Mg/Ca variation in planktonic foraminifera tests: implications...

Mg/Ca variation in planktonic foraminifera tests:implications for reconstructing palaeo-seawater temperature

and habitat migration

Stephen Eggins a;�, Patrick De Deckker b, John Marshall a

a Research School of Earth Sciences, The Australian National University, Canberra, ACT 0200, Australiab Department of Geology, The Australian National University, Canberra, ACT 0200, Australia

Received 5 December 2002; received in revised form 14 May 2003; accepted 15 May 2003

Abstract

The nature of compositional variability within the tiny calcitic shells (tests) that are precipitated by planktonicforaminifera has been investigated using laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS).Systematic large and correlated variation of Mg/Ca, Mn/Ca, Ba/Ca and Zn/Ca but relatively uniform Sr/Ca areobserved through the test walls of analysed species (Globigerinoides sacculifer, Globigerinoides ruber, Neogloboquadrinapachyderma and Neogloboquadrina dutertrei). Distinct chamber and chamber-wall layer compositions can be resolvedwithin individual tests, and Mg/Ca compositional differences observed in sequentially precipitated test components ofthe different species analysed are consistent with seawater temperature changes occurring with habitat migrationduring their adult life-cycle stages. Estimated test calcification temperatures are in keeping with available seawatertemperature constraints, indicating the potential for accurate seawater temperature reconstruction using LA-ICP-MS.Mg-rich (6 1^6 mol% Mg) surface veneers that are also enriched in Mn, Ba, and Zn have been found on all speciesand all fossil tests, as well as on live-sampled tests of G. ruber, with the latter suggesting a possible biogenic origin.These Mg-rich surfaces bias bulk test compositions toward higher Mg/Ca values by between 5 and 35%.7 2003 Elsevier Science B.V. All rights reserved.

Keywords: Mg/Ca seawater thermometry; trace elements; laser ablation ICP-MS; planktonic foraminifera; palaeoceanography

1. Introduction

The incorporation of Mg into the tiny calciticshells (tests) that are secreted by planktonic fora-minifera is extraordinarily sensitive to calci¢ca-

tion temperature and is the basis of a new andrapidly emerging tool for reconstructing palaeo-seawater temperature. Large exponential increasesin shell Mg/Ca ratio, of the order of 10; 1% per‡C, have been documented under both controlledlaboratory conditions and in modern shell materi-al recovered from sea£oor sediments [1^4]. Theserelationships underpin a range of seawater ther-mometer calibrations that may be applied to asmall but expanding number of planktonic fora-minifera species [1^7]. Given the widespread dis-

0012-821X / 03 / $ ^ see front matter 7 2003 Elsevier Science B.V. All rights reserved.doi:10.1016/S0012-821X(03)00283-8

* Corresponding author.E-mail address: [email protected] (S. Eggins).

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Earth and Planetary Science Letters 212 (2003) 291^306

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tribution and abundance of fossil foraminiferatests in deep-sea sediments, these thermometersare proving invaluable for reconstructing longand detailed records of temperature change inthe oceans [4^7]. This complements the use ofseveral other trace elements and stable isotopesin foraminiferal calcite, most notably N

18O butalso N

13C, Cd, Ba, Zn and Sr, which are estab-lished proxies for past seawater temperature, com-position, nutrient levels, and productivity [8,9].Moreover, by combining Mg/Ca thermometrywith N

18O measurements on the same shell mate-rial, palaeo-seawater N

18O can be isolated fromthe temperature-dependent fractionation of N

18Othat occurs during shell precipitation [7,10,11],and palaeo-salinity (and seawater density) canbe estimated from relationships between seawaterN18O, temperature and salinity [12]. The con-

straint of seawater temperature and salinityfrom the Mg/Ca and N

18O compositions of fora-miniferal calcite presents the possibility of recon-structing past changes in glacial ice volume, localprecipitation/evaporation, and water mass den-sity. Establishing spatial and temporal changesin these variables is fundamental to evaluatinglinked palaeocean and palaeo-climate events,and forecasting the nature and rate of future cli-mate change [13,14].

In this study we investigate the distribution ofMg/Ca and several other trace elements within thetests of a small number of planktonic species thatare commonly employed for palaeocean recon-struction. This has been driven by the need tounderstand those factors that in£uence the incor-poration of Mg into foraminiferal calcite, the sig-ni¢cance of bulk test Mg/Ca compositions, andthe reliability and accuracy of Mg/Ca thermome-try as currently applied to di¡erent planktonic fo-raminifera species. The feasibility of applying la-ser ablation inductively coupled plasma massspectrometry (LA-ICP-MS) to analyse Mg/Caand other trace elements in planktonic foraminif-era is also demonstrated.

