Geochemistry, Geophysics, Geosystems
  • Open Access

Incorporation of uranium in benthic foraminiferal calcite reflects seawater carbonate ion concentration

Authors


Abstract

[1] The chemical and isotopic composition of foraminiferal shells (so-called proxies) reflects the physicochemical properties of the seawater. In current day paleoclimate research, the reconstruction of past seawater carbonate system to infer atmospheric CO2 concentrations is one of the most pressing challenges, and a variety of proxies have been investigated, such as foraminiferal U/Ca. Since in natural seawater and traditional CO2 perturbation experiments the carbonate system parameters covary, it is not possible to determine the parameter of the carbonate system causing, e.g., changes in U/Ca, complicating the use of the latter as a carbonate system proxy. We overcome this problem by culturing the benthic foraminifer Ammonia sp. at a range of carbonate chemistry manipulation treatments. Shell U/Ca values were determined to test sensitivity of U incorporation to various parameters of the carbonate system. We argue that inline image is the parameter affecting the U/Ca ratio and consequently, the partitioning coefficient for U in Ammonia sp., DU. We can confirm the strong potential of foraminiferal U/Ca as a inline image proxy.

1 Introduction

[2] Reconstruction of past atmospheric CO2 concentrations is one of the most pressing challenges in current day paleoclimate research. Climate sensitivity due to atmospheric CO2 doubling will likely cause global temperature to increase by 2.0–4.5°C [International Panel on Climate Change (IPCC), 2007]. While the direct effect of increasing CO2 is straightforward, the eventual impact of CO2 rise is uncertain due to the various positive and negative feedbacks in the climate system. In combination with temperature reconstructions, accurate atmospheric paleo-CO2 estimates are necessary to validate models that aim at predicting global temperature rise related to CO2-forcing mechanisms. Reconstructions of atmospheric pCO2 from ice cores are confined to the last 800 kyr [Lüthi et al., 2008], while reconstruction of atmospheric pCO2 going further back in time relies on sedimentary archives [e.g., Hönisch et al., 2012]. Within the latter, foraminifera play a central role since the chemical and isotopic composition of their shells reflects the physicochemical properties of the seawater that these organisms grew in [Emiliani, 1955].

[3] On glacial-to-interglacial timescales, atmospheric CO2 concentrations are largely driven by the amount of dissolved inorganic carbon in the ocean since the latter functions as a large reservoir of CO2 being in equilibrium with the atmosphere [Broecker and Peng, 1982]. Consequently, past seawater [CO2(aq)] may be used to estimate paleo-atmospheric CO2. To reconstruct paleo-seawater [CO2(aq)], two out of six parameters of the ocean's carbonate system ([CO2], inline image, inline image, pH, DIC (total dissolved inorganic carbon), and TA (total alkalinity)) must be known.

[4] Foraminiferal boron isotopes are known to reflect seawater pH [Hemming and Hanson, 1992; Hönisch et al., 2009; Sanyal et al., 1995] and hence are used to reconstruct paleo-seawater pH [Hönisch et al., 2009]. A second carbonate system parameter needed to complete past atmospheric CO2 concentration calculations could be total alkalinity, which can be estimated from reconstructed changes in salinity [Hönisch and Hemming, 2005]. The uncertainty that is associated with such salinity reconstructions (derived from combining foraminiferal δ18O measurements with an independent temperature proxy such as Mg/Ca) [Nürnberg et al., 1996], however, call for a direct, independent proxy for one of the other carbonate system parameters. Foraminiferal B/Ca is thought to reflect inline image, but the errors in reconstructed carbonate ion concentrations may be too large to reliably reconstruct the complete carbonate system and thus paleo-pCO2 [Yu and Elderfield, 2007; Yu et al., 2010].

