Highly bioavailable dust-borne iron delivered to the Southern Ocean during glacial periods

Fe(II) Fluxes in the Subantarctic South Atlantic and South Pacific.

Our solid-phase Fe speciation and bioavailability reconstructions are based on two sediment cores in the subantarctic Southern Ocean: TN057-06 [42.91°S, 8.9°E, 3,751 m water depth, the site survey core for Ocean Drilling Program (ODP) 1090 (20)] from the subantarctic South Atlantic (9) and PS75/56-1 (55.16°S, 114.79°W, 3,581 m water depth) from the subantarctic South Pacific (8) (SI Appendix, Fig. S1). All samples were obtained from 1-cm widths in the core and freeze-dried without further processing. These cores have both been used to show that Fe fluxes to the subantarctic Southern Ocean were ∼3 to 5 times higher in glacial versus interglacial periods, and to link high dust and Fe fluxes at the LGM to Fe fertilization of phytoplankton (1, 8, 9). In this paper, we use the ²³⁰Th-normalized ²³²Th flux as a proxy for terrestrial dust inputs (21, 22), and convert to dust flux using the average ²³²Th content of upper continental crust (10.7 ppm) (23, 24) (Fig. 1A).

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Fig. 1.

(A) The ²³⁰Th-normalized ²³²Th-based dust flux (gray) from the South Atlantic marine sediment core (TN057-06) plotted with representative high (blue stars), medium (purple triangles), and low (red squares) dust flux samples. (B) Fe(II)/Fe_total values for the representative samples calculated using LCF of the sample with mineral standards of known Fe(II) content, using the Fe K-edge k³-weighted chi function. All error bars on Fe(II)/Fe_total values are based on the goodness of fit and are produced using Larch (25). The colors and open and closed symbols in A match those in B. (C) Fe K-edge XAS spectra for the representative samples. Colors in C are the same as in A and B, with dashed lines corresponding to open symbols and solid lines corresponding to filled symbols. Lower edge positions indicate Fe that is more reduced and therefore more bioavailable, and vice versa (10). Possible ice-rafted debris and other terrestrial mineral contributions to the ²³⁰Th-normalized ²³²Th dust proxy are the topic of ongoing research, especially for the high peaks in Marine Isotope Stage 3 (blue stars).

Representative bulk Fe K-edge XAS spectra (Fig. 1C) from South Atlantic core samples across the last glacial cycle (Fig. 1A) are distinctly different due to variable Fe(II)/Fe_total (shown as percentages, Fig. 1B). Bulk XAS uses a typical X-ray beam size of 1 mm × 10 mm, and obtains the average Fe(II)/Fe_total of a given sediment sample as a result (26). During glacial periods with high dust fluxes (Fig. 1A), positions of maximum absorption are ∼7,130 eV, which indicate high Fe(II) content (10) (Fig. 1C). In contrast, during interglacial periods with low dust fluxes (Fig. 1A), positions of maximum absorption are ∼7,133 eV, which indicate high Fe(III) content [and thus low Fe(II)] (10) (Fig. 1C).

We present paleorecords of Fe(II) flux through the last glacial cycle, based on XAS of our minimally processed marine sediment core samples from the subantarctic Atlantic and Pacific sectors of the Southern Ocean (Fig. 2). The Fe(II) flux reconstructions span the last 100,000 and 140,000 y for the South Atlantic and South Pacific, respectively (Fig. 2 B and D). The Fe(II)/Fe_total values (Figs. 1B and 2 A and C and SI Appendix, Fig. S2) were determined using bulk Fe K-edge XAS and linear combination fitting (LCF) to find the combination of published standards with known Fe(II) content that best describes the spectral features (10) (see Materials and Methods). The Fe(II)/Fe_total values were then multiplied by the ²³⁰Th-normalized total Fe flux to create the Fe(II) flux (Fig. 2). Fe quantification for PS75/56-1 is detailed in SI Appendix, Fig. S3. The Fe(II)/Fe_total is positively correlated with both dust flux and total Fe flux across the full range of data in both cores (correlation plots, R² values, and P values are shown in SI Appendix, Fig. S4), and the Fe(II)/Fe_total was ∼6× higher at the LGM compared with the current interglacial period in both regions of the ocean (from ∼5 to ∼30% Fe(II)/Fe_total; Fig. 2 A and C). Edge position data were used to confirm the oxidation state information obtained by LCF (SI Appendix, Figs. S5 and S6). We also collected XAS spectra on wet (unprocessed), freeze-dried, and oven-dried sediments (50 °C overnight) all from TN057-06 at 90 cm to 91 cm depth (dated 25.47 ka), to test the impacts of sample handling on Fe speciation. All spectra, Fe(II) concentrations, and mineral compositions were the same (within error) for all treatments, suggesting Fe speciation in the sediments is not observably altered with typical sediment core sample preparation (SI Appendix, Fig. S7).

