A comparison of benthic foraminiferal Mn / Ca and sedimentary Mn / Al as proxies of relative bottom-water oxygenation in the low-latitude NE Atlantic upwelling system

Trace element incorporation into foraminiferal shells (tests) is governed by physical and chemical conditions of the surrounding marine environment, and therefore foraminiferal geochemistry provides a means of palaeooceanographic reconstructions. With the availability of high-spatial-resolution instrumentation with high precision, foraminiferal geochemistry has become a major research topic over recent years. However, reconstructions of past bottom-water oxygenation using foraminiferal tests remain in their infancy. In this study we explore the potential of using Mn /Ca determined by secondary ion mass spectrometry (SIMS) as well as by flow-through inductively coupled plasma optical emission spectroscopy (FT-ICP-OES) in the benthic foraminiferal species Eubuliminella exilis as a proxy for recording changes in bottom-water oxygen conditions in the low-latitude NE Atlantic upwelling system. Furthermore, we compare the SIMS and FT-ICP-OES results with published Mn sediment bulk measurements from the same sediment core. This is the first time that benthic foraminiferal Mn /Ca is directly compared with Mn bulk measurements, which largely agree on the former oxygen conditions. Samples were selected to include different productivity regimes related to Marine Isotope Stage 3 (35–28 ka), the Last Glacial Maximum (28–19 ka), Heinrich Event 1 (18–15.5 ka), Bølling Allerød (15.5–13.5 ka) and the Younger Dryas (13.5–11.5 ka). Foraminiferal Mn /Ca determined by SIMS and FT-ICP-OES is comparable. Mn /Ca was higher during periods with high primary productivity, such as during the Younger Dryas, which indicates lowoxygen conditions. This is further supported by the benthic foraminiferal faunal composition. Our results highlight the proxy potential of Mn /Ca in benthic foraminifera from upwelling systems for reconstructing past variations in oxygen conditions of the sea floor environment as well as the need to use it in combination with other proxy records such as faunal assemblage data.


Introduction
Foraminifera, being extensively distributed and highly abundant in most marine environments, are essential proxies for reconstructing the chemical and physical properties of past oceans.Several trace-element-to-calcium (Ca) ratios anal-

