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Mg in aragonitic bivalve shells: Seasonal variations and mode of incorporation in Arctica islandica
Chemical Geology 254 (2008) 113–119
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Chemical Geology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / c h e m g e o
Mg in aragonitic bivalve shells: Seasonal variations and mode of incorporation in Arctica islandica L.C. Foster a,⁎, A.A. Finch a, N. Allison a, C. Andersson b, L.J. Clarke c a b c
School of Geography and Geosciences, University of St. Andrews, Irvine Building, St. Andrews, KY16 9AL, UK Bjerknes Centre for Climate Research, Allegaten 55, 5007, Bergen, Norway School of Ocean Sciences, College of Natural Sciences, Bangor University, Menai Bridge, Isle of Anglesey, Wales LL59 5AB,UK
A R T I C L E
I N F O
Article history: Received 22 February 2008 Received in revised form 23 May 2008 Accepted 7 June 2008 Editor: D. Rickard Keywords: Arctica islandica Mg/Ca Climate reconstruction Synchrotron XANES
A B S T R A C T The potential of Mg in Arctica islandica as a climate proxy is explored through analysis of live-collected shells from Irvine Bay, NW Scotland. Laser Ablation Inductively Coupled Plasma Mass Spectrometry (LA-ICP-MS) analysis of the right hand valve from two specimens indicates that seasonal Mg/Ca variations do not correlate with seawater temperature. The highest Mg/Ca typically occurs at the annual growth checks in ~November– February. Mg/Ca variations between growth checks are significant in one specimen but usually not significant in the other. Mg/Ca measurements taken laterally across the band (i.e. perpendicular to direction of the growth) to determine heterogeneity of the aragonite deposited at the same time indicates that Mg/Ca concentration decreases with increasing distance from the periostracum in both shells. X-ray Absorption Near Edge Spectroscopy (XANES) indicates that Mg is not substituted into aragonite but is hosted by a disordered phase e.g. organic components or nanoparticles of an inorganic phase. Shell Mg/Ca variations may reflect changes in the concentration or composition of the disorded phase, as well as changes in the composition of the extrapallial fluid used for calcification. Such changes could reflect the relative transportation rates of Mg and Ca to the calcification site. © 2008 Elsevier B.V. All rights reserved.
1. Introduction The trace element geochemistry of biogenic carbonates is commonly used as an indicator of climate conditions, particularly water temperatures, at the time of formation. In this context the marine bivalve Arctica islandica has great potential to provide an archive of palaeoenvironmental conditions. This long lived organism, which can be N300 years old (Schöne et al., 2004) produces an aragonite shell with annual growth bands, which are delimited by growth checks and are marked by a relative increase in the concentration of the organic components. This lamination allows the timings of shell deposition to be accurately reconstructed. Mg concentrations of biogenic carbonates such as foraminifera have been used as proxies for seawater temperatures (e.g. Elderfield and Gansen, 2000; Anand et al., 2003). Thermodynamic calculations and inorganic precipitation experiments indicate a relationship between Mg/Ca of aragonite and the precipitating seawater temperature (Gaetani and Cohen, 2006). Takesue and van Geen (2004) found only one specimen of four to have a relationship between shell Mg/Ca ⁎ Corresponding author. Current address: Leibniz-Institut für Meereswissenschaften, IFM-GEOMAR, Wischhofstr.1-3, 24148, Kiel, Germany. Tel.: +49 431 600 2109; fax: +49 431 600 2928. E-mail address: [email protected] (L.C. Foster). 0009-2541/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.chemgeo.2008.06.007
and water temperature in the aragonitic bivalve Protothaca staminea indicating that the controls on Mg/Ca and temperature may be complex. Seasonal variations in Mg/Ca have been reported in A. islandica shells (Toland et al., 2000; Epplé, 2004). However, the processes controlling the incorporation of Mg in biogenic aragonites are poorly understood. Here we present a Laser Ablation-Inductively Coupled Plasma Mass Spectrometry (LA-ICP-MS) study of Mg/Ca variations across A. islandica shells. The organisms were collected live from a well characterised site at Irvine Bay, NW Scotland allowing us to correlate shell Mg/Ca with known water temperature variations. Calculations from equilibrium-based thermodynamic models assume that Mg is ideally hosted in the aragonite lattice i.e. substitutes randomly for Ca. However, if Mg is hosted in other phases e.g. associated with organic components (as with corals; Finch and Allison, 2008) or present as another mineral phase, then the nature of the partition would differ. In other words, the temperature relationship for Mg hosted by aragonite is likely to differ significantly to that of Mg hosted by organic components or in other mineral phases that may be present in concentrations below the limit of detection by XRD. No studies have been presented on Mg substitution within bivalves and it is not known whether Mg is ideally hosted, with some studies (e.g. Oomori et al., 1987; Dietzel et al., 2004) hypothesising that Mg may be occluded in lattice defects or complex adsorption onto the crystal surface rather than ideal substitution. We have used XANES (X-ray
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Absorption Near Edge Structure) to study the coordination of Mg in selected specimens. 2. Method and materials Four A. islandica specimens were used in this study; specimens 228, 248, 389 and VO5-257-3. Specimens 228, 248 and 389 were all livecollected from Irvine Bay on the North-west coast of Scotland (55 45'N, 4 54'W) in May 2001 at a water depth of 6 m by University of Wales, Bangor. VO5-257-3 was a dead collected specimen from Viking Bank, Northern North Sea radiocarbon dated as modern (i.e. post-1955). Two of the shells (228 and 248) were used for LA-ICP-MS and two (389 and VO5-257-3) for XANES analysis, as insufficient material was left from the shells used for LA-ICP-MS. One sample was prepared from shell 389, which was collected at the same site and another sample from VO5-257-3, which was dead-collected (postmodern) in order to determine if any changes in the shell occurred shortly after death. The shell consists of an outer prismatic layer (aragonite) and an inner nacre layer (divided by the myostracum). The timing of shell deposition in samples 228 and 248 was recorded by taking a peel of each sample (see e.g. Ropes et al., 1984) and counting the number of annual growth bands within the prismatic layer. δ18O and δ13C confirmed that these growth checks were annual with growth slow down/cessation approximately November to February (Foster, 2007). Millport marine station, Isle of Cumbrae ~ 22 km from the A. islandica collection site in Irvine Bay provides instrumental sea surface temperatures (SST) collected daily from 1953–1983 and from 1983 onwards working days only. In Irvine Bay, intermittent seawater temperature/depth profiles (typically 3–4 per year) were taken in water of N30 m. Comparison of the temperatures recorded at 7 m in this profile show that Millport data provide a good indication of temperature fluctuations within Irvine Bay, with temperatures differing by 1.2 °C (2σ). The seasonal seawater temperature range at Millport marine station is ~6–8 °C to 13–15 °C. 2.1. Preparation of thick sections for LA-ICP-MS Two shells (228 and 248) were sectioned along the axis of maximal growth (Fig. 1). The outermost ~ 1.5 cm of the shell was set in Buehler Epo-thin epoxy and polished to 1 µm using diamond paste. After analysis the samples were etched using 0.1 N HCl for 60 s, carbon
Fig. 2. Secondary electron images of the growth check (1999) from the outer shell prismatic layer of shell 248. The main image highlights the distinct changes between the growth band (left) and the increased concentration of organic components indicating the growth check (right). The insert highlights that the concentration of organic components at the growth check decrease laterally away from the periostracum (top of insert).