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Fig. 2.

(A and C) Dust fluxes and Fe(II)/Fe_total records, with (B and D) total Fe fluxes and Fe(II) fluxes over the last glacial cycle for (A and B) the South Atlantic (TN057-06) and (C and D) the South Pacific (PS75/56-1). (A and C) Dust fluxes are represented with gray solid lines (gray axes). Fe(II)/Fe_total records are blue circles connected with a dotted line (blue axes), and they are calculated the same way as those in Fig. 1B. The error bars for Fe(II)/Fe_total are based on the goodness of fit using the best-fit combination of standards, and are produced using Larch (25). (B and D) Fe fluxes are ²³⁰Th-normalized (red lines), and LCF-based Fe(II) fluxes (blue circles connected with a dotted line) are the Fe(II)/Fe_total fraction multiplied by the Fe flux. The error bars for Fe(II) flux were calculated by propagating the errors on Fe(II)/Fe_total, Fe concentration, and ²³⁰Th MAR. (E) The LR04 δ¹⁸O benthic stack (27) (climate proxy) shows the glacial−interglacial cycle for the period of time spanned by the samples in this study. High δ¹⁸O values indicate cold glacial climates, and vice versa (28). Note that the axis is inverted, by convention. (F) The mineral dust flux to the Antarctic EPICA Dome C (EDC) ice core shows trends in dust supply in this time period (29).

The Fe(II) content of dust-borne Fe reaching the Southern Ocean is higher in glacial periods than in interglacial periods. Thus, glacial dust sources contain more reduced Fe species than interglacial dust sources, which is likely the result of higher and lower glacial activity (10⇓–12), respectively, in the source regions.

Glaciogenic Primary Fe(II) Minerals Modulating Fe(II) Fluxes over Time.

Primary Fe(II) silicate minerals (e.g., biotite and hornblende) represent the largest contributions to Fe(II)/Fe_total and thus Fe(II) flux in glacial periods, as determined with bulk XAS (SI Appendix, Figs. S2 and S8). The spectra were fully described by a mix of crystalline mineral phases (e.g., biotite, hornblende) and more amorphous inorganic Fe (e.g., ferrihydrite). Our XAS method is sensitive to organic Fe species (30), but these were not observed.

The observed Fe(II)/Fe_total and the contributions from Fe(II) silicates are both higher in glacial periods, and lower in interglacial periods. The primary Fe(II) silicate minerals that dominate glacial Fe fluxes are consistent with physical weathering/glacial activity, based on mineralogical studies of modern glaciogenic dust sources (10, 11). In previous work, we have shown that biotite and hornblende minerals in natural South American dust can alleviate Fe limitation when added as the sole Fe source in diatom cultures (10). The solubility (11), general lability, and direct bioavailability (10) of these minerals, combined with their prevalence in modern glaciogenic dust sources (10), suggest that they are important to phytoplankton in the mixed layer of the ocean. Secondary Fe(II) minerals describe good portions of the low interglacial Fe(II) fluxes (SI Appendix, Fig. S8), which is consistent with chemical weathering processes that are more important in interglacial periods (31).

