Marine Micropaleontology 78 (2011) 113–120

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Marine Micropaleontology

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Research paper

Mg/Ca and δ18O in the brackish shallow-water benthic foraminifer Ammonia ‘beccarii’

Takashi Toyofuku a,h,⁎,Masayuki Suzuki b,1, HisamiSuga a, SaburoSakai a, Atsushi Suzuki c, Tsuyoshi Ishikawa d,h,Lennart Jan de Nooijer e, Ralf Schiebel f, Hodaka Kawahata g, Hiroshi Kitazato a,h

a Institute of Biogeosciences (BioGeos), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Natsushima-cho 2-15, Yokosuka, 237-0061, Japanb Research Institute for Hazards in Snowy Areas and Disaster Recovery, Niigata University, Ikarashi Ni-no-cho 8050, Niigata, 950-2181, Japanc Geological Survey of Japan, National Institute of Advanced Industrial Science and Technology (AIST), AIST Tsukuba Central 7, 1-1-1 Higashi, Tsukuba 305-8567, Japand Kochi Institute for Core Sample Research, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), B200 Monobe, Nankoku, Kochi, 783-8502, Japane Dept of Geosciences, Utrecht University, Budapestlaan 4, 3584 CD Utrecht, The Netherlandsf Laboratoire des Bio-Indicateurs Actuels et Fossiles (BIAF), University of Angers, 2 Boulevard Lavoisier, 49045 Angers CEDEX, Franceg Graduate School of Frontier Sciences, the University of Tokyo, Kashiwa, Chiba, 277-8561, Japanh Department of Geosciences, Shizuoka University, Oya 836, Suruga-ku, Shizuoka, 422-8529, Japan

⁎ Corresponding author. Fax: +81 46 867 9775.E-mail address: toyofuku@jamstec.go.jp (T. Toyofuk

1 Presentaddress: E&ESolutions, inc., AkihabaraUDXBuChiyoda-Ku, Tokyo 101-0021, Japan.

0377-8398/$ – see front matter © 2010 Elsevier B.V. Aldoi:10.1016/j.marmicro.2010.11.003

a b s t r a c t

a r t i c l e i n f o

Article history:Received 8 October 2007Received in revised form 14 November 2010Accepted 26 November 2010

Keywords:Benthic foraminiferaMg/Caδ18OTemperatureSalinityCulture experimentShallow water environmentBrackish water

Specimens of the benthic foraminifer Ammonia beccariiwere cultured in the laboratory in order to determinethe relation between temperature and Mg/Ca and oxygen isotope values in their tests. Asexual reproductionin this species provides a large number of juveniles that were allowed to grow into maturity at temperaturesranging from 10 to 27 °C and at salinities ranging from 18 to 33 PSU. The Mg/Ca in a calcite increaseexponentially and δ18O decreases linearly with the temperature. Salinity has no significant impact on eitherMg/Ca or δ18O. We show how the combination of these two parameters can be used to reconstruct seawaterδ18O and temperature in shallow marine habitats.

u).ilding14-1, Sotokanda4-chome,

l rights reserved.

© 2010 Elsevier B.V. All rights reserved.

1. Introduction

Benthic, shallow-water foraminiferal assemblage compositions areideally suited to be used for the temporal and spatial reconstruction ofthe sea level change and salinity (thus freshwater discharge) sincedifferent species vary in their sensitivity to changes in salinity (Murray,1968). Species vary in their tolerance to long-term and short-termchanges in salinity. One of the species best adapted to the changes insalinity is the calcareous Ammonia ‘beccarii’ (Fig. 1), which oftendominates foraminiferal mud flat communities (e.g., Murray, 1968,1979, 2006;Matoba, 1970; Scott, 1976; Haake, 1982;Wang andMurray,1983). This species is common in brackish waters and salt marshes,capable of thriving under short-term (e.g., N1 h) variability in temper-ature and salinity. This ability to cope with environmental variabilitymakes it a species particularly suitable for culture and manipulation inlaboratory settings (e.g. De Nooijer et al., 2007; Toyofuku et al., 2008;

Dissard et al., 2010a, b; Raitzsch et al., 2009). Its capacity to calcify undera range of salinities and temperatures makes it possible to use thechemical and isotopic compositions of its calcareous shell an ideal tool toreconstruct shallow-water environmental changes (e.g., Hayward et al.,2004a; Leorri and Cearreta, 2004; Cabral et al., 2006).