coated and then imaged by Scanning Electron Microscopy (SEM) to examine the shell architecture (Fig. 2). LA-ICP-MS analyses were carried out at the University of Bergen, Norway using a New Wave UP213 laser ablation system coupled to an ELEMENT2 ICP-MS. For each spot analysis, the laser warm-up time was 40 s, pulsed at 10 Hz with 110 s dwell time per sample, with washout delay of 40 s. The pulse energy was ~0.3 mJ (60% energy). NIST (US National Institute of Standard and Technology Standard Reference Material) glass standards (NIST610, NIST612) were run every 20 samples to confirm that instrument drift was insignificant. NIST612 glass (Pearce et al., 1997) was used as the calibration standard for data processing in GLITTER© software (van Achterbergh et al., 2001). The software uses a linear fit of the count ratio of the internal normalising isotope (in this case 43 Ca) to the element of a standard to calculate the concentrations of the unknowns based on an estimate of the weight percent CaO. Analyses on cracks within the shell were removed from the dataset. All data were normalised to the carbonate standard OKA carbonatite, as it provided a closer matrix match than NIST glass standards. The precision of the multiple analyses (n =6) on the OKA was typically better than ±6% (2σ). To estimate the precision of analyses on A. islandica we performed multiple analyses in a region of the shell (along a transect of ~800 µm) which contained relatively low Mg/Ca (~0.6 mmol/mol) and which preliminary analysis had indicated was relatively homogeneous with respect to Mg. Multiple analyses (n =8) had a precision of better than ±5% (2σ). The prismatic layer of shells 228 and 248 (termed PL228 and PL248 respectively) were analysed with spot sizes of ~60 µm and 40 µm respectively with analyses every 100 µm. This resulted in a minimum of 6 spots analysed per year and maximum of N15 per year during the earlier, faster growing parts of the shells. The sections analysed by LAICP-MS covered the period from 1993–1998 for PL228 and 1992–2001 for PL248. Three transects (T1, T2, T3) were analysed across each section, running parallel to the periostracum. T1, T2 and T3 were positioned ~250, ~500 and ~1000 µm respectively from the periostracum (see Fig. 1) and each transect comprising of material deposited during the same time period. This allows the determination of sample heterogeneity and whether fluctuations in Mg/Ca are reproducible with increasing distance from the periostracum. 2.2. Sample preparation for XANES
Fig. 1. Schematic of A. islandica section of the prismatic layer, with photomicrograph image showing T1, T2 and T3 from shell 248.
Two A. islandica aliquots were analysed for Mg coordination. One was taken from a live-collected shell 389 from Irvine Bay, Scotland.
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Fig. 3. Mg/Ca variations (1988–1989) along parallel transects across the prismatic layer of A. islandica specimen 228. Data are smoothed with a five point running mean to compensate for small differences in the beam positioning between transects. The slight offset of the peaks is due to curvature of the growth bands. Errors (SE) for LA-ICP-MS analyses were b ±5% (2σ).
The second from the last ~10–15 years of growth of sample VO5-2573. The slices (with the periostracum mechanically removed) were crushed in an agate mortar and pestle under acetone to a finely ground powder. The sample consisted of both the nacre and the prismatic layer, as it was not possible to separate the two layers as micromilling causes inversion of the aragonite to calcite (Foster et al., 2008). X-ray diffraction (XRD) detected aragonite as the only phase in both samples within the limits of detection (limits of detection for calcite in aragonite are b1% (Finch, unpublished data)). XANES analysis was carried out at two synchrotron facilities. Both shells were analysed (389 and VO5-257-3) at station 3.4 at SRS Daresbury Synchrotron facility, Warrington, UK (www.srs.ac.uk/srs) with an average beam current of 200 mA. The samples tested the Daresbury beamline to its limit since Mg concentrations were so low (typically 100–200 ppm). Therefore sample 389 was also analysed on
the Lucia beamline (Flank et al., 2006) at the 3rd generation Swiss Light Source (SLS), Switzerland (sls.web.psi.ch) to ensure that the conclusions drawn from the data were consistent when there was a greater X-ray flux. All samples were analysed with increasing residence time away from the K-edge. Interpretation of the substitution of Mg in aragonite is possible by comparison of the spectra to a number of known standards and references (Finch and Allison, 2007). At Daresbury 3.4, the beam was focused with a double crystal Si(111) monochromator. The powdered sample was mounted onto carbon tape stuck to an aluminium holder. At Lucia, the monochromator was beryl and the samples were prepared as thin pellets stuck to carbon tape. Procedural blanks were carried out on both beamlines and failed to show any Mg signals. Data analysis was carried out manually to remove the background and qualitatively analyse the XANES signal. Comparison of the Mg spectrum with standards and reference
Fig. 4. Mg/Ca variations across the prismatic layers of the two shells (a) PL228 and (b) PL248 (measured 250 µm from the periostracum). Errors (SE) for LA-ICP-MS analyses were b ±5% (2σ). The position of growth check of each year is marked with a solid line with the doublets (D) determined from an acetate peel and further supported by δ18O analyses. Shell damage was visible in the prismatic layer of shell 248 in the 1998 annual band.
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material covering different states of Mg coordination (from Finch and Allison, 2007) was used. These standards include dolomite, calcite, aragonite, bentonite, glauconite, organically hosted Mg (indicative of a disordered phase) and hydromagnesite. In addition, dolomite was used to normalise the K-edge of Mg between analytical sessions and between data from Daresbury and Lucia (Finch and Allison, 2007). Analysis of standards on both beamlines (Daresbury and Lucia) showed no systematic differences. 3. Results 3.1. Mg/Ca variations in the prismatic layer 3.1.1. Parallel transects across the same growth bands Both shells (228 and 248) show significant Mg/Ca variations between parallel transects across the same annual bands (Fig. 3 shows data for shell 228). In PL228 transects, T1 and T2 are broadly consistent in terms of Mg/Ca concentrations and seasonal trends however T3 contains significantly lower Mg/Ca concentrations and does not exhibit the high peaks in Mg concentration observed in the other transects. Hence the data show significant lateral compositional variation in material inferred to have been deposited at the same time.
