Earth and Planetary Science Letters 273 (2008) 260–269

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Controls on shell Mg/Ca and Sr/Ca in cultured planktonic foraminiferan,Globigerinoides ruber (white)

B. Kısakürek a,⁎, A. Eisenhauer a, F. Böhm a, D. Garbe-Schönberg b,1, J. Erez c,2

a Leibniz-Institute of Marine Sciences, IFM-GEOMAR, Wischhofstr. 1-3, 24148 Kiel, Germanyb Christian-Albrechts University of Kiel, Ludewig-Meyn-Straße 10, 24118 Kiel, Germanyc Institute of Earth Sciences, The Hebrew University, Givat Ram, Jerusalem, 91904, Israel

⁎ Corresponding author. Tel.: +49 431 6002111; fax: +E-mail addresses: bkisakurek@ifm-geomar.de (B. Kıs

aeisenhauer@ifm-geomar.de (A. Eisenhauer), fboehm@idgs@gpi.uni-kiel.de (D. Garbe-Schönberg), erez@vms.hu

1 Tel.: +49 431 880 2872; fax: +49 431 880 4376.2 Tel.: +972 2 6584882; fax: +972 2 6520041.

0012-821X/$ – see front matter © 2008 Elsevier B.V. Adoi:10.1016/j.epsl.2008.06.026

A B S T R A C T

A R T I C L E I N F O

Article history:

Mg/Ca and Sr/Ca ratios we Received 12 February 2008Received in revised form 29 May 2008Accepted 17 June 2008Available online 27 June 2008

Editor: P. DeMenocal

Keywords:planktonic foraminiferaMg/CaSr/CasalinitytemperaturepHgrowth rateculturing

re determined on a single species of planktonic foraminiferan, Globigerinoidesruber (white), collected from the Gulf of Eilat and cultured in seawater at five different salinities (32 to 44),five temperatures (18 to 30 °C) and four pH values (7.9 to 8.4). The Mg/Ca-temperature calibration of culturedG. ruber (with an exponential slope of 8±3%/°C) agrees well with previously published calibrations from core-tops and sediment traps. However, the dependence of Mg/Ca on salinity (with an exponential slope of 5±3%/psu) is also significant and should be included in the calibration equation. With this purpose, we calculated acalibration equation for G. ruber dependent on both temperature and salinity within the 95% confidence limits:

Mg=Ca mmol=molð Þ ¼ exp 0:06 �0:02ð ÞTS psuð Þ þ 0:08 �0:02ð ÞTT 0Cð Þ−2:8 �1:0ð Þ½ �;R2 ¼ 0:95

The influence of pH on Mg/Ca ratios is negligible at ambient seawater pH (8.1 to 8.3). However, we observe adominating pH control on shell Mg/Ca when the pH of seawater is lower than 8.0. Sr/Ca in G. ruber shows asignificant positive correlation with average growth rate. Presumably, part of the variability in shell Sr/Ca inthe geological record is linked to changes in growth rates of foraminifera as a response to changingenvironmental conditions.

© 2008 Elsevier B.V. All rights reserved.

1. Introduction

Mg/Ca paleothermometry is based on the temperature depen-dence of the partitioning of Mg into inorganic calcite (Katz, 1973).However, there is a tight biological control on the uptake of Mg, asrevealed by the highly variable partition coefficients (DMg) forbiogenic calcite (Blackmon and Todd, 1959) compared to that forinorganic calcite (Mucci and Morse, 1983). Furthermore, DMg inplanktonic foraminifera is usually much lower than that of inorganiccalcite (Segev and Erez, 2006). Hence, species based calibrations areessential. The Mg/Ca ratio of planktonic foraminifera shells hasalready been established as a proxy for sea surface temperatures(SST) through calibrations from core-tops (Dekens et al., 2002;Elderfield and Ganssen, 2000; Hastings et al., 1998; Lea et al., 2000;Rosenthal and Lohmann, 2002), culturing experiments (Lea et al.,1999; Mashiotta et al., 1999; Nürnberg et al., 1996; von Langen et al.,

49 431 6002928.akürek),fm-geomar.de (F. Böhm),ji.ac.il (J. Erez).

ll rights reserved.

2005) and sediment traps (Anand et al., 2003; McConnell and Thunell,2005). Even though inter-species differences exist in the calibration ofthe exponential dependence of Mg/Ca on temperature, a well-definedcalibration equation has been proposed for all planktonic species(except for Orbulina universa and Globigerinella siphonifera that havedistinctly higher Mg/Ca ratios), with an exponential slope of ~9%/°C(Anand et al., 2003). There has been growing interest in applying thisproxy to foraminifera shells from sediment cores in a number ofoceanic settings to study changes in past SST. This is importantbecause Mg/Ca constitutes an independent temperature proxy thatcan be measured in the same phase as δ18O, thereby allowingtemperature and salinity (as a function of δ18Ow) signals to beseparated (Lea et al., 2000; Lear et al., 2000; Mashiotta et al., 1999;Nürnberg and Groeneveld, 2006; Rosenthal et al., 2000).

In contrast to Mg incorporation into inorganic calcite that appearsto be independent of precipitation rate (Mucci andMorse,1983; Mucciet al., 1985), the partition coefficient of Sr increases with higherprecipitation rates in inorganically precipitated calcite (Lorens, 1981;Nehrke et al., 2007) as well as in biogenic calcite from coccolithophor-ids (Rickaby et al., 2002; Stoll and Schrag, 2000). Temperature-dependence of Sr incorporation in planktonic foraminifera appears tobe species dependent. Globorotaliid species show significant tempera-ture sensitivity (2 to 3% increase in Sr/Ca per °C) whereas non-glo-borotaliid species do not show resolvable temperature sensitivity in

261B. Kısakürek et al. / Earth and Planetary Science Letters 273 (2008) 260–269

both core-tops and water-column catches (Elderfield et al., 2000;Mortyn et al., 2005). Even though Mg and Sr incorporation into calciteseem to have different controls, there exists a positive linearcorrelation between Sr and Mg contents of both abiotic and bioticmarine calcite (Carpenter and Lohmann, 1992; Mucci and Morse,1983). This is attributed to the calcite growth mechanism whereincorporation of Mg ion on the calcite crystal structure causesdeformations, creating sites where incorporation of the larger Sr ioncan be accommodated (Mucci and Morse, 1983). The interpretation ofMg/Ca and Sr/Ca proxies in foraminiferal calcite is complicated by thefact that uptake of these trace elements into the shell during bio-mineralization appears to be dependent on more than one environ-mental factor (Ferguson et al., 2008; Lea et al., 1999; Nürnberg et al.,1996; Russell et al., 2004) as well as on shell size (Elderfield et al.,2002; Ni et al., 2007).