TheMg content of the foraminiferal calciumcarbonate (expressed asits Mg/Ca value) is a function of the temperature at which it isprecipitated (Cronblad and Malmgren, 1981; Delaney et al., 1985). TheMg/Ca in the foraminiferal calcite has therefore been used as atemperature proxy in paleoceanography (e.g. Nürnberg, 1995;Rosenthal et al., 1997). The relation between temperature andforaminiferal Mg/Ca is species-dependent and calibration is availablefor a number of planktonic (e.g. Nürnberg et al., 1996; Hasting et al.,1998; Lea et al., 1999;McKenna and Prell, 2004; Russell et al., 2004) andbenthic species (Izuka, 1988; Rathburn andDeDeckker, 1997; Toyofukuet al., 2000; Toler et al., 2001; Billups and Schrag, 2002, 2003; Lear et al.,2002;Martin et al., 2002;Marchitto and deMenocal, 2003; Skinner et al.,2003; Rathmann et al., 2004; Raja et al., 2005; Elderfield et al., 2006;Rosenthal et al., 2006;Marchitto et al., 2007; Kristjánsdóttir et al., 2007;Bryan and Marchitto, 2008; Healey et al., 2008).

The ratio between incorporated 16O and 18O in the calcite (δ18Ocalcite)has been a popular paleotemperature proxy since several decades.

Fig. 1. Scanning Electron Micrograph of Ammonia beccarii from Hamana.

Table 1Experimental settings.

1st batch

Temperaturesettings

Salinity conditions (PSU)

18.4±0.1 21.5±0.1 24.0±0.1 26.1±0.1 27.8±0.1 33.3±0.1

10.3±0.3 °C √15.2±0.3 °C √17.6±0.9 °C √24.0±0.4 °C √ √ √ √ √27.3±0.4 °C √

2nd batch

Temperaturesettings

Salinity conditions (PSU)

22.4±0.1 28.3±0.1 33.6±0.1

27.5±0.4 °C √ √ √

114 T. Toyofuku et al. / Marine Micropaleontology 78 (2011) 113–120

Foraminiferal δ18O does not only reflect the temperature (Urey, 1947;Emiliani, 1954), but also the δ18O of the seawater (Emiliani, 1966;Shackleton, 1967; Duplessy et al., 1970). For timescales on which theδ18Oof the seawater is expected to vary, orwhen there is local variabilityin δ18O of seawater, the Mg/Ca and calcitic δ18O may be combined toreliably reconstruct paleotemperatures (and seawater δ18O). Salinityaffects bothparameters, but its effect isminor compared to the impact oftemperature in open marine environments (e.g. Nürnberg et al., 1996).However, for environments with variable salinities such as coastalregions, the Mg/Ca and δ18O of the foraminiferal calcite reflects acombination of salinity and temperature.

With reliable calibrations for foraminiferal Mg/Ca and δ18O againstseawater temperature, it has been possible to reconstruct the sea surface(e.g.Mashiotta et al., 1999; Lea et al., 2000; Elderfield andGanssen, 2000)anddeepwater temperatures (e.g. Lear et al., 2008). BothMgpartitioningand stable oxygen isotope fractionation during foraminiferal calcifica-tion, however, are usually influenced by more than one environmentalparameter (Nürnberg et al., 1996). It is therefore necessary to isolate theeffects of changes in e.g. temperature and salinity under controlledconditions. Laboratory-based culturing experiments allow the calibra-tion outside the range found in today's environments.

For species living predominantly in shallow water environments,the relationships of Mg/Ca and δ18O with temperature and salinity arenot yet widely available. We present a calibration for Mg/Ca and δ18Oversus temperature and salinity for the shallow water species A.beccarii. The obtained relationships can be used to reconstruct salinityand temperature in these environments from measurements on fossilspecimens, although such reconstructions may be made morecomplex due to seasonal and other short-term variability (Toyofukuet al., 2000; Diz et al., 2009).