In general, both shells demonstrate that Mg/Ca concentration decreases with increasing distance from the periostracum and that the amplitude of seasonal variations reduces. 3.1.2. Seasonal Mg/Ca variations In PL228 Mg/Ca concentrations are typically ~ 0.6 mmol/mol and show little significant variation within annual bands except at the annual growth checks where Mg/Ca concentration usually shows a large increase to ~ 1.0–1.3 mmol/mol (Fig. 4). In contrast significant Mg/Ca variations occur throughout the annual bands in PL248 with intra-annual ratios varying between ~ 0.8 to 1.2 mmol/ mol (Fig. 4). Mg/Ca concentrations are usually relatively high at the annual growth check (typically 0.9–1.5 mmol/mol) but these peaks in Mg/Ca concentration are not as well defined as in PL228. An ANOVA comparison of Mg/Ca from the same years (1993–1998) in the two shells indicates that Mg/Ca is significantly higher in PL248 (p b 0.001). We find no direct correlations with SST data at Millport and the Mg data (Fig. 5). Although initially it appears the growth checks (which occur during the winter months) coincide with the high Mg/Ca concentrations, the presence of doublets (e.g. 1998/9 winter growth check where a narrow growth check occurs just prior to the main
Fig. 5. Seawater temperature measured at Millport with Mg/Ca variations across the prismatic layers of the two shells PL228 and PL248 (measured 250 µm from the periostracum). Errors for LA-ICP-MS analyses were b± 5% (2σ). The position of the end of the growth check of each year is marked (i.e. the start of the new year's growth), with a solid line with the doublets (D) determined from an acetate peel and further supported by δ18O analyses. Shell damage was visible in the prismatic layer of shell 248 in the 1998 annual band.
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Fig. 6. a: XANES of Mg from two A. islandica samples; V05-257-3, and 389 (data from SLS and Daresbury) together with organic, aragonite and calcite standard (standards from Finch and Allison, 2007). Note that VO5-257-3 and 389 show similar spectrum, however the higher signal to noise in 389 measured at SLS reflects the higher beam energy available. Lines are added to identify the characteristic peaks of calcite (1323 eV) and aragonite (1332 eV). b XANES of Mg from A. islandica sample 389 collected at SLS compared to organic, aragonite and calcite standard (shown in grey) (standards from Finch and Allison, 2007). Lines are added to identify the characteristic peaks of calcite (1323 eV) and aragonite (1332 eV).
winter growth check) in both A. islandica specimens indicates that Mg variability is not dominantly temperature driven. Damage to shell 248 during 1998 was noted during visual examination. This can be seen by interruption of shell growth and an external scar (a dip in the shell height). The internal growth bands also showed evidence of infilling in which the material is more porous over N400 µm (in the transect). This damage was accompanied by an increase in Mg/Ca concentration for b100 µm of the transect (i.e. one spot analysis). Note that Ca counts of the more porous infilling were not significantly lower and hence this is a significant increase in Mg concentration. 3.2. Mg XANES The XANES spectrum of A. islandica specimens 389 (measured at SLS and Daresbury) and VO5-257-3 are presented in Fig. 6a with standards (calcite, aragonite and organics, Finch and Allison, 2007). XANES from 389 and VO5-257-3 measured at Daresbury and Lucia are identical, albeit Daresbury data have greater noise. The concentrations of Mg within the A. islandica shells are typically 100–200 ppm, which is only just above the limit of detection for the Daresbury beamline.
Despite being single-phase aragonite to XRD, both A. islandica spectra show no increase in intensity of absorption at ~1330 eV, which indicates Mg hosted in aragonite (Fig. 6a). The XANES are neither indicative of Mg hosted within clays. Comparison to the organic standard (Mytilus edulis tissue) shows the best fit (Fig. 6b). 4. Discussion 4.1. Compositional variation by LA-ICP-MS In the two shells analysed here, Mg/Ca concentrations vary significantly between the two specimens and the seasonal profiles also have some differences e.g. significant variations in Mg/Ca concentration are observed between growth checks in PL248 but are not seen in PL228. In PL228 the pattern of increased Mg/Ca concentration at the growth checks is very clear with the exception of 1994 when Mg/Ca ratio does not increase. The 1994 growth check was not well defined visually and its presence as an annual band was confirmed by δ18O analysis (Foster, 2007). It is noticeable that in PL248 however that some growth checks are not associated with the highest Mg/Ca concentration. Instead Mg/Ca concentration is sometimes higher in
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the growth band than in the growth check. (Epplé, 2004) reported a similar observation in A. islandica from the German Bight. In addition, the lateral decrease in Mg/Ca concentration indicates that Mg is affected by internal factors such as changes in shell architecture or variation in the composition of the extrapallial fluid (EPF) used for calcification. 4.2. XANES studies The Mg XANES profiles presented here from A. islandica is inconsistent with the dominant host being aragonite or calcite (Fig. 6b). The closest fit is to the organic M. edulis tissue standard. Superficially such a fit suggests that Mg is hosted by organic components, but the profile is effectively featureless because Mg is surrounded by elements with poor electron scattering, (such as C, H, O etc.) and has little long-range order beyond the first shell. Other disordered materials fit such a description and would give similar XANES. For example, nanoparticulate basic Mg carbonates would also give featureless XANES. Amorphous calcium carbonates (ACCs) are nanoparticulate solids which comply with such a description and which are found in some biogenic systems, including larvae of molluscan bivalves (Weiss et al., 2002). We do not know of a nanoparticulate standard and hence we cannot determine whether disordered phases can be distinguished by XANES. Hence, at present, we cannot distinguish these two structural states and both are credible. Most importantly, XANES is not a fit to aragonite and hence Mg is not substituted in aragonite. Hence, simple partitioning models of Mg into aragonite (as modelled by Gaetani and Cohen, 2006 for example) are unlikely to be applicable to this system. Any partition coefficients that have been determined (e.g. Takesue and van Geen, 2004) are unlikely to be universal since they are not underpinned by inorganic partitioning. 4.3. Changes in shell architecture Well defined changes in shell architecture occur at the growth checks; with increased concentration of organic components present (Fig. 2). The width of the growth checks typically decreases with ontogeny in both shells but there is year-to-year variation. The growth checks can become extremely narrow during the latter years, e.g. b100 µm in the 1999 growth check of PL248, (which resulted in the LA-ICP-MS spots analysed either side of the growth check, Fig. 2). In PL228 increases in Mg concentration are strongly linked with the position of the growth checks, but the pattern for PL248 is less clear. Lateral variation in the shell architecture also occurs at the growth checks (Fig. 2) with the presence of organic components becoming less marked with increased distance from the periostracum (see also Foster et al., in review). No changes in the organic concentration or composition during the growth band (including laterally) were distinguishable by SEM. However, Mg concentration decreases laterally in both shells with significant intra-annual variation occurring in one shell (248). The relationship between shell architecture and Mg concentration is likely to differ depending on how Mg is hosted. We first consider how variations in architecture may relate to changes in Mg concentration if it is hosted within organic components. In biogenic CaCO3 (e.g. bivalves, corals), organic material does not simply exist between the crystals, but the crystals themselves are composed of densely packed mosaic of nanograins embedded in a thin layer of organic material (see Stolarski and Mazur, 2005 and references therein). While it is well detailed that the concentration of organic material increases at the growth check (see Richardson, 2001 and references therein), we have found no data detailing how the organic content varies in terms of concentration and composition both laterally and seasonally (i.e. intra-annually). S may provide some indication of the distribution of organic materials as it is found mainly within organic sulphate (Cuif et al., 2003; Dauphin et al., 2005). A detailed study is required to determine how this complex mixture of