[5] The U/Ca ratio of both planktic and benthic foraminifera is known to correlate with carbonate system parameters such as pH and inline image [Raitzsch et al., 2011; Russell et al., 2004] and hence is a potential alternative to the B/Ca ratio to reconstruct seawater inline image. It is, however, not known which of these correlations represent a causal relationship and which correlations are merely accidental regularities. To make this distinction, experiments are necessary in which different parameters of the carbonate system are manipulated independently. The classical approach in carbonate chemistry perturbation experiments [Smith and Roth, 1979] is insufficient since this changes several parameters of the carbonate system simultaneously, and it is impossible to distinguish, e.g., pH effects and carbonate ion effects. To overcome this problem, we have conducted experiments following both the classical approach, i.e., covarying pH and inline image, as well as keeping pH constant while varying inline image. The experimental setup used allows us hence to independently quantify effects of pH and inline image on foraminiferal U/Ca. The carbonate chemistry perturbation experiments were conducted with specimens of the benthic foraminifer “Ammonia molecular type T6” [Hayward et al., 2004] further referred to as Ammonia sp.

2 Material and Methods

2.1 Sample Collection and Culturing

[6] Surface sediments were collected from intertidal mudflats in the Wadden Sea (Dorum, Germany) at regular intervals between January and May 2011. Upon return to the laboratory, sediments were sieved over a 630 µm screen to remove macrofauna. Sieved sediment was transferred to small aquaria and covered with seawater collected at the same site. The aquaria were stored at 10°C and provided a set of stock cultures for the culturing experiments.

[7] From the stock material, specimens of Ammonia sp. were isolated by sieving sediment over a 230 µm screen. Living specimens were distinguished by having brightly colored yellow cytoplasm and pseudopodial activity. A number of specimens were transferred to well plates and placed at 25°C. Reproduction was stimulated by addition of food (living specimens of the green algae Dunaliella salina). Seawater was replaced and new food was added every 2–3 days. After 1 week, approximately 10% of the specimens had reproduced asexually, yielding 50–200 juveniles per specimen, consisting of a macrospheric proloculus (diameter approximately 40 µm). Juveniles were kept in well plates and fed for an additional 2–3 days, during which they added another approximately three chambers before being transferred to the controlled culture experiments.

2.2 Seawater Preparation

[8] Sterile-filtered North Sea water (0.2 µm pore size) was filled into an 80 L container and kept at 10°C in the dark. This batch was subsampled to determine pH, TA, and DIC. Culture media for the experiments were prepared from this batch by manipulating the carbonate chemistry in two different ways:

2.2.1 Experimental Set A: Acid/Base Manipulation

[9] Four sets of culture media were prepared by addition of acid (1 M HCl) or base (1 M NaOH). One culture medium consisted of not-manipulated seawater (Table 1, treatment A2). Culture media of this experimental set are characterized by a range of pH values and inline image, while the total inorganic carbon concentration was kept constant.

Table 1. Carbonate System Parameters, U/Ca, and DU (Calculated Partition Coefficient)a
 Treatments
A1A2A3A4B1B2B3B4
  1. aU/Ca of the seawater media (sw) and calcite (cc) as well as calculated partition coefficient DU for acid/base manipulation (A1–A4) and pH-stable manipulation (B1–B4) treatments. pH and DIC were measured and used as input parameters to calculate the carbonate system (together with salinity and temperature using the CO2SYS software [Pierrot et al., 2006]). pCO2 values supplied from the gas-mixing system are additionally listed (nominal). Average precision of DIC based on repeated measurements of an in-house standard was 10 µmol/kg-sw. Stability was checked over the course of the experiment by regular pH measurements and control of the pCO2 provided by the gas-mixing system (precision approximately 10 µatm).
pCO2 (µatm) “nominal”18038095014001803809501400
pCO2 (µatm)2174798501301633968291252
inline image (µmol/kg-sw)4012241368821152405563
inline image (µmol/kg-sw)1798199920732063223149935365131
DIC (µmol/kg-sw)2205223622322187246166239655729
TA (µmol/kg-sw)2747253524002277342188444366343
pH total scale8.328.027.797.607.957.988.038.01
Ωcc9.85.53.32.20.53.79.913.8
Salinity32.832.832.832.832.732.732.832.6
U/Casw (nmol/mol)13441364136513641366132813541520
U/Cacc (nmol/mol)32431061177971872527
DU × 1000233178855831411818

2.2.2 Experimental Set B: pH-Stable Manipulation

[10] In this set of experiments, seawater was manipulated by adjusting the inline image, while keeping pH stable. The four treatments were chosen, such that the accompanying pCO2 values matched those of the acid/base manipulation (Table 1).