2. Materials and methods

Living individuals of the benthic foraminifer A. beccarii (Linné, 1758:Fig. 1) were collected from Lake Hamana, Shizuoka Prefecture, CentralHonshu, Japan, in October, 1998. Lake Hamana is a brackish lake (meansalinity approximately 28 PSU). The sampling water depth was ~2 m.Thewater temperature varies from5 °C to28 °C at the bottom through ayear (Shizuoka Prefectural Research Institute of Fishery; http://www11.

ocn.ne.jp/~hamanako/date/teiten.htm). In addition, the juveniles of A.beccarii were produced from the specimens collected at Ariake Bay,Yanagawa, Kyushu Island, Japan in March 2003. These juveniles weremaintained under controlled temperature and salinity in order todetermine the effect of salinity on the oxygen isotopic composition oftheir calcitic tests. The calcite of the field samples and laboratory grownA. beccariiwas analyzed for theirMg/Ca and δ18O. Toyofuku-Suzuki et al.(2004) confirmed that our Ammonia ‘beccarii’ from both Hamana andAriake belong to the molecular type T6 in Hayward et al. (2004b).

2.1. Culture procedures

After the collection of the sediment, more than 100 living specimenswere isolated, transferred to Petri dishes and cleaned from an excess ofsediment and detritus. Culturing procedures follow those described byKitazato (1994). Specimens were incubated in filtered, in-situ collectedwater from Lake Hamana, at a salinity of 28 PSU and a constanttemperature of 20 °C. The Petri dishes were kept under a whitefluorescent light at ~100 μmol/m2/s in a 12 h:12 h light–dark cycle.Specimenswere fed livingmicro-algaeDunaliella sp. three times aweek,andwater was replaced at the same time tomaintain constant chemicalconditions and to avoid the accumulation of harmful compounds.Specimens were observed to ingest the provided algae, to produce newchambers regularly and occasionally, and to reproduce asexually. Mostoffspring (typically between 50 and 200 individuals) added chambersaccording to the typical growth curves (Bradshaw, 1957), and grew to asize of N300 μm within 60 days.

2.2. Culture settings

A few days after asexual reproduction, 30 specimens were separatedfor each treatment. Even though the juvenile specimens had alreadyformed three or four chambers, this amount of calcite is negligible (i.e.b1 wt.%) in comparison to the total amount of calcite at the end of theincubation. This estimation is basedon the so-called bilammelarmodeofcalcification in rotallids (Erez, 2003).When adding a chamber,A. beccariiprecipitates an extra layer of calcite on top of the existing chambers aswell. This reduces the percentage of the first chambers exponentiallycompared to the total weight as an individual continues to grow.

For the first experiment, the juveniles weremaintained at a range oftemperatures and salinity conditions (Table 1). The specimenswere cultivated in Petri dishes (diameter 60 mm, height 10 mm) for30 days. The disheswere sealed by laboratory film to avoid evaporation.A second batch of culture experiment was conducted in cell cultureflasks (BDFalcon, 250 ml). Each culture vesselwas incubated for30 daysat one of the six temperatures (10.3, 15.2, 17.6, 24.0, 27.3 and 27.5 °C) inseparate incubators. Temperatures were recorded automatically every30 min by a temperature logger during both culturing experiments.Filtered open ocean seawater (35 PSU) was diluted with Milli-Q water

0

1

2

3

4

5 10 15 20 25 30

Mg/Ca (mmol/mol) = 0.575*e0.0531T(°C), r = 0.810

Mg/Ca (mmol/mol) = 0.0950T(°C) – 0.105, r = 0.790

Temperature (°C)

Mg/

Ca

(mm

ol/m

ol)

Fig. 2. Mg/Ca from cultured A. beccarii at different temperatures.

115T. Toyofuku et al. / Marine Micropaleontology 78 (2011) 113–120

to adjust the experimental salinity conditions. Sufficient (N20 l)seawater was kept in tightly closed plastic bags to provide water forthe full experiment for each salinity condition. The water used in theexperiments was taken from these large bags and its salinity wasadjusted for each experiment. For thefirst experiment, seawater salinitywas kept at 26.1±0.1 PSU at all temperatures, except the batch at10.3 °C, for which salinity was 24.0±0.1. In addition, specimens weregrownat 24.0±0.4 °C atfive salinities (18.4±0.1, 21.5±0.1, 26.1±0.1,27.8±0.1 and 33.3±0.1 PSU).

