Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 52–64

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Palaeogeography, Palaeoclimatology, Palaeoecology

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Sr/Ca and Mg/Ca ratios of ontogenetically old, long-lived bivalve shells (Arcticaislandica) and their function as paleotemperature proxies

Bernd R. Schöne a,⁎, Zengjie Zhang a,b, Pascal Radermacher a, Julien Thébault a,c, Dorrit E. Jacob a,Elizabeth V. Nunn a, Anne-France Maurer a

a Department of Applied and Analytical Paleontology and INCREMENTS Research Group, Earth System Science Research Center, Institute of Geosciences, University of Mainz,Johann-Joachim-Becher-Weg 21, 55128 Mainz, Germanyb Institute of Mineral Resources, Chinese Academy of Geological Sciences, Baiwanzhuang Road 26, Beijing 100037, Chinac Université de Bretagne Occidentale, Institut Universitaire Européen de la Mer, Laboratoire des Sciences de l'Environnement Marin (UMR6539 UBO/IRD/CNRS), Technopôle Brest-Iroise,Place Nicolas Copernic, 29280 Plouzané, France

⁎ Corresponding author.E-mail address: schoeneb@uni-mainz.de (B.R. Schön

0031-0182/$ – see front matter © 2010 Elsevier B.V. Adoi:10.1016/j.palaeo.2010.03.016

a b s t r a c t

a r t i c l e i n f o

Article history:Received 9 October 2009Received in revised form 8 March 2010Accepted 8 March 2010Available online 12 March 2010

Keywords:Metal-to-calcium ratioBivalve shellVital effectSea surface temperatureLongevity

The Sr/Ca and Mg/Ca ratios of many biogenic skeletons provide useful paleotemperature estimates. As yethowever, it has remained largely impossible to obtain such information from bivalve shells. In the presentstudy, metal-to-calcium values in the hinge plate (aragonite, outer shell layer) of four ontogenetically old (85to 374 year-old) specimens of the long-lived bivalve, Arctica islandica, were measured on a LA–ICP–MS. Theshells were collected alive in 1868, 1986 and 2003 from three different localities around Iceland. Withincreasing ontogenetic age and decreasing growth rate, a distinct trend toward increasing Sr/Ca (max.5.17 mmol/mol) andMg/Ca values (max. 0.89 mmol/mol) and greater variancewere observed. Three potentialexplanations for these trends include a reduced capacity for element selection due to cell ageing, changingmetabolism and/or a relative increase in the number of organic-rich (=Mg-rich) and organic-poor (=Sr-rich)shell portions through ontogeny. Partition coefficients however, remained far below 1, indicating thatphysiology exerted a strong control over the element partitioning between the shells and the ambient water.After mathematical elimination of these vital effects, residuals exhibited a highly significant negativecorrelation (e.g., age-detrended Sr/Ca data: R=−0.64, R2=0.41, pb0.0001, growth rate-detrended Mg/Cadata: R=−0.52, R2=0.27, pb0.0001)with sea surface temperature. These results are in good agreement withresults obtained from the precipitation of abiogenic aragonite. The results of the present study can help todevelop new techniques to extract environmental signals from the metal-to-calcium ratios of bivalve shells.

e).

1 It is worth notinduring abiogenic preffects are likely alwartificially grown carbiologically controllstill strongly debatedLiang, 1995; Watson

ll rights reserved.

© 2010 Elsevier B.V. All rights reserved.

g that thermodynamic equilibrium is difficult to maintain evenecipitation experiments (Gaetani and Cohen, 2006), i.e. kinetic

1. Introduction

Metal-to-calcium ratios (Me/Ca) of biogenic carbonates likelycontain a broad array of paleoenvironmental information. Withoutdoubt, strontium (Sr) andmagnesium (Mg) are themost studied traceelements. For example, past water temperatures have been recon-structed from Sr/Ca and Mg/Ca ratios of many different taxonomicgroups, such as brachiopods (Lowenstam, 1961; Powell et al., 2009),corals (Beck et al., 1992; Mitsuguchi et al., 1996; Goodkin et al., 2007),foraminifera (Nürnberg et al., 1996), ostracods (Corrège, 1993),echinoids (Pilkey and Hower, 1960), sclerosponges (Rosenheimet al., 2004), belemnites (McArthur et al., 2007), gastropods (Sosdianet al., 2006) and bivalves (Dodd, 1965, 1967; Hart and Blusztajn,1998). In general, temperature reconstructions based on Sr/Ca andMg/Ca ratios are considered superior to oxygen isotope based

reconstructions because, unlike δ18O values, the concentration ofthese elements in seawater above 10 PSU (Dodd and Crisp, 1982)remains relatively constant over time.

However, the empirically determined relationship between Me/Caratios of biogenic carbonates–especially bivalve shells–and environ-mental parameters often depart significantly from results obtained byabiogenic precipitation experiments1. At equilibrium, the distributioncoefficient

KDðMeÞ =MeCa

� �CaCO3

/ MeCa

� �solution

ð1Þ

ays present. In fact, the mechanisms for producing impurities inbonate crystals–much less complex systems because of the lack ofed reaction compartments, e.g., semipermeable membranes–are(e.g., Tiller et al., 1953; Albarede and Bottinga, 1972; Watson and, 1996, 2004).