2. Background

Mg/Ca in the tests of many planktonic species

has been shown to vary as an exponential func-tion of calci¢cation temperature (i.e. Mg/Ca=AexpBT ) [1,2,4]. The exponential temperaturedependence (B) appears to be similar for allplanktonic species and is within the range0.10; 0.01. However, calibrations for di¡erentspecies are often characterised by signi¢cantly dif-ferent values for the pre-exponential constant (A).Moreover, where more than one Mg/Ca ther-mometer calibration has been determined for thesame species (e.g. Globigerinoides sacculifer orGlobigerinoides ruber), signi¢cant disagreement isoften found in derived seawater temperature esti-mates that cannot be accounted for by typicallyquoted calibration uncertainties (i.e. ; 0.5^1.5‡C[7,15,16]). It has become apparent that di¡erencesbetween these same species calibrations re£ect, inpart, the variable preservation of deep-sea corematerial due to the lowering of bulk test Mg/Cacompositions by sea£oor dissolution [15,16,17].This process preferentially dissolves and removesmore Mg-rich test compositions with decreasingcarbonate ion activity and increasing depth inthe oceans [17]. A method of correcting for thesechanges in bulk test Mg/Ca composition, basedon the reduced weight of dissolution-a¡ectedtests, has been proposed recently for G. ruberand G. sacculifer [18]. It should also be notedthat some calibrations are referenced to sea-sur-face temperature (SST) and others to calci¢cationtemperature, which can di¡er signi¢cantly for spe-cies other than those that calcify near the surface(e.g. G. ruber).

Mg/Ca thermometry is conventionally appliedby analysis of between ¢ve and 50 whole fossiltests of the same species. Mg/Ca ratios can bemeasured using this approach to better than 1%reproducibility with modern instrumental tech-niques [19,20], which suggests the possibility ofconstraining palaeo-seawater temperatures towithin a few tenths of a ‡C. However, in practice,achieving this degree of accuracy and precision iscompromised by: (1) compositional variationwithin a population of tests due to the calci¢ca-tion of individual foraminifera at varying temper-atures in di¡erent seasons and years [21], (2) un-certainties associated with the deconvolution ofsea£oor dissolution e¡ects [18], and (3) the con-


S. Eggins et al. / Earth and Planetary Science Letters 212 (2003) 291^306292

sistency with which tests can be cleaned of con-tamination by diagenetic and detrital phases [22^25].

Because foraminifera grow their tests by se-quentially adding chambers and new layers to ex-isting chambers, individual tests may comprise arange of diverse compositions that re£ect chang-ing habitat and seawater conditions during an in-dividual foraminifer’s lifetime [26]. Indeed, manyspecies migrate through the water column, ini-tially as juveniles into warmer surface watersand with maturity into deeper colder water toreproduce [26]. Most planktonic species also adda ¢nal, often thick, outer calcite crust (or ‘game-togenic crust’) in deeper colder water immediatelyprior to reproduction and ensuing death [26,27].Electron-probe microanalysis studies have con-¢rmed the presence of relatively Mg-poor, outer-wall layers in the tests of Globorotalia truncatuli-noides [28], Globorotalia tumida [17], and Globige-rina bulloides [7], consistent with the growth of¢nal outer calcite crusts on these species inmuch colder water. Signi¢cant Mg concentrationvariation, albeit spatially incoherent, has been re-ported in N. pachyderma [29]. Systematic Mg-en-richment has been documented toward test exte-rior surfaces across the ¢nal outer crusts that havebeen precipitated by G. sacculifer in laboratory-culture experiments [1]. Reduction in bulk testMg/Ca composition with partial sea£oor dissolu-tion indicate G. sacculifer grow more Mg-de-pleted, ¢nal outer-crust compositions in deepercolder water [11] ; however, no signi¢cant Mg var-iability was found in an electronprobe study offossil G. sacculifer tests [17]. Changes in bulktest compositions with progressive sea£oor disso-lution also provide qualitative evidence for theexistence of signi¢cant compositional heterogene-ity between and/or within tests in species that in-clude G. ruber, N. dutertrei, and G. tumida [15,17,18]. Collectively, these results point to the oc-currence of signi¢cant compositional heterogene-ity within the tests of many planktonic foraminif-era species, and indicate the interpretation of bulktest Mg/Ca compositions may not be straightfor-ward. Furthermore, the conventional bulk analy-sis approach to foraminiferal seawater thermom-etry potentially averages signi¢cant compositional

heterogeneity and, in so doing, may destroy avaluable record of seawater temperature variationin time and space.

3. Experimental method

We have employed a high-resolution LA-ICP-MS depth-pro¢ling technique to investigate thenature and extent of compositional variationwithin the tests of a number of planktonic fora-minifera species that are commonly used for pa-laeocean reconstruction, including N. dutertrei,N. pachyderma, G. ruber and G. sacculifer. Fossiltests of each species were obtained from a smallnumber of deep-sea cores (see Table 1 for coreand sample details) and analysed after cleaningby repeated rinsing and ultrasonication in ultra-pure water (s 18 M6) and AR-grade methanolto remove adhering detrital material (the lattercon¢rmed by subsequent inspection of tests usingscanning electron microscopy, SEM). ModernG. ruber tests, sampled by plankton tow, werealso analysed following treatment in AR-gradeH2O2 to remove organic material and applyingthe same cleaning procedures used for fossil tests.

Highly controlled and precise test sampling isachieved using a pulsed ArF Excimer laser(V=193 nm) ¢tted with simple image-projectionoptics [30]. It should be noted that poor absorp-tion and catastrophic ablation of calcite occurwith use of signi¢cantly longer-wavelength laserlight [31]. In this regard, the capabilities of ourlaser sampling system are demonstrated by thegeneration of £at-bottomed pits in gem-qualitycalcite after application of 10 and 100 laser pulses(Fig. 1A,B). Each laser pulse shaves a uniform,V0.1 Wm thick, layer from the calcite sample sur-face and the application of multiple laser pulsesproceeds with preservation of original subtle sur-face features down to a depth of about 5Wm (Fig.1A,B). Approximately 50% higher ablation ratesare observed under the same conditions in fora-miniferal calcite, based on ablation experimentsconducted on the smooth-walled planktonic spe-cies Pulleniatina obliquiloculata (Fig. 1C,D). How-ever, due to reduced laser £uence and increasedre£ection at inclined surfaces, uniform ablation


S. Eggins et al. / Earth and Planetary Science Letters 212 (2003) 291^306 293

does not occur across the target site in planktonicspecies with outward-opening pore structures (e.g.G. sacculifer ; see Fig. 2). SEM images reveal thatlaser sampling proceeds through the test wall inthese species by preferentially sampling outerlayers from the tops of interpore ridges and spinebases, before developing more £at-bottomed pitsand removing inner layers from deeper within testwalls (Fig. 2).