In the second experiment, specimens were grown at threesalinities (22.4±0.1, 28.3±0.1, and 33.6±0.1 PSU) at 27.5±0.4 °C.The culturewater in the petri dishwas changed three times aweek forthe first experiment. The culture water in the culture flasks in thesecond experiment was changed once a week. The Mg/Ca of ambientseawater was 5.2 atomic ratios, and fluctuated less than 1% betweenthe beginning and the end of the experimental periods. Oxygenisotopic compositions of culture water were measured at thebeginning and end of each incubation experiment. The δ18Owater

changed little during the experiments (±0.1‰). The pH wasmeasured by a semi-conductor pH probe during the incubations.The maximum pH fluctuations were less than 0.10 around 8.10 ineither experiment.

2.3. Elemental measurement

Laboratory grown specimens were rinsed with Milli-Q water, driedat 50 °C, and stored to performMg/Ca analyses. Specimenswere cleanedfollowing the methods developed by Boyle (1981) and Boyle andKeigwin (1985), withmodifications according to Toyofuku et al. (2000).The reductive cleaning steps were skipped because the culture speci-menswere free of adherentmaterial such as clayminerals. Several (~5)specimenswere included in each sample solution for each temperature/salinity combination. Foraminiferal specimens were gently crushedbetween two acid-rinsed glass plates, to open the chamber spaces.Crushed shell fragments were placed in a solution of alkaline peroxide(0.02 mM H2O2 in 0.1 M NaOH) at 90 °C for 10 min, then rinsed with0.001 M HNO3 for 1 min. Between each step, specimens were rinsedwith Milli-Q. Each specimen was dissolved in 0.5 ml 0.1 M HNO3, andMg concentrations were measured from 0.4 ml of the solution. For Cameasurements, the remaining 0.1 ml of the solution was diluted up to1 ml 0.1 N using HNO3. TheMg and Ca concentrationswere determinedby graphite furnace-atomic absorption spectrometry (GF-AAS, HITACHIZ-8270) at Shizuoka University. Each sample solution was measuredthree times, at 3% (Mg) and 5% (Ca) precision.

2.4. Oxygen isotopic measurement

Isotopic analyses were conducted on MicroMass Optima isotoperatio mass spectrometer (IRMS) at Geological Survey of Japan andMicroMass Isoprime IRMS at JAMSTEC. The foraminiferal specimenswere dried after cleaning with Milli-Q twice before the IRMSmeasurement, then reacted with pure phosphoric acid at 90 °C bythe automated carbonate analytical device. Results are reported asδ18O foram values defined by the relationship

δ18Oforam = 18O=16Osample−

18O=16Ostandard

� �=18O=

16Ostandard × 1000:

The analytical precision of δ18O was better than ±0.05‰ relativeto the Vienna Pee Dee belemnite (VPDB) standard by replicateanalyses of NBS-19.

The oxygen isotopic compositions of cultured water weremeasured on Fisons Prism IRMS at Research Institute for Hazards inSnowy Areas, Niigata University and the Isoprime IRMS at JAMSTEC.The samples were equilibrated with CO2 at 25 °C for 8 h. Wateroxygen isotopic compositions are described as δ18Owater and the

precision of replicated measurements was better than ±0.02‰.Foraminiferal oxygen isotopic compositions are expressed both asδ18Oforam and as the isotopic difference between calcite and water(δ18Oforam−δ18Owater), where both values are indicated in theconventional δ notation relative to VPDB.

3. Results

3.1. Temperature experiment

Cultured specimens of A. beccarii precipitated the calcite with Mg/Ca ranging from 1 mmol/mol to 4 mmol/mol, with a positivecorrelation with ambient temperature (Fig. 2, Table 2). The temper-ature–Mg/Ca correlation is best described by the formula;

Mg=Ca mmol=molð Þ = 0:575Te0:0531 T; r = 0:810 ð1Þ

Mg=Ca mmol=molð Þ = 0:0950 T–0:105; r = 0:790 ð1′Þ

where T is temperature, r indicates the regression coefficient.TheMg/Ca values vary at each temperature, but the variability was

smaller at lower seawater temperatures.The oxygen isotopic composition of foraminiferal calcite also

correlates significantly and negatively with water temperature (Fig. 3,Table 3). Here, the obtained relation between temperature andforaminiferal oxygen isotopic composition is described by:

T = − 4:49ðδ18Oforam−δ18OwaterÞ + 17:18; r = 0:95 ð2Þ

where r indicates the regression coefficient.