C. L. McKay et al.:
A comparison of benthic foraminiferal Mn / Ca and sedimentary Mn / Al ysed on foraminiferal tests have been developed as proxies in the last decades.Perhaps one of the most conventional approaches is the reconstruction of seawater temperatures using Mg / Ca (e.g.Nürnberg et al., 1996;Elderfield et al., 2006).Other established trace-elemental proxies also include Ba / Ca to trace salinity changes due to continental run-off (Lea and Boyle, 1989;Hönisch et al., 2011) and Cd / Ca to reconstruct water masses (Marchitto and Broecker, 2006).Whilst there is a wealth of research applying the geochemistry of foraminiferal calcite for palaeo-oceanographic reconstruction and copious sedimentary redox proxies have been developed (e.g.Gooday et al., 2009), utilising the trace-elemental composition of foraminiferal shells (tests) to reconstruct oxygen conditions is still in its infancy.One redox-sensitive element that has recently gained more interest is manganese (Mn), both as a trace element in biogenic foraminiferal calcite (Mn / Ca) and in bulk sediment samples (Reichart et al., 2003;Glock et al., 2012, Groeneveld andFilipsson, 2013;Lenz et al., 2014;Koho et al., 2015).Here we aim to explore the potential of Mn / Ca by analysing both benthic foraminiferal tests and comparing them to Mn / Al of bulk sediment samples from an upwelling record to determine if changes in oxygen conditions during different primary productivity regimes are detectable by these methods.
At the sediment-water interface, the concentration of dissolved redox-sensitive elements such as Mn varies significantly between oxic and hypoxic (hypoxia defined as < 1.42 mL L −1 O 2 following Levin et al., 2009) settings.In sea water, redox-sensitive Mn is mainly present as Mn 2+ , which under oxic conditions precipitates as Mn oxyhydroxide (Burdige, 1993;Glasby, 2006).The Mn flux across the sediment-water interface is driven by reductive dissolution of reactive Mn oxyhydroxide (Froelich et al., 1979).
Under oxic conditions, dissolved O 2 is present in the pore waters, and thus benthic foraminiferal tests are expected to incorporate less Mn into their test.In contrast, under lowoxygen conditions, Mn oxyhydroxide is reduced and the Mn 2+ concentration increases (Tribovillard et al., 2006), becoming available to be incorporated in the foraminiferal tests.Especially under hypoxic conditions, Mn concentrations will be concentrated in the pore water because the Mn cannot escape into the overlying oxic bottom water, meaning that benthic foraminiferal Mn / Ca will be highest.Hence foraminiferal Mn / Ca has potential to be used as a proxy of hypoxic conditions.Accordingly, we expect bulk Mn to be depleted in the sediment and exhibit the opposite trend.On the other hand, under anoxic conditions the Mn is able to diffuse upwards and into the overlying water column, or, when pore waters become supersaturated with respect to Mn, it is precipitated as MnCO 3 (rhodochrosite) (Froelich et al., 1979;Pedersen and Price, 1982;Tribovillard et al., 2006).Therefore, under low-oxygen conditions, foraminiferal Mn / Ca is expected to be higher during hypoxic conditions than during anoxic conditions, but still higher than under oxic conditions.
Whilst benthic foraminiferal Mn / Ca has been conventionally used as an indicator of contamination by Mn oxyhydroxide or Mn carbonate (Boyle, 1983;Barker et al., 2003), new studies are pioneering Mn / Ca as a potential proxy of related changes in bottom/pore-water oxygen and redox conditions (Ní Fhlaithearta et al., 2010;Glock et al., 2012;Groeneveld and Filipsson, 2013;Koho et al., 2015).Mn / Ca signatures of the ambient bottom water are recorded by benthic foraminifera.For example, culture experiments have confirmed that the species Ammonia tepida incorporates Mn into the test proportional to the concentration in the ambient water masses (Munsel et al., 2010).Thus, during benthic foraminiferal calcification under hypoxic conditions, more Mn will be assimilated into their calcite tests, whereas under anoxic conditions, or oxic conditions in particular, Mn is expected to decrease, albeit to different amounts (Pena et al., 2005).Hence Mn / Ca used in this study could provide a reliable means of reconstructing the former seafloor oxygen settings at the time of deposition as opposed to sediment bulk measurements, which can continue to oxidise and be mobilised post-deposition.
Traditionally, trace element / Ca is analysed on solutionbased samples containing larger numbers of foraminifera specimens to give a representative result (Groeneveld and Filipsson, 2013).When a sufficient amount of specimens are not available for solution-based techniques, or if diagenesis has affected the tests, a micro-analytical technique upon single specimens such as secondary ion mass spectrometry (SIMS) is a valuable tool.From an analytical perspective SIMS has enhanced our ability to determine how trace elements are distributed within foraminiferal tests at high spatial resolution and precision on individual foraminifera (Allison and Austin, 2003;Bice et al., 2005;Kunioka et al., 2006;Glock et al., 2012).Recently, SIMS-determined Mn / Ca of benthic foraminifera has been found to be representative of Mn / Ca in the top centimetre of the pore water, confirming that the foraminiferal calcite composition relates to the level of oxygen depletion (Glock et al., 2012).
