean “ ” ( export production ) effectively transfers CO2 from the surface Significance waters and the overlying atmosphere into the dark, deep ocean. In parallel with carbon, the nutrients required in large quantities by all The concentration of atmospheric carbon dioxide (pCO2) varies by phytoplankton (the “major nutrients” nitrogen, N, and phosphorus, 80–100 ppm on glacial–interglacial timescales, with lower pCO2 P) are also exported out of the surface ocean and stored in the deep during the ice ages. In the modern Southern Ocean, the surface ocean. The “efficiency” of the biological pump is a global measure nutrients are not fully consumed by phytoplankton, resulting in of the degree to which marine organisms exploit the major nutrients leakage of deeply sequestered CO2 to the atmosphere. It has been in the ocean to produce sinking organic matter. A higher efficiency suggested that more complete nutrient consumption in the of the biological pump stores more CO2 in the deep ocean, lowering Southern Ocean would have caused the lower pCO2 during the ice the partial pressure of CO2 (pCO2) in the atmosphere (1). ages. Here, we provide the most spatially comprehensive evi- In today’s Southern Ocean, due to limitation by light and the dence to date in support of the proposal that the entire Southern trace nutrient iron (2, 3), phytoplankton consume only a small Ocean was nutrient-depleted during the last ice age relative to fraction of the available N and P, lowering the efficiency of the modern conditions. These data are consistent with the hypothesis global ocean’s biological pump, which is manifested regionally as that Southern Ocean changes contributed to the lower atmo- p the leakage of deeply stored CO2 through the Southern Ocean spheric CO2 of the ice ages. surface and back to the atmosphere (4). Changes in the degree of N and P consumption in the Southern Ocean may have played a role Author contributions: X.T.W., D.M.S., M.G.P., and G.H.H. designed research; X.T.W., D.M. p – S., and M.G.P. performed research; X.T.W., J.F.A., L.F.R., S.K.H., A.S.S., A.M.-G., and T.C. in past changes in atmospheric CO2, especially on glacial contributed new reagents/analytic tools; X.T.W. and J.C. analyzed data; and X.T.W. and interglacial timescales (5). Since the discovery that the ice age D.M.S. wrote the paper. p p CO2 was approximately one-third lower than the preindustrial CO2 The authors declare no conflict of interest. (6), research has been ongoing to reconstruct the biogeochemistry of This article is a PNAS Direct Submission. the Southern Ocean over glacial cycles (5, 7, 8). Relative to inter- 1Present address: Division of Geological and Planetary Sciences, California Institute of glacials such as the Holocene, reconstructed ice age export pro- Technology, Pasadena, CA 91125. duction was higher in the Subantarctic Zone (SAZ) but lower in the 2To whom correspondence should be addressed. Email: [email protected]. Antarctic Zone (AZ) (5, 9). Understanding this pattern requires This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. additional biogeochemical information. A complementary constraint, 1073/pnas.1615718114/-/DCSupplemental. 3352–3357 | PNAS | March 28, 2017 | vol. 114 | no. 13 www.pnas.org/cgi/doi/10.1073/pnas.1615718114 Downloaded by guest on September 27, 2021 can be precisely dated with uranium–thorium (U–Th) and also be contributing to the range in recent coral δ15N at those sites. radiocarbon methods, with each coral being an independent Among the Southern Ocean corals studied here (Fig. S2) and others constraint on past conditions; and (iii) they are found in both the that have been investigated (14), there is no shared trend in δ15N SAZ and AZ and thus can provide a complete picture of the through individual septa. Thus, the δ15N variability both within septa Southern Ocean from a single fossil type, down to the species and across specimens is best explained by environmental variability, level. The >250 fossil corals used in this study were collected as opposed to an ontogenetic effect, but this does not allow us to from the Drake Passage (DP), with collection sites in both the distinguish between regional change in sinking N δ15N(thesignalof AZ and SAZ, and from the SAZ south of Tasmania (Fig. 1). interest) and local deep-particle dynamics. Further ground-truthing All of the corals used in this study are of the solitary species will be required to assess the significance of such short timescale Desmophyllum dianthus. The corals were dated by radiocarbon, variation in coral δ15N, which we avoid interpreting here. However, with ∼50 of them also dated using U–Th techniques (Fig. 2). it is worth noting that there may be changes in interspecimen δ15N Prior work dating these corals by both approaches provides a variability through the records, for example, greater variability be- basis for the radiocarbon reservoir age correction (15, 16). The tween 15 and 13 kyr; if confirmed, this may yield important insights five coral sites in the DP can be separated into an SAZ group into past biogeochemical and environmental conditions. Although (Burwood Bank and Cape Horn, to the north of the Subantarctic the inherent high temporal resolution of deep-sea corals raises their Front) and an AZ group (Sars, Interim, and Shackleton Fracture potential for studying high-frequency marine N cycle dynamics in Zone, to the south of the Subantarctic Front, Fig. 1 and Fig. S1). the past, it currently complicates the identification of modest millennial-scale changes.