53B.R. Schöne et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 52–64

for an element (Me) should be close to 1. However reported KD(Me)

values of bivalve shells, gastropods and otoliths deviate from thisvalue (e.g., Gillikin et al., 2005; Freitas et al., 2006). Furthermore, theSr/Ca and Mg/Ca ratios of artificial aragonite decrease with increasingtemperature. Likewise, tropical shallow-water corals show a negativecorrelation between Sr/Ca ratios and ambient temperature (Corrège,2006; however, Gaetani and Cohen, 2006, reported the opposite).Moreover, element partitioning in corals can be affected by variationsin precipitation rate (de Villiers et al., 1995; Cohen et al., 2001) andreportedly varies within a single colony (Alibert and McCulloch,1997). Such discrepancies are typically ascribed to “vital effects”(Urey et al., 1951) or “physiological effects” (Epstein et al., 1951), i.e.metabolic processes that modify the way in which environmentaldata are recorded in the geochemical composition of biogenic hardparts.

The empirical Me/Ca-environment relationships of many organ-isms seem to provide useful environmental proxies, but the number ofstudies using bivalve shells has remained disproportionately small. Infact, published results on the relationship between the Sr/Ca or Mg/Caratios of bivalve shells and calcification temperature are highlyambiguous. Shell Mg/Ca and Sr/Ca ratios vary significantly amongdifferent bivalve species and even among conspecific and contempo-raneous specimens from one locality (Gillikin et al., 2005; Lorrain etal., 2005; Freitas et al., 2008). Dodd (1965) reported an inverserelationship between temperature and Sr/Ca ratios in the nacreousshell layer (aragonite) of Mytilus edulis and so did Surge and Walker(2006) for the middle layer (aragonite) of Mercenaria campechiensis,while Gillikin et al. (2005) observed the opposite in Saxidomusgigantea (aragonite). Various authors also noted a correlation of theMg and Sr content with growth rate (Swan, 1956; Takesue and vanGeen, 2004; Gillikin et al., 2005; Lorrain et al., 2005) or ontogeneticage (Palacios et al., 1994; Freitas et al., 2005). Why are the Me/Caratios of bivalves more difficult to interpret than those of other taxa?Is the elemental composition of bivalves more severely affected by“vital effects” than that of other taxa?

The present study is the first to measure skeletal Me/Ca ratios ofontogenetically old, very-long-lived bivalves, in this case Arcticaislandica. The studied bivalves lived at different localities aroundIceland and during different time intervals of the past 500 years. Wepresent a potential model for reconstructing environmental signals

Fig. 1.Map showing sampling localities around Iceland. F=near Flatey Island, N Iceland, 1 sTable 1 for further locality details.

from Me/Ca records. This new approach makes use of a combinedanalysis of growth rates (sclerochronology) together with theelemental composition (laser ablation–inductively coupled plasma–mass spectrometry, LA–ICP–MS data) of the shells. We describe amethod for identifying and removing physiological (“vital”) effectsfrom Mg/Ca and Sr/Ca ratios of the shells, hence enabling recovery ofinformation on calcification temperature. Our approach may helppaleoclimatologists to develop techniques for a precise reconstructionof environmental data recorded in the Me/Ca ratios of bivalve shells.

2. Material and methods

Four specimens of Arctica islandicawere used in the present study.They were collected alive by dredging from ca. 30 m of water deptharound Iceland (Fig. 1; Table 1). Two specimens (Möller-A5R andMöller-A9L) lived contemporaneously at the same locality andallowed us to identify the degree of similarity in the Me/Ca ratios(Table 2). In order to distinguish environmental and ontogenetictrends, two additional specimens were used that lived at differenttime intervals during the past five centuries (Table 1).

Soft tissues were removed immediately after collection. One valveof each specimen was selected and mounted on a plexiglass cube. Aquick-drying epoxy resin (JB KWIK Weld) was applied to the valvesurface along the axis of maximum growth. On that axis, two ca.three-millimeter thick sections were cut from each valve with aBuehler Isomet low-speed saw. Then, the sections were mounted onglass slides with the mirroring sides facing up, ground on glass plateswith 800 and 1200 grit SiC powder, and finally polished on a BuehlerG-cloth with 1 µm Al2O3 powder. All samples were ultrasonicallyrinsed in Milli-Q (18.2 MΩ cm) water.

2.1. LA–ICP–MS analyses

One polished cross-section of each valve was used for LA–ICP–MSanalysis. Mg (measured as 24Mg) and Sr (as 88Sr) concentrations weredetermined in the hinge portion of the shells, where a condensedannual growth increment record is preserved (Fig. 2). This portion ofthe hinge plate was precipitated by the outer extrapallial fluid andbelongs to the outer shell layer (terminology follows Ropes et al.,1984). Like the outer shell layer at the ventral margin, the analyzed

hell; L=near Langanes peninsula, NE Iceland, 2 shells; E=East Iceland, 1 shell. Refer to

Table 1List of Arctica islandica shells used in the present study and details on LA–ICP–MS measurements. Number of LA sample swaths (#swaths) does not include overlapping portions ofline scans. LA=laser ablation.

Shell ID Locality Life span Valve LA–ICP–MS

# line scans # swaths Time coverage(yr AD)

M071868-A3R E Iceland; ca. N65°, W013° 1494–1868 Right 11 2999 1500–1860HM-Fla86-A1L near Flatey Island, N Iceland; ca. N66°11′, W017°50′ 1761–1986 Left 15 4013 1761–1970Möller-A5R Near Langanes, NE Iceland; N66°16′, W014°55.20′ 1897–26 Nov. 2003 Right 13 3141 1897–1998Möller-A9L 1918–26 Nov. 2003 Left 10 1773 1923–2003

54 B.R. Schöne et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 52–64

portion of the hinge plate was not subject to repeated dissolution andCaCO3 deposition (Crenshaw, 1990) as is the case for the inner shelllayer. Therefore the studied section represents a faithful record of thelife history of the animal (e.g., Butler et al., 2009) consisting of annualgrowth increments delimited by growth lines (Fig. 2).