3.2. Salinity experiment

The foraminiferal Mg/Ca show no systematic correlation tosalinity. ThemeasuredMg/Ca are similar values in specimens culturedat salinities ranging from 18.4 to 33.3 PSU at 24.0 °C. TheMg/Ca valuesin specimens cultured at salinity 26.1 PSU are slightly higher thanaverage (Fig. 4, Table 2). The linear regression between the Mg/Ca andsalinity is described as:

Mg= Ca mmol=molð Þ = 0:0201salinity + 0:878; r = 0:266 ð3Þ

TheMg/Caat different salinities are not significantlydifferent (t-test;p=0.32: ANOVA; F=2.76, p=0.08).

Table 2Experimental Mg/Ca of Ammonia beccarii.

Condition Mg/Ca (mmol/mol) Mean Mg/Ca (mmol/mol) Standard deviation

Temperature experiment10.3±0.3 °C 1.087 0.950 0.118

0.8830.881

15.2±0.3 °C 1.442 1.466 0.0481.4721.5311.419

17.6±0.9 °C 1.754 1.480 0.3951.3751.8240.967

24.0±0.4 °C 1.525 1.759 0.3631.9171.6872.2791.355

27.3±0.4 °C 2.755 2.765 0.6133.4481.9162.7073.4562.308

Salinity experiment18.4 PSU 0.843 1.133 0.314

1.4671.089

21.5 PSU 1.332 1.133 0.2820.934

26.1 PSU 1.525 1.759 0.3631.9471.6872.2791.355

27.8 PSU 1.070 1.223 0.3221.5931.006

33.3 PSU 1.618 1.403 0.1971.3621.230

Fig. 3. Oxygen isotopic composition (δ18Oforam−δ18Owater) from specimens of A. beccariicultured at different temperatures.

Table 3Experimental δ18O of Ammonia beccarii.

Condition 103×δ18O(VPDB)

103×δ18Ocalcite−δ18Owater

Mean δ18O(VPDB)

Standarddeviation

Temperature experiment10.3±0.3 °C (at 24.0 PSU) 0.272 2.305 2.101 0.177

−0.026 2.007−0.043 1.990

15.2±0.3 °C (at 26.1 PSU) −1.028 0.612 0.541 0.2181.133 0.507

−0.989 0.651−1.456 0.184−0.890 0.750

17.6±0.9 °C (at 26.1 PSU) −1.310 0.330 0.118 0.373−1.953 −0.313−1.303 0.337

24.0±0.4 °C (at 26.1 PSU) −2.502 −0.862 −0.800 –

−2.379 −0.73927.5±0.4 °C (at 28.3 PSU) −3.710 −1.710 −2.009 0.268

−4.227 −2.227−4.091 −2.091

Salinity experiment (24.0 °C)18.4 PSU −4.254 −0.434 −0.434 –

21.5 PSU −3.553 −0.653 −0.116 1.060−1.795 1.105−3.700 −0.800

26.1 PSU −2.502 −0.862 −0.800 –

−2.379 −0.73927.8 PSU −1.686 −0.516 −0.469 0.196

−1.806 −0.636−1.424 −0.254

33.3 PSU 0.210 −0.200 −0.332 0.1140.018 −0.3920.007 −0.403

Salinity experiment (27.5 °C)22.4 PSU −5.311 −1.951 −2.035 0.118

−5.344 −1.984−5.529 −2.169

28.3 PSU −3.710 −1.710 −2.009 0.268−4.227 −2.227−4.091 −2.091

33.6 PSU −2.451 −1.866 −2.285 0.375−3.175 −2.590−2.983 −2.398

15 20 25 30 350

1

2

3

4

Mg/

Ca

(mm

ol/m

ol)

Salinity (PSU)

Fig. 4. Measured Mg/Ca in specimens of A. beccarii cultured at different salinities.

116 T. Toyofuku et al. / Marine Micropaleontology 78 (2011) 113–120

Fig. 6. Oxygen isotopic composition (δ18Oforam−δ18Owater) versus salinity. Black circlesfrom 24.0 °C and grey circles from 27.5 °C.