Culturing studies offer the great advantage that foraminiferaare calcified under controlled laboratory conditions, where eachenvironmental factor can be simulated independently. Accuratelyknown temperatures (along with salinities, solution chemistry, etc.)can be assigned and dissolution effects that may exist in core-topsamples are eliminated. In this study, we reportMg/Ca and Sr/Ca ratiosin Globigerinoides ruber (white) from the Gulf of Eilat (Red Sea)cultured under different salinity, temperature and pH conditions.G. ruber constitutes a very important archive for studying past changesin sea surface conditions since it dwells in the top 50 m of the watercolumn (Anand et al., 2003; Deuser et al., 1981). It is confined to thephotic zone due to its symbiotic relationship with photosynthesizingdinoflagellates. Moreover, G. ruber does not deposit a gametogeneticcalcite of any significant thickness (Caron et al., 1990). Gametogeneticcalcite, a final outer calcite crust laid by most planktonic species priorto gametogenesis, is associated with lowMg/Ca due to its formation atgreater water depth and, hence, lower temperatures (Brown andElderfield, 1996; Eggins et al., 2003; Elderfield and Ganssen, 2000).Therefore, G. ruber has a rather homogenous distribution of Mg acrossits shell (Eggins et al., 2003; Gehlen et al., 2004). In our study, weextend on the temperature calibrations of Mg/Ca from culturing expe-riments that are covering four species of planktonic foraminifera todate (Globigerinoides sacculifer, Globigerina bulloides, Orbulina universaand Neogloboquadrina pachyderma; Lea et al., 1999; Mashiotta et al.,1999; Nürnberg et al., 1996; von Langen et al., 2005) and revisit theeffects of salinity and pH on shell Mg/Ca. These results have importantimplications for past SST estimates based on Mg/Ca ratios of G. ruber.

2. Methods

2.1. Culturing and experimental setup

Culturing experiments were carried out between April and June2006 at the Interuniversity Institute for Marine Sciences in Eilat (IUI),Israel. Live planktonic foraminifera were collected by towing a planktonnet (with a 102 μmmesh size) in the surfacewaters of the northern Gulfof Eilat, offshore where the water depth exceeds 300 m. Concurrently,surface seawater was collected for culturing. The samples were broughtback into the laboratory within an hour of collection. G. ruber (white)specimens were hand picked under a binocular microscope using aPasteur pipette and left to recover under strong light in a glass jar filledwith seawater for 1–2 days. Unrecovered specimens were kept as acontrol group to assess the initial shell Mg/Ca and Sr/Ca (Section 2.4).Recovered individuals that had a diameter of less than 300 μm(corresponding to a shell mass of less than 5 μg) were each placed inan individual 100 ml glass-stoppered Erlenmeyer flask filled withseawater filtered to 0.45 μm. The flasks were tightly capped and placedinwater baths where the temperature was regulated by employing (i) athermostatic circulator to stabilize the temperature down to 15 °C, (ii) atemperature controller to heat the bath to a higher constant tempera-ture (with a precision of ±0.2 °C), and (iii) a pumpto keep thewaterwell-

mixed. The experiments were carried out under artificial light providedby a metal halide lamp (420 W, Osram™) at constant irradiance of200 μmol photonsm−2 s−1. An autotimerwas set so as to allow 14 h lightand 10 h dark cycles. The irradiance provided artificially corresponds tothat at 15 to 20m depth in the openwaters of the northern Gulf of Eilatbetween April and June (Shaked andGenin, 2006). This agreeswell withthe reported depth habitat for G. ruber (0–50 m) (Anand et al., 2003).Light intensity is expected to have no apparent influence onwhole shellMg/Ca and Sr/Ca as shown by previous culturing studies on Orbulinauniversa (Lea et al., 1999; Russell et al., 2004).

Each individual was fed with one newly hatched brine shrimp(Artemia sp.) daily unless its ability to capture and digest food wasimpaired,which can be judged by the stickiness and length of its spinesas well as its floatation capacity. Each experiment usually lasted from 5to 10 days and was terminated when the individual went throughgametogenesis at the end of its life cycle. The remaining shell was thenrinsed free of seawater by passage through five consecutive washes ofdeionized water, dried down and then assessed for its diameter underan inverted microscope. The shell mass was measured using a Kahnmicrobalancewith a precision of ±0.1 µg. The shells that were selectedfor the chemical analysis comprised individuals that at least doubled intheir diameter andhad amass increase of 4 to 13 times the original one.

We manipulated three basic environmental parameters; salinity,temperature and pH. In the first set of experiments, salinity wasaltered either by adding deionized water to seawater for lowersalinities or by evaporating for higher salinities. The salinity experi-ments cover a range from 32 to 44 in 5 steps (32.1, 35.0, 38.0, 40.7 and44.3) and were run at a constant temperature of 24 °C. In the secondset of experiments, the water temperaturewas varied from 18 to 30 °Cin 5 steps (18, 21, 24, 27 and 30 °C) while salinity was kept constant at35. In the third set of experiments, the carbonate system wasmanipulated by keeping the dissolved inorganic carbon (DIC) constantat a level of 1.87±0.05 mmol kg−1 (2σ) while altering the pH (thustotal alkalinity-TA) by adding dilute base and acid to the seawater. Thesolutions were used immediately after preparation and not allowed toexchange with the atmosphere. The range of pH (in NBS scale) wasfrom 7.9 to 8.4 in 4 steps (7.9, 8.1, 8.3, 8.4), and the experiments wererun at a constant salinity of 35 and a constant temperature of 27 °C.

The culturing fluids of the salinity and temperature experimentswere sampled using a plastic syringe, filtered to 0.2 μm and stored inplastic tubes below 10 °C in the dark for chemical analysis. Salinitymeasurements were conducted on a 2100Model AGE™ salinometer atthe IUI, Israel. The culturing fluids from the pH experiments weresampled for TA and DIC prior to and immediately following culturingwithout allowing contact with the atmosphere. TA samples werestored in syringes under cool temperatures (b10 °C) in the dark,whereas DIC samples were stored in 60 mL brown glass bottles withgas-tight screw and poisoned with 0.6 mL of saturated HgCl2 solutionimmediately after sampling to avoid any microbial activity. TA wasmeasured using an automatic potentiometric titration method withan automated burette (Radiometer ABU91) at the Institute of EarthSciences, the Hebrew University of Jerusalem, Israel. DIC wasmeasured using an autoanalyzer QUAATRO spectrophotometricsystem at the Leibniz Institute of Marine Sciences (IFM-GEOMAR) inKiel, Germany (Stoll et al., 2001). Given TA and DIC, the carbonate ionconcentrations and pH were calculated using the computer programwritten by Lewis and Wallace (1998).

A grab sample was collected from the surface sediments at 490 mwater depth in the Gulf of Eilat, sieved through a 63μm sieve and thendried. G. ruber (white) specimens were hand picked and examined fortheir morphological structure for comparisonwith cultured individuals.

2.2. Sample preparation

Our cultured samples were not contaminated by sediment phases.However, they were observed to occasionally contain small amounts

Table 1Mg/Ca and Sr/Ca of external and internal standards; and the inter-instrumentalcalibration of two samples

Mg/Ca±2σ Sr/Ca±2σ

(mmol/mol) (mmol/mol)

StandardsJCP-1 Measured 4.24 8.65

Certified 4.19±0.08 8.66±0.19CS-1 (in-house standard) Measured 3.36 7.33

Calculated 3.30 7.32CS-2 (in-house standard) Measured 5.06 8.16

Calculated 4.95 8.23Reinie Kindly (in-houseforam std.)