Multiple trace elements are simultaneously pro-¢led during laser sampling through individualchamber walls by repeated, rapid sequentialpeak hopping (dwell time= 30 ms) between se-lected isotopes (24Mg, 25Mg, 43Ca, 44Ca, 55Mn,68Zn, 88Sr, 138Ba) using a quadrupole ICP-MS(Agilent 7500s). The ICP-MS is optimised for sen-sitivity across the analyte mass range subject tomaintaining ThOþ/Thþ 6 0.5%. Data reductionfollows established protocols for time-resolvedanalysis [32]. This involves initial screening ofspectra for outliers, followed by subtraction of

mean background intensities (measured with thelaser o¡) from analyte isotope intensities. Quanti-¢cation is performed by external calibration usingNIST610 and NIST612 glass standard referencematerials and correction for yield variation byratioing to an internal standard isotope (43Ca)measured during each mass spectrometer cycle(V0.25 s). Internal standardisation using 43Caavoids detector non-linearity e¡ects that can beencountered with higher-intensity 44Ca signals inthe analogue detection mode. Measured 44Ca/43Ca ratios on the NIST glasses and foraminiferalcalcite are found to be equivalent within analyti-cal uncertainty, indicating that interference of27Al16O on 43Ca and 12C16O2 on 44Ca duringNIST glass and calcite analysis, respectively, con-tribute biases of less than 0.5%.

Optimum spatial resolution is achieved byablating small-diameter (30 or 40 Wm) spots at 2or 3 laser pulses per second using a moderatelylow laser £uence (5 J/cm2), and by minimising

Fig. 1. SEM images of laser ablation pits formed in (A,B) gem-quality Iceland spar using 10 and 100 laser pulses, and (C) a fos-sil P. obliquiloculata test by 10, 20, 50, 100 and 500 laser pulses using a laser £uence of 5 J/cm2. (D) Detail of the 50 pulse pitshown in panel C, which is approximately 7.5 Wm deep. (E) A fossil N. dutertrei test, in which 14 separate composition pro¢leshave been analysed by LA-ICP-MS and up to four replicates on each chamber. Inset E(1) shows detail of the reticulate surfacetexture present on the ¢nal chamber. Inset E(2) shows detail of 30 Wm diameter pits in chamber f-4 and the surrounding blockycalcite textured test surface. Labels f, f-1, f-2, etc. indicate the chamber calci¢cation order, counting back from the ¢nal chamber(f). Note scale bars.



Fig. 2. SEM images and a schematic cross-section illustrating the e¡ects of test surface topography on laser ablation pit develop-ment in G. sacculifer (an adult test with multiple ablation pits is shown at the upper right for reference). SEM images A and Bshow details of 30Wm diameter pits formed by 20 and 40 laser pulses, respectively, and images C and D show the formation ofdeeper and £atter-bottomed pits by the application of 100 and 200 laser pulses. Note scale bars and the dashed white line in im-age C, which outlines the ablation pit periphery. These SEM images demonstrate the preferential ablation of material from surfa-ces that lie orthogonal to the incident laser beam, which results in greater ablation from the tops of interpore ridges and spinebases, and the development of increasingly £atter-bottomed pits as ablation progresses into the test wall. A schematic cross-sec-tion through interpore ridges that form G. sacculifer test walls illustrates the construction (right to left) of chamber walls by theaddition of ontogenetic calcite layers to form the inner wall (dark grey with solid dark lines) and capping of ridges and spinebases by the ¢nal, outer (gametogenic) calcite crust (adapted from ¢gure 6 in [27]). Dashed lines indicate the recession of the testsurface with increasing numbers of laser pulses (values associated with adjacent dashed lines). Note scale bars on both the SEMimages and the schematic cross-section.



mean particulate residence times (t1=2V0.35 s) inthe ablation cell volume following each laserpulse. These short residence times are facilitatedby a two-volume ablation cell design that incor-porates a small ablation volume (V2 cm3), whichis e¡ectively isolated from a much larger(10U10U3 cm) volume containing samples andstandards. This unique design also avoids cross-contamination between samples and standards byablation products that can be widely dispersedbeyond the immediate ablation environment insimpler, single-volume ablation cell designs.Each analysis consumes only 10^20 ng of test

material, or about 0.1% of the total test mass,and typically requires between 20 and 60 s, de-pending on test wall thickness. Multiple pro¢lescan be obtained from individual chambers of asingle test (Fig. 1E) and several hundred cham-ber-wall pro¢les can be acquired in a day.