organic components may vary through the shell and the impact that it has on Mg distribution and concentration. The Mg-XANES profile of A. islandica is also consistent with Mg hosted within a nanoparticulate material similar to ACC (see Addadi et al., 2003 for a review on ACC). ACC is a precursor in the formation of aragonite within larvae of molluscan bivalves (Weiss et al., 2002). Weiss et al. (2002) also commented that the adult shell of the aragonite bivalve Mercenaria mercenaria, contains aragonite that is less crystalline than non-biogenic aragonite and thus ACC may also be involved in adult shell formation. In particular, ACC has a high Mg content (Addadi et al., 2003). ACC is invisible to XRD and the individual particles are too small to be resolved in conventional SEM. Hence the presence or absence of nanoparticulate Mg-bearing materials is difficult to explore. Within the growth checks (Fig. 2) the organic matrix obscures the crystals at the growth checks. If ACC plays an important role in biomineralization, the initiation of crystal growth after growth had stopped (e.g. at an annual growth check) could promote the formation and stability of nanoparticulate carbonates. Thus understanding how Mg is hosted, whether by nanoparticulates, organic components or a combination of the two is important in understanding Mg behaviour. MicroXANES work will provide further details on how Mg is hosted in different parts of the shell e.g. growth check vs. growth band and thus could provide further important data on the controls on Mg e.g. the impact EPF has on fluctuations in Mg concentration recorded within the bivalve shell. 4.4. Changes in the EPF Seasonal changes in the relative transport rates of Mg and Ca to the EPF would affect the Mg concentrations found within the shell. Mg, although a divalent cation, is thought to follow a different transport pathway to that of Ca2+ due to its low affinity with pore binding sites and that they sometimes do not permeate at all through Ca2+ channels (Carré et al., 2006). If the lateral decrease in Mg/Ca concentration results from changes in the EPF composition one would infer that the EPF is not homogeneous. The effect of such a process is relatively unexplored, but Sr data from A. islandica (the same specimens presented here — Foster et al., in review) also show a lateral change in Sr, despite Sr being ideally hosted, i.e. found randomly substituted within the aragonite lattice. Measurements however of δ13C show that, for the isotopes at least, there is no lateral change (Foster, 2007). Further research is required to determine the pathway of Mg2+ during calcification and to determine the heterogeneity of the EPF during calcification. 4.5. Summary of Mg behaviour Our XANES results highlight that Mg is not hosted by aragonite, but is found within organic components or disordered material akin to ACC. Results from LA-ICP-MS highlight the inter and intra-annual variability. Thus Mg may provide crucial information on understanding the growth and extension mechanism of the bivalve shell in a manner similar to mapping of sulphated compounds in corals and molluscs, which indicates their involvement in the mineralization process (Cuif et al., 2003; Dauphin et al., 2005). 5. Conclusion Mg/Ca varies significantly between A. islandica shells and the seasonal patterns are not the same between two individuals. In one shell the highest Mg/Ca concentration occurred at the growth check, but in the second shell this relationship was less clear. The XANES spectrum of Mg within A. islandica is inconsistent with the dominant host being aragonite. Comparison to the M. edulis tissue standard suggests that Mg is hosted by organic material or another disordered phase akin to amorphous calcium carbonate (ACC). Further work is required to determine the exact compositional changes through the
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shell including microXANES and EXAFS to determine whether amorphous calcium carbonate may be present. X-ray absorption spectroscopy may find an important niche in groundtruthing environmental proxies in a manner similar to that applied here. Acknowledgements XAS analysis was generously supported with Daresbury SRS grants (41339 and 45027), with additional support from the Marine Studies Postgraduate Award. Work at SLS was supported by grant number 20070871 with travel support from NERC Envirosynch2 initiative. Special personal thanks go to A. Calder (University of St. Andrews, U.K.); A. Smith (station 3.4, Daresbury); T. Huthwelker and P. Lagarde (LUCIA beamline, SLS); E. S. Erichsen, (SEM facility, University of Bergen); O. Tumyr, C. Kruber, H. Almelid and J. Kosler (ICP-MS laboratory, University of Bergen) who all provided invaluable assistance on running the various instruments. LA-ICP-MS work was supported by a Marie Curie Training Fellowship (EVK2-GH-0057123-10) with additional support from QRA New Researcher's Award. LF would also like to express thanks for support from the LASSO project, IFM-GEOMAR, Germany. This work was completed as part of a PhD for LF, which was supported by the Lapsed bursary scheme, University of St. Andrews, U.K. The specimens were kindly provided by the University of Wales, UK. This article has benefited greatly from the constructive reviews of two anonymous reviewers. References Addadi, L., Raz, S., Weiner, S., 2003. Taking advantage of disorder: amorphous calcium carbonate and its roles in biomineralization. Advanced Materials 15 (12), 959–970. Anand, P., Elderfield, H., Contre, M.H., 2003. Calibration of Mg/Ca thermometry in planktonic foraminifera from a sediment trap time series. Paleoceanography 18 (2), 1050. doi:10.1029/2002PA000846. Carré, M., Bentaleb, I., Bruguier, O., Ordinola, E., Barrett, N.T., Fontugne, M., 2006. Calcification rate influence on trace element concentrations in aragonitic bivalve shells: evidences and mechanisms. Geochimica et Cosmochimica Acta 70 (19), 4906–4920. Cuif, J.-P., Dauphin, Y., Doucet, J., Salome, M., Susini, J., 2003. XANES mapping of organic sulfate in three scleractinian coral skeletons. Geochimica et Cosmochimica Acta 67 (1), 75–83. Dauphin, Y., Cuif, J.-P., Salome, M., Susini, J., 2005. Speciation and distribution of sulfur in a mollusk shell as revealed by in situ maps using X-ray absorption near-edge structure (XANES) spectroscopy at the S K-edge. American Mineralogist 90 (11–12), 1748–1758. Dietzel, M., Gussone, N., Eisenhauer, A., 2004. Co-precipitation of Sr2+ and Ba2+ with aragonite by membrane diffusion of CO2 between 10 and 50 °C. Chemical Geology 203 (1–2), 139–151.