To confirm the presence of distinct primary Fe(II) silicate minerals in the unaltered marine sediment core samples, we use an X-ray microprobe with a 2 μm × 2 μm X-ray beam size to identify and characterize individual Fe-rich particles in a glacial (42.7 ka) and interglacial (92.34 ka) sediment sample from the South Atlantic (Fig. 3). The small beam size allows us to probe the speciation of Fe in individual particles in the sediment sample (32), in contrast to bulk XAS, which provides the average Fe speciation and identifies the mix of minerals. Using μXRF maps, we observe large (∼5 μm to 10 μm) Fe hotspots over a diffuse Fe signal representing most particles (SI Appendix, Fig. S9). We attribute these large hotspots to primary Fe minerals that are ground from bedrock, and we attribute the background to secondary Fe species (clays, Fe oxides) that are predominantly small (<2 μm) particles and aggregates (33⇓–35). We use μXAS to determine the speciation and mineral composition of the hotspots; LCF at the near-edge region with standard spectra show that parts of these Fe hotspots are ∼100% Fe(II) attributed solely to primary Fe(II) silicate minerals (biotite and hornblende were used as representative standards; Fig. 3). The particles in the glacial sediment are more reduced, on the whole, than those in the interglacial sediment (Fig. 3), and the Fe(II) hotspot/Fe_total estimates from the μXRF maps (SI Appendix, Fig. S9) are nominally similar to the LCF-based Fe(II)/Fe_total calculations (Fig. 2). Our identification of biotite- and hornblende-rich particles in the glacial and interglacial sediment provides evidence that distinct Fe(II) primary minerals are deposited to the Southern Ocean and preserved through the processes of sediment deposition, core collection, and core storage. We show evidence of pure Fe(II) silicates in both glacial and interglacial sediments (Fig. 3), which suggests glaciogenic minerals likely contribute to Fe(II)/Fe_total throughout the glacial cycle, simply to a greater degree in glacial periods and to a lesser degree in interglacial periods.

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Fig. 3.

Microprobe-based XAS of individual particles in a South Atlantic core (TN057-06), at a glacial and interglacial depth. The black solid lines are μXAS of three individual particles from the glacial sediment sample (42.7 ka), and the gray solid lines are μXAS of three individual particles from the interglacial sediment sample (92.34 ka). The spectra are labeled with their Fe(II)/Fe_total concentrations. Fe(II)/Fe_total was calculated using LCF of the sample with standards run contemporaneously, using the normalized intensity in the near-edge region (7,100 eV to 7,180 eV). The glacial particles were more reduced, on the whole, than the interglacial particles. A primary Fe(II) silicate standard (biotite, blue), an Fe(III) oxide/hydroxide standard (goethite, orange), and a secondary phyllosilicate standard (glauconite, goldenrod) are also plotted and labeled. The pure Fe(II) particles were >99% biotite and hornblende [primary Fe(II) silicates]. The vertical lines guide the eye to differences in edge positions (green) and postedge features (magenta) between the Fe(II) and Fe(III) rich samples. Spectra are offset for clarity.

We can rule out diagenetic controls on Fe speciation in the cores, because Fe(II) silicates dominate the Fe(II) signal. In marine sediments, the unknown impacts of diagenesis have precluded previous efforts to reconstruct dust-borne Fe speciation and bioavailability in the Southern Ocean over the last glacial cycle, since reducing conditions in the sediment can alter Fe oxidation state and speciation (36). Since primary Fe(II) silicates form only from cooling magma (37) and metamorphic processes above 500 °C (38, 39), changes in primary Fe(II) silicate concentrations represent glacial−interglacial changes in dust source [mainly the degree of physical weathering versus chemical weathering (31)] rather than diagenesis. Specifically, the primary Fe(II) silicates that are most commonly identified in sediments, including chlorite, biotite, and hornblende, cannot form under the low temperature and pressure conditions of sediment cores (37⇓–39), and dominate glaciogenic dust sources impacted by physical weathering of bedrock (10, 11, 40). Secondary phyllosilicates (e.g., smectite, kaolinite, glauconite) produced during chemical weathering and diagenesis (41) can also contain some Fe(II), but they are structurally distinct from primary Fe(II) silicates (shown with biotite and glauconite XAS in Fig. 3) and represent minor contributions to the total Fe(II) signal except in interglacial periods [low dust, low Fe(II) content; SI Appendix, Fig. S8]. Iron sulfide minerals (e.g., pyrite, which was used in all LCF analyses), which would likely dominate any authigenic Fe(II) signal (36), contribute only minimally to the mineral composition of all samples as determined using LCF (SI Appendix, Fig. S8). However, sulfide minerals may not be well preserved in storage under ambient air conditions. Iron carbonate is also minimal in all samples based on the LCF analysis. We thus expect that our Fe(II)/Fe_total values are lower-bound estimates but accurately represent changes in highly bioavailable primary Fe(II) silicate deposition to the subantarctic Southern Ocean on glacial−interglacial timescales.