Ablation was achieved with a NewWave Research UP-213 Nd:YAGlaser ablation system using a pulse rate of 4–10 Hz, a pulse energy of∼0.3 mJ per spot, and ca. 50 µm spot diameters (in “spot”mode) withAr as the ablation gas. Elemental analyses were performed on anAgilent 7500ce quadrupole ICP–MS coupled to the UP-213 platform(one point per peak and 10 ms dwell time) following the methodsdescribed in Jacob (2006). NIST SRM 612 was used as the externalstandard (Pearce et al., 1997), and the U.S. Geological Survey glassstandard BCR-2G was measured to monitor accuracy and instrumen-tal drift. 43Ca was used as the internal standard (38 wt.% measured byICP–OES). Detection limits generally ranged between 1 and 500 ppbfor these elements, and relative standard deviations (based onrepeated measurements of the external standard) were 7.2% for Mgand 7.8% for Sr. In order to produce trace element time-series, thesingle-line scan method for ablation was applied. In this method, thelaser is moved over the sample along a straight line at a scan speed of10 µm per second while continuously ablating the sample surface.Data were integrated over time slices of 0.323 s. Individual ablationlines (taken perpendicular to the axis of growth; Fig. 2) measuredbetween 765 and 1470 µm in length. The line scans were taken so thattheir ends overlapped by several 100 µm (Fig. 2). Later, the line scanswere stitched together to obtain a single time-series for eachspecimen. The total number of time slices (excluding overlappingportions) amounted to 11,926 (Table 1).

2.2. Sclerochronological analyses

In order to temporally align the Me/Ca record and to compare thedata with shell growth rates and ontogenetic age, the remainingpolished cross-section of each valve was immersed in Mutvei'ssolution (Schöne et al., 2005a) under constant stirring for 25 min at37–40 °C. Immediately afterward, the etched sections were rinsed indemineralized water and allowed to air-dry. Mutvei's solution(0.5 vol.% acetic acid, 12.5 vol.% glutar[di]aldehyde, 5 wt.‰ alcianblue powder) produces a three-dimensional relief consisting of ridges(, i.e. organic-rich annual growth lines which are strongly stained byalcian blue,) and valleys (, i.e. deeply etched annual growthincrements between adjacent growth lines). Annual growth incre-

Table 2List of basic shell dimensions and metal-to-calcium ratios of Arctica islandica shells used in

Shell ID Shell height(mm)

Shell age(yr)

Average ±1σ//minimum//ma

Sr/Ca(mmol/mol)

M071868-A3R 82.98 374 1.48±0.50//0.73//3.86HM-Fla86-A1L 89.68 225 1.53±0.49//0.71//5.17Möller-A5R 83.09 106 1.02±0.22//0.59//2.34Möller-A9L 79.68 85 1.06±0.33//0.54//2.72

ment widths were determined on digitized images (Nikon Coolpix995 digital camera mounted to an Olympus SZX16 stereomicroscope)of the etched thick-sections of the hinge portions to the nearest 2 µmusing the image processing software Panopea (© Peinl and Schöne).

2.3. Instrumental data

Because Sr/Ca and Mg/Ca ratios function as paleotemperatureproxies in many organisms (e.g., Beck et al., 1992), Me/Ca data of theshells were compared to instrumental sea surface temperature duringthe growing season of Arctica islandica, i.e. November to August(Schöne et al., 2005b; Schöne, 2008). NOAA_ERSST_V3 data (Xueet al., 2003; Smith et al., 2007) were obtained from NOAA/OAR/ESRLPSD, Boulder, Colorado, USA, from their Web site at http://www.cdc.noaa.gov. For direct comparison with Me/Ca time-series, we haveextrapolated themonthly SST time-series over a larger area (62–68°N,334–352°E), because (1) no data exists for the locality where thebivalves lived and (2) SST data may not necessarily be representativeof temperature in 30 m water depth. Average Sr/Ca and Mg/Ca valuesfor seawater were taken from Elderfield (2006).

2.4. Data analysis

Wecompared Sr/Ca andMg/Ca groups of all four shells. TheWilcoxonMann–Whitney test was used to test whether the group means aresignificantly different from each other.We used this non-parametric testbecause it does not require the assumption that the population isnormally distributed. The null hypothesis (i.e. no difference between themedians) is rejected for p-values smaller than 0.05.