[11] To manipulate the carbonate ion concentration, calculated volumes of a bicarbonate stock solution were added to seawater. In one treatment (B1), the target carbonate ion concentration was lower than that of seawater; consequently DIC was reduced prior to addition of bicarbonate. This was achieved by acidification of the seawater with HCl (1510 μL 1 M HCl/L sw) followed by bubbling with CO2 free air, to strip out DIC in the form of CO2. Carbonate ion concentration was then determined first and used to calculate the volume of the bicarbonate stock solution to be added.

[12] In each treatment for the pH-stable manipulation, pH was subsequently adjusted with HCl (1 M) and NaOH (1 M) to 8.0 (Table 1). All media were filled bubble-free into borosilicate flasks, sealed gas tight with Teflon-lined caps and kept at 3°C upon usage in the experiments.

2.3 Experimental Setup and Culturing

[13] Petri dishes containing manipulated seawater and juveniles were placed into one of four controlled pCO2 boxes. These boxes were connected to a gas-mixing system, supplying water-saturated air with set pCO2 (Table 1). Gas flow rates were kept constant and set to 60 L per hour, which is sufficient to allow complete replacement of the atmosphere inside the box six times each hour. Boxes were installed in a temperature-controlled room kept at 26°C and subjected to a day/light cycle (12 h/12 h). The pCO2 values of the gas mixtures were checked regularly and did not vary more than 10 µatm. Borosilicate bottles containing the pre-mixed media were opened and stored in the appropriate controlled pCO2 box for 2 days prior to being used in the experiment to allow for equilibration. Water was replaced and foraminifera were fed photosynthetically inactive (sterilized) algae (D. salina) every 2–3 days. The algae were centrifuged to minimize dilution of the culturing media through food addition (approximately 1% dilution per feeding event). Petri dishes were exchanged every 2 weeks, to minimize potential effects of bacteria growing on the bottom of the dishes. Foraminifera were kept in the dishes for 59–96 days, after which they were taken out and cleaned. Foraminiferal tests were placed in concentrated NaOCl for approximately 20 min to remove the cytoplasm. Specimens were subsequently rinsed three times in deionized water and dried at room temperature.

2.4 Sample Analysis

2.4.1 Seawater Composition: Elemental Concentrations and the Carbonate System

[14] The calcium concentration of the culture media was determined via ICP-OES (inductively coupled plasma optical emission spectrometry). Seawater uranium concentrations were calculated from salinity, using the re-evaluated U-salinity relationship in seawater from Owens et al. [2011].

[15] The DIC samples were filled without headspace into acid-washed 13 mL borosilicate flasks. Samples were measured within days and stored at 0°C until measurement. DIC was measured in duplicates photometrically [Stoll et al., 2001] with a TRAACS CS800 QuaAAtro autoanalyzer (Seal Analytica, Meqon, USA). Average precision was 10 µmol/kg-sw based on repeated measurements of an in-house standard calibrated against Batch No. 54 of A. Dicksons CRMS (Certified Reference Material Seawater, Marine Physical Laboratory, Scripps Institution of Oceanography). pH was measured potentiometrically using an NBS-calibrated glass electrode (Schott Instruments, Mainz, Germany) interfaced to a WTW pH meter. Conversion to the total scale was performed by means of a seawater buffer: Tris/Tris-HCl prepared according to the recipe described in Dickson et al. [2007]. pH values reported are always on the total scale. Salinity and temperature were measured with a conductivity meter (WTW Multi 340i), interfaced with a TetraCon 325 sensor.

[16] Not all parameters of the carbonate system can be measured directly. However, only two measurable parameters are required to calculate the full system. Depending on the choice of input parameters, differences in the calculated parameters can occur (for a more thorough discussion, see Hoppe et al. [2012]). The values reported in Table 1 were calculated from pH and DIC, measured directly upon manipulation and are supplemented by three additional types of input-parameter combinations in the Supporting Information (See Table S1). The CO2SYS software adapted to Excel by Pierrot et al. [2006] was used to calculate the carbonate system with the equilibrium constants for K1 and K2 of Mehrbach et al. [1973] as reformulated by Dickson and Millero [1987]. All values, figures, tables, and regression equations in the text are based on the values given in Table 1.