Where a sufficient amount of foraminiferal specimens are available, we additionally used flow-through inductively coupled plasma optical emission spectroscopy (FT-ICP-OES; Haley and Klinkhammer, 2002).Flow-through analysis is a means of determining elemental composition from samples of foraminiferal tests which permits complete monitoring of the effects of cleaning and dissolution (Haley and Klinkhammer, 2002).However, due to the small size of Eubuliminella exilis, a larger number (up to 50 specimens in this case) of foraminiferal tests from the same core sample is required to give a representative average signal.Therefore we utilise both SIMS and FT-ICP-OES to explore the potential of Mn / Ca for interpreting down-core oxygen studies.
To explore how Mn / Ca works as a potential proxy for bottom/pore-water oxygen conditions, we study a site from the low-latitude NE Atlantic upwelling system.Upwelling systems are an ideal environment to test this proxy, as they are renowned for high export rates of labile organic matter from surface waters, which provokes severe oxygen depletion in the underlying intermediate waters and at the seafloor (Böning et al., 2004).We study core GeoB7926-2 from the upwelling region off coastal NW Africa (Fig. 1) and compare foraminiferal and sedimentary Mn with published diatom and benthic foraminiferal species composition (Romero et al., 2008;Filipsson et al., 2011;Kim et al., 2012;McKay et al., 2014).In general, coastal upwelling systems are the most productive of the world ocean, resulting in vulnerability to oxygen minima within the water column and underlying seafloor (Helly and Levin, 2004;Bakun et al., 2010).At present, the benthic environment of this particular upwelling system is not especially susceptible to low-oxygen conditions and is well ventilated with bottom-water oxygen of ca. 5 mL l −1 (Goretski and Koltermann, 2004).However, based on benthic foraminiferal faunal studies, there is evidence of previous periods of oxygen depletion at the sea floor during the Younger Dryas (YD, 13.5-11.5ka) and Heinrich Event 1 (H1, 18-15.5 ka) in particular.This is inferred from the predominance of the low-oxygen-tolerant benthic foraminiferal species Eubuliminella exilis (synonymised taxa: Bulimina exilis) (Filipsson et al., 2011;McKay et al., 2014).Therefore, we selected samples allocated to late Marine Isotope Stage 3 (MIS3, 35-27 ka), the Last Glacial Maximum (LGM), Heinrich Event 1 (H1), Bølling Allerød (BA) and the Younger Dryas (YD) to reconstruct past bottom-water oxygen.These climatic intervals were chosen in order to test if Mn / Ca can confirm the low-oxygen conditions during different productivity regimes as reported by previous studies from this particular sediment core (Filipsson et al., 2011;McKay et al., 2014).We focus on utilising SIMS and compare this method with FT-ICP-OES where a sufficient number of E. exilis specimens were available.We also present Mn / Al sediment bulk measurements from the same sediment for further comparison.
The low-oxygen-tolerant benthic foraminiferal species Eubuliminella exilis is an infaunal species and therefore has the ability to migrate within the sediment and experience variable pore-water conditions.This migration could affect the Mn / Ca incorporated within the test; however as E. exilis is so low oxygen tolerant, it possibly migrates less than other infaunal species which are not as tolerant.Therefore E. exilis likely incorporates more Mn and is therefore the right recorder, suitable for reconstructing oxygen levels.Furthermore, abundant populations of this taxon are reported from a range of settings, including coastal upwelling sites, sapropels, oxygen minimum zones and other environments, for example, in the Bering Sea and the Mississippi River mouth (Caralp, 1989;Jorissen, 1999;Jannink et al., 1998;Rasmussen et al., 2002;Khusid et al., 2006).Thus E. exilis also has potential to be a useful proxy for other marine environments susceptible to strong oxygen deficiency and high fluxes of organic export.Eubuliminella exilis has been found to correlate with diatom accumulation rate and clearly dom- inates the foraminiferal fauna during very high diatom input (Caralp, 1984;Filipsson et al., 2011;McKay et al., 2014McKay et al., , 2015)).Therefore E. exilis, being present (albeit in considerably varying abundance) throughout the GeoB7926-2 record, is an ideal candidate to record oxygen changes in the environment in which they lived and also provide an opportunity to test if export productivity is causing low-oxygen conditions as opposed to the dominance of this species merely being a fresh phytodetritus diet signal (Caralp, 1989).
We hypothesise that higher foraminiferal Mn / Ca will occur during times of high diatom accumulation rate and lower bottom-water oxygen concentrations and accordingly higher E. exilis abundance, with the opposite effect during times of low surface productivity.