3. Results

3.1. Habitat-specific Sr/Ca and Mg/Ca ratios

The average, minimum and maximum Sr/Ca and Mg/Ca ratios(intra-annual data) and corresponding KD(Sr)

and KD(Mg)values

varied considerably among specimens from different localities (allp-valuesb0.0001), but Sr/Ca ratios were statistically indistinguishablein the two shells from NE Iceland (Table 2; t-statistics, p=0.50). Forexample, average Sr/Ca ratios of shells from E Iceland (M071868-A3R)and N Iceland (HM-Fla86-A1L) were about 0.50 mmol/mol higherthan specimens from NE Iceland. Mg/Ca ratios in the shell from E

the present study. σ=standard deviation.

ximum

Mg/Ca(mmol/mol)

KD(Sr)KD(Mg)

0.42±0.10//0.14//0.86 0.17±0.06//0.08//0.43 0.08±0.02//0.03//0.170.30±0.09//0.15//0.89 0.17±0.06//0.08//0.58 0.06±0.02//0.03//0.170.30±0.13//0.14//0.85 0.11±0.02//0.07//0.26 0.06±0.03//0.03//0.160.26±0.11//0.12//0.79 0.12±0.04//0.06//0.31 0.05±0.02//0.02//0.15

Fig. 2. Cross-sectioned shell of Arctica islandica revealing major shell structures (upper panel) and annual growth patterns (middle panel). The hinge plate (lower panel) wasanalyzed for Sr, Mg and Ca by means of LA–ICP–MS (line scan method). Open circles denote position where pallial line meets internal surface (i.e. position of pallial muscleattachment).

55B.R. Schöne et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 52–64

Iceland differed significantly (0.42 mmol/mol) from values deter-mined in the remaining three shells (ca. 0.30 mmol/mol).

3.2. Sr/Ca and Mg/Ca trends related to ontogenetic age and shell size

Over their lifetime, all four specimens of Arctica islandica showed ageneral trend toward increasing Sr/Ca andMg/Ca ratios (Fig. 3). This isremarkable because all specimens lived during different time intervalsand three of the four specimens dwelled at different localities aroundIceland (Table 1). Aside from this general trend however, individualdifferences occurred particularly during the early years of life. Inspecimen M071868-A3R, annually averaged Mg/Ca values increasedrapidly from 0.2 to 0.5 mmol/mol (KD(Mg)

=0.04 to 0.10) early inontogeny, but decreased toward ca. 0.4 mmol/mol (KD(Mg)

=0.08)between LA sample swath 400 and 2000 (Fig. 3A). Thereafter, valuesincreased again late in the adult stage of life (Mg/Ca=0.6 mmol/mol,KD(Mg)

=0.12). Sr/Ca values in this shell increased gradually from ca. 1.2to 2.5 mmol/mol (KD(Sr)

=0.13 to 0.28). In contrast, until LA sampleswath 2500, annual Sr/Ca and Mg/Ca values of HM-Fla86-A1L from NIceland were fluctuating around 1.4 and 0.3 mmol/mol (KD(Sr)

=0.16;KD(Mg)

=0.06) and then gradually increased to attain values of 2.5 and0.5 mmol/mol (KD(Sr)

=0.28; KD(Mg)=0.10), respectively (Fig. 3B).

However, in the two specimens from NE Iceland, Möller-A5R and

Möller-A9L (Fig. 3C and D), annual Sr/Ca and Mg/Ca ratios declinedduring early ontogeny before reaching a plateau at about LA sampleswath 500. Me/Ca values decreased from ca. 1.2 and 0.4 mmol/mol(KD(Sr)

=0.13; KD(Mg)=0.08) to 0.9 and 0.2 mmol/mol respectively

(KD(Sr)=0.10; KD(Mg)

=0.04) early in ontogeny. Values of 2.0 and ca.0.8 mmol/mol respectively (KD(Sr)

=0.22; KD(Mg)=0.15) were then

attained near the end of the specimens' lives. Furthermore, whileMe/Ca values typically changed gradually, Mg/Ca ratios of specimenMöller-A9L showed an abrupt increase at ca. LA sample swath 1500(Fig. 3D). In addition, there was an apparent tendency toward greaterMe/Ca variability from one laser sample swath to the next withincreasing ontogenetic age in all four shells (Fig. 3).

When arranged by ontogenetic age, annual Me/Ca values (arith-metically averaged) were best described by linear regression lines(least-squares method; Fig. 4). Due to the abruptly changing Me/Cavalues in specimenMöller-A9L (Fig. 4D), two separate regression lineswere computed. Note that annual increment widths of laterontogenetic years were sometimes smaller than the LA samplediameter (50 µm). Therefore, time averaging in these portionsincreased significantly which accounts for the staircase-like appear-ance at the end of the chronologies (towards older shell portions).

Although the number of shells was too low to obtain statisticallymeaningful results (all p-values were larger than 0.05), older shells

Fig. 3. Sr/Ca and Mg/Ca ratios in shells of Arctica islandica from E Iceland (A=specimen M071868-A3R), N Iceland (B=specimen HM-Fla86-A1L) and NE Iceland (C=specimenMöller-A5R; D=specimen Möller-A9L). Irrespective of the locality and the time interval during which the shells lived, all four shells show a general trend toward increasing Sr/Caand Mg/Ca values. However, note deviations from this general trend in juvenile portions (e.g., C and D versus A and B). All four shells also show an ontogenetic increase in Me/Cavariability. LA=laser ablation.

56 B.R. Schöne et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 52–64

tended to have higher overall Mg/Ca and Sr/Ca values (Table 2).However, neither ratio seemed to be strongly linked to shell height(size; Table 3). It should be emphasized that the oldest bivalves didnot necessarily grow the biggest shells. For example, Möller-A5R was“only” 106 years old, but had a similar sized shell to the 374 year-oldspecimen from E Iceland (Table 2).