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Elderfield, H., Gansen, G., 2000. Past temperature and δ18O of surface ocean waters inferred from foraminiferal Mg/Ca ratios. Nature 405, 422–445. Epplé, V.M., 2004. High-resolution climate reconstruction for Holocene based on growth chronologies of bivalve Arctica islandica from the North Sea. Ph.D. Thesis, University of Bremen, 90 pp. Finch, A.A., Allison, N., 2007. Coordination of Sr and Mg in calcite and aragonite. Mineralogical Magazine 71 (5), 539–552. Finch, A.A., Allison, N., 2008. Mg structural state in coral aragonite and implications for the paleoenvironmental proxy. Geophysical Research Letters 35, L08704. doi:10.1029/2008GL033543. Flank, A.-M., Cauchon, G., Lagarde, P., Bac, S., Janousch, M., Wetter, R., Dubuisson, J.-M., Idir, M., Langlois, F., Moreno, T., Vantelon, D., 2006. LUCIA, a microfocus soft XAS beamline. Nuclear Instruments and Methods in Physics Research Section B 246, 269–274. Foster, L.C., 2007. The potential of high resolution palaeoclimate reconstruction from Arctica islandica. Ph.D. Thesis, University of St. Andrews, 400 pp. Foster, L.C., Allison, N., Finch, A.A. and Andersson, C., in review. Strontium distribution in the shell of the aragonite bivalve Arctica islandica. Geochemistry, Geophysics, Geosystems. Foster, L.C., Andersson, C., Høie, H., Allison, N., Finch, A.A., Johansen, T., 2008. Effects of micromilling on δ18O in biogenic aragonite. Geochemistry Geophysics Geosystems 9, Q04013. doi:10.1029/2007GC001911. Gaetani, G.A., Cohen, A.L., 2006. Element partitioning during precipitation of aragonite from seawater: a framework for understanding paleoproxies. Geochimica et Cosmochimica Acta 70 (18), 4617–4634. Oomori, T., Kaneshima, H., Maezato, Y., Kitano, Y., 1987. Distribution coefficient of Mg2+ ions between calcite and solution at 10–50 °C. Marine Chemistry 20, 327–336. Pearce, N.J.G., Perkins, W.T., Westgate, J.A., Gorton, M.P., Jackson, S.E., Neal, C.R., Chenery, S.P., 1997. A compilation of new and published major and trace element data for NIST SRM 610 and NIST SRM 612 glass reference materials. Geostandards Newsletters 21, 115–144. Richardson, C., 2001. Molluscs as archives of environmental change. Oceanography and Marine Biology 39, 103–164. Ropes, J.W., Jones, D.S., Murawski, S.A., Serchuk, F.M., Jearld, J.A., 1984. Documentation of annual growth lines in ocean quahog, Arctica islandica. Fishery Bulletin 82 (1), 1–20. Schöne, B.R., Castro, A.D.F., Fiebig, J., Houk, S.D., Oschmann, W., Kroncke, I., 2004. Sea surface water temperatures over the period 1884–1983 reconstructed from oxygen isotope ratios of a bivalve mollusk shell (Arctica islandica, southern North Sea). Palaeogeography Palaeoclimatology Palaeoecology 212 (3–4), 215–232. Stolarski, J., Mazur, M., 2005. Nanostructure of biogenic versus abiogenic calcium carbonate crystals. Acta Palaeontologica Polonica 50 (4), 847–865. Takesue, R.K., van Geen, A., 2004. Mg/Ca, Sr/Ca, and stable isotopes in modern and Holocene Protothaca staminea shells from a northern California coastal upwelling region. Geochimica et Cosmochimica Acta 68 (19), 3845–3861. Toland, H., Perkins, W.T., Pearce, N.J.G., Keenan, F., Leng, M.J., 2000. A study of sclerochronology by laser ablation ICP-MS. Journal of Analytical Atomic Spectrometry 15, 1143–1148. van Achterbergh, E., Ryan, C., Jackson, S.E., Griffin, W.L., 2001. Data reduction software for LA-ICPMS. In: Sylvester, P. (Ed.), Laser Ablation-ICPMS in the Earth Sciences. Mineralogical Association of Canada Short course handbook, pp. 239–243. Weiss, I.M., Tuross, N., Addadi, L., Weiner, S., 2002. Mollusc larval shell formation: amorphous calcium carbonate is a precursor phase for aragonite. Journal of Experimental Zoology 293 (5), 478–491.
Contents lists available at ScienceDirect
Chemical Geology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / c h e m g e o
Mg in aragonitic bivalve shells: Seasonal variations and mode of incorporation in Arctica islandica L.C. Foster a,⁎, A.A. Finch a, N. Allison a, C. Andersson b, L.J. Clarke c a b c
School of Geography and Geosciences, University of St. Andrews, Irvine Building, St. Andrews, KY16 9AL, UK Bjerknes Centre for Climate Research, Allegaten 55, 5007, Bergen, Norway School of Ocean Sciences, College of Natural Sciences, Bangor University, Menai Bridge, Isle of Anglesey, Wales LL59 5AB,UK
A R T I C L E
I N F O
Article history: Received 22 February 2008 Received in revised form 23 May 2008 Accepted 7 June 2008 Editor: D. Rickard Keywords: Arctica islandica Mg/Ca Climate reconstruction Synchrotron XANES
A B S T R A C T The potential of Mg in Arctica islandica as a climate proxy is explored through analysis of live-collected shells from Irvine Bay, NW Scotland. Laser Ablation Inductively Coupled Plasma Mass Spectrometry (LA-ICP-MS) analysis of the right hand valve from two specimens indicates that seasonal Mg/Ca variations do not correlate with seawater temperature. The highest Mg/Ca typically occurs at the annual growth checks in ~November– February. Mg/Ca variations between growth checks are significant in one specimen but usually not significant in the other. Mg/Ca measurements taken laterally across the band (i.e. perpendicular to direction of the growth) to determine heterogeneity of the aragonite deposited at the same time indicates that Mg/Ca concentration decreases with increasing distance from the periostracum in both shells. X-ray Absorption Near Edge Spectroscopy (XANES) indicates that Mg is not substituted into aragonite but is hosted by a disordered phase e.g. organic components or nanoparticles of an inorganic phase. Shell Mg/Ca variations may reflect changes in the concentration or composition of the disorded phase, as well as changes in the composition of the extrapallial fluid used for calcification. Such changes could reflect the relative transportation rates of Mg and Ca to the calcification site. © 2008 Elsevier B.V. All rights reserved.