Measured (n=8) 3.84±0.22 1.18±0.04

SamplesBK2-27R Quadrupole (Kiel) 4.84 1.37

Quadrupole (Kiel) 4.86 1.38Element 2 (Bremen) 4.86 1.41ICP-OES (Bremen) 4.88 1.36Average (n=4) 4.86±0.03 1.38±0.05

BK2-30R Quadrupole (Kiel) 6.12 1.42Quadrupole (Kiel) 6.12 1.46Quadrupole (Kiel) 6.18 1.44Element 2 (Bremen) 6.25 1.48ICP-OES (Bremen) 6.27 1.42Average (n=5) 6.19±0.14 1.44±0.05

The certified elemental ratios for JCP-1 are calculated from the concentrations specifiedin GSJ Certificate of Analysis, where errors have been propagated. The instruments usedare: 1) Agilent 7500cs series Quadrupole ICP-MS at the Institute of Geosciences, theUniversity of Kiel; 2) Thermo Finnigan Element 2 series ICP-MS at the University ofBremen; 3) Perkin Elmer Optima 3300 R type ICP-OES at the University of Bremen.

262 B. Kısakürek et al. / Earth and Planetary Science Letters 273 (2008) 260–269

of remnant cytoplasm similar to sediment trap samples (Anand et al.,2003). The absence of clay particles excludes employing vigorouscleaning procedures, while the presence of organic matter mightelevate theMg/Ca ratios (Barker et al., 2003; Rathburn and DeDeckker,1997). Given the specific cleaning target and the small sample sizes inthis study, we employed a gentle cleaningmethod using dilute sodiumhypochlorite solution rather than the common “Mg cleaning”procedures that use ~1% hydrogen peroxide solution for removal oforganic matter (Boyle and Keigwin, 1985; Elderfield and Ganssen,2000). In this way, we tried to minimize sample loss. Flow-throughsequential leaching analysis of foraminiferal calcite has shown thatMg-and Sr-rich phases go into dissolution first and thus extensivecleaningmight fractionate Mg from Ca (Benway et al., 2003; Haley andKlinkhammer, 2002). Moreover, our sample preparation was opti-mized for paired analysis of calcium isotopes and trace elements.

Two to six shells (20–170 μg) were grouped together for eachexperiment and transferred into a pre-cleaned Eppendorf vial. Theshells were kept intact throughout the cleaning procedure, thussonicationwas avoided. The samples were first suspended in 100 μL ofhypergrade methanol (Merck) using a vortex shaker; this step helps tomake the shells more hydrophilic so that the next cleaning steps canaccess through the apertures. Themethanolwas immediately removedand its remainder was washed out 3 times in between each chemicalstep, using 500 μL of ultrapure water that had been adjusted to a pH of8–9 by adding ultrapure NH4OH (J.T. Baker). The organic matter wasremoved from the shells by keeping them in 100 μL of dilute sodiumhypochlorite (bleach) solution (Sigma Aldrich, 1:20 dilution or b1%active reagent) for 10 min and occasionally shaking the vials with avortex shaker. After removing the bleach and conducting 3 washeswith water, the shells were examined under the microscope to makesure that total cleaning had been achieved. This check is importantbecause the findings of an inter-laboratory comparison study regard-ing cleaning procedures performed on samples from core-topssuggests that the relatively rapid cleaning via oxidation with sodiumhypochlorite might be inadequate for organics and produce high Mg/Ca and Sr/Ca ratios (Rosenthal et al., 2004). A quick step with 100 μL ofalkali buffered 1% H2O2 (made up of suprapur 30% H2O2 and 0.1 MNaOHMerckwith a ratio of 1:100)was employed to release any residueof bleach that might have stuck to the surface of the shells. Finally, thesamples were washed 5 times with water, dissolved in 10 μL of doubledistilled 2.5 N HCl and transferred at once to Savillex beakers. Thedissolutions were dried down, taken up in 100 μL of thermally distilled2% HNO3, evaporated to dryness and re-dissolved in a pre-calculatedamount of 2% HNO3 to give a Ca concentration of 10 ppm (±10%).

2.3. Elemental analysis

Elemental ratios were measured on an Agilent 7500cs seriesquadrupole ICP-MS at the Institute of Geosciences at the University ofKiel. The samples were calibrated against a set of multi-elementalstandard solutions prepared from single-element primary standards(ALFA, SPEX) and matrix-matched to 10 ppm Ca. The calibrationstandards covered the Mg/Ca and Sr/Ca range in our foraminiferashells. Sample introduction comprised 70 s of wash-in using a PFAmicro-flow-nebulizer (with a sample take-up of 200 µL/min), followedby data acquisition of 3 individual measurements with an integrationtime of 300 ms. The method uses ~0.5 ml of solution volume. Theinternal error was better than 0.8% (1σ) for both Mg/Ca and Sr/Ca. Themeasured average intensities of samples (i.e., raw counts per second)have been corrected for the procedural blank measured on the samesession, prior to calibration against the standards. Procedural blanksfor Ca and Sr were b0.2% for all samples. Procedural blank for Mgranged from 0.2 to 0.9% for all samples with digested CaCO3 mass ofN50 μg, but as high as 2.4 to 3.5% for samples with CaCO3 mass ofb20 μg (highest salinity and lowest temperature experiments,Table 2). All data were finally normalized to an in-house consistency

standard (coral Mayotte 5a) that has recently been analyzed for aninter-laboratory calibration (Mg/Ca=5.13 and Sr/Ca=8.82; DieterGarbe-Schönberg, pers. comm.).

The precision was mainly assessed from repeats of an internalforaminifera standard, prepared from Globigerina bulloides, Neoglobo-quadrina pachyderma and Turborotalita quinqueloba from core 23525-3in the Nordic Sea (Simstich, 1999). Repeat analysis of this internalstandard gave a precision of ±0.2 and ±0.04 (2σ, n=8) mmol/mol forMg/Ca and Sr/Ca, respectively (Table 1). Two samples (from the samebatch as the initial preparations) have been cross-calibratedonThermoFinnigan Element 2 series ICP-MS as well as on Perkin Elmer Optima3300 R type ICP-OES at the University of Bremen. The inter-instrumental precision is ±0.03 and ±0.14 (2σ) for Mg/Ca analysis ofBK2-27R and BK2-30R, respectively (Table 1). The inter-instrumentalSr/Ca precision is ±0.05 (2σ) for both of these samples. The measuredvalues of Mg/Ca and Sr/Ca in JCP-1 coral standard are within error ofthe certified values (Table 1). Two in-house calibration standards (CS-1andCS-2) preparedgravimetrically from single element solutionswereused as a further check on the accuracy (Table 1).