4. Results

Compositional pro¢les that illustrate the rangeof chemical variation found through the test wallsof the analysed foraminifera species are shown in

Fig. 3. Trace element compositional pro¢les through the test walls of fossil specimens of (A) G. sacculifer, (B) G. ruber,(C) N. dutertrei (same specimen as shown in Fig. 1), and (D) a modern G. ruber test that was sampled by plankton tow. Mea-sured metal/Ca molar ratios are plotted on a log scale, and the pro¢le depth is calculated from the number of laser pulses ap-plied, assuming an ablation rate of 0.15 Wm per pulse based on measured rates of ablation of P. obliquiloculata tests (see Fig.1C,D). Note the narrow zone of Mg^Mn^Zn^Ba enrichment that occurs at the external surface (0 Wm in all pro¢les) of eachchamber and the development of distinct inner- and outer-wall layers in G. sacculifer and N. dutertrei pro¢les. Test sample num-bers follow the species name.



Fig. 4. Compositional pro¢les showing the variation of Mg/Ca molar ratios through each analysed chamber wall of individualtests of (A,B) N. dutertrei, (C) N. pachyderma, (D,E) G. ruber, and (F^H), G. sacculifer (note the vertical log scale, and pro¢ledepth has been calculated as in Fig. 3). Observe that the di¡erent species display characteristic pro¢le forms and compositions,and in the case of N. dutertrei, systematic variation of pro¢le forms and thickness with chamber calci¢cation order. Further notethe thin Mg-rich external surfaces present at the beginning of all wall pro¢les, and the development of low-Mg outer-wall (crust)layers in some G. sacculifer tests. Labels f, f-1, f-2, etc. indicate the chamber calci¢cation order, counting back from the ¢nalchamber (f). The reproducibility of pro¢les is indicated by replicate pro¢le analyses (denoted a and b) made on the same cham-ber (see panels D, F and G). Test sample numbers follow the species name.



Fig. 3. Measured trace element concentrations areconsistent with abundance ranges reported previ-ously for planktonic foraminifera [8]. Mg, Mn,Zn, and Ba are notable for their systematic, largeand correlated variation through test walls,whereas Sr shows unrelated, comparatively uni-form distributions. To help clarify the subsequentdiscussion of these composition pro¢les, we usethe term ‘surface veneer’ to refer to the thinMg^Mn^Ba^Zn enrichments that occur at the be-ginning of each compositional pro¢le and coin-cide with the test outer surface. The terms ‘outerwall’ and ‘inner wall’ are used to distinguish be-tween distinct layer compositions, where devel-oped, within test walls.

Thin (typically 6 1^3 Wm) Mg-, Mn-, Zn- andBa-rich surface veneers are observed on all cham-bers and all tests of each species analysed. Com-parable trace element-rich surface veneers are alsopresent on G. ruber tests sampled by plankton tow(Fig. 3D). Close examination of the pro¢les inFig. 3C,D reveals variation in the width andform of the surface enrichment for di¡erent ele-ments. For example, the zone of anomalous Mn,Ba and Zn enrichment in the N. dutertrei testpro¢le shown in Fig. 3C is only 1^2 Wm thick,whereas Mg increases toward the test surface in

this pro¢le over a distance of almost 10 Wm (seepro¢le f-2 in Fig. 4A for greater detail).

Compositionally distinct inner-wall and outer-wall layers, of varying relative thickness, are ob-served in several species, particularly N. dutertreiand often also N. pachyderma and G. sacculifer(Figs. 3 and 4). Where present, inner-wall layersare usually enriched in Mg and other trace ele-ments (except Sr) but these enrichments do notoccur to the same extent, nor do they match indetail the characteristics of the surface veneers.The relative thickness of the inner- and outer-wall layers di¡ers between species, and in thecase of N. dutertrei tests also varies signi¢cantlybetween chambers (see Figs. 3C and 4A,B). Thelatter compares to G. sacculifer tests where lowMg outer-wall layers, although not always evident(Figs. 3A and 4F^H), tend to be of similar thick-ness and to comprise a relatively small proportion(25^50%) of the total wall thickness in mostchambers. The often complex multi-layered wallpro¢les of these two species contrast with the rel-atively simple pro¢les of G. ruber, which are char-acterised by strong asymmetry due to the presenceof surface veneers but otherwise exhibit compara-tively uniform internal wall compositions (Figs.3B,D and 4D,E). Furthermore, Mg/Ca composi-

Table 1Deep-sea core and plankton tow details

Core ID Location Latitude andlongitude

Depth belowsea£oor

Intervalbelowsea£oor

Species and sizerange

Agea Modern meanannual SST[33]

(m) (cm) (Wm) (yr BP) (‡C)

SH9016 Timor Sea 8‡27PS,128‡14PE

1805 5^6 N. dutertrei,G. ruber, 300^450

1 711 28.2

65^66 19 323RS122/GC/003

Cartier Trough,Timor Sea

11‡28PS,124‡35PE

416 97.5^102.5 G. sacculifer,350^550

V6 000b 28.6

297.5^302.5 18 140GC5 Prydz Bay 67‡04PS,

69‡01PE320 0^1 N. pachyderma,

250^35030.6

Plankton tow Depth belowsea surface

Measuredseawatertemperature

Fr2/96-station 5

O¡shore WesternAustralia

28‡43PS,113‡24PE

0^60 G. ruber, 350 26.5, 26.0 at60 m

a Ages are radiocarbon years determined by accelerator mass spectrometry.b Age inferred on the basis of 6664 yr BP age at 110 cm.



tions and pro¢le forms tend to be similar in allchambers of G. ruber and G. sacculifer, whereaslarge di¡erences are observed between chambersin N. dutertrei (Fig. 4A,B) and occasionally alsoin N. pachyderma (Fig. 4C).