We observe higher Fe(II) content [dominated by highly bioavailable glaciogenic Fe(II) silicates] in dust-borne Fe reaching the Southern Ocean during glacial periods versus interglacial periods. Thus, the speciation of Fe amplifies the impact of higher total Fe on the bioavailable Fe supply that increases phytoplankton productivity in the Southern Ocean in glacial periods.

The Impact of Glacial Activity and Fe Speciation on Bioavailable Fe Supply over the Last Glacial Cycle.

When dust from modern sources is added to Fe-limited diatoms, diatom growth responds linearly to the particulate Fe(II) content (10). Thus, we suggest that Fe(II) flux is a more importance estimator of bioavailable Fe supply than total Fe flux. We use Fe supply amplification factors [Fe(II) flux and total Fe flux values from Fig. 2 for a given core at a given time point divided by the corresponding Holocene value] to determine the likely impact of Fe(II) versus total Fe on Fe fertilization over the last glacial cycle. Based on Fe(II) flux amplification factors for both the South Atlantic and South Pacific, there is consistently a ∼15× to 20× higher bioavailable Fe supply to support phytoplankton growth in highly productive glacial periods compared with the current interglacial in both sectors of the Southern Ocean, and up to 30× higher bioavailable Fe supply in the South Atlantic during Marine Isotope Stage 3 between ∼40 ka and 55 ka (Fig. 4). These Fe(II) flux amplification factors are at least 2× and up to 9× higher than corresponding total Fe flux amplification factors in all periods where dust flux is at a maxima and CO₂ is at a minima over the last glacial cycle (1) (Fig. 4), suggesting that Fe(II) fluxes are likely more important to Fe fertilization than total Fe fluxes throughout the Southern Ocean.

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Fig. 4.

Amplification factors for two measures of Fe supply [Fe flux in red solid lines and Fe(II) flux in blue circles connected with a dotted line] in (A) the South Atlantic (TN057-06) and (B) the South Pacific (PS75/56-1), with (C) alkenones and (D) atmospheric CO₂ and foraminifera-bound δ¹⁵N records. (A and B) Amplification factors for Fe flux and Fe(II) flux show the relative increase from Holocene values, for each time point. Errors are propagated for Fe concentration, MAR, Fe(II)/Fe_total quantification, and the Holocene Fe(II) flux estimate. Dust flux maxima corresponding to atmospheric CO₂ minima in the last glacial cycle (1) are indicated in gray shaded bars in all plots, where Fe supply and productivity is high. In C, the alkenones flux (1, 42), a productivity proxy for the subantarctic South Atlantic core TN057-06/site OPD 1090, correlates with Fe supply over the last glacial cycle. In D, the Globigerina bulloides foraminifera-bound δ¹⁵N record (1) from ODP 1090 (cyan solid line) and the atmospheric CO₂ record as recorded in Antarctic ice cores (43) (purple solid line) show the impacts of Fe fertilization over the last glacial cycle on surface nitrate utilization and climate, respectively.