Elemental ratios of the culturing fluids weremeasured on Jobin YvonJY 170 Ultratrace series ICP-OES at the Leibniz-Institute of MarineSciences at the University of Kiel, Germany. The Mg/Ca and Sr/Ca of theculturing solutions from the Gulf of Eilat (covering the entire range insalinity and pH experiments) were determined as 5.35±0.07 mol/moland 8.87±0.11 mmol/mol (2σ, n=19), respectively. This is in goodagreementwith theMg/Ca andSr/Ca ratios of IAPSOmeasuredduring thesame analytical session (5.30±0.06 mol/mol and 8.79±0.07 mmol/mol,respectively, n=6).

2.4. Correction for initial mass

Since we are only interested in the fraction of the shells thatcalcified under controlled laboratory conditions, it is essential to applya correction on foraminiferal Mg/Ca and Sr/Ca for the initial mass of G.ruber. To do this, we draw on our control group that consists ofindividuals with a diameter of 200–300 μm and carries the tracerrecord of the natural conditions in the Gulf of Eilat prior to the onset of

263B. Kısakürek et al. / Earth and Planetary Science Letters 273 (2008) 260–269

the culturing experiments. The corrected value is calculated by thefollowing mass balance equation:

Pculture=(Pf⁎mf−Pi⁎mi) / (mf−mi), where P stands for the elementalratio under investigation and m represents the shell mass. The finalvalues of the elemental ratio andmass (Pf,mf) are determined from theculturing experiments. The initial value of the elemental ratio (Pi) isestablished by the control group, whereas the initial mass (mi) isestimated from the shell size (diameter; D) versus shell masscorrelation for G. ruber found in this study [mass (μg)=0.00008⁎D1.95

(μm), R2=0.89)]. A power-type regression was preferred over anexponential one because thefit better approximates for low shellmass.

3. Results

The results of this study are given in Table 2. Culturing experimentsBK1-35R and BK2-24R were conducted under the same experimentalconditions (at 35 psu and 24 °C). Mg/Ca and Sr/Ca of G. ruber (white)from these two experiments are within 2σ error of each other.

The trends for Mg/Ca and Sr/Ca with temperature, salinity and pHare given in Fig. 1. There is no significant overall correlation betweenMg/Ca and Sr/Ca in our experiments, lending support to differentcontrols on the uptake of these trace elements.

The control group consists of 9 individuals (200–300 μm indiameter) collected from the Gulf of Eilat on 25/04/2006. Calcificationtemperature, salinity and pH were assigned to this control group fromthe oceanographic data measured monthly by the Israel NationalMonitoring Program at the Gulf of Eilat (Table 2; Shaked and Genin,2006). Mg/Ca and Sr/Ca of the control group (calcified at 40.7 psu and22 °C) agree well with the results of the culturing experiment run at40.7 psu and 24 °C (i.e., BK1-41R).

G. ruber is a sensitive species to manipulations during culturingexperiments as documented previously (Hemleben et al., 1989). In ourexperiments with G. ruber from the Gulf of Eilat, specimens culturedat different salinities and temperatures (experimental setups 1 and 2

Table 2Mg/Ca and Sr/Ca in cultured G. ruber (white)

Sample Totalinitialmass

Totalfinalmass

Av. growthrate±1σ

Culturing fl

Salinity

(μg) (μg) (μg/day/ind) (psu)

Control Group from 25/04/2006 (n=9) 37.7 – – 40.7Experiment I (temperature kept constant; salinity varied)BK1-32R (n=2) 6.0 41 1.3±0.2 32.1BK1-35R (n=5) 12.0 106 2.2±0.3 35.0BK1-38R (n=5) 17.8 73 2.3±0.7 38.0BK1-41R (n=3) 7.9 55 2.3±0.4 40.7BK1-44R (n=2) 5.7 18 1.0±0.3 44.3

Experiment II (temperature varied; salinity kept constant)BK2-18R (n=3) 5.5 20 0.6±0.1 35.0BK2-21R (n=4) 10.7 40 1.1±0.4 35.0BK2-24R (n=3) 10.4 61 2.7±1.2 35.0BK2-27R (n=5) 14.8 118 2.9±0.8 35.0BK2-30R (n=6) 25.1 168 3.6±0.8 35.0

Experiment III (temperature, salinity and dissolved inorganic carbon kept constant; pH varied)BK3-7.9R (n=2) 5.3 29 1.9±0.2 35.0BK3-8.1R (n=3) 7.8 88 2.8±0.5 35.0BK3-8.3R (n=3) 7.0 76 2.8±1.1 35.0BK3-8.4R (n=2) 4.3 59 3.1±1.0 35.0

Total initial mass and total final mass are given for “n” number of specimens grouped for eacindividual during the duration of each culture and averaged over for “n” number of specimensgroup from oceanographic data measured at the Gulf of Eilat (Shaked and Genin, 2006). Mg/Cprior to the onset of the experiment (i.e., correction for initial mass; Section 2.4). 2σ errors(Section 2.3) and have been propagated through the correction for initial mass. The samplem⁎Carbonate system parameters were estimated by assuming that total alkalinity and total in40.7 psu in the northern part of the Gulf of Eilat), using the computer program written by L

in Table 2) reached a weight of ~20 μg per individual, except at lowtemperatures (18 and 21 °C) and extremely high salinity (44.3), wherethe growth of the individuals was impaired and the final shell masswas ≤10 μg per individual. Kummerform chambers were morecommon and the secondary apertures were very large at temperaturesof ≥27 °C. G. ruber cultured at different pH levels (experimental setup3) grew irregular chambers, with unusual patterns of arrangementthat do not follow the axis of coiling and with occasionally more thanone aperture. It appears that the tight biological control over growthwas impaired in this experimental set-up. This may partly be due tothe high temperature (27 °C) in this experiment or may be a responseto manipulations in the carbonate chemistry. Amorphous G. rubershells with irregular chamber growth were also observed in the grabsample from the surface sediments of the Gulf of Eilat, so appear not tobe only an artifact of culturing.

3.1. Mg/Ca ratios

Mg/Ca in cultured G. ruber (white) shows a positive correlation withtemperature, where Mg/Ca increases exponentially by 8±3%/°C(R2=0.97, pb0.01; Fig. 1a). Mg/Ca in G. ruber shows a secondarydependence on salinity, where Mg/Ca ratios increase exponentially by5±3%/psu (R2=0.96, pb0.02; Fig. 1b). The data point at 44 psu shows alowerMg/Ca ratio than expected from the trend line. Such a high salinityvalue is beyond the sea surface variability during theCenozoic (Hayet al.,2006) and has no implications for the glacial-interglacial record, exceptwhile investigating unique local conditions (e.g., the Red Sea; Hemlebenet al., 1996). Mg/Ca in G. ruber shows no change with pH in the ambientseawater range (8.1 to 8.3, NBS scale; Fig. 1c), but increases by ~80±10%(2σ) when pH decreases from 8.1 to 7.9, corresponding to a decrease incarbonate ion concentration from ~200 to 140 μmol/kg. When pH isvaried above the ambient seawater range from 8.3 to 8.4, correspondingto an increase in carbonate ion concentration from ~280 to ~380 μmol/kg, Mg/Ca values decrease by 35±11% (2σ).