2.4.2 Element Analysis: LA-ICP-MS

[17] Element concentrations of cleaned foraminiferal shells were determined using laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS) at Utrecht University [Reichart et al., 2003]. We used an Excimer laser (Lambda Physik) with GeoLas 200Q optics connected to a sector-field mass spectrometer (Element2, Thermo Scientific). Ablation beam diameter was set to 80 µm, and pulse repetition rate was 6 Hz with an energy density at the sample surface of ~1 J/cm2. Elemental concentrations were calculated from isotopic counts of 24Mg, 26Mg, 27Al, 43Ca, 44Ca, 55Mn, 88Sr, and 238U, assuming standard natural abundance ratios [Jochum et al., 2011]. Analytical parameters of the MS were set such that it took 0.52 s for a complete cycle through all masses. 27Al was monitored to identify potential surface contaminations in the ablation profiles. Between approximately every 10 measurements, a NIST SRM 610 silicate glass was ablated three times and an in-house matrix-matched calcite standard once [Raitzsch et al., 2010]. The glass standard was ablated with an energy density of ~5 J/cm2, the calcite standard was ablated with the same energy density as used for the foraminifera [Dueñas-Bohórquez et al., 2009]. The 43Ca isotope was used as internal standard, assuming 40 wt % calcium in calcite, whereas 44Ca was used to check for consistency. We analyzed six specimens per treatment and carried out five to seven measurements per individual, summing up to 276 spot measurements in total. Five measurements were discarded, due to thin chamber walls and consequently short ablation profiles. Using calculated seawater U/Ca ratios, the partition coefficient for uranium in foraminiferal calcite (DU) was calculated according to (cc = calcite, sw = seawater)

display math

3 Results

3.1 U/Cacc and DU

[18] The overall mean U/Cacc ranges from 32 to 797 nmol/mol between the different treatments, resulting in a DU of 23–584 × 10−3 (Table 1). Since highest U/Cacc (797 nmol/mol) was measured on shells grown in media undersaturated with respect to calcium carbonate, SEM (scanning electron microscopy) micrographs of the shell surface were taken after LA-ICP-MS analysis. Surface features did not show signs of dissolution (Figure 1b), when compared to the shells grown in supersaturated waters (Figures 1a and 1c).

Figure 1.

The SEM images of cultured Ammonia sp. shell surfaces. ((a) Specimen from treatment A2 (“control group”—modern day carbonate system parameters, ΩCa = 5.5), scale bar represents 20 µm. (b) Specimen from treatment B1 with the lowest ΩCa (0.5), scale bar = 20 µm. (c) Specimen from treatment B4 with the highest ΩCa (13.8), scale bar = 50 µm.

[19] Variability in U/Cacc, expressed as relative standard deviation (RSD), indicates a relatively homogenous U/Cacc (~50% on average) over the range of pH/inline image (Figure 2) in the acid/base manipulation, whereas foraminiferal U/Cacc in the pH-stable manipulation varies between ~25% and ~75%. Highest carbonate ion concentrations resulted in a high relative variability in U/Cacc. The average intra-individual RSD was on average slightly lower (44%) than the average inter-individual RSD (51%). The associated uncertainty when measuring U/Cacc on a number of specimens can be calculated from the RSD: the estimated standard error when measuring five individuals would be 23% and when measuring 10 individuals 16%. The detection limit for U in foraminiferal calcite was calculated as described in Longerich et al. [1996], which was on the order of 1 × 10−5 ppm, approximately four orders of magnitude lower than measured uranium in cultured foraminifers.

Figure 2.

The DU (Log DU) versus (a) carbonate, (b) bicarbonate, (c) DIC, and (d) TA in µmol/kg-sw. Grey crosses represent individual laser-ablation measurements, whereas squares indicate mean values. Open squares represent data from acid/base manipulation and closed squares from pH-stable manipulation. Figures 2a–2d contain data of all treatments combined. Inset in Figure 2a depicts Log DU versus carbonate (µmol/kg-sw). Insets in Figures 2b–2d represent data from the acid/base manipulation only; labeling for x and y axes is the same as in Figures 2b–2d and has been omitted. Please note that depiction of treatments A1 and B3 overlaps in Figure 2a (nearly identical DU values at a carbonate ion concentration of approximately 400 µmol/kg-sw).