The nature and extent of compositional vari-ability within and between tests of the di¡erent

species can be most readily appreciated and as-sessed using histograms that compile the individ-ual Mg/Ca measurements that form the composi-tional pro¢les obtained from each chamber ineach test (Figs. 5 and 6). These histograms exhibita range of characteristic, and often di¡erent,forms for each species. N. dutertrei tests exhibit

Fig. 5. Histograms of the natural logarithm of individual (Mg/Ca) mmol/mol ratios compiled from the pro¢led compositions ofeach analysed chamber of individual tests of G. ruber, N. pachyderma and N. dutertrei. Note that calci¢cation temperatures varylinearly with ln(Mg/Ca), and have been estimated for G. ruber using the calibration reported for this species by Rosenthal andLohmann [17], by applying a nominal shell weight of 11 Wg to avoid calibration bias related to sea£oor dissolution. Calci¢cationtemperature estimates for N. pachyderma and N. dutertrei have been calculated using the multi-species calibration of Nu«rnberg etal. [2], following adjustment for original electron-probe analytical bias relative to ICP techniques [5]. f, f-1, f-2, etc. denote thedi¡erent chamber compositions in each test (see Fig. 1 for notation). Note the distinctive Mg/Ca distribution characteristics ofthe di¡erent species (see text for discussion). The N. dutertrei and the upper two G. ruber tests are from an LGM sample intervalin core SH9106, the lower two G. ruber tests from a Holocene sample interval in the same core, and the N. pachyderma are fromcore GC5. See Table 1 for core location, interval ages, and sample details. The test sample number is indicated above the legendin each panel.



Fig. 6. Histograms of the natural logarithm of individual (Mg/Ca) mmol/mol ratios compiled from the pro¢led compositions ofeach analysed chamber of individual G. sacculifer tests. Note the variation in distribution forms in this species, which range fromsimple unimodal to bimodal distributions that have a characteristic dominant mode with higher Mg/Ca. Tests from an early- tomid-Holocene interval in the core RS122/GC/003 are shown on the left and from an LGM interval on the right (see Table 1 forcore location, interval ages and sample details). Calci¢cation temperature estimates have been calculated using the G. sacculifercalibration of Rosenthal and Lohmann [17], by applying a nominal shell weight of 45 Wg to avoid calibration bias related to sea-£oor dissolution. Note the lower overall temperatures recorded by the LGM tests. f, f-1, f-2, etc. denote the chamber composi-tions (see Fig. 1 for notation). Test sample numbers are above the legend in each panel.



the largest Mg/Ca compositional range (typicallyspanning 1.5^2 natural log units) and possesscomplex distributions with three or more well de-veloped modes. Much simpler distributions areobserved in other species, in particular G. ruber,which is notable for its tight, usually unimodaldistributions that tend to be skewed toward high-er Mg/Ca values by the Mg-rich surface veneers.Much broader unimodal distributions that areoften strongly positively skewed are characteristicof some but not all N. pachyderma tests fromPrydz Bay. Simple tight unimodal distributions,similar to those of G. ruber, are observed insome G. sacculifer tests, but many have either asecondary mode at lower Mg/Ca or a tail towardlower Mg/Ca compositions. The multiple compo-sition modes that are observed in all N. dutertreiand many G. sacculifer tests (Figs. 5 and 6), andoccasionally in other species, are typically associ-ated with speci¢c chambers or groups of cham-bers. In some cases, individual chambers are rep-resented in more than one Mg/Ca compositionmode, this being a re£ection of the developmentof compositionally distinct inner- and outer-walllayers in these chambers.

The observed compositional range and thespacing of Mg/Ca modes in the individual testsin Figs. 5 and 6 are related linearly to calci¢cationtemperature through the exponential form of fo-raminiferal Mg/Ca seawater thermometers. Ac-cordingly, we have derived temperature estimatesfor each Mg/Ca mode in each test by applyingthermometer calibrations that are (as far as pos-sible) appropriate for each species and that arefree of dissolution-related biases (see captions toFigs. 5 and 6 for details). The temperatures ob-tained for the primary composition modes of theG. sacculifer, G. ruber and N. pachyderma tests,and the highest Mg/Ca composition modes ob-served in the N. dutertrei tests, are notable forbeing broadly consistent with present-day, meanannual SSTs for the deep-sea core locations fromwhich these tests originate (i.e. 28.6 and 28.2‡Cfor cores RS122/GC/003 and SH9016 in the Ti-mor Sea, and 30.6‡C for GC5 in Prydz Bay [33]).However, all the N. dutertrei tests and half the G.ruber and G. sacculifer tests are derived from LastGlacial Maximum (LGM) core intervals, and the

remaining G. ruber and G. sacculifer tests are fromearly to mid-Holocene core intervals (see Table 1for details). In this context, the LGM G. sacculifertests are notable for clustering within a lower tem-perature range (23.8^25.5‡C) than their Holocenecounterparts (27.2^30.8‡C), and three of fourLGM G. ruber tests for registering temperaturesnear 25.5‡C (one at 29‡C) whereas three of fourHolocene tests register near 29‡C (the other, #5-6B, 25.6‡C; Fig. 6). These estimates suggest calci-¢cation temperatures for LGM tests that are onaverage about 3.5‡C lower than Holocene tests ofthe same species. This temperature di¡erence isslightly higher than the estimated change in SSTin the tropical eastern Indian Ocean between theLGM and today (i.e. 1^2‡C), based on applica-tion of the Modern Analogue Technique toplanktonic foraminifera assemblages [34]. Thetemperature ranges recorded by the di¡ering pri-mary Mg/Ca composition modes of the Holoceneand LGM G. sacculifer tests (i.e. 27.2^30.8‡C and23.8^27.1‡C) are in keeping with the magnitude ofmodern, average monthly SST variation at theRS122/GC/003 core site (i.e. 26.7^29.9‡C [33]).Similar ranges, spanning about 3.5‡C, are alsoobserved for the smaller numbers of Holoceneand LGM G. ruber tests from SH9016, whichhas a modern, average monthly SST range from26.7 to 29.5‡C [33].