uid Mg/Ca±2σ Sr/Ca±2σ

T pH±2σ Alkalinity±2σ [CO32−] ±2σ

(°C) (NBS) (μeq/kg) (μmol/kg) (mmol/mol) (mmol/mol)

22 8.3⁎ 2490⁎ 297⁎ 4.9±0.2 1.40 ±0.04

24 8.4⁎ 1964⁎ 228⁎ 3.6±0.3 1.26±0.0524 8.3⁎ 2141⁎ 251⁎ 3.8±0.3 1.37±0.0524 8.3⁎ 2325⁎ 276⁎ 4.7±0.3 1.41±0.0624 8.3⁎ 2490⁎ 297⁎ 5.5±0.3 1.40±0.0524 8.3⁎ 2710⁎ 327⁎ 5.1±0.3 na

18 8.4⁎ 2141⁎ 249⁎ 2.5±0.3 na21 8.4⁎ 2141⁎ 250⁎ 2.8±0.3 1.33±0.0624 8.3⁎ 2141⁎ 251⁎ 3.4±0.3 1.40 ±0.0527 8.3⁎ 2141⁎ 252⁎ 4.9±0.3 1.38±0.0530 8.3⁎ 2141⁎ 253⁎ 6.4±0.3 1.45±0.05

27 7.91±0.06 2040±5 140±24 7.5±0.3 1.43±0.0527 8.09±0.08 2133±14 197±21 4.2±0.2 1.34±0.0527 8.27±0.07 2259±7 276±28 4.2±0.2 1.39±0.0527 8.43±0.08 2423±4 384±25 3.1±0.2 1.37±0.05

h experiment. Average growth rates have been calculated from the increase in mass perin each experiment. Calcification temperature, salinity and pH are assigned to the controla and Sr/Ca ratios reported for each experiment have been corrected for the componenton Mg/Ca and Sr/Ca are estimated from repeat measurements of an in house standardaterial from BK1-44R and BK2-18R was adequate only for runningMg/Ca (but not Sr/Ca).organic carbon behaved conservatively (2490 μeq/l and 2060 μmol/kg, respectively, atewis and Wallace (1998).

Fig. 1. Variations in shell Mg/Ca and Sr/Ca in G. ruber (white) with temperature, salinity and pH. Temperature and salinity calibrations of Mg/Ca are statistically significant andrepresented by solid lines, whereas temperature and salinity calibrations of Sr/Ca are not statistically significant and represented by dashed lines. Error bars are in 2σ.

264 B. Kısakürek et al. / Earth and Planetary Science Letters 273 (2008) 260–269

The temperature calibration of G. ruber obtained in this study iscompared with previous calibrations from core-tops and sedimenttraps in Fig. 2. The temperature dependence of Mg/Ca ratios incultured G. ruber from the Gulf of Eilat is similar to sediment trapsamples from the Gulf of California (7%/°C; McConnell and Thunell,2005) and the North Atlantic (9%/°C; Anand et al., 2003), as well ascore top samples from the Atlantic and the Pacific (9%/°C; Dekens etal., 2002; Lea et al., 2000). The absolute values of Mg/Ca in cultured G.ruber from the Red Sea basin are in good agreementwith the sedimenttrap samples from the North Atlantic Ocean (Anand et al., 2003), butare offset from Atlantic core top and Pacific Ocean samples. Theobserved offsets between the Mg/Ca-temperature calibrations indifferent ocean basins were attributed to dissolution (Dekens et al.,

Fig. 2.Mg/Ca ratios in G. ruber (white) plotted against temperature. Results of this studyare given in diamonds, with the best fit givenwith the grey line (Mg/Ca=0.5e0.08T). Errorbars are in 2σ. The dashed lines from 1 to 5 give the previous calibrations for G. ruberw.from sediment traps and core-tops for the temperature range investigated; 1) sedimenttrap samples from the Sargasso Sea, North Atlantic Ocean (Mg/Ca=0.48e0.085T; 350–500 μm fraction size; Anand et al., 2003), 2) core top samples from the Atlantic Ocean(Mg/Ca=0.38e0.09(T −0.61D) where D denotes the depth of core in km which is set to 0;Dekens et al., 2002), 3) sediment trap samples from Gulf of California, Pacific Ocean(Mg/Ca=0.69e0.068T; McConnell and Thunell, 2005), 4) core top samples from the PacificOcean (Mg/Ca=0.38e0.09(T−0.61D −1.6) where D denotes the depth of core in km which isset to 0; Dekens et al., 2002), 5) core top samples from Equatorial Pacific (Mg/Ca=0.3e0.089T; Lea et al., 2000).

2002; Rosenthal and Lohmann, 2002); dissolution appears to shift thebulk chemistry towards that acquired in deeper water. The offsetbetween the existing calibrations for G. ruber were also linked to thedifferences in the salinity ranges of the sampling locations (Fergusonet al., 2008), where positive shifts in the Mg/Ca calibrations areassociated with higher salinities.

Temperature response of Mg/Ca in cultured G. ruberwas suggestedto show a slight dependence on size, where smaller size fraction hashigher temperature sensitivity than the bigger size fraction (10%/°C in250–350 μm fraction vs. 8.5%/°C in 350–500 μm fraction; Anand et al.,2003). Increasing size fractions of G. ruber (white) from a single coretop were associated with higher Mg/Ca ratios, attributed to variationsin calcification rate (Elderfield et al., 2002). However, a recent studyfound no significant variation of Mg/Ca with size fraction in G. ruber(white) from two different core top locations (Ni et al., 2007). Theauthors proposed that the size-related variations in Mg/Ca ofplanktonic foraminifera are not related to growth rate, but ratherrelated to a higher relative proportion of gametogenetic calcite insmall specimen in contrast to large specimen. Accordingly, G. ruber isnot expected to show a variation in Mg/Ca with shell size because itdoes not deposit any gametogenetic calcite. In any case, the finaldiameters of our cultures were relatively similar (N500 μm), except forcultures at 18 °C and 44 psu (with a diameter of 350 to 420 μm).Therefore, we can exclude a dependence of Mg/Ca on shell size in thisstudy.

Fig. 3 shows the salinity dependence of Mg/Ca in G. ruber inrelation to other cultured planktonic foraminifera species. Nürnberget al. (1996) used an electron microprobe to perform multiple spotanalysis of chamber MgO concentration in cultured Globigerinoidessacculifer. The salinity response as well as the absolute values of Mg/Cain cultured G. ruber (5±3%/psu) compare well with those reported incultured G. sacculifer (~7%/psu; Nürnberg et al., 1996), implying asimilar salinity effect for shallow dwelling species. In contrast,cultured Orbulina universa has higher absolute Mg/Ca values, but asimilar salinity response (4±3%/psu; Lea et al., 1999).