3.2 Correlation Between DU and the Carbonate System

[20] The correlation of DU with the carbonate system parameters (pH, inline image, etc.) was analyzed by means of regression analysis (Table 2). All regressions are highly significant (p < 0.001), despite one, and from reported R2 values, a correlation with all parameters but pH and pCO2 seems possible and is discussed further below (section 'Correlation Between DU and the Carbonate System'). An exponential correlation results in higher R2 values, seeming thus more likely. Tukey post hoc tests (see Supporting Information for more details on statistical treatment) were performed to determine which treatments (based on DU) were statistically different from each other, and the results also support an exponential correlation (here explained with inline image as an example, see Figure S1): On the higher end of the carbonate ion concentration (>200 µmol/kg-sw), DU values are statistically indifferent from each other (e.g., A1 and B3). For carbonate ion concentration <100 µmol/kg-sw, all DU are statistically different. This pattern fits a negative exponential correlation between DU and carbonate ion concentration due to the mathematical properties of the exponential function. However, it has to be stressed that changes in carbonate ion concentration values at the lower end of the carbonate ion concentration (especially <100 µmol/kg-sw) range yield high differences in DU, whereas those changes at the higher end of the concentration range yield only small or no appreciable changes in DU.

Table 2. The DU Relationships With Carbonate System Parametersa
 R2p
  1. aRegression and statistics are based on individual measurements (n = 271 in total for all treatments). 95% confidence intervals are reported for intercepts and slopes of regressions. Units: DU = 1000 × DU and Log DU = Log 1000 × DU).
DU = 239(±27)–0.55(±0.09) inline image0.35<0.001
Log DU = 2.30(±0.07)–0.0027(±0.0002) inline image0.65<0.001
DU = 286(±29)–0.06(±0.01) [TA]0.42<0.001
Log DU = 2.43(±0.08)–2.78 × 10−4(±0.25 × 10−4) [TA]0.63<0.001
DU = 240(±27)–22.47(±3.68) [Ω]0.35<0.001
Log DU = 2.30(±0.07)–0.11(±0.01) [Ω]0.65<0.001
DU = 282(±29)–0.08(±0.01) inline image0.41<0.001
Log DU = 2.39(±0.09)–3.26 × 10−4(±0.33 × 10−4) inline image0.58<0.001
DU = 283(±29)–0.07(±0.01) [DIC]0.42<0.001
Log DU = 2.41(±0.09)–2.97 × 10−4(±0.29 × 10−4) [DIC]0.60<0.001
DU = 782(±814)–84.74(±102.30) [pH]0.010.06
Log DU = 9.91(±2.76)–1.04(±0.35) [pH]0.11<0.001
DU = 244(±30)–0.19(±0.04) [pCO2]0.19<0.001
Log DU = 2.09(±0.11)–6.07 × 10−4(±1.33 × 10−4) [pCO2]0.14<0.001

4 Discussion

4.1 Correlation Between DU and the Carbonate System

[21] We used two different methods to manipulate the seawater carbonate chemistry: an acid/base manipulation (treatments A1–A4, see Table 1) and a pH-stable manipulation (treatments B1–B4, see Table 1). Since the carbonate system parameters covary differently in the two experimental approaches, it is possible, by exclusion, to reject certain parameters of the carbonate system as causes for the observed changes in DU (Table 1). In the acid/base manipulation DU displays a positive correlation with pCO2, whereas the correlation of DU and pCO2 is negative in the pH-stable manipulation. Therefore, pCO2 cannot be the parameter of the carbonate system causing a change in DU. The change in DU under constant pH (pH-stable manipulation) was almost a factor of 10 larger than in the acid/base manipulation, where pH covaried. Consequently, pH can be excluded as a controlling factor and the negative correlation of DU with pH in the acid/base manipulation must be regarded as inherent to the carbonate system and not causal.