The highest Mg/Ca composition modes of theLGM N. dutertrei tests are notable for havingtemperature estimates that are on average about2^3‡C higher than LGM G. ruber and G. saccu-lifer tests. This suggests the thermometer appliedto these tests [2] may be overestimating these cal-ci¢cation temperatures for N. dutertrei by severaldegrees.

The large spread in Mg/Ca compositions andthe lower Mg/Ca composition modes that are ob-served in N. dutertrei and many G. sacculifer testsrange to signi¢cantly cooler temperatures than thenear-SST estimates that are recorded by the high-est Mg/Ca modes in the same tests. The inter-mediate Mg/Ca compositions that dominatemost N. dutertrei tests correspond to temperatureestimates in the range 12^23‡C; however, temper-atures below 13‡C and as low as 4‡C are indicatedfor the lowest Mg/Ca mode compositions in this



species. The secondary, lower Mg/Ca compositionmodes that are observed in many G. sacculifertests, which are a manifestation of low-Mg out-er-wall layer development, register calci¢cationtemperatures between 3 and 7.5‡C lower thanthe principal Mg/Ca composition modes in thesetests. The compositions of these low-Mg outer-wall layers re£ect calci¢cation temperatures be-tween 20 and 22‡C in LGM tests, and between23 and 25‡C in Holocene tests (see Fig. 6).

The anomalously high Mg/Ca compositions ofthe surface veneers that have been documented onall tests correspond to calci¢cation temperatureestimates that greatly exceed acceptable limits(i.e. SSTs at each core locality). The N. pachyder-ma tests from Prydz Bay (Fig. 5) are further no-table for exhibiting a range of Mg/Ca composi-tions that extends well beyond acceptablecalci¢cation temperatures for this locality (boththe monthly mean SST range and variation withdepth span only 31.3 to 0.5‡C [33]). Di¡erentchambers in the same test also often have verydistinct compositions, with ¢nal chambers usuallyhaving the lowest Mg/Ca.

5. Discussion

The Mg/Ca and other trace element composi-tional variability that we have documented inplanktonic foraminifera tests, considerably ex-tends current knowledge of the nature and extentof compositional variability within several keyspecies that are widely used in palaeoceano-graphic reconstruction. Our results demonstratefor each analysed species that bulk pooled testcompositions are likely to integrate diverse com-positional variation that occurs both within andbetween tests. Furthermore, comparison withpresent-day seawater temperatures indicates thatreasonable calci¢cation temperature estimatesmay be obtained from each analysed species usingLA-ICP-MS. However, the high Mg/Ca composi-tions found in parts of many N. pachyderma testsfrom Prydz Bay and the Mg-rich surface veneersthat have been observed on all analysed tests cor-respond to unacceptably high calci¢cation tem-peratures.

5.1. Origin of Mg-rich test surfaces

The presence of similar, if not identical, Mg-rich surface veneers on both modern (planktontow-sampled) tests and fossil tests suggests thisMg enrichment may be of primary biogenic ori-gin. In support of this possibility we note that Be¤[27] reported the precipitation of thin (V0.2 Wm),smooth-surfaced, veneers upon the terraced pre-gametogenic shell surfaces of G. sacculifer, andSEM images (see Plate IX in [27]) revealed thesethin surface veneers to be preferentially removedby sea£oor dissolution, indicating they are likelyto be more Mg-rich than underlying pre-gameto-genic calcite. Brown and Elder¢eld have also ob-served, in their seminal paper on the e¡ects ofsea£oor dissolution [17], that both the outer sur-faces and inner walls of fossil G. sacculifer testsare ¢rst a¡ected by sea£oor dissolution. More-over, the large Mg enrichments documented tooccur toward test surfaces across the ¢nal outercrusts of laboratory-cultured G. sacculifer, indi-cates that anomalous, Mg-rich calcite compo-sitions can be precipitated under physiologicalcontrol by this species [1]. Collectively theseobservations lend support to the possibility thatanomalous, Mg-rich calcite could be precipitatedduring the ¢nal stages of test calci¢cation,although the reasons why this may occur are un-clear (see also [1]).

On the other hand, if adhering Mg-rich clays,carbonates, organic material or other phases areresponsible for the Mg-rich surface veneers we areable to provide some useful constraints on theirnature. In this regard, the test surfaces are notablefor reaching Mg-rich calcite compositions (6 1^6mol % MgCO3) and for having elevated yet stilltrace level concentrations of Mn, Zn and Ba(Figs. 3). These relatively low Mn concentrationsare inconsistent with the Mn^Mg^CO3 coatingsthat were originally suggested to develop on fossiltests during diagenesis below the Mn-reductionfront in sea£oor sediments [22]. Furthermore,the Mg-rich surface enrichment and the observedMg distribution across chamber walls is unlikelyto re£ect residual Mg-rich organic matter uponand within tests (see also [24]), as indicated bythe failure of strong oxidants to remove Mg-rich



surfaces from live-sampled G. ruber tests and thevery acceptable temperature estimates that arecalculated for wall interiors based on measuredMg/Ca concentrations. Integration of wall com-position pro¢les, to both include and excludethe Mg-rich test surfaces, indicates they biaswhole-test compositions toward higher Mg/Cavalues by between 5 and 35%, which is broadlyconsistent with the extent to which bulk test com-positions are lowered by test cleaning procedures(e.g. [6]).