Method
Gravity core GeoB7926-2 from the NE Atlantic upwelling system (20 • 13 N, 18 • 27 E, 2500 m water depth) was recovered during R/V Meteor cruise M53/1 (Meggers et al., 2003).The age model for the core was published by Kim et al. (2012), and the timing and duration of the climatic intervals were adopted from the δ 18 O of the North Greenland Ice Core Project (NGRIP Members, 2004) and Sánchez Goñi and Harrison (2010).We selected well-preserved foraminiferal specimens based on the criteria of high-and low-surface-productivity regimes as demonstrated from diatom abundance (Romero et al., 2008).Details of sample preparation for benthic foraminiferal faunal analysis have www.biogeosciences.net/12/5415/2015/Biogeosciences, 12, 5415-5428, 2015 previously been published (Filipsson et al., 2011;McKay et al., 2014).

SIMS analysis
From the > 150 µm size fraction, a total of 48 specimens of the benthic foraminifera species Eubuliminella exilis were hand-picked under a binocular microscope for SIMS analysis (Table 1).We acknowledge that the presence of Mnrich authigenic coatings (e.g.Mn (oxyhydr)oxides and organic matter) can be problematic for trace-elemental analysis of foraminifera (Boyle, 1983;Pena et al., 2005;Klinkhammer et al., 2009).Therefore, we employed a rigorous pretreatment cleaning technique to remove possible organic contamination following the method of Glock et al. (2012) and avoided potential diagenetic coatings during the SIMS analysis by measuring within the massive centre of the test walls (Fig. 2).
For the SIMS analysis, foraminifera from individual sample depths were rinsed over a 63 µm sieve with Milli-Q water.After this rinsing step, the foraminifera were transferred into vials and sonicated for 20 s.Subsequently, the foraminifera were rinsed with methanol and sonicated again for 1 min.Any residual methanol was then removed with Milli-Q water.An oxidative cleaning step was performed to remove organic matter which consisted of mixing the following reagents: 100 µL 30 % H 2 O 2 to 10 mL of 0.1 M NaOH solution.Three hundred and fifty microlitres of this reagent was added to each individual vial, and the vials were put into a water bath at 92 • C for 20 min.Afterwards another 20 s sonic bath was undertaken; the foraminifera samples were rinsed again with Milli-Q water in the 63 µm sieve to remove any residues.For the final step, the specimens were transferred back into their respective vials and 250 µL of 0.001 M HNO 3 was added to each vial.The vials were put into a sonic bath for 20 s and finally rinsed one last time with Milli-Q water.After the cleaning procedure, the specimens were checked under a binocular microscope to ensure sufficient cleaning and that the tests remained intact.
Foraminifera specimens were embedded in low-viscosity epoxy resin at JAMSTEC, Japan.The foraminifera were then ground to expose a cross section across the test wall using 16 µm silicon carbide paper at the Department of Geosciences, University of Edinburgh, UK.Resin pieces were mounted into low-viscosity epoxy resin disks (Struers) at the NORDSIM laboratory, Laboratory for Isotope Geology at the Swedish Museum of Natural History, Stockholm, Sweden.The mounts were polished using a Struers Rotopol-2 at 150 rpm for 1 min, first with 3 µm diamond suspension and again with 1 µm diamond suspension.Between each grinding and polishing step, mounts were cleaned with ethanol.Each cross-sectioned foraminifera test was examined under high-power reflected light microscopy to evaluate the quality of the carbonate and to assist in assessing the progress of polishing until the cross sections were clear.Subsequently, the mounts were cleaned in high-purity ethanol and coated in a 20-nm thick, high-purity Au coat.
The reference material used for the SIMS was a polished piece of Oka calcite crystal supplied from GEOMAR, Kiel University, Germany (E.Hathorne, pers.comm).This standard was obtained from a matrix-matched specimen for which Mn / Ca has been reported by solution ICP-MS (Glock et al., 2012).During calibration, the Oka was analysed n = 16 times, yielding a high sensitivity with 1 standard deviation repeatability of 1.2 % for Mn concentration.
The Mn / Ca analyses of the test cross sections were performed using a Cameca IMS 1280 ion microprobe at the NORDSIM laboratory at the Swedish Museum of Natural History, Stockholm, Sweden.Analysis used a 16 O − 2 ion beam accelerated at 23 kV impact energy (−13 kV primary beam, +10 kV secondary beam).It is vital to only analyse Mn which is located internally within the original test wall to attain the most representative Mn / Ca for developing it as a redox proxy.Therefore, a 50 µm aperture in the primary column was used to shape a slightly elliptical 5 µm spot on the sample surface, which, together with careful placement, reduced the effects of sample contamination from the test wall outer surface.Prior to each analysis, the analytical location was pre-sputtered for 2 min with the ion beam rastered over a 10 × 10 µm raster to remove the Au coat and any remain-  44 Ca distribution was monitored using the ion imaging system of the instrument and maximised to ensure highprecision beam targeting on the fine foraminiferal test walls.The mass spectrometer was operated at a mass resolution of M/ M ∼ 6000 to resolve the 55 Mn peak from nearby molecular interferences.A 400 µm contrast aperture was employed for maximum transmission together with a 60 µm entrance slit, a 2001 µm field aperture restricting the field of view on the sample to an area of ca. 12 × 12 µm at the transfer magnification of ca.160×, and a 45 eV wide energy window -all of which combined to yield adequately flat-topped peaks on the species of interest.Each analysis comprised of 16 cycles of 44 Ca (1 s integration cycle −1 ) and 55 Mn (2 s).Each analysis lasted approximately 9 min.Secondary ions were measured using a low-noise (< 0.01 cps) ion-counting electron multiplier.Multiple analysis points were undertaken upon each individual test of E. exilis (ca.6-10 targets per individual specimen) starting from the aperture and taking measurements alternating between the outer wall and internal walls.For the best targets, programming was performed manually to ensure that widest chamber walls and "t" junctions were targeted since they provide a wider test wall for the analyses (Fig. 2).Furthermore, at such high spatial resolution and precision, it is easy to visually observe and avoid encrusting prior to selecting analysis targets via the connected screen and avoid measuring secondary calcite or authigenic clays which would otherwise affect measurements.With cautious positioning of the primary beam on the test walls and observations of the element distributions during measurements, such detrital material and potential contaminants were avoided and annulled.Therefore only the elements actually incorporated into the calcitic tests were measured.As an additional prerequisite to this, analyses with Ca values > 500 kcps were classified as being reliable.Mn / Ca was first normalised to those determined in the Oka standard and subsequently converted to the true value in the Oka based on the Glock et al. (2012) value for Mn / Ca of 4920 µmol mol −1 .The advantage of SIMS is that it is non-destructive, and, as the foraminiferal cross sections are preserved within the mounts, they can be stored for further analyses.Mounts are archived at the NORDSIM laboratory.