20

117T. Toyofuku et al. / Marine Micropaleontology 78 (2011) 113–120

The δ18O values of the calcite of cultured A. beccarii are correlatedto salinity because of the relation between salinity and δ18O of thewater in which they are grown (Fig. 5).

A constant relation between salinity and foraminiferal δ18Oforam

can be assumedwhen the oxygen isotopic composition of the ambientseawater (δ18Owater) is within these ranges (Fig. 6). The linearregressions are described as:

δ18Oforam−δ18Owater = 0:022salinity−1:14; r = 0:51 for 24:0 -C ð4Þ

δ18Oforam−δ18Owater = 0:021salinity−1:50; r = 0:39 for 27:5 -C ð5Þ

The δ18Oforam−δ18Owater in specimens cultured at differentsalinities are not significantly different (t-test; p=0.11: ANOVA;F=4.49, p=0.05 for 24.0 °C and t-test; p=0.310: ANOVA; F=0.92,p=0.45 for 27.5 °C).

4. Discussion

4.1. Environmental effects on the calcite chemistry

Our results show that Mg/Ca and δ18O in the calcite of A. beccariiare significantly correlated to seawater temperature in the rangebetween 10 and 27 °C. The range of measuredMg/Ca values (from 1 to4 mmol/mol) is one of the lowest among rotallid foraminiferal species(e.g. as compared to Fig. 1 in Bentov and Erez, 2006). Contrarily, theobtained values for δ18O are similar to those of other biogenic calcites(Figs. 7, 8). Previous studies have reported similar low Mg/Ca, such asapproximately 1 mmol/mol (for Ammonia batavus; Allison and Austin,2003) and 0.4–0.8 mmol/mol (for Ammonia tepida; Dissard et al.,2010a).

The correlation between Mg/Ca of A. beccarii and temperature canbe described as either an exponential (Eq. (1)) or a linear regression(Eq. (1)′). We consider that the exponential relation is biologicallymore reasonable. The Mg/Ca of A. beccarii shows the highestincrement per degree at high rather than at low temperatures. Thedataset of this study supports the previous studies describing therelation between Mg/Ca and as an exponential equation as expectedfrom theoretical thermodynamical prediction (Lea et al., 1999).

In addition, the temperature dependence of Mg/Ca in A. beccarii isrelatively small at low temperatures, especially in the range of 10 °C to17 °C. Perhaps 10 °C is near to the lowest growth limit of the species

Fig. 5. Oxygen isotopic composition (δ18Oforam) of the calcite of A. beccarii cultured atdifferent salinities. Black circles from 24.0 °C and grey circles from 27.5 °C.

according to Bradshaw (1957) and our laboratory observation (e.g.Koshio, 1992), the equation predicts that Mg/Ca at much lowertemperatures will approach a specific value and cannot fall belowthan 0 mmol/mol. Therefore, we suggest that fitting to a linearregression is not suitable for Mg/Ca-temperature calibration in thisspecies. In addition, the exponential fit shows a higher regressioncoefficient than the linear fit.

When comparing the temperature dependence of Mg/Ca in thecalcite formed by A. beccariiwith the previous studies (Fig. 7), we notethat the ability of Ammonia spp. to modify endocytosed seawater(Bentov et al., 2009; de Nooijer et al., 2009) in order to produce aninternal Ca-pool is extraordinary. The benthic genera Cibicides,Uvigerina and the planktonic genus Neogloboquadrina produce thecalcite with comparable Mg/Ca (0.5–2 mmol/mol), but these valuesare found in the calcite produced at lower temperatures only (b5 °C).

0

5

10

15

-5 0 5 10 15 20 25 30 35

G. sacc

ulifer

G. b

ullo

ides

O. u

nive

rsa

O. u

nive

rsa

N. pach

yderm

a

G. ruber

Archaias angulatus

B. aculeata

Cib

icid

oide

s sp

p

Cibicides spp

H. elegans0

Ammonia batavus

Ammonia tepida

Islandiella norcrossi/helenaeCassidulina neoteretis

Melonis spp

Globobulimina affinis

Oridorsalis umbonatus

Planuli

na sp

p

Uvigerina spp

Temperature (°C)

Mg/

Ca

(mm

ol/m

ol)