3.3. Sr/Ca and Mg/Ca trends related to growth rate

A strong non-linear, inverse correlation was found betweenMe/Caratios and annual increment widths below 30 to 200 µm (Fig. 5). Therelationship between the two variables was fitted with non-flexiblecubic splines, so that the resulting curves were as smooth as possible.Slower shell growth was associated with higher Sr/Ca and Mg/Cavalues. However, when annual increment widths (measured in thehinge plate) were above 30 µm in the specimen from E Iceland(Fig. 5A), 100 µm in the shell fromN Iceland (Fig. 5B) or 200 µm in thespecimens from NE Iceland (Fig. 5C and D), the correlation betweenshell growth and Me/Ca ratios was much less uniform among the fourspecimens. Above these thresholds, some shells showed slightlypositive linear relationships between growth and Me/Ca ratios

(Fig. 5B, C), others negative relationships (Fig. 5D). In the shell fromN Iceland, however, Sr/Ca ratios decreased with increasing growthrate, whereas Mg/Ca values increased (Fig. 5A). In general, thecorrelation between shell growth and Me/Ca ratios was stronger inslow-growingmature and gerontic shell portions than in fast-growingjuvenile portions.

3.4. Sr/Ca and Mg/Ca data related to sea surface temperature

In Fig. 6 annual Sr/Ca and Mg/Ca time-series are arranged bycalendar year. As expected from the strong correlation with age andshell growth, the Me/Ca chronologies do not correlate with each otheror with sea surface temperature. The Me/Ca time-series aredominated by ontogenetic trends.

4. Discussion

The results of this study clearly indicate that vital effects(ontogenetic age, growth rate; the latter is influenced by the habitat,e.g., food availability) exert a major control over the Sr/Ca and Mg/Caratios of Arctica islandica shells. Element partitioning between the

Fig. 4. Annually averaged Sr/Ca and Mg/Ca ratios in shells of Arctica islandica plotted versus ontogenetic age. With increasing ontogenetic age, all four shells show a distinct trendtoward higher Sr/Ca and Mg/Ca values which is best described by linear regression lines. A=M071868-A3R; B=HM-Fla86-A1L; C=Möller-A5R; D=Möller-A9L.

Table 3Linear regression analysis of shell age and shell size (height) versus metal-to-calciumratios for combined data from all four shells (R2, p). All correlations were positive;therefore only R2 values are provided.

57B.R. Schöne et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 52–64

shells and the ambient water does not occur in equilibrium2. Ingeneral, these findings are in agreement with the majority of otherstudied bivalve species (e.g., Gillikin et al., 2005; Lorrain et al., 2005;Freitas et al., 2005, 2006, 2009; Elliot et al., 2009).

4.1. Reasons for ontogenetic Sr/Ca and Mg/Ca trends?

While the KD(Sr)and KD(Mg)

values of synthetic aragonite areindependent of precipitation rate (e.g., Mucci et al., 1989; Zhong andMucci, 1989), Sr/Ca andMg/Ca ratios of Arctica islandica shells increasedwith decreasing growth rates (Fig. 5) and increasing ontogenetic age(Fig. 4). However, skeletal Sr/Ca and Mg/Ca ratios remained far belowthat of the ambientwater (Mg/Ca: 5.2 mmol/mol; Sr/Ca: 8.9 mmol/mol;Elderfield, 2006) and, accordingly, KD(Sr)

and KD(Mg)values remained well

below 1 (Table 2). Can the observed trends be explained by age-relatedchanges of the ion discrimination systems of the mantle epithelium?

Functional structures in the semipermeable membrane of themantle epithelium are believed to select Ca2+ against other ions and,thus, generate an elemental concentration in the calcifying fluid that

2 Interestingly, such physiological controls do not affect shell δ18O and δ13C values ofA. islandica (Schöne et al., 2005b).

differs from the ambient environment (Wheeler, 1992). Currently,there are two major models that explain how the high Ca2+ demandof the calcification process can be satisfied, while maintaining asuitable, alkaline reaction environment and keeping the concentra-tion of other metals in the calcifying fluid low: (1)an energy-consuming Ca2+ pumpmediated by Ca2+-ATPase enzymes (Wheeler,1992; Cohen and McConnaughey, 2003) and (2)a passive transportthrough ion channels (Gattuso et al., 1999; Carré et al., 2006).

However, both models fail to explain the observed ontogenetic Me/Ca trends in Arctica islandica. For every calcium ion that is pumped intothe calcifying fluid, two protons are pumped away by the Ca2+-ATPaseenzymes. This process elevates the pH and lowers theMg/Ca ratio in thecalcifyingfluid, because of the relative increase in Ca (and Sr, see below)ions. Due to its smaller size and differing electrochemical characteristics,

R2, p (Sr/Ca) R2, p (Mg/Ca)

Ontogenetic age 0.72, 0.15 0.87, 0.07Shell height 0.49, 0.30 0.01, 0.93

Fig. 5. Annually averaged Sr/Ca andMg/Ca ratios in shells of Arctica islandica plotted versus annual increment width.With decreasing growth rate, all four shells show a distinct trendtoward higher Sr/Ca and Mg/Ca values. These trends are best described by non-flexible cubic splines. Note that metal-to-calcium ratios can be positively or negatively correlated toannual increment width in fast-growing shell portions. In addition, the correlation is nearly linear in such shell portions. The point at which the relationship becomes nearly linear(indicated by the vertical dashed lines) varies among shells: 30 µm in A, 100 µm in B and 200 µm in C and D.