The pH dependence of Mg/Ca in G. ruber is compared to resultsfrom previous culturing studies in Fig. 4. Our observations support thefinding of Russell et al. (2004) that foraminiferal Mg/Ca changessignificantly (~16% and ~7% per 0.1 pH units in G. bulloides and O.universa, respectively) below the ambient pH of modern seawater. Theabsolute values ofMg/Ca in culturedG. ruber compare particularlywell

Fig. 4. (a) Carbonate ion concentration and (b) pH dependence of Mg/Ca in planktonicforaminifera from culturing studies. Grey diamonds are used for G. ruber (this study);triangles are assigned for O. universa (filled triangles for culturing experiments ofRussell et al., 2004; empty triangles for culturing experiments of Lea et al., 1999);squares indicate G. bulloides (filled squares for culturing experiments of Russell et al.,2004; empty squares for culturing experiments of Lea et al., 1999). G. ruberwas culturedat 27 °C, whereas all other species were cultured at 24 °C. All experiments wereconducted at oceanic salinity. pH is in NBS scale. Error bars are in 1σ. No error bars areavailable for G. bulloides data from Russell et al. (2004).

Fig. 3. Salinity dependence of Mg/Ca in planktonic foraminifera from culturing studies.Mg/Ca of G. ruber (cultured at 24 °C; shown by grey diamonds; this study) and ofO. universa (cultured at 22 °C; shown by empty triangles; Lea et al., 1999) represent bulkanalysis, whereas Mg/Ca of G. sacculifer (cultured at 26.5 °C; shown by filled squares;Nürnberg et al., 1996) represent in situ analysis of consequent chambers of onespecimen. Error bars are in 1σ for G. ruber and O. universa, but in 1SEM for G. sacculifer.

265B. Kısakürek et al. / Earth and Planetary Science Letters 273 (2008) 260–269

with those in cultured G. bulloides (Lea et al., 1999; Russell et al., 2004),even though the latter is a species without symbionts.

Since changes in salinity are correlated with changes in thecarbonate chemistry of seawater, it is important to assess how thecarbonate ion concentration varies with salinity. Although the setup ofthe salinity experiments was not designed to obtain information aboutthe carbonate system, carbonate system parameters can be estimatedby assuming that total alkalinity and total inorganic carbon behavedconservatively. This assumption is acceptable since, firstly, the doubledistilled water used for dilutions contained no alkalinity andnegligible amount of inorganic carbon and, secondly, the Erlenmeyerflasks were tightly sealed allowing no exchange with the atmosphereexcept for a few minutes each day when the animals were fed. Hence,we estimated [CO3

2−] in the culturing solutions (Table 2) from totalalkalinity and total inorganic carbon of seawater in the northern partof the Gulf of Eilat (2490 μeq/l and 2060 μmol/kg, respectively, at asalinity of 40.7; Silverman et al., 2007). These calculations show thatincreasing the salinity from ~32 to ~41 causes an increase in CO3

2−

concentration from ~230 to ~300 μmol/kg. Bearing in mind thefindings of the pH experiments, carbonate ion concentration isexpected to have no effect on Mg/Ca in G. ruber between salinities of32 and 41. On the other hand, at the extreme salinity of 44.3, theestimated CO3

2− concentration of ~330 μmol/kg may at least partlyexplain the low Mg/Ca ratio of G. ruber. The expected Mg/Ca ratio at44.3 psu is 6.4 mmol/mol, whereas the observed value is 5.1 mmol/mol (Fig. 1b). This 20% offset from the expected value is comparable tothe 35% decrease caused by increasing [CO3

2−] above the ambientseawater concentration (Fig. 4a).

3.2. Sr/Ca ratios

Sr/Ca in cultured G. ruber (white) increases with increasingtemperature; the calculated slope (Δ(Sr/Ca)/ΔT of 0.01 mmol/mol/°C) is the same as that for cultured G. bulloides (0.01 mmol/mol/°C; Lea et al., 1999). However, given the limited data set (n=4) andthe current external reproducibility (0.04mmol/mol; 2σ) compared tothe total variability in Sr/Ca (~0.1 mmol/mol), the temperature effecton Sr/Ca in cultured G. ruber is not resolvable with statisticalsignificance (R2=0.73, p=0.14). A previous study observed a similartemperature sensitivity of Sr/Ca, which was not statistically resolvableeither, in five species of planktonic foraminifera (non-globorotaliidspecies including G. ruber and G. bulloides) from core tops in the NorthAtlantic (Elderfield et al., 2000), whereas net catches from the sameregion showed no clear trend (Mortyn et al., 2005).

Sr/Ca in cultured G. ruber increases with increasing salinity; thecalculated slope (Δ(Sr/Ca)/ΔT of 0.02 mmol/mol/psu) is about twotimes higher than the one calculated for cultured O. universa(~0.008 mmol/mol/psu; Lea et al., 1999). The salinity effect on Sr/Cain cultured G. ruber is not resolvable with statistical significance(R2=0.81, p=0.10).

We observe no significant response of Sr/Ca in G. ruber to changesin the pH. This is similar to cultured G. bulloides that appears to haveno significant pH (or carbonate ion) dependence (Lea et al., 1999;Russell et al., 2004). However, Sr/Ca in cultured O. universa has apositive correlation with carbonate ion concentration and differs inbehavior (Lea et al., 1999; Russell et al., 2004).

Sr/Ca shows a significant positive correlationwith average growth rate(R2=0.72,pb0.01; Fig. 5). The results of pHexperiments are excluded fromthe computation of this regression since the growth of individuals in thisset of experiments appears tohave additional controls as discussed earlier.

4. Discussion

4.1. Controls on foraminiferal Mg/Ca

Mg/Ca in cultured G. ruber (white) is dependent on temperature(8±3%/°C) and salinity (5±3%/psu). In addition, pH also controlsshell Mg/Ca below and above ambient seawater values (pHb8.1;pHN8.3). Local variations of about 0.2 pH units (with absolute

Fig. 5. Growth rate dependence of Sr/Ca in salinity and temperature experiments(Experiments I and II in Table 2). Growth rates are calculated from the total weightincrease of an individual over the experimental duration and averaged over the numberof individuals grouped together in each experiment. Error bars are in 1σ for growthrates and in 2σ for Sr/Ca ratios.

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values of ~8.1 to ~8.3 in NBS scale) occur in the present day ocean(Pelejero et al., 2005) due to factors like temperature, upwellingand surface productivity. On a glacial-interglacial timescale, glacialseawater pH values are established to be consistently higher by~0.2 U (Hönisch and Hemming, 2005; Palmer and Pearson, 2003;Sanyal et al., 1995; Yu et al., 2007) due to lower atmospheric CO2

concentrations (Petit et al., 1999). Since the pH of the surface oceanincreased by only ~0.2 U during glacial periods, Mg/Ca basedpaleotemperatures should not be biased significantly by variationsin pH. However, local heterogeneities in pH are expected in theglacial ocean as in the present day ocean. Our calculations suggestthat if the pH of the glacial surface ocean reached 8.4 (NBS scale),glacial SST based on Mg/Ca in G. ruber would be underestimated by3.5±1.5 °C. Such a pH effect on Mg/Ca derived temperatures isimprobable since this would completely compensate for theglacial/interglacial variation in SST (~2.5 to 3.5 °C based on G.ruber w. records; Lea et al., 2000; Rosenthal and Lohmann, 2002;Rosenthal et al., 2003; Steinke et al., 2006; Weldeab et al., 2006).