FT-ICP-OES analysis
For FT-ICP-OES, 20-50 specimens per sample depth of E. exilis from the GeoB7926-2 record were selected from samples corresponding to H1, BA and the YD for comparisons with the SIMS data.These three climatic intervals encompassed the only samples where a sufficient number of pristine E. exilis individuals were present.The tests were gently crushed in a 0.5 mL vial, and fragments were transferred into a PTFA filter with 0.45 µm mesh.
For analysis, the filters were connected to a flow-through automated cleaning device (Klinkhammer et al., 2004;Haar-man et al., 2011).Automatic cleaning prevents the loss of material which occurs with traditional cleaning, allowing the analysis of very small samples (∼ 20 µg).The flow-through was then connected to an ICP-OES (Agilent Technologies, 700 Series with autosampler (ASX-520 Cetac) and micronebulizer).Time-resolved analysis (TRA) was used to analyse the samples at MARUM, University of Bremen, Germany.After an initial rinse (5 min) with buffered Seralpur water to remove clays, the samples were slowly dissolved using an acid ramp formed by mixing of Seralpur with 0.3 M QD HNO 3 (no additional oxidative and/or reductive cleaning was performed).Starting with pure Seralpur the acid contribution was stepwise increased every minute to 100 % acid after 30 min.The flow speed of the solution was 250 µL L −1 .Mn / Ca of the foraminiferal calcite was determined by identifying the TRA interval which showed a consistent linear relationship between Mn and Ca counts.Potential diagenetic phases like Mn(oxy)hydroxides are avoided this way, as they would have a different slope, i.e. a significant Mn signal along with the absence of a Ca signal.Mn / Ca was then calibrated using the characteristic slope of this linear relationship of a known in-house standard solution analysed on the same acid ramp.The average standard error on the determination of the slope for Mn / Ca was 0.75 %.We analysed an international limestone standard (ECRM752-1) for Mg / Ca to validate the results following the same FT protocol.The average Mg / Ca of the ECRM752-1 (n = 4) was 3.76 mmol mol −1 , which compares well with the average published value of 3.75 mmol mol −1 (Greaves et al., 2008).

Mn bulk measurements
For geochemical bulk analyses, samples were dried and ground in an agate mortar and homogenised.Total dissolution of samples was undertaken using HF and HNO 3 following the standard procedures of Gallego-Torres et al., (2007).Mn and Al content for samples corresponding to 35-10 ka was determined by atomic absorption spectrometry, using Re and Rh as internal standards at the Analytical Facilities (Centro de Instrumentación Cientifica) at the University of Granada, Spain.Redox-sensitive Mn was normalised to Al content in order to correct for detrital variations (van der Weijden, 2002).Mn / Al data corresponding to 25-10 ka have previously been published (Gallego-Torres et al., 2014), and here we extend the Mn / Al record to 35 ka.
In order to determine statistically significant differences between samples from different productivity regimes, Kruskal-Wallis tests were run and showed a statistically significant difference between the mean Mn / Ca values (per individual foraminifera specimen) between all five climatic intervals (p = 0.003).By testing the mean Mn / Ca of each foraminifera between each climatic interval individually in turn, using post hoc (Mann-Whitney U) tests, significant differences lay between climatic intervals with high-and lowexport-productivity regimes (based on diatom accumulation rate).Namely, significant differences in Mn / Ca were evident between the YD interval and the LGM and MIS3 (Table 2).
Mean SIMS-derived Mn / Ca per sample depth compares well with FT-ICP-OES results (Table 1), agreeing with maximum differences of 15-24 µmol mol −1 (Fig. 4).Mn / Ca from the FT-ICP-OES on bulk foraminiferal samples tended to be slightly higher compared to the mean ratios obtained from the SIMS microanalyses for the same sediment depth (for example 140 µmol mol −1 compared to 116 µmol mol −1 during the YD).

Mn bulk data
Bulk sedimentary Mn / Al showed highest values during MIS3 at 30-24 ka as well as during 19-17.5 ka and the YD.The YD was characterised by a sharp Mn / Al increase at 12.3 ka, coinciding with maximum diatom productivity (Fig. 4).Relatively low Mn values occurred during 35-32 ka, and during the LGM, Mn was below the level of detection (< 0.06 %).Between 32 ka and the onset of the LGM, a progressive increase was observed.