58 B.R. Schöne et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 52–64

Mg is therefore effectively excluded from the site of calcification.However, Sr2+ and Ca2+ are nearly identical in size and have similaratomic properties. Therefore, the Ca2+-ATPase allows Sr2+ to enter thecalcification fluid along with Ca2+, so that the Sr/Ca ratios of thebiomineral should be nearly identical to that of the ambient water(Gaetani andCohen, 2006). This is clearly not the case inA.islandica. Likethe ion-pump model, the presence of Ca2+ and H+ ion channels isbelieved to guarantee a constant supply of calcium and removal of theprotons that build up during calcification. Due to similar bindingaffinities to Ca2+, Sr2+ is expected to reach the calcification sites thoughthe Ca2+ ion channels. With increasing biomineralization rate, higheramounts of Ca2+ and Sr2+ are expected to pass the semipermeablemembrane. Following this hypothesis, the Sr/Ca ratio wouldincrease with increasing growth rate (Carré et al., 2006). However, theopposite trend was found for A.islandica. We suggest three alternativeexplanations for the positive Me/Ca trends in A.islandica throughontogeny.

(1) Cell ageing (e.g., Abele et al., 2008) may cause the transpor-tation mechanisms of the mantle epithelium to loose theircapability to properly select Ca2+ against other ions as thebivalve becomes older and growsmore slowly. As a result more

Mg and Sr can reach the calcification sites when bivalves areolder and therefore Mg/Ca and Sr/Ca ratios increase.

(2) Metabolism and biomineralization processes change through-out ontogeny and modify the amount of impurities in newlyforming biominerals. Support for this assumption comes fromontogenetic changes in the amount and composition of aminoacids in Arctica islandica shell (Goodfriend and Weidman,2001). The total amount of amino acids and the relativeabundance of less acidic, structural proteins increase withontogenetic age. During youth, however, acidic amino acidsprevail.

(3) Relative increase of organic-rich and organic-poor shell por-tions through ontogeny. With increasing ontogenetic age andslowing shell growth, annual increment widths becomenarrower and the number of annual growth lines per shellunit increases. While growth lines are enriched in water-insoluble organic matrices and organic-boundMg (Foster et al.,2008; Schöne et al., 2010), the shell portions immediately afterthese lines are depleted in organics and rich in Sr (Schöne et al.,2010). When measured in situ for example, by means of LA–ICP–MS, Mg values tend to be three times higher at the growthlines, while distinct Sr peaks occur immediately adjacent to the

Fig. 6. Annual Sr/Ca (A) and Mg/Ca (B) time-series of Arctica islandica shells plotted against calendar year. Note that no agreement exists between metal-to-calcium ratios and seasurface temperature (SST, grey curve). Due to ontogenetic trends (Figs. 4 and 5), the metal-to-calcium chronologies of contemporary specimens have little in common.

59B.R. Schöne et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 52–64

growth lines (Schöne et al., 2010). It should be noted, however,that in situ measurements are not sensitive to elementspeciation, i.e. lattice-bound and organic-bound elements aredetected (Schöne et al., 2010). The increased density oforganic-rich and organic-poor shell portions in older speci-mens would result in an overall enrichment of Mg and Sr andcould also account for the observed larger Mg and Sr variabilitybetween individual laser sample swaths in older shell portions.

4.2. Can Sr/Ca and Mg/Ca ratios still be used as paleothermometers?

Only a few previous studies have suggested that the Sr/Ca or Mg/Ca ratios of bivalve shells can be used as proxies for ambient watertemperature during calcification. According to Dodd (1965), Sr/Caratios of Saxidomus gigantea are negatively correlated to temperature.The same trend was observed for Spisula solidissima by Stecher et al.(1996). However, the same authors also found the opposite to be truefor Mercenaria mercenaria (Stecher et al., 1996). In addition, Hart andBlusztajn (1998) claimed that Sr/Ca ratios of Arctica islandica arepositively correlated to temperature. However, these authors did notprovide any supportive data and only reported the finding in theappendix of a paper in which the Sr/Ca-paleothermometer wasapplied to the deep-sea bivalve, Calyptogena magnifica.

Themajority of previous studies have concluded that the Sr/Ca andMg/Ca ratios of bivalves do not reflect water temperatures, but merelygrowth rates or other physiological parameters. This conclusion is wellsupported by the findings herein (Fig. 6). Some authors have assumedan indirect correlation between calcification temperatures and shellSr/Ca and Mg/Ca values, because metabolism is influenced by theambient environment (e.g., Gillikin et al., 2005; Freitas et al., 2006;Elliot et al., 2009). However, no previous approach has tested whetherenvironmental variables can be reconstructed fromMe/Ca ratios if thevital effects, including the heteroscedascity (high correlation betweenmean and variance), are mathematically eliminated.

The method applied here is modified from a technique routinelyused by dendrochronologists (Cook and Kairiukstis, 1990) and bivalvesclerochronologists (Marchitto et al., 2000; Schöne et al., 2003), i.e.detrending and standardization. The regression curves included inFigs. 4 and 5were used to estimate (or predict) the ontogenetic age- andgrowth-rate-related changes in Me/Ca ratios. For detrending, indiceswere calculated by dividing measured by predicted Me/Ca values.Then, the indexed Me/Ca data were standardized by subtracting themean and dividing by the standard deviation of the indexed Me/Cadata. By doing this, we obtained age-detrended and growth rate-detrended, standardized Sr/Ca (Sr/CaSI(age), Sr/CaSI(growth)) and Mg/Ca (Mg/CaSI(age), Mg/CaSI(growth)) chronologies, i.e. dimensionless mea-sures of Me/Ca ratios (unit: standard deviation). Two sets of average

60 B.R. Schöne et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 52–64

Fig. 8. Sea surface temperature (grey curve;NOAA_ERSST_V3; averaged over larger area stretching from62°N, 334 °C to 68°N, 352°E) indirect comparisonwith detrended and standardizedSr/Ca and Mg/Ca time-series (black curves) of Arctica islandica shells. (A) shows a multi-regional, age-detrended Sr/Ca chronology including three specimens from N and NE Iceland(equivalent to data depicted in Fig. 7A), while (B) is a growth rate-detrendedMg/Ca chronology including two specimens from the same locality (NE Iceland) (equivalent to data shown inFig. 7H).