Assuming that the pH of the surface ocean has not been below 8.0or above about 8.3 U during at least the last four glacial cycles asimplied by the record of atmospheric concentration of CO2 (Petit et al.,1999), we conclude that themain glacial interglacial controls onMg/Caratios in G. ruber are expected to be temperature and salinity of thesurface ocean. In fact, the salinity effect on foraminiferal Mg/Ca haslong been neglected, but can evidently alter the temperaturecalibrations. In order to account for simultaneous variations in tem-perature and salinity, we performed multiple regression analysis(Eq. 1) on Mg/Ca data from cultured G. ruber (excluding the pH experi-ments and the data point at 44 psu). Note that the control group isincluded in the regression:

Mg=Caðmmol=molÞ ¼ exp½0:06ð�0:02Þ�SðpsuÞ þ 0:08ð�0:02Þ�Tð0CÞ−2:8ð�1:0Þ�ðn ¼ 10;R2 ¼ 0:95;p ¼ 0:05Þ

G. ruber grown at low temperatures (18–21 °C) and extreme salinities(32 and 44) had low growth rates (b1.5 μg/day/ind; Table 2) and mayhave been stressed. Excluding these samples from the multipleregression results in Eq. 2 that is identical to Eq. 1 within statisticalerror (calculated for the 95% confidence interval):

Mg=Ca mmol=molð Þ ¼ exp½0:08 F0:03ð Þ�S psuð Þ þ 0:09 F0:03ð Þ�T 0Cð Þ−3:6 �1:6ð Þ� n ¼ 7;R2 ¼ 0:96; p ¼ 0:05

� �

In a recent study on planktonic foraminifera from 11 core tops fromthe Mediterranean, Ferguson et al. (2008) observed unusually high

(1)

(2)

foraminiferal Mg/Ca compared to that expected from previoustemperature calibrations. The authors proposed that these highforaminiferal Mg/Ca ratios are predominantly controlled by salinity(with a range of ∼36.5 to 39). The slope of Mg/Ca dependence onsalinity in G. ruber (not including a correction for changes intemperature) was found to be 16±15%/psu for N250 μm size fractionand 29±13%/psu for N150 μm size fraction, compared to a salinitysensitivity of ~6±2%/psu found in this study. As a matter of fact, thesalinity dependence of Mg/Ca ratios in N250 μm size fraction fromcore-tops (Ferguson et al., 2008) is within error of that in our culturedspecimen with a similar size (final diameter of N300 μm). Never-theless, the observed inconsistency in the salinity sensitivity of Mg/Cain G. ruber from core-tops versus laboratory cultures requiresclarification. One obvious explanation could be the precipitation ofinorganic calcite (with Mg/Ca ratios of ~50 mmol/mol) within bottomsediments or in the water column (Ellis and Milliman, 1985 andreferences therein), causing shell Mg/Ca ratios to increase. In hyper-saline basins like the Mediterranean, relatively high temperatures andsalinities are expected to produce waters supersaturated with respectto calcium carbonate and, hence, promote precipitation. Indeed,Ferguson et al. (2008) observed a high-Mg calcite encrusting onsamples from one site in the Eastern Mediterranean by ScanningElectron Microscope (SEM). However, based on SEM observations ofsamples from two other sites that do not display such an apparentencrusting as well as on sequential dissolution experiments, theauthors concluded that the Mg/Ca they observed in all other sitescannot be explained via contamination by high-Mg-calciteovergrowth.

The mean ocean salinity today is 34.7 (Montgomery, 1958).Estimates of the increase in sea surface salinities (SSS) betweentoday and the last glacial maximum (LGM) based on modeling resultsas well as on morphology of coccoliths have revealed values between~1 to 2 (Bollmann and Herrle, 2007; Fairbanks, 1989; Schäfer-Nethand Paul, 2003). Contrary to the deep ocean, SSS are influenced byfactors such as continental fluxes, precipitation patterns, etc. andtherefore show a large variability in the present day ocean (N8 psu;World Ocean Atlas 2005; Antonov et al., 2006) as well as in the glacialocean (N8 psu as modelled; Schäfer-Neth and Paul, 2003). Thus, SSSfor a given location may vary between glacial and interglacial periodsnot only due to the eustatic sea level change, but also due to changesin environmental conditions. Multiple regression analysis on Mg/Cadata from cultured G. ruber (Eq. 1) indicates that 1 unit increase in seasurface salinity causes theMg/Ca based sea surface temperatures to beover-estimated by ~0.7 °C.

In basins like the Caribbean,where cooler SST during glacial periodswere coupledwith increased SSS due to hydrological changes (Schmidtet al., 2004), the glacial-interglacial salinity oscillationswork to reducethe amplitude of Mg/Ca derived temperatures. Caribbean SST duringLGM were calculated to be 2.1 to 2.6 °C colder than the present usingMg/Ca ratios in G. ruber (white) from ODP cores 806B (Lea et al., 2000)and 999A (Schmidt et al., 2006). If the Caribbean salinitywas ~2 higherduring the LGM (Schmidt et al., 2004), thiswould lower theMg/Ca-SSTduring LGM further by ~1.5 °C. To calculate the absolute sea surfacesalinity and temperature changes, Mg/Ca and δ18O of foraminiferalcalcite should be used in combination, solving for 2 unknowns from 2sets of equations. This remains to be accomplished in future studies.

A recent study by Groeneveld et al. (2008) constructed a coupledMg/Ca and δ18O record on Globigerinoides sacculifer from ODP Site1000 in the Caribbean, covering the time interval for the closure of thePanamanian Gateway (4.5 to 3.9 million years ago). The authors madea leading approach to correct the Mg/Ca-SST for the large salinityfluctuations due to hydrological changes using the salinity depen-dence of Mg/Ca in G. sacculifer (~7%/psu) as determined by Nürnberget al. (1996). Their results emphasize the importance of employing asalinity correction, which gave up to 3.5 °C lowerMg/Ca-SST. However,the authors do not discuss a possible pH effect on shell Mg/Ca.

267B. Kısakürek et al. / Earth and Planetary Science Letters 273 (2008) 260–269

. Controls on foraminiferal Sr/Ca

The main control on shell Sr/Ca in G. ruber (white) appears to bethe average growth rate (0.06 mmol/mol/(µmol/day/individual)),whereas the temperature and salinity dependences of Sr/Ca are notresolvable with the current reproducibility. The observed growth ratedependence of Sr/Ca is in agreement with the direct rate dependenceof Sr/Ca observed in both inorganically precipitated calcite and inbiogenic calcite from coccolithophorids (Lorens, 1981; Stoll andSchrag, 2000). Moreover, Sr/Ca in G. ruber was found to decreasewith increasing size (Elderfield et al., 2002), where changes in shellsize were attributed to reflect changes in growth rate with slowergrowth rates in the later stages of development. The experimentalobservations of Erez (2003) revealed that the partition coefficient of Sr(DSr) in cultured G. sacculifer increases twofold when growth rateincreases from ~15%/day to ~25%/day, whereas DSr shows a negativecorrelation with growth rate in both planktonic and benthicforaminifera at growth rates of less than ~10%/day. The growth ratescalculated for G. ruber in this study lie between 15 and 27%/day, butthe corresponding range in DSr is only from 0.14 to 0.16.