A. beccarii (This Study)

Fig. 7. Mg/Ca–temperature relation for various species of benthic foraminifera (Learet al., 2002; Martin et al., 2002; Lear et al., 2003; Rosenthal et al., 1997; Skinner et al.,2003; Lear et al., 2000; Toler et al., 2001; Hintz et al., 2006; Izuka, 1988; Marchitto andDeMenocal, 2003; Billups and Schrag, 2002; Rathburn and De Deckker, 1997;Kristjánsdóttir et al., 2007; Nürnberg et al., 1996; Kisakürek et al., 2008; Lea et al.,1999; Russell et al., 2004; von Langen et al., 2005.) Summary of Mg/Ca calibrations forbenthic species are cited by Kristjánsdóttir et al. (2007) and for cultivated planktonicspecies are cited in Sagawa (2010).

Fig. 8. Comparison of oxygen isotopic composition of A. beccarii with those of speciespreviously studied (McCrea, 1950; Epstein et al., 1953; Craig, 1965; O'Neil et al., 1969;Horiba and Oba, 1972; Shackleton, 1974; Erez and Luz, 1983; Bouvier-Soumagnac andDuplessy, 1985; Kim and O'Niel, 1997; Bemis et al., 1998). Summary of calibrations arecited by Bemis et al. (1998).

118 T. Toyofuku et al. / Marine Micropaleontology 78 (2011) 113–120

At higher temperatures (i.e. N10 °C) all other genera have higherMg/Ca than Ammonia. Interestingly, the only extant aragoniticspecies, Höglundina elegans, produces its tests with low Mg/Cabetween 5 °C and 20 °C (Rosenthal et al., 2006).

The temperature-dependence of δ18Oforam of A. beccarii iscomparable with those in the previous studies (Fig. 8). The interceptfor benthic species and inorganic precipitation is similar, but differentfor the planktonic species. This suggests that A. beccarii calcifies nearthe equilibrium values at the full range of temperatures studied, andthat any vital effect on oxygen isotopic fractionation is minor.

Our results show that Mg incorporation and oxygen isotopicfractionation in A. beccarii are not significantly influenced by salinity,indicating that the species may well be used in the reconstruction ofpaleo environments. Slightly higher Mg/Ca values were found at asalinity of 26.1 PSU at a temperature of 24.0 °C. Possibly, thiscombination of temperature and salinity represents the optimalconditions for this species (Bradshaw, 1957). If this is indeed the case,the higher growth rates at these optimum conditions may havecaused an enhanced incorporation of trace elements.

In contrast to our data on shallow water benthic species, somerecent studies reported that the Mg/Ca of some planktonic species areaffected by salinity (e.g., Ferguson et al., 2008; Dueñas-Bohórquez etal., 2009). Other environmental conditions (e.g., pH, carbonate systemor calcite saturation state) are known to affect foraminiferal Mguptake (Lea et al., 1999; Elderfield et al., 2006; Rathmann andKuhnert, 2008). In nature, however, changes in salinity have acorresponding effect on alkalinity. If we assume that the alkalinity ofthe seawater which we used (with a salinity of 35 PSU) is 2338 μmol/kg (as extrapolated from Pacific Ocean values observed in waters nearthe islands of central Japan; Japan Oceanographic Data Center: http://www.jodc.go.jp/), our salinity differences reflect a difference in Ω of5.3 to 2.3 (CO2SYS, Lewis and Wallace, 1998). This change in calcitesaturation thus had no significant impact on Mg/Ca in A. beccarii, inagreement with other studies (Dueñas-Bohórquez et al., in prep).

Foraminifera intertidal to shallow subtidal environments such as A.beccarii must be resilient to changes in environmental perturbations.Particularly salinity in these environments varies due to fluctuations

in river input, rainfall, tidal movement and evaporation during lowtide, and human actions (e.g. changes in run-off due to changes inland-use). The low Mg content of their calcite may be an adaptationthat helps them resist dissolution due to changes in salinity and theassociated calcite saturation state. TheMg content of the calcite affectsits dissolution characteristics (Berner, 1975; Mucci and Morse, 1983),so that the occurrence of a low-Mg calcite in the intertidal speciesmaywell suggest an evolutionary history of this trait.