Comparison of analytical methods
Our results indicate that Mn / Ca in benthic foraminifera might prove to be a valuable proxy for oxygen in the bottom and pore waters.The down-core variability in foraminiferal Mn / Ca at site GeoB7926-2 displays a consistent agreement between the mean SIMS-determined Mn / Ca of each sample depth and the bulk foraminifera Mn / Ca measured by FT-ICP-OES.In general, the agreement in values suggests that the SIMS-determined Mn / Ca is likely to be a true signal within our reconstruction.The slightly higher Mn / Ca determined by FT-ICP-OES in comparison to SIMS-derived Mn / Ca highlights the issue of comparing bulk foraminiferal samples with individual tests comprising only 6-10 analytical targets.Overall, when a sufficient number (minimum weight of 0.1 mg) of benthic foraminiferal specimens are not available in sediment samples for solution-based analyses (in this case from 35 to 18 ka), SIMS has the potential to provide reliable results from a few individuals to compensate for this.
Recent culturing experiments on benthic foraminifera demonstrate that calcification can occur even under anoxic conditions (Nardelli et al., 2014).This is key for the discussion of trace-elemental data derived from the foraminiferal tests, as not only does the timing of the calcification determine the geochemical signature, but it also shows that the signature is recorded in a wide range of oxygen conditions.
When comparing foraminiferal Mn / Ca to previously published sediment measurements of Mn / Al (Fig. 4) for site GeoB7926-2 (Gallego-Torres et al., 2014), in general we do not find a continuous relationship in trends throughout the record, but overall they largely agree on the former oxygen conditions.This is most likely due to diagenetic processes and migration of redox fronts through the sediment which redistributes the bulk Mn after deposition, whereas the foraminiferal tests record the Mn concentration at the time of calcification.In fact, bulk sediment Mn concentrations are often interpreted as being related to diagenetic (post-production) oxidation fronts and less often to the syn-sedimentary environment (e.g.Thomson et al., 1995;de Lange et al., 2008).Thus, two different processes govern Mn fixation in sediment and foraminifera tests, and consequently we can expect an offset between the two signals.oxygenated (Fig. 5a).These low Mn / Ca results are in agreement with the benthic foraminiferal response of a low abundance (ca. 2 specimens cm −3 ) of low-oxygen-tolerant E. exilis (McKay et al., 2014) to the extent that not enough wellpreserved specimens were available for FT-ICP-OES analysis.Such low Mn / Ca and lack of low-oxygen dwellers are to be expected since benthic foraminifera living in an environment where productivity export does not fluctuate at great magnitudes are potentially less exposed to a wide range of oxygen conditions and corresponding Mn concentrations in the pore waters during their growth.This stable and relatively low export productivity is exhibited not only by diatom accumulation but also by carbonate (CaCO 3 = 30-45 %) during the late MIS3 to the late LGM (Romero et al., 2008;McKay et al., 2014).However, by late Heinrich Event 3 (H3: 32.5-29 ka), whilst foraminiferal Mn / Ca is low, there is an increase in bulk sediment Mn / Al, suggesting penetration of oxygenrich bottom waters within the upper centimetres of the sediment column.Dissolved Mn available for the precipitation of Mn (oxyhydr)oxides would most likely be sourced by diffusion from underlying sediments where anoxic conditions prevail (Burdige, 1983).Based on this increase in sedimentary Mn / Al coinciding with relatively low foraminiferal Mn / Ca, we therefore infer that the Mn / Al enrichment occurred immediately below the oxygen-rich pore waters during the late H3 and throughout the period 30-25 ka, delimiting the oxygen penetration front and the upward diffusion of Mn (Fig. 5a).Therefore we suggest that the oxygen penetration depth is deeper, and thus the precipitation of Mn too, than the living depth of E. exilis, which has been documented to live at 1-2 cm sediment depth (Caulle et al., 2014).As both foraminiferal and sedimentary Mn results correspond to low relative abundances (< 5 %) of the low-oxygen indicator E. exilis and low diatom input (Romero et al., 2008;McKay et al., 2014), this reinforces our interpretation of more-oxygenated conditions at the sea floor during H3.It corresponds with the scenario that, during low primary productivity export, oxygen levels are not lowered by the decomposition of large amounts of fresh phytodetritus.
During the LGM, Mn / Ca show a greater range between specimens (three specimens exhibit consistent Mn / Ca of the order of 4-16 µmol mol −1 , whilst others suggest a greater intra-test variability of 16-230 µmol mol −1 ) than samples from MIS3 (Fig. 3) despite diatom input being relatively low and stable during this interval.We interpret the greater range in Mn / Ca as more variable oxygen levels and a relative decrease within the pore water overall, in comparison to earlier times within the record (Fig. 5b), but not to the extent of hypoxia since E. exilis abundance remains low whilst species diversity is high (McKay et al., 2014).Simultaneously, Mn / Al remains low (Mn content < 0.06 %), which could correspond to bottom-water masses since Mn can be transported to deep waters via scavenging (Glasby, 2006).In particular, Gallego-Torres et al. (2014) suggest that site GeoB7926-2 was under the influence of Antarctic Bottom Water (AABW) during the LGM.AABW contains lower Mn concentrations relative to North Atlantic water masses (Statham et al., 1998;Idrus, 2013).Mn is scavenged from AABW as it flows north, and thus when reaching site GeoB7926-2 is Mn-impoverished.However, we propose that low Mn fixation in the sediment during the LGM is due to low export production leading to relatively more Mn being located in the water column.