It is difficult to distinguish the effects of temperature, salinity andgrowth rate on shell Sr/Ca given that temperature and salinity exertcontrol on growth rate as well (Fig. 6). Our data indicate that the maincontrol on shell Sr/Ca is growth rate and that temperature and salinitymay have an indirect effect on shell Sr/Ca through their control overgrowth rates. Indeed, results from inorganic experiments indicate thatthere is a positive linear correlation between calcite precipitation rateand ionic strength of the solution (Zhang and Dawe, 1998; Zuddas andMucci, 1998). However, our results indicate that growth rates in G.ruber are lowest at extreme salinities (i.e., 32 and 44) and that thecorrelation between growth rate and salinity follows an optimumcurve. On the other hand, there is a positive correlation betweengrowth rate and temperature, with lower growth rates at lowertemperatures. Hence, G. ruber appears to be stressed at extremesalinities and low temperatures, impairing shell growth and reducingSr incorporation into foraminiferal calcite. These extreme salinity andtemperature conditions that led to low growth rates in our culturesare outside the natural variability found in field studies. Nevertheless,other factors might restrict growth of foraminifera in their naturalhabitats (e.g., species competition, food availability). Thus, the effect ofgrowth rate on foraminiferal Sr/Ca needs to be confirmed by fieldstudies.

It is important to note that shell precipitation in foraminifera is avariable incremental function. For instance, the formation of a new

4.2. Controls on foraminiferal Sr/Ca

Fig. 6. Average growth rate of G. ruber (white) versus salinity, temperature and pH. Errorbars are in 1σ.

chamber in G. ruber was observed to take place within about 90 min,while the thickening of the walls continued for another 2 h (Bé et al.,1977). Therefore growth rates used in this study (μg/day/ind) aredistinctively different from precipitation rates (usually reported inμmol/m2/h), which are difficult to determine in foraminifera due touncertainties associated with calcification time and surface area. Thus,estimates of precipitation rates in planktonic foraminifera areextremely variable and range from ~40 μmol/m2/h (Erez, 2003) to ashigh as 1000–4000 μmol/m2/h (Carpenter and Lohmann, 1992; Lea etal., 1995). Absolute precipitation rates in planktonic foraminifera needto be better constrained.

Sr/Ca records of foraminifera show variations within Quaternaryglacial-interglacial cycles, which have partly been attributed to pastchanges of the marine seawater ratio (Sr/Ca)SW (Martin et al., 1999;Stoll et al., 1999). A potential cause of glacial-interglacial (Sr/Ca)SWvariation has been proposed to be chemical weathering and recyclingof shelf carbonates at low sea levels (Schlanger, 1988). Increased shelfcarbonate deposition during interglacials and subsequent preferentialweathering of Sr-rich aragonite during low sea level stands has beenmodelled to produce a 1 to 3% change in (Sr/Ca)SW on glacial/interglacial timescales (Stoll and Schrag, 1998). However, there isconsiderable dispute as to what extent foraminiferal Sr/Ca can indeedbe ascribed to (Sr/Ca)SW variation. Records of diverse foraminiferaspecies from various oceanic settings reveal systematic Sr/Ca varia-tions of 3 to 5%, with generally higher Sr/Ca recorded during glacialintervals (Martin et al., 1999; Stoll et al., 1999). However, theamplitude of this foraminiferal Sr/Ca variation exceeds modelpredictions of glacial-interglacial (Sr/Ca)SW changes and requiresunrealistic changes in riverine Sr fluxes, which would imply pastchanges in seawater 87Sr/86Sr that disagree with the oceanic record(Stoll et al., 1999). A study on time series records of four species offoraminifera from core BOFS 31K in the north Atlantic has shownincoherent Sr/Ca trends between species, implying that factorsadditional to (Sr/Ca)SW changes must be involved (Elderfield et al.,2000). Part of the past variability in shell Sr/Ca might be linked tochanges in growth rates of foraminifera as a response to changingenvironmental conditions. The idea of faster growth rates inplanktonic foraminifera during optimal environmental conditionshas previously been proposed and linked to shell sizes (Schmidt et al.,2003). An earlier study on planktonic foraminifera shells in two coresfrom the Southern Red Sea infers strong oscillations in bothMg/Ca andSr/Ca dependent on salinity, with higher ratios at the LGM (Yusuf,1980). Our calculations suggest that an increase of 3–5% in shell Sr/Caas observed during glacial intervals can be explained by anapproximated doubling of the growth rates in planktonic foraminifera.However, the relative influences of growth rate variations and changesin the glacial/interglacial Sr weathering flux on foraminiferal Sr/Cahave to be examined in more detail.

. Conclusions

Mg/Ca in cultured Globigerinoides ruber (white) shows a depen-dence on pH, temperature and salinity. However, Mg/Ca in G. rubershows no dependence on pH at ambient seawater range (8.1 to 8.3;NBS scale). The main glacial interglacial controls on Mg/Ca ratios in G.ruber are expected to be temperature and salinity of the surface oceanas determined by a newly proposed multiple regression equation thatreveals a temperature dependence with an exponential slope of 8±2%/°C and a salinity dependence with an exponential slope of 6±2%/psu. This double dependence may increase the amplitude of glacial–interglacial temperature estimates based onMg/Ca in G. ruber. Sr/Ca incultured G. ruber shows a dependence on the average growth rate. Itappears that the shell Sr/Ca in G. ruber (white) is mainly controlled bygrowth rates and that temperature and salinity have an indirect effecton shell Sr/Ca through their biological control over growth rates. Partof the glacial/interglacial variations observed in foraminiferal Sr/Ca

5. Conclusions

268 B. Kısakürek et al. / Earth and Planetary Science Letters 273 (2008) 260–269

may be linked to changes in growth rates of foraminifera as a responseto changing environmental conditions.

Acknowledgements

This work was funded by the German Science Foundation (DFGEi272/21-1), the European Science Foundation (ESF) CollaborativeResearch Project CASIOPEIA (04 ECLIM FP08) and the Israel ScienceFoundation (Grant # 870/05). We would like to thank threeanonymous reviewers for improving the manuscript significantlyand Jeroen Groeneveld for helpful comments on an earlier version ofthe manuscript as well as for optical emission spectrometric analysis.The field work was carried out at the IUI-Eilat, with the assistance ofMoty Ohavia, Oded Ben Shaprut and Tanya Rivlin in collection ofplanktonic foraminifera and the culturing experiments. Wewould liketo thank Reinhard Kozdon for assistance in picking, Ulrike Wester-nströer and Ed Hathorne for mass spectrometric analysis.

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