Our results show that glacial activity-driven changes in Fe speciation are positively correlated with dust flux and total Fe flux on glacial−interglacial timescales (SI Appendix, Fig. S4), suggesting that glacial activity is likely more important to both dust production and bioavailable Fe supply for a given dust/Fe flux than previously believed. We show that a given Fe flux is ∼6× more bioavailable at the LGM compared with today, based on an increase in glaciogenic dust sources rich in highly bioavailable primary Fe(II) silicates. Thus, changes in Fe speciation are likely crucial to glacial Fe fertilization events in the Southern Ocean. Our observations are consistent with Antarctic ice core experiments demonstrating that dust-borne Fe is more soluble at the LGM than predicted by current models (13). Antarctic ice core LGM dust also supports persistent and relatively high dissolved Fe concentrations in diatom cultures (17), which could be explained by continuous dissolution of labile glaciogenic Fe(II) minerals. Our results suggest that Fe speciation should always be considered when evaluating the Fe supply and its impact on the biological pump. The tight correlation between Fe flux and Fe speciation (SI Appendix, Fig. S4) means that impacts of speciation may be misinterpreted as impacts of total Fe. Thus, the importance of Fe speciation on Fe fertilization of the Southern Ocean should be investigated further by looking for preserved molecular indicators of Fe nutrition in marine sediment cores and probing the impacts of dust-borne Fe speciation on bioavailable Fe supply in biogeochemical models.

The trends in Fe speciation over the last glacial cycle are remarkably similar between the subantarctic South Atlantic and South Pacific cores, which suggests there is a universal mechanism controlling the speciation and bioavailability of the dust sources in both of these regions. We show that Fe(II)/Fe_total reaches a minimum of ∼5% to a maximum of ∼45% across the full glacial cycle in both cores (Fig. 2), despite total Fe fluxes being ∼3× lower in the South Pacific compared with the South Atlantic throughout the last glacial cycle. In sediments, primary Fe(II) minerals are characteristic of conditions of relatively high physical weathering, which mobilizes them from bedrock, and relatively low chemical weathering, which slows their transformation into secondary minerals (31). Clay mineral and quartz/feldspar ratios from the South Atlantic show that, compared with interglacial sediments, glacial sediments have undergone more physical weathering relative to chemical weathering (40). Given the link between modern glaciers and the primary Fe(II) content of dust sources (10), it is likely that physical glacial weathering influences the changes in dust-borne Fe speciation that we observe at high latitudes. Lower chemical weathering (drier climates) characteristic of glacial periods (44) could also contribute to higher Fe(II)/Fe_total in glacial periods, but some important South Atlantic and South Pacific dust sources experienced wetter conditions at the LGM (45, 46), so glacial weathering may be the dominant driver of Fe speciation on glacial−interglacial timescales. Despite the lower magnitude of dust fluxes in the South Pacific, which are thought to be dominated by Australian and New Zealand dust sources (8), the glacial−interglacial speciation changes are robust and similar to those in the South Atlantic, which are dominated by Patagonia dust sources (47, 48) that are highly impacted by glaciers (10). If glacial processes contributed significantly to high glacial Fe(II)/Fe_total in the South Pacific core, New Zealand may be a significant South Pacific dust source, as suggested by modern, modeled dust trajectories (49), since glacial activity was much more extensive at the LGM in New Zealand (50) versus Australia (51).

Our results suggest that dust sourced across the subantarctic Southern Ocean is more highly impacted by glacial activity at the LGM compared with today, which impacts its speciation and bioavailability. We show that glacial activity increases the highly bioavailable Fe(II) silicate content of dust reaching the Southern Ocean, during periods of high total dust-borne Fe flux. This phenomenon is likely due to more mountain glaciers causing more physical weathering and more dust production in glacial outwash plains (52) at the LGM. We demonstrate that Fe(II) silicate-rich glacially derived Fe increases the bioavailable Fe supply by a factor of ∼15 to 20 in glacial versus interglacial periods, which is in comparison with the factor of ∼3 to 5 increases in total Fe flux that have been considered in biogeochemical models to date. Thus, the speciation of Fe should be included in models considering the importance of dust-borne Fe to Southern Ocean Fe fertilization. Our results suggest there is a positive feedback between glacial weathering and cold glacial temperatures, since glacial activity is associated with more bioavailable Fe for a given Fe flux. Thus, changes in the Fe speciation and bioavailability of dust sources are likely important drivers of glacial−interglacial changes in atmospheric CO₂ concentrations.