Heinrich Event 1-Younger Dryas (18-11.5 ka)
During H1, the increase in foraminiferal Mn / Ca indicates lower-oxygen conditions in the pore waters (Fig. 5c).Loweroxygen conditions are evidenced in terms of both the greater variability within the individual tests (Fig. 3) and the higher average Mn / Ca per sample depth (Fig. 4).The comparably lower oxygen conditions are consistent with our hypothesis which stemmed from the benthic foraminiferal faunal assemblage composition (Filipsson et al., 2011;McKay et al., 2014) whereby the dominance of E. exilis indicated lowoxygen conditions at the seafloor as a result of high primary productivity and export flux.Bulk Mn / Al is moderately low (below average of 3.4 × 10 −2 at the corresponding sample depth of the benthic foraminifera analysed by SIMS) when compared to the rest of the record, despite high diatom accumulation rate.The combined interpretation of Mn-, Mo-and U-to-Al ratios presented in Gallego-Torres et al. (2014) evidenced that the H1 period experienced suboxic (< 0.1 mL L −1 O 2 as defined by Morrison et al., 1998) to anoxic bottom-water conditions.Under these conditions, the redoxcline would have been very shallow or even located at the sediment-water interface, so that Mn was not preferentially fixed in the sediment.Furthermore, the sedimentary layer might have acted as a source of reduced dissolved Mn to the water column and/or the uppermost pore waters, allowing for higher Mn availability for incorporation into benthic foraminiferal tests.
During the BA, foraminiferal Mn / Ca determined by SIMS exhibit a similar range of values and intra-test variability to those during H1 (Fig. 3).We relate this similarity in oxygen conditions to comparable diatom accumulation rates during both climatic intervals.Previously, from the relative decrease in E. exilis abundance during the BA, the bottom-water oxygen concentrations were interpreted to have increased in comparison to H1 and the YD (Filipsson et al., 2011).Despite this benthic faunal response to productivity export, the diatom input itself was relatively higher at the core depth sampled for SIMS analysis within the BA than the one in H1.Subsequently, our SIMSderived Mn / Ca results do not suggest vast redox shifts between the two climatic intervals; generally the values follow the diatom input.This emphasises that, whilst the benthic foraminiferal community composition is a reliable indicator of past environmental conditions, the trace-elemental composition of foraminiferal tests has potential to reveal a more detailed palaeoenvironmental interpretation.Furthermore, the foraminiferal Mn / Ca coincides with the lack of Mn enrichment in the bulk sediment, and Mn / Al does not substantially differ from the previous climatic interval either.Mo and U suggest prevailing suboxic conditions during the BA (Gallego-Torres et al., 2014), and, further, we infer that the redoxcline would be shallow within the sediment, which is a similar scenario to H1.
From both SIMS and FT-ICP-OES, the highest foraminiferal Mn / Ca and greatest Mn variability within individual tests are found during the YD (Fig. 3).This consistent pattern of Mn enrichment coincides with high primary productivity, high export flux and the dominance of low-oxygen-tolerant E. exilis.As MnO 2 is rapidly reduced to soluble Mn 2+ in hypoxic pore waters (Burdige 1983;Limburg et al., 2011, and references therein) and since high phytodetritus export typically causes low bottom-water oxygen concentrations or even anoxia within millimetres of the sediment-water interface, we can expect a high accumulation of Mn (Hunt, 1983;McKay et al., 2005) as represented in Fig 5d .Furthermore, the sediment accumulation rate during the interval is the highest of the record (350 cm ka −1 , Fig. 4), which can also intensify the low oxygen concentrations and promote Mn enrichment (McKay et al., 2005).This confirms our hypothesis that Mn / Ca values in E. exilis respond to the oxygen deficiency instigated by the large increase in diatom input.Furthermore, the redox front would also vary in position during this oxygen-depleted period, with diatom export fluctuating at such great magnitude.Therefore the strong intra-test variability (Fig. 3) may be representative of actual changes in oxygenation of the habitat during test growth, due to amplified seasonal fluctuations in diatom export.Moreover, since E. exilis is an infaunal species, it is influenced by the microhabitat of the pore waters.Therefore, the sediment depth at which this species resided and to which it possibly migrated during calcification in such low-oxygen conditions could further explain the greater Mn / Ca variability during the YD.
We emphasise that the benthic foraminiferal Mn / Ca seems to represent a more regional signal due to diatom input as opposed to being generated by deep bottom-water formation and poor ventilation.However, whilst we interpret that the sheer level of diatom input provoked O 2 deficiency in the bottom and pore waters, we acknowledge that even in the modern ocean it is difficult to separate the effects of productivity and deep-water oxygen concentrations since they are inter-related.Gallego-Torres et al. (2014) interpret the YD as a phase of reduced ventilation coinciding with reduced Atlantic Meridional Overturning Circulation (AMOC), promoted by intense export productivity.Both effects provided dissolved Mn available for incorporation into the foraminiferal calcite.Therefore, whilst Mn / Ca has potential for oxygen level reconstruction, supplementary proxies are required in order to determine the precise factor driving the conditions.