5.2. Calci¢cation conditions for di¡erent testcomponents

The distribution of Mg within test wall interi-ors, in particular the depletion of Mg in the outer-wall layers of N. dutertrei and many G. sacculifertests, is consistent with previously documentedlow-Mg outer-crust development in G. bulloidesand Globorotalid species, and documents directly,for the ¢rst time, the calci¢cation of low-Mg ¢nalouter-crust compositions in G. sacculifer. Interest-ingly, inspection of the N. dutertrei pro¢les shownin Fig. 5 reveals that the low-Mg outer-wall layercompositions are inconsistently developed on dif-ferent chambers in the same test, with particularlythick and Mg-poor layers (comprising s 60^70%of the wall width) occurring on only a few cham-bers (usually f-2, f-3 or f-4; see Fig. 1 for chambernotation). The very low calci¢cation temperatures(between 4 and 13‡C) estimated from the compo-sitions of these outer crusts correspond to present-day temperatures at depths below 225 m and asdeep as 1100 m at the SH9016 core site [33]. Thiscompares to the intermediate Mg/Ca composi-tions that dominate most tests, which re£ectwarmer temperatures (12^23‡C) that correspondto the approximate position of the present-daymain thermocline, between 100 and 250 m [33].In contrast to N. dutertrei, the low-Mg outer-wall compositions in G. sacculifer tests comprisea relatively small proportion of the total wallthickness (typically between 20 and 50%), and rec-ord calci¢cation temperatures that are between 3and 7.5‡C lower than the primary Mg/Ca modetemperatures of the same tests. For HoloceneG. sacculifer tests, estimates of the outer-crust cal-

ci¢cation temperature range between 23 and 25‡C.This corresponds to present-day mean annualtemperatures at water depths between 70 and100 m at the RS122/GC/003 core site [33]. Amongthe small number of G. ruber tests analysed in thisstudy, several show signi¢cant Mg/Ca variationthat is manifested as compositionally distinctchambers and also, outer- and inner-wall layersin some chambers. The bimodal Mg/Ca distri-butions observed in two tests (one of which is il-lustrated in Fig. 5) indicate a calci¢cation tem-perature di¡erence of order 2^3‡C. Indeed, thelimited calci¢cation temperature range of G. rubertests, as evidenced by their tight Mg/Ca composi-tion distributions, is consistent with the exclu-sively near-surface habitat of this species (e.g.[26]). Nonetheless, our results suggest someG. ruber may calcify over a small but signi¢cantdepth range, su⁄cient to encounter a 2^3‡C tem-perature variation.

The reason for the anomalously high temper-ature estimates (in the range 7^8‡C) that havebeen obtained for parts of N. pachyderma testsfrom Prydz Bay is unclear, and suggests that var-iation in calci¢cation kinetics, other physiologicalcontrols, or possibly salinity changes, could dom-inate over temperature control at very low tem-peratures.

5.3. Reconstruction of habitat migration

The ability to measure compositional variationwithin the sequentially precipitated components(chambers and wall layers) that form single testspresents the possibility of being able to recon-struct habitat migration during the adult life-cyclestages of individual foraminifera. In the case ofG. sacculifer tests this is relatively straightforward,with the low Mg/Ca crusts that are developed onmany tests indicating descent from near-surfaceconditions to undergo ¢nal calci¢cation at tem-peratures in the range 23^25‡C. The latter corre-sponds to depths between 70 and 100 m, givenearly- to mid-Holocene ocean temperatures arecomparable to the present-day one at theRS122/GC/003 core site [33]. The temperature of¢nal outer-crust growth is similar to estimatesbased on sea£oor dissolution e¡ects upon bulk



G. sacculifer test compositions from the tropicalAtlantic (i.e. 21; 1.5‡C), for which correspondingdepths ranged between 100 and 225 m, east towest, across the tropical Atlantic [11]). Theseand our depth estimates are signi¢cantly shal-lower than some previously reported estimates(i.e. s 200 m in the Red Sea [35], 300^800 m[36]).