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chronologieswere computed fromdata of at least two contemporaneousshells, i.e. one multi-regional chronology (N and NE Iceland: HM-Fla86-A1R, Möller-A5R, Möller-A9L) and one NE Iceland chronology (Möller-A5R, Möller-A9L). Large-scale temperature effects on trace metalimpurities in the shellswere estimated fromspatial correlationdiagrams(Sr/CaSI and Mg/CaSI versus SST) for growing season (November toAugust) averages using the KMNI Explorer (http://www.climexp.knmi.nl) and NOAA_ERSST_V3 data (Fig. 7). Furthermore, two selectedrelationships (Fig. 7A and H) were plotted as time-series (Fig. 8).

All Sr/CaSI and Mg/CaSI time-series exhibited a statisticallysignificant negative correlation with calcification temperature duringthe growing period (Figs. 7 and 8). These findings compare well withinorganic precipitation experiments. Mg/Ca and Sr/Ca ratios ofsynthetic aragonite also show a negative relationship with temper-ature (Kinsman and Holland, 1969; Gaetani and Cohen, 2006).Typically, age-detrended time-series revealed stronger relationshipswith SST (up to 41% explained variability; Figs. 7A–D, 8A) than growthrate-detrended data (up to 27% explained variability; Figs. 7E–H, 8B.This suggests that ageing has a stronger effect on the amount of

Fig. 7. Spatial correlation charts between detrended and standardized Sr/Ca and Mg/Ca ratrepresent averages from November of the previous year to August of the current year, i.e. theincluded in the correlation analysis: A–D=specimens HM-Fla86-A1R from N Iceland and MIceland. Age-detrended (A, B, E, F) metal-to-calcium ratios exhibited a stronger negative coKMNI explorer (http://www.climexp.knmi.nl).

impurities in the shells than growth rate, i.e. physiological effects havea stronger effect than kinetic effects (here: calcification rate).

Although the trend elimination did not result in 100% explainedvariability, the correspondence between SST and detrended andstandardized Mg/Ca or Sr/Ca data is intriguing (Fig. 8). The remainingunexplained variability may be partly due to the low temporalresolution in slower growing shell portions (LA–ICP–MS swath width:50 µm, annual increment widths in older shell portions were asnarrow as 5 µm). Furthermore, instrumental temperature records didnot come from exactly the same locality as where the shells lived, butwere averaged over a larger area.

4.3. Are vital effects species-specific or related to ontogenetic age?

Although vital effects reportedly control the elemental chemistryof most bivalves, different species seem to exhibit diametricallyopposed relationships between Me/Ca ratios and growth rate orontogenetic age, irrespective of the CaCO3 polymorph. For example,the Sr/Ca ratios of some aragonitic (Protothaca staminea: Takesue and

ios of Arctica islandica shells and sea surface temperature (NOAA_ERSST_V3). SST dataduration of the growing season of the ocean quahog. Red circles denote the specimens

öller-A5R and Möller-A9L from NE Iceland; E–H=Möller-A5R and Möller-A9L from NErrelation than growth-rate-detrended data (C, D, G, H). Diagrams were made with the

62 B.R. Schöne et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 52–64

van Geen, 2004; Saxidomus gigantea: Gillikin et al., 2005; Mesodesmadonacium and Chione subrugosa: Carré et al., 2006) and calciticbivalves (Pecten maximus: Lorrain et al., 2005) are positivelycorrelated with growth rate and negatively correlated with ontoge-netic age. Likewise, Klein et al. (1996) found decreasing Sr/Ca ratios inthe slower growing (calcitic) shell portions of Mytilus trossulus.Conversely, the calcitic portion of Pinna nobilis (Freitas et al., 2005)showed an inverse relationship between Sr/Ca and growth rate, whilethe Sr/Ca ratios of Tridacna gigas (aragonitic; Elliot et al., 2009) andMercenaria mercenaria (Gillikin et al., 2005) did not vary with growthrate or age at all. Mg/Ca ratios do not have not provide coherentrelationships with ontogeny either. In T.gigas, Elliot et al. (2009)observed a negative correlation between Mg/Ca ratios and growthrate. Yet no such relationship seems to exist in Mytilus edulis andPecten maximus (calcitic shell portions; Freitas et al., 2008). As such,are there species-specific vital effects?