1. Introduction The trace element geochemistry of biogenic carbonates is commonly used as an indicator of climate conditions, particularly water temperatures, at the time of formation. In this context the marine bivalve Arctica islandica has great potential to provide an archive of palaeoenvironmental conditions. This long lived organism, which can be N300 years old (Schöne et al., 2004) produces an aragonite shell with annual growth bands, which are delimited by growth checks and are marked by a relative increase in the concentration of the organic components. This lamination allows the timings of shell deposition to be accurately reconstructed. Mg concentrations of biogenic carbonates such as foraminifera have been used as proxies for seawater temperatures (e.g. Elderfield and Gansen, 2000; Anand et al., 2003). Thermodynamic calculations and inorganic precipitation experiments indicate a relationship between Mg/Ca of aragonite and the precipitating seawater temperature (Gaetani and Cohen, 2006). Takesue and van Geen (2004) found only one specimen of four to have a relationship between shell Mg/Ca ⁎ Corresponding author. Current address: Leibniz-Institut für Meereswissenschaften, IFM-GEOMAR, Wischhofstr.1-3, 24148, Kiel, Germany. Tel.: +49 431 600 2109; fax: +49 431 600 2928. E-mail address: [email protected] (L.C. Foster). 0009-2541/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.chemgeo.2008.06.007
and water temperature in the aragonitic bivalve Protothaca staminea indicating that the controls on Mg/Ca and temperature may be complex. Seasonal variations in Mg/Ca have been reported in A. islandica shells (Toland et al., 2000; Epplé, 2004). However, the processes controlling the incorporation of Mg in biogenic aragonites are poorly understood. Here we present a Laser Ablation-Inductively Coupled Plasma Mass Spectrometry (LA-ICP-MS) study of Mg/Ca variations across A. islandica shells. The organisms were collected live from a well characterised site at Irvine Bay, NW Scotland allowing us to correlate shell Mg/Ca with known water temperature variations. Calculations from equilibrium-based thermodynamic models assume that Mg is ideally hosted in the aragonite lattice i.e. substitutes randomly for Ca. However, if Mg is hosted in other phases e.g. associated with organic components (as with corals; Finch and Allison, 2008) or present as another mineral phase, then the nature of the partition would differ. In other words, the temperature relationship for Mg hosted by aragonite is likely to differ significantly to that of Mg hosted by organic components or in other mineral phases that may be present in concentrations below the limit of detection by XRD. No studies have been presented on Mg substitution within bivalves and it is not known whether Mg is ideally hosted, with some studies (e.g. Oomori et al., 1987; Dietzel et al., 2004) hypothesising that Mg may be occluded in lattice defects or complex adsorption onto the crystal surface rather than ideal substitution. We have used XANES (X-ray
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Absorption Near Edge Structure) to study the coordination of Mg in selected specimens. 2. Method and materials Four A. islandica specimens were used in this study; specimens 228, 248, 389 and VO5-257-3. Specimens 228, 248 and 389 were all livecollected from Irvine Bay on the North-west coast of Scotland (55 45'N, 4 54'W) in May 2001 at a water depth of 6 m by University of Wales, Bangor. VO5-257-3 was a dead collected specimen from Viking Bank, Northern North Sea radiocarbon dated as modern (i.e. post-1955). Two of the shells (228 and 248) were used for LA-ICP-MS and two (389 and VO5-257-3) for XANES analysis, as insufficient material was left from the shells used for LA-ICP-MS. One sample was prepared from shell 389, which was collected at the same site and another sample from VO5-257-3, which was dead-collected (postmodern) in order to determine if any changes in the shell occurred shortly after death. The shell consists of an outer prismatic layer (aragonite) and an inner nacre layer (divided by the myostracum). The timing of shell deposition in samples 228 and 248 was recorded by taking a peel of each sample (see e.g. Ropes et al., 1984) and counting the number of annual growth bands within the prismatic layer. δ18O and δ13C confirmed that these growth checks were annual with growth slow down/cessation approximately November to February (Foster, 2007). Millport marine station, Isle of Cumbrae ~ 22 km from the A. islandica collection site in Irvine Bay provides instrumental sea surface temperatures (SST) collected daily from 1953–1983 and from 1983 onwards working days only. In Irvine Bay, intermittent seawater temperature/depth profiles (typically 3–4 per year) were taken in water of N30 m. Comparison of the temperatures recorded at 7 m in this profile show that Millport data provide a good indication of temperature fluctuations within Irvine Bay, with temperatures differing by 1.2 °C (2σ). The seasonal seawater temperature range at Millport marine station is ~6–8 °C to 13–15 °C. 2.1. Preparation of thick sections for LA-ICP-MS Two shells (228 and 248) were sectioned along the axis of maximal growth (Fig. 1). The outermost ~ 1.5 cm of the shell was set in Buehler Epo-thin epoxy and polished to 1 µm using diamond paste. After analysis the samples were etched using 0.1 N HCl for 60 s, carbon
Fig. 2. Secondary electron images of the growth check (1999) from the outer shell prismatic layer of shell 248. The main image highlights the distinct changes between the growth band (left) and the increased concentration of organic components indicating the growth check (right). The insert highlights that the concentration of organic components at the growth check decrease laterally away from the periostracum (top of insert).
coated and then imaged by Scanning Electron Microscopy (SEM) to examine the shell architecture (Fig. 2). LA-ICP-MS analyses were carried out at the University of Bergen, Norway using a New Wave UP213 laser ablation system coupled to an ELEMENT2 ICP-MS. For each spot analysis, the laser warm-up time was 40 s, pulsed at 10 Hz with 110 s dwell time per sample, with washout delay of 40 s. The pulse energy was ~0.3 mJ (60% energy). NIST (US National Institute of Standard and Technology Standard Reference Material) glass standards (NIST610, NIST612) were run every 20 samples to confirm that instrument drift was insignificant. NIST612 glass (Pearce et al., 1997) was used as the calibration standard for data processing in GLITTER© software (van Achterbergh et al., 2001). The software uses a linear fit of the count ratio of the internal normalising isotope (in this case 43 Ca) to the element of a standard to calculate the concentrations of the unknowns based on an estimate of the weight percent CaO. Analyses on cracks within the shell were removed from the dataset. All data were normalised to the carbonate standard OKA carbonatite, as it provided a closer matrix match than NIST glass standards. The precision of the multiple analyses (n =6) on the OKA was typically better than ±6% (2σ). To estimate the precision of analyses on A. islandica we performed multiple analyses in a region of the shell (along a transect of ~800 µm) which contained relatively low Mg/Ca (~0.6 mmol/mol) and which preliminary analysis had indicated was relatively homogeneous with respect to Mg. Multiple analyses (n =8) had a precision of better than ±5% (2σ). The prismatic layer of shells 228 and 248 (termed PL228 and PL248 respectively) were analysed with spot sizes of ~60 µm and 40 µm respectively with analyses every 100 µm. This resulted in a minimum of 6 spots analysed per year and maximum of N15 per year during the earlier, faster growing parts of the shells. The sections analysed by LAICP-MS covered the period from 1993–1998 for PL228 and 1992–2001 for PL248. Three transects (T1, T2, T3) were analysed across each section, running parallel to the periostracum. T1, T2 and T3 were positioned ~250, ~500 and ~1000 µm respectively from the periostracum (see Fig. 1) and each transect comprising of material deposited during the same time period. This allows the determination of sample heterogeneity and whether fluctuations in Mg/Ca are reproducible with increasing distance from the periostracum. 2.2. Sample preparation for XANES
Fig. 1. Schematic of A. islandica section of the prismatic layer, with photomicrograph image showing T1, T2 and T3 from shell 248.
Two A. islandica aliquots were analysed for Mg coordination. One was taken from a live-collected shell 389 from Irvine Bay, Scotland.
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Fig. 3. Mg/Ca variations (1988–1989) along parallel transects across the prismatic layer of A. islandica specimen 228. Data are smoothed with a five point running mean to compensate for small differences in the beam positioning between transects. The slight offset of the peaks is due to curvature of the growth bands. Errors (SE) for LA-ICP-MS analyses were b ±5% (2σ).