[22] In the pH-stable manipulation experiments, TA, DIC, inline image, inline image, and Ω correlate negatively with DU over a wide range of values (Table 1 and Figure 2 closed squares; note that the correlation of DU with Ω has not been plotted, since [Ca2+] was kept constant and consequently the distribution of Ω is essentially that of inline image; Figure 2a). By contrast, the ranges covered in the acid/base manipulation are, with the exception of inline image and Ω, much smaller (Table 1). In the case of DIC (acid/base manipulation), most DU are similar. Nevertheless, when DU is plotted versus DIC, a conspicuous clustering of values can be seen, namely the DU of treatments A3 and A4 are similar, and so are the DU of treatments A1 and A2 (small inset in Figure 2c). The same clustering is obvious when DU is plotted versus inline image and TA (insets in Figures 2b and 2d). Combining values of the acid/base and the pH-stable manipulation in one plot (Figures 2b–2d) might, especially in the case of TA (Figure 2d), suggest that TA causes the change in DU and that the curious clustering of treatments A3 and A4, and A1 and A2, respectively, simply reflects the transition of the curve from a steep to a shallow slope. If DIC or inline image was the controlling factor, DU values should be more or less identical in the pH-stable manipulation, given the small range in DIC and inline image. Since there is no reason why, given identical DIC/inline image, there should be such a distinct cluster pattern, and DIC and inline image cannot be the parameter affecting DU. The cluster pattern, however, is absent when plotting DU versus inline image (Figure 2a). Hence, based on the correlations only, inline image or Ω are likely candidates to be instrumental in changing DU, but leave open the possibility that TA might still be involved. It has to be noted, that Ca2+ was kept constant in all treatments and foraminifera do not respond to Ω as such, but to the concentrations of Ca2+ and inline image (which also holds true for TA) [Dueñas-Bohórquez et al., 2011; Raitzsch et al., 2010]. Consequently, the correlation between DU and Ω is only caused by the concentration change in carbonate ions, leaving carbonate ions as the only candidate affecting foraminiferal U/Ca. Furthermore, we cannot exclude the possibility of parameters, such as TA and/or pH, exerting a modulating influence on the obtained correlations. While the modulating influence cannot be unambiguously identified using the data set presented here, we will point out that the correlation can be explained by a sole influence of carbonate ion concentration on DU. Hence, a modulating influence of other parameters, although possible, is not needed in order to interpret the changes in DU.

[23] The effect of inline image on foraminiferal U incorporation could be explained in terms of uranium speciation in seawater. Uranium easily complexes with carbonate ions, and speciation thus strongly depends on inline image of the seawater (Figure 3). With increasing inline image, the percentage of the sum of the different carbonate complexes [UO2(CO3)(aq)], inline image, and inline image increases, whereas the percentage of the sum of the free forms inline image and [UO2OH+] decreases. This change in speciation is not linear and particularly prominent below ~200 µmol/kg-sw inline image (Figure 3). Interestingly, the correlation of foraminiferal DU with inline image is also not linear, but exponential (see Figure 2a), with the largest change in DU µmol/kg-sw inline image at the lower range of inline image used here, i.e., below ~200 µmol/kg-sw (Table 1 and Figure 2). This matches the increase in inline image and [UO2OH+] at low inline image. We hypothesize that the free forms (inline image and [UO2OH+]) are more readily taken up by Ammonia sp. than the carbonate complexes. This speculation would explain the observed dependency of DU on inline image. In support of this hypothesis, it was reported that the bioavailability of U (i.e., its ability to bind to or traverse the cell surface) in green algae increases with decreasing inline image [Fortin et al., 2004; Markich, 2002]. The latter authors attribute this effect to the fact that primarily the free forms of U (especially inline image) are taken up by the cells. In analogy, we speculate that the free forms of U can cross the cell membrane of Ammonia sp. more easily than the carbonate complexes can. This would imply that U is taken up via transmembrane transport during chamber formation, which therewith would be a major pathway of ion transport for chamber formation in Ammonia sp. The latter assumption was also put forth in the context of proton transport [Glas et al., 2012]. We are aware that ion transport in foraminifera is usually assumed to be endocytosis mediated [Erez, 2003], but the latter hypothesis is based on experiments with a different species, and there might be species-specific differences in transport mechanism. We will point out that our explanation of the change in DU with seawater inline image is consistent with a constancy of U fractionation during calcite precipitation. This is advantageous, because pH homeostasis in the calcifying fluid most likely leads to a constant U speciation which would be decoupled from seawater U speciation.

Figure 3.