Scrutiny of the published data admits alternative interpretations forthe observed incoherent trends between Me/Ca ratios and ontogenyamong different species. Notably, published data on element chemistryand its relation to growth rate or ontogenetic age were exclusivelyobtained from relatively short-lived bivalves (e.g., Freitas et al., 2005;Gillikin et al., 2005; Lorrain et al., 2005; Surge andWalker, 2006) or fromthe juvenile portions of short-lived (Klein et al., 1996; Pearce andMann,2006) or long-lived species (Elliot et al., 2009). Howwas it assured thatthe alleged ontogenetic or growth rate-related trends observed over atime interval of five, ten or twenty yearswere not actually influenced byenvironmental factors, when these remained unexamined and perhapsfluctuated on decadal time scales? Furthermore, it may be that elementpartitioning during youth is subject to stronger biological influencesthan during adulthood. It should be kept in mind that bivalves need toquickly escape the predation window and they therefore rapidly growbig shells during the first few years of their life in order to reachreproductive size (e.g., Seed and Brown, 1978). This ontogenetic growthpattern is genetically predetermined, affects evolutionary success andmay have a significant influence on metabolic rates and, therefore, onelement partitioning between the shell and the ambient water.

According to the results of the present study, Mg/Ca and Sr/Ca ratiosof the juvenile portions of Arctica islandica shells can differ significantlyamong specimens that lived at different time intervals during the pastfive centuries (and in different environmental settings). At least in fast-growing shell portions, no consistent species-specific Me/Ca trendsrelated to ontogeny seem to exist (Fig. 5). Such trends seem to developonly in the later stages of life when growth was slower. It is alsointeresting to note that the correlation between shell growth rate andMg/Ca or Sr/Ca values only occurs at growth rates below ca. 30–200 µm(hinge plate), i.e during mature and gerontic stages of life. At fastergrowth rates, Me/Ca ratios are only weakly correlated to growth rate, ifat all. Some specimens showed a slight positive (linear) correlation,others a negative correlation. Apparently, the influence of vital effectschanges through ontogeny.

Further studies are certainly required in order to analyze how theamount of impurities in biominerals is controlled by physiologicalprocesses and also, how their effectsmay change during the lifetime ofthe organism. What are the roles of proteins, metabolism andphysiological ageing? Verification of the existence of ontogenetictrends in short-lived bivalves requires analyses of multiple specimensof the same species that lived during different time intervals and/or indifferent habitats. By using this approach, the effects of decadal climatefluctuations and local environmental variables that are likely to affectthe shell growth and the Me/Ca content of the shells can be excluded.

4.4. Why are long-lived species more suitable for paleoclimatereconstructions?

Despite the undeniably great value of short-lived bivalves forpaleoseasonality studies, such shells can hardly provide paleoclimate

data. By definition, “climate” represents an average of environmentalvariability over at least 30 years. Therefore, bivalve sclerochronology-based paleoclimate studies require long-lived species (and oldindividuals of these). As yet, however, element data from long-livedbivalve shells have rarely been reported and, moreover, such studieshave typically relied merely on the youth portions of such specimens(Hart and Blusztajn, 1998 and Toland et al., 2000: Arctica islandica;Elliot et al., 2009: Tridacna gigas; Purton et al., 1999 and Purton-Hildebrand et al., 2001: Venericarda planicosta). Recently, Wisshaket al. (2009) presented element maps of a deep-sea oyster,Neopycnodonte zibrowii, which may have attained a lifespan of ca.500 years. However, due to the absence of verified annual growthpatterns, the data were not aligned by ontogenetic age and age-related trends remained unmentioned. The present study closes thisgap of knowledge by measuring metal-to-calcium ratios across theentire lifespan of a long-lived species.

5. Summary and conclusions

In this study, the element chemistry in the hinge portion ofontogenetically old shells of Arctica islandica, collected alive fromdifferent localities around Iceland, was analyzed. Sr/Ca and Mg/Caratios are strongly regulated by physiological effects. Values increasewith ontogenetic age and decreasing growth rates. However, theseontogenetic trends can be estimated and mathematically eliminatedby fitting regression lines to the Me/Ca time-series. Over 40% of thevariability of the detrended and standardized Sr/Ca and Mg/Ca ratiosis explained by calcification temperature. In agreement with syntheticaragonite, Me/Ca ratios of A. islandica are inversely proportional tocalcification temperature.

The approach presented here may open up new perspectives inusing the Me/Ca ratios of bivalve shells as environmental proxies.However, our approach needs to be tested in other long-livedbivalves. Furthermore, the biochemical pathway of trace and minorelements, changes through ontogeny, and changes in different crystalfabrics, deserve further investigation.

Acknowledgements

Arctica islandica specimen M071868-A3R was provided by Wolf-gang Dreyer (Zoological Museum of the University of Kiel, Germany;Möbius collection), specimen HM-Fla86-A1 by Harry Mutvei (Muse-um of Natural History, Stockholm, Sweden) and Möller-A5R and A9Lby Alda Möller (Ministry of Fisheries and Agriculture, Reykjavìk,Iceland). NOAA_ERSST_V3 data were provided by the NOAA/OAR/ESRL PSD, Boulder, Colorado, USA, from their Web site at http://www.cdc.noaa.gov. The KMNI Explorer (http://www.climexp.knmi.nl) wasused for the preparation of spatial correlation charts. This study hasbeen made possible by a German Research Foundation (DFG) grant(to BRS: SCHO 793/4). A PhD scholarship to Zengjie Zhang by theGerman Academic Exchange Service (DAAD) is kindly acknowledged.Julien Thébault gratefully acknowledges the Alexander von HumboldtFoundation (Bonn, Germany) for the award of a Research Fellowshipfor Postdoctoral Researchers. Comments made by the two reviewers,Donna Surge and Andy Johnson are kindly acknowledged. We thankthe guest-editors for their hard work editing this special issue. This isGeocycles publication number 636.

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