The second from the last ~10–15 years of growth of sample VO5-2573. The slices (with the periostracum mechanically removed) were crushed in an agate mortar and pestle under acetone to a finely ground powder. The sample consisted of both the nacre and the prismatic layer, as it was not possible to separate the two layers as micromilling causes inversion of the aragonite to calcite (Foster et al., 2008). X-ray diffraction (XRD) detected aragonite as the only phase in both samples within the limits of detection (limits of detection for calcite in aragonite are b1% (Finch, unpublished data)). XANES analysis was carried out at two synchrotron facilities. Both shells were analysed (389 and VO5-257-3) at station 3.4 at SRS Daresbury Synchrotron facility, Warrington, UK (www.srs.ac.uk/srs) with an average beam current of 200 mA. The samples tested the Daresbury beamline to its limit since Mg concentrations were so low (typically 100–200 ppm). Therefore sample 389 was also analysed on
the Lucia beamline (Flank et al., 2006) at the 3rd generation Swiss Light Source (SLS), Switzerland (sls.web.psi.ch) to ensure that the conclusions drawn from the data were consistent when there was a greater X-ray flux. All samples were analysed with increasing residence time away from the K-edge. Interpretation of the substitution of Mg in aragonite is possible by comparison of the spectra to a number of known standards and references (Finch and Allison, 2007). At Daresbury 3.4, the beam was focused with a double crystal Si(111) monochromator. The powdered sample was mounted onto carbon tape stuck to an aluminium holder. At Lucia, the monochromator was beryl and the samples were prepared as thin pellets stuck to carbon tape. Procedural blanks were carried out on both beamlines and failed to show any Mg signals. Data analysis was carried out manually to remove the background and qualitatively analyse the XANES signal. Comparison of the Mg spectrum with standards and reference
Fig. 4. Mg/Ca variations across the prismatic layers of the two shells (a) PL228 and (b) PL248 (measured 250 µm from the periostracum). Errors (SE) for LA-ICP-MS analyses were b ±5% (2σ). The position of growth check of each year is marked with a solid line with the doublets (D) determined from an acetate peel and further supported by δ18O analyses. Shell damage was visible in the prismatic layer of shell 248 in the 1998 annual band.
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material covering different states of Mg coordination (from Finch and Allison, 2007) was used. These standards include dolomite, calcite, aragonite, bentonite, glauconite, organically hosted Mg (indicative of a disordered phase) and hydromagnesite. In addition, dolomite was used to normalise the K-edge of Mg between analytical sessions and between data from Daresbury and Lucia (Finch and Allison, 2007). Analysis of standards on both beamlines (Daresbury and Lucia) showed no systematic differences. 3. Results 3.1. Mg/Ca variations in the prismatic layer 3.1.1. Parallel transects across the same growth bands Both shells (228 and 248) show significant Mg/Ca variations between parallel transects across the same annual bands (Fig. 3 shows data for shell 228). In PL228 transects, T1 and T2 are broadly consistent in terms of Mg/Ca concentrations and seasonal trends however T3 contains significantly lower Mg/Ca concentrations and does not exhibit the high peaks in Mg concentration observed in the other transects. Hence the data show significant lateral compositional variation in material inferred to have been deposited at the same time.
In general, both shells demonstrate that Mg/Ca concentration decreases with increasing distance from the periostracum and that the amplitude of seasonal variations reduces. 3.1.2. Seasonal Mg/Ca variations In PL228 Mg/Ca concentrations are typically ~ 0.6 mmol/mol and show little significant variation within annual bands except at the annual growth checks where Mg/Ca concentration usually shows a large increase to ~ 1.0–1.3 mmol/mol (Fig. 4). In contrast significant Mg/Ca variations occur throughout the annual bands in PL248 with intra-annual ratios varying between ~ 0.8 to 1.2 mmol/ mol (Fig. 4). Mg/Ca concentrations are usually relatively high at the annual growth check (typically 0.9–1.5 mmol/mol) but these peaks in Mg/Ca concentration are not as well defined as in PL228. An ANOVA comparison of Mg/Ca from the same years (1993–1998) in the two shells indicates that Mg/Ca is significantly higher in PL248 (p b 0.001). We find no direct correlations with SST data at Millport and the Mg data (Fig. 5). Although initially it appears the growth checks (which occur during the winter months) coincide with the high Mg/Ca concentrations, the presence of doublets (e.g. 1998/9 winter growth check where a narrow growth check occurs just prior to the main
Fig. 5. Seawater temperature measured at Millport with Mg/Ca variations across the prismatic layers of the two shells PL228 and PL248 (measured 250 µm from the periostracum). Errors for LA-ICP-MS analyses were b± 5% (2σ). The position of the end of the growth check of each year is marked (i.e. the start of the new year's growth), with a solid line with the doublets (D) determined from an acetate peel and further supported by δ18O analyses. Shell damage was visible in the prismatic layer of shell 248 in the 1998 annual band.
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Fig. 6. a: XANES of Mg from two A. islandica samples; V05-257-3, and 389 (data from SLS and Daresbury) together with organic, aragonite and calcite standard (standards from Finch and Allison, 2007). Note that VO5-257-3 and 389 show similar spectrum, however the higher signal to noise in 389 measured at SLS reflects the higher beam energy available. Lines are added to identify the characteristic peaks of calcite (1323 eV) and aragonite (1332 eV). b XANES of Mg from A. islandica sample 389 collected at SLS compared to organic, aragonite and calcite standard (shown in grey) (standards from Finch and Allison, 2007). Lines are added to identify the characteristic peaks of calcite (1323 eV) and aragonite (1332 eV).
winter growth check) in both A. islandica specimens indicates that Mg variability is not dominantly temperature driven. Damage to shell 248 during 1998 was noted during visual examination. This can be seen by interruption of shell growth and an external scar (a dip in the shell height). The internal growth bands also showed evidence of infilling in which the material is more porous over N400 µm (in the transect). This damage was accompanied by an increase in Mg/Ca concentration for b100 µm of the transect (i.e. one spot analysis). Note that Ca counts of the more porous infilling were not significantly lower and hence this is a significant increase in Mg concentration. 3.2. Mg XANES The XANES spectrum of A. islandica specimens 389 (measured at SLS and Daresbury) and VO5-257-3 are presented in Fig. 6a with standards (calcite, aragonite and organics, Finch and Allison, 2007). XANES from 389 and VO5-257-3 measured at Daresbury and Lucia are identical, albeit Daresbury data have greater noise. The concentrations of Mg within the A. islandica shells are typically 100–200 ppm, which is only just above the limit of detection for the Daresbury beamline.