Uranium speciation as a function of carbonate ion concentration. Conditions of acid/base manipulation are seen in the top image and of pH-stable manipulation in the bottom image. Chemical speciation calculations were performed with the software Visual Minteq ver. 3.0 [Gustafsson, 2010]. The original thermodynamic database supplied with the software was used without alteration. The main components added to simulate a seawater water matrix were Ca2+ (10 mM), Mg2+ (60 mM), Na+ (0.7 M), and Cl (0.7 M). The speciation of the carbonate and uranium system for the two experimental manipulations (acid/base manipulation and pH-stable manipulation) was calculated as follows: the acid/base manipulation was represented by an open system where the pH was allowed to vary (calculated from the mass balance) and the pH-stable manipulation was represented by a closed system with a pH fixed at 8.2. H+ concentration and pCO2 have been adjusted to fit the inline image range of interest. All calculations were performed using a temperature of 25°C.

4.2 Paleoceanographic Implications

[24] Previous studies [e.g., Russell et al., 2004] reported a correlation between foraminiferal U/Ca and carbonate chemistry of seawater. While these studies attributed the effect to carbonate ion concentration/calcite saturation state, this inference remained conjectural, because in all available data sets, the parameters of the carbonate system covaried, rendering it impossible to tell, e.g., pH from carbonate ion effects. The reported U/Cacc values for benthic [Raitzsch et al., 2011] and planktic foraminifera [Russell et al., 2004] were 2–10 times lower than the ones determined by us for the same range of inline image (80–110 µmol U/kg seawater). The difference in calcitic U/Cacc may be the result of species-specific fractionation against U during calcification and underscores the need for species-based calibrations when applying U/Cacc to reconstruct past inline image. However, it needs to be stressed that the species used here, Ammonia sp., is not commonly used in paleoceanographic studies, due to its shallow-water benthic habitat. Nevertheless, its abundance, easy accessibility, the relatively common asexual reproduction, and the tolerance of a broad range of environmental parameters make it a suitable candidate when determining basic foraminiferal responses. Applying the here-introduced experimental protocol of decoupling C-system parameters to more relevant species in terms of paleoceanography is a step that should be undertaken in the future to analyze the DU-inline image relationship further. While the slope of this relationship apparently is species specific, it is likely that the causal basis for this relationship is not. Our results therefore put the application of U/Cacc as a inline image proxy on a firm footing.

[25] Even if not primarily of interest for paleoceanographic studies, a few properties of the correlation found here shall be given to facilitate comparability between different studies. The large range of inline image applied in our culture study supports an exponential relation between carbonate ion concentration and calcitic U/Cacc as previously proposed by Russell et al. [2004]:

display math

[26] Based on this calibration, we can infer that a decrease of 100 µmol/kg-sw in carbonate ion concentration from 300 to 200 µmol/kg-sw, as anticipated for a transition from full glacial to interglacial conditions, would be expected to result in an increase of 54% in foraminiferal U/Cacc. With our analytical approach, those changes can be quantified within the 95% confidence intervals. This sensitivity is approximately twice as high as that reported for two planktic species, Orbulina universa and Globigerinoides sacculifer by Russell et al. [2004].

5 Conclusion

[27] The partitioning coefficient for U in Ammonia sp., DU, shows a negative correlation with TA, DIC, inline image, inline image, and Ω. By exclusion we argue that inline image is the parameter controlling DU. While Ammonia sp. might not be a species traditionally used in paleoceanographic reconstructions, the underlying processes of a carbonate chemistry-induced change in DU are assumed to be the same for all foraminiferal species. Therefore, our data support the proposed use of foraminiferal U/Cacc as a inline image proxy.

Acknowledgments

[28] We in particular wish to thank Caroline Otten for support with the culturing and Klaus-Uwe Richter for support with the experimental setup. Yvette Bublitz, Marc Bullwinkel, Antje Funcke, Jana Hölscher, Beate Müller, and Charlyn Völker are thanked for laboratory assistance. We thank Cathleen Zindler for unraveling the secrets of R. This research was funded by the Alfred Wegener Institute through Bioacid (Gerald Langer FKZ: 03F0608) and the European Community's Seventh Framework Programme under grant agreement 265103 (Gerald Langer, Project MedSeA). This work contributes to EPOCA “European Project on Ocean Acidification” under grant agreement 211384. This work was funded in part by The European Research Council (ERC grant 2010-NEWLOG ADG-267931 HE). Nina Keul is the beneficiary of a doctoral grant from the AXA Research Fund.

Ancillary