Conclusions
Our study contributes to the development of Mn / Ca in benthic foraminiferal calcite as a proxy for reconstructing past oxygen conditions.The results based on data from the lowlatitude NE Atlantic upwelling system indicate that shifts in oxygen levels occurred during different productivity regimes between 35 and 11.5 ka, and thus foraminiferal Mn / Ca can assist our understanding of the past environment in the region studied.The foraminiferal Mn / Ca results are supported by benthic foraminiferal faunal data.
The highest foraminiferal Mn / Ca and greatest Mn variability within individual tests were obtained during the YD and indicate Mn enrichment which coincides with very high primary productivity and the dominance of low-oxygentolerant benthic foraminifera Eubuliminella exilis.The results confirm our hypothesis that Mn / Ca in E. exilis can be applied as a proxy for oxygen deficiency, in this case instigated by the increase in diatom input.Therefore, whilst the benthic faunal abundance data are indicative of such a scenario, foraminiferal Mn / Ca allows a more comprehensive interpretation.Our initial down-core data set raises the implication of calibrations.Once developed, Mn / Ca determined by the SIMS method in particular may have the potential to be applied to other study regions and foraminiferal species for reconstructing former bottom-water oxygen conditions.
Furthermore, we conclude that SIMS-determined Mn / Ca in individual tests is comparable with bulk foraminiferal Mn / Ca measured by FT-ICP-OES.However, due to the processing time required to program and target delicately thin foraminiferal test walls, SIMS may not be practical for Mn / Ca studies where large numbers of samples must be processed.Nevertheless, we emphasise that SIMS has great potential to provide reliable Mn / Ca results from just a few individual foraminifera.Therefore, SIMS is a robust alternative method to FT-ICP-OES; idea for employment on samples that lack a sufficient abundance of individual benthic foraminiferal specimens for solution-based bulk analyses.Furthermore, SIMS is also non-destructive, and thus foraminiferal test cross sections can even be remeasured.
In contrast, foraminiferal Mn / Ca data do not continuously exhibit a consistent trend with Mn / Al determined from bulk sediment measurements.The reason for this discrepancy is that Mn related to redox fronts within the sediment provides a diagenetic signal, and thus it continues to react and shift after deposition, whereas foraminiferal tests record the Mn concentration at the time of calcification.

Figure 1 .
Figure 1.Locality of gravity core GeoB7926-2 (black star) in the low-latitude NE Atlantic upwelling area.Arrows indicate the major oceanic currents in the study area.Inset: location of the study area off coastal NW Africa.Modified after Romero et al. (2008).

Figure 2 .
Figure2.SEM image (scale bar: 100 µm) and cross-section image during SIMS analysis of a single Eubuliminella exilis specimen.The white circles highlight the selected spots for SIMS analyses, measuring 5 µm in diameter.Note that the black areas of the SIMS measurement targets visible in this image are actually the 5 µm spots plus the 10 µm pre-sputters.Inset is a close-up of the SIMS targets: the red square is the approximate pre-sputter area (15 × 15 µm, i.e. 5 µm spot +10 µm raster), the yellow area is the field of view admitted to the mass spectrometer (controlled by magnification and field aperture) and the blue ellipse is the nominal 5 µm spot.

ForaminiferalFigure 3 .
Figure 3.The Mn / Ca (µ mol mol −1 ) variability within each individual Eubuliminella exilis specimen for each climatic interval (labelled on the x axis), determined by SIMS.

Table 1 .
Sample list: climatic intervals, export productivity according to diatom export, average foraminiferal Mn / Ca for different samples determined by SIMS and FT-ICP-OES.

Table 2 .
Post hoc test (Mann-Whitney U) z values between the mean foraminiferal Mn / Ca (per individual) between climatic intervals.Significant differences are highlighted in bold.