The record of calci¢cation temperature con-tained in N. dutertrei tests is considerably morecomplex than in G. sacculifer. Using the test illus-trated in Fig. 1E as an example, for which pro¢lesare shown in Figs. 3C and 4A, it can be seen thatthe more Mg-rich composition of the ¢nal twochambers (f and f-1) compares closely to the in-ner-wall layers of earlier formed chambers (partic-ularly f-2 and f-4). Calci¢cation temperature esti-mates for the ¢nal two chambers (f and f-1) in thistest are near 27.8‡C (see Fig. 5, top left histo-gram), whereas temperatures of 20 and 13.5‡Care observed for the inner- and outer-wall layersof chambers f-2 and f-4, respectively, and 20^28‡Cfor chamber f-5. The greater thickness and coarse,euhedral, calcite surface textures of chambers f-2and f-4 (Fig. 1E) indicate ¢nal crust developmentwas concentrated on the exterior of these cham-bers, and the low Mg/Ca compositions of thesecrusts indicate they grew under much colder con-ditions than other test components. Further notethat the surface texture variations on the di¡erentchambers of this test are also consistent with thedocumented development of reticulate and crys-talline (euhedral calcite) surface textures in thisspecies under warmer and colder conditions, re-spectively [37]. We interpret the Mg/Ca variationobserved within this test to re£ect calci¢cation ofearlier chambers, f-5 through f-2, under relativelycool conditions (V20‡C) in the upper thermo-cline, prior to migration into warmer (V27.5‡C)near-surface waters, where the ¢nal two chamberswere added, followed by rapid descent into muchcolder (6 14‡C) water near the base of the ther-mocline, where the ¢nal outer calcite crust wasadded. Other N. dutertrei tests show a similarpattern of Mg/Ca variation in sequentially pre-cipitated test components (Fig. 5) that also re£ectinitial residence above or within the upper ther-mocline, followed by descent to depths near the

base or below the thermocline. This migrationpattern is compatible with existing knowledge ofthe life-cycle of N. dutertrei based on planktontow and sediment trap studies, which indicatethis species resides predominantly in or abovethe thermocline subject to the position of thechlorophyll maximum and that reproduction oc-curs deeper within the thermocline [38,39]. De-spite the limited nature of these results they dem-onstrate the potential power of using LA-ICP-MSmicroanalysis to trace habitat changes during theadult life-cycle stages of planktonic foraminifera.They also highlight the fact that such habitatchanges can produce very large Mg/Ca variationswithin individual tests, particularly in species thatmigrate large vertical distances in the water col-umn. Understanding the impact these habitatchanges have on test Mg/Ca and N

18O composi-tion is required if reliable reconstructions of pa-laeocean conditions are to be made using suchspecies.

5.4. Application of LA-ICP-MS to palaeoceanreconstruction

The results of this study provide ‘proof of con-cept’ that LA-ICP-MS may be used to extractrecords of past ocean temperature from fossilplanktonic foraminifera tests. Compared to con-ventional bulk analysis this technique o¡ers sig-ni¢cant advantages through its potential to derivethe range and variability of seawater temperature,in addition to a simple mean value, from a pop-ulation of fossil tests. Improved constraints onthermocline structure and depth could potentiallyalso be obtained from analysis of sequentially pre-cipitated test components in species that migratethrough signi¢cant vertical ranges. Moreover,sample preparation is straightforward, and contri-butions from anomalously Mg-rich surface coat-ings (whatever their origin) can be readily ex-cluded from the analysis without invokingcomplex and time-consuming cleaning proce-dures. LA-ICP-MS can also analyse multiple traceelements in addition to Mg/Ca (e.g. Sr, Zn, Ba,Cd) and, perhaps most signi¢cantly, allows forsubsequent N18O analysis of the same test materi-al, and possibly more precise and accurate con-



straints to be placed on palaeo-salinity and sea-water density.

6. Summary

Systematic large and correlated variation ofMg/Ca, Mn/Ca, Ba/Ca and Zn/Ca but relativelyuniform Sr/Ca has been documented within thetest walls of several planktonic species (G. saccu-lifer, G. ruber, N. pachyderma and N. dutertrei) byhigh-resolution depth pro¢ling using LA-ICP-MS.Distinct chamber and wall layer compositions canbe resolved using this technique, and composi-tional variation associated with sequentially pre-cipitated test components can be quanti¢ed. Thevariation observed within tests of the analysedplanktonic species is found to be consistent withseawater temperature and associated habitatchanges experienced during the adult stages ofthese species (with the notable exception of N. pa-chyderma, which exhibits Mg/Ca variation ex-tending well beyond that able to be explained bytemperature variation alone). Shallow-dwellingspecies, in particular G. ruber, but also G. saccu-lifer, tend to have more uniform chamber andwall layer compositions than deeper-dwelling spe-cies, such as N. dutertrei. Low-Mg/Ca outer-walllayer compositions developed on G. sacculifer andN. dutertrei tests are consistent with ¢nal outer-crust growth on these species near the top of thethermocline and at the base and below the ther-mocline, respectively. The Mg-rich calcite (6 1^6mol% Mg) veneers that are observed on the ex-ternal surfaces of both fossil and modern tests areof uncertain but possible biogenic origin. TheseMg-rich surface coatings bias bulk test composi-tions toward higher Mg/Ca values by between 5and 35%

LA-ICP-MS shows considerable promise as ameans for reconstructing palaeo-seawater temper-atures from fossil planktonic foramifera tests.This technique stands to add value to deep-seacore-derived palaeoceanographic and climate re-cords by yielding (1) the range and variability ofpast seawater temperature from a population oftests, and (2) insights into thermocline depth andstructure by analysis of speci¢c test parts in spe-

cies that migrate through large vertical ranges.The technique may also be used to track habitatchanges that take place during the adult life-cyclestages of planktonic foraminifera.

Acknowledgements

We thank Michael Shelley for assisting withLA-ICP-MS analysis, Judith Shelley for pickingforaminifera from deep-sea core material, GeorgeChaproniere for con¢rming the identi¢cation ofspecies and for discussing aspects of foraminiferaecology, and Wolfgang Mu«ller for critical assess-ment of an early draft of this manuscript. Weparticularly wish to thank Dr. G.J. Reichart andtwo anonymous reviewers for critical reviews thathave resulted in improvements to this manu-script.[BARD]

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