The weak response of the Mg-incorporation to temperature in A.beccarii supports this hypothesis. A higher Mg-incorporation in theforaminiferal calcite with increasing temperatures can be explainedby a combination of kinetic effects during precipitation (Morse et al.,2007), and the decreased ability to reduce the Mg/Ca in the internalcalcification pools at higher temperatures (Bentov and Erez, 2006).Since the kinetic impacts are similar for all species, the variousresponses of the Mg-incorporation to temperature are determined bydifferences in physiological controls on the composition of thecalcifying fluids. The low Mg/Ca in A. beccarii and its relatively slowincrease with temperature indicate that this species in particular hasevolved cellular tools to effectively remove Mg from its calcifyingfluid.

4.2. Paleoceanographic implications

Salinity does not significantly affect the Mg/Ca of A. beccarii(Fig. 4). Consequently, the Mg/Ca of this species can be used toreconstruct temperature in shallow marine environments, wheresalinity is highly variable. However, the effect of temperature on Mg/Ca in A. beccarii is relatively small at temperatures between 10 °C and27 °C (Fig. 2), and extending this calibration to higher temperatures infuture work may reduce the uncertainty in the correlation and hencethe temperature-reconstruction using the Mg/Ca of this species. Theseparate Mg/Ca- and δ18O-temperatures based on our results aregiven below:

Mg=Ca mmol=molð Þ = 0:575Te0:0531T ð1Þ

T = −4:49ðδ18Oforam−δ18OwaterÞ + 17:18 ð2Þ

Eqs. (1) and (2) can now be rearranged to produce:

T = 18:8T ln 1:74TMg=Ca mmol=molð Þ½ � ð6Þ

δ18Owater = δ18Oforam + 0:22T–3:83 ð7Þ

The δ18Owater should be corrected to VSMOW scale, since δ18Owater

is calculated using the VPDB scale. The correction value 0.20‰ isapplied to Eq. (7). Obtaining theMg/Ca and the δ18O of the calcite of A.beccarii could therefore be used to reconstruct both the temperatureand salinity of the shallow water environments. Recent analyticaladvances now make it possible to combine the measurements of Mg/Ca and δ18O on the same specimen (Reichart et al., 2003; Allison andAustin, 2003; Toyofuku and Kitazato, 2005; Allison and Austin, 2008).This allows the reconstruction of the short-term variability inshallow-water temperature and salinity, rather than the long-termaverage values.

In order to reliably use species that live in intertidal environments,however, the timing of the calcification in those species needs to beknown. It may be, for example, that A. beccarii in intertidal habitatsdoes not calcify at low tide, when evaporation increases the salinity ofinterstitial waters. Such preferences could bias the reconstruction ofthe average and the range of salinities naturally occurring.

119T. Toyofuku et al. / Marine Micropaleontology 78 (2011) 113–120

5. Summary

The Mg/Ca of the calcite of the cultured A. beccarii is correlatedexponentially to the temperature of ambient seawater over a range oftemperatures between 10 and 27 °C. In contrast, our data onspecimens grown at salinities between 18 and 33 PSU show thatMg-incorporation is not affected by salinity. For all experimentalconditions, the Mg/Ca in A. beccarii are among the lowest (1–4 mmol/mol) recorded in the foraminifera grown at those temperatures. Theextreme control on Mg-incorporation may be an adaptation to thelarge environmental variability in the intertidal areaswhere A. beccariicalcifies. The calcite with such a low Mg content is more resistant todissolution, so that this species may be able to maintain the integrityof its test at low saturation states, as commonly occuring in intertidalenvironments. The oxygen isotopic composition of the calcite of A.beccarii is close to the isotopic equilibrium with seawater. Theobtained relationships indicate that the combination of δ18Oforam andMg/Ca of A. beccarii can be applied to reconstruct δ18Owater as well asthe salinity of the paleo-seawater.

Acknowledgements

We appreciate the discussion of our data and manuscript withMasashi Tsuchiya and Hidetaka Nomaki. We thank Osamu Satoh andKayo Minoshima for the isotope measurements. Kayo Minoshima isthanked for kindly assisting with the isotope measurement at AIST.David Naafs and two anonymous reviewers are thanked forconstructive and useful comments. The fruitful discussion, Englishcollection and editing of Ellen Thomas is also acknowledged. Thisstudy was supported by KAKENHI-fund from Japan Society for thePromotion of Science (JSPS) (No. 22684027 to TT and No. 21244079 toHK).

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