Despite being single-phase aragonite to XRD, both A. islandica spectra show no increase in intensity of absorption at ~1330 eV, which indicates Mg hosted in aragonite (Fig. 6a). The XANES are neither indicative of Mg hosted within clays. Comparison to the organic standard (Mytilus edulis tissue) shows the best fit (Fig. 6b). 4. Discussion 4.1. Compositional variation by LA-ICP-MS In the two shells analysed here, Mg/Ca concentrations vary significantly between the two specimens and the seasonal profiles also have some differences e.g. significant variations in Mg/Ca concentration are observed between growth checks in PL248 but are not seen in PL228. In PL228 the pattern of increased Mg/Ca concentration at the growth checks is very clear with the exception of 1994 when Mg/Ca ratio does not increase. The 1994 growth check was not well defined visually and its presence as an annual band was confirmed by δ18O analysis (Foster, 2007). It is noticeable that in PL248 however that some growth checks are not associated with the highest Mg/Ca concentration. Instead Mg/Ca concentration is sometimes higher in
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the growth band than in the growth check. (Epplé, 2004) reported a similar observation in A. islandica from the German Bight. In addition, the lateral decrease in Mg/Ca concentration indicates that Mg is affected by internal factors such as changes in shell architecture or variation in the composition of the extrapallial fluid (EPF) used for calcification. 4.2. XANES studies The Mg XANES profiles presented here from A. islandica is inconsistent with the dominant host being aragonite or calcite (Fig. 6b). The closest fit is to the organic M. edulis tissue standard. Superficially such a fit suggests that Mg is hosted by organic components, but the profile is effectively featureless because Mg is surrounded by elements with poor electron scattering, (such as C, H, O etc.) and has little long-range order beyond the first shell. Other disordered materials fit such a description and would give similar XANES. For example, nanoparticulate basic Mg carbonates would also give featureless XANES. Amorphous calcium carbonates (ACCs) are nanoparticulate solids which comply with such a description and which are found in some biogenic systems, including larvae of molluscan bivalves (Weiss et al., 2002). We do not know of a nanoparticulate standard and hence we cannot determine whether disordered phases can be distinguished by XANES. Hence, at present, we cannot distinguish these two structural states and both are credible. Most importantly, XANES is not a fit to aragonite and hence Mg is not substituted in aragonite. Hence, simple partitioning models of Mg into aragonite (as modelled by Gaetani and Cohen, 2006 for example) are unlikely to be applicable to this system. Any partition coefficients that have been determined (e.g. Takesue and van Geen, 2004) are unlikely to be universal since they are not underpinned by inorganic partitioning. 4.3. Changes in shell architecture Well defined changes in shell architecture occur at the growth checks; with increased concentration of organic components present (Fig. 2). The width of the growth checks typically decreases with ontogeny in both shells but there is year-to-year variation. The growth checks can become extremely narrow during the latter years, e.g. b100 µm in the 1999 growth check of PL248, (which resulted in the LA-ICP-MS spots analysed either side of the growth check, Fig. 2). In PL228 increases in Mg concentration are strongly linked with the position of the growth checks, but the pattern for PL248 is less clear. Lateral variation in the shell architecture also occurs at the growth checks (Fig. 2) with the presence of organic components becoming less marked with increased distance from the periostracum (see also Foster et al., in review). No changes in the organic concentration or composition during the growth band (including laterally) were distinguishable by SEM. However, Mg concentration decreases laterally in both shells with significant intra-annual variation occurring in one shell (248). The relationship between shell architecture and Mg concentration is likely to differ depending on how Mg is hosted. We first consider how variations in architecture may relate to changes in Mg concentration if it is hosted within organic components. In biogenic CaCO3 (e.g. bivalves, corals), organic material does not simply exist between the crystals, but the crystals themselves are composed of densely packed mosaic of nanograins embedded in a thin layer of organic material (see Stolarski and Mazur, 2005 and references therein). While it is well detailed that the concentration of organic material increases at the growth check (see Richardson, 2001 and references therein), we have found no data detailing how the organic content varies in terms of concentration and composition both laterally and seasonally (i.e. intra-annually). S may provide some indication of the distribution of organic materials as it is found mainly within organic sulphate (Cuif et al., 2003; Dauphin et al., 2005). A detailed study is required to determine how this complex mixture of
organic components may vary through the shell and the impact that it has on Mg distribution and concentration. The Mg-XANES profile of A. islandica is also consistent with Mg hosted within a nanoparticulate material similar to ACC (see Addadi et al., 2003 for a review on ACC). ACC is a precursor in the formation of aragonite within larvae of molluscan bivalves (Weiss et al., 2002). Weiss et al. (2002) also commented that the adult shell of the aragonite bivalve Mercenaria mercenaria, contains aragonite that is less crystalline than non-biogenic aragonite and thus ACC may also be involved in adult shell formation. In particular, ACC has a high Mg content (Addadi et al., 2003). ACC is invisible to XRD and the individual particles are too small to be resolved in conventional SEM. Hence the presence or absence of nanoparticulate Mg-bearing materials is difficult to explore. Within the growth checks (Fig. 2) the organic matrix obscures the crystals at the growth checks. If ACC plays an important role in biomineralization, the initiation of crystal growth after growth had stopped (e.g. at an annual growth check) could promote the formation and stability of nanoparticulate carbonates. Thus understanding how Mg is hosted, whether by nanoparticulates, organic components or a combination of the two is important in understanding Mg behaviour. MicroXANES work will provide further details on how Mg is hosted in different parts of the shell e.g. growth check vs. growth band and thus could provide further important data on the controls on Mg e.g. the impact EPF has on fluctuations in Mg concentration recorded within the bivalve shell. 4.4. Changes in the EPF Seasonal changes in the relative transport rates of Mg and Ca to the EPF would affect the Mg concentrations found within the shell. Mg, although a divalent cation, is thought to follow a different transport pathway to that of Ca2+ due to its low affinity with pore binding sites and that they sometimes do not permeate at all through Ca2+ channels (Carré et al., 2006). If the lateral decrease in Mg/Ca concentration results from changes in the EPF composition one would infer that the EPF is not homogeneous. The effect of such a process is relatively unexplored, but Sr data from A. islandica (the same specimens presented here — Foster et al., in review) also show a lateral change in Sr, despite Sr being ideally hosted, i.e. found randomly substituted within the aragonite lattice. Measurements however of δ13C show that, for the isotopes at least, there is no lateral change (Foster, 2007). Further research is required to determine the pathway of Mg2+ during calcification and to determine the heterogeneity of the EPF during calcification. 4.5. Summary of Mg behaviour Our XANES results highlight that Mg is not hosted by aragonite, but is found within organic components or disordered material akin to ACC. Results from LA-ICP-MS highlight the inter and intra-annual variability. Thus Mg may provide crucial information on understanding the growth and extension mechanism of the bivalve shell in a manner similar to mapping of sulphated compounds in corals and molluscs, which indicates their involvement in the mineralization process (Cuif et al., 2003; Dauphin et al., 2005). 5. Conclusion Mg/Ca varies significantly between A. islandica shells and the seasonal patterns are not the same between two individuals. In one shell the highest Mg/Ca concentration occurred at the growth check, but in the second shell this relationship was less clear. The XANES spectrum of Mg within A. islandica is inconsistent with the dominant host being aragonite. Comparison to the M. edulis tissue standard suggests that Mg is hosted by organic material or another disordered phase akin to amorphous calcium carbonate (ACC). Further work is required to determine the exact compositional changes through the
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shell including microXANES and EXAFS to determine whether amorphous calcium carbonate may be present. X-ray absorption spectroscopy may find an important niche in groundtruthing environmental proxies in a manner similar to that applied here. Acknowledgements XAS analysis was generously supported with Daresbury SRS grants (41339 and 45027), with additional support from the Marine Studies Postgraduate Award. Work at SLS was supported by grant number 20070871 with travel support from NERC Envirosynch2 initiative. Special personal thanks go to A. Calder (University of St. Andrews, U.K.); A. Smith (station 3.4, Daresbury); T. Huthwelker and P. Lagarde (LUCIA beamline, SLS); E. S. Erichsen, (SEM facility, University of Bergen); O. Tumyr, C. Kruber, H. Almelid and J. Kosler (ICP-MS laboratory, University of Bergen) who all provided invaluable assistance on running the various instruments. LA-ICP-MS work was supported by a Marie Curie Training Fellowship (EVK2-GH-0057123-10) with additional support from QRA New Researcher's Award. LF would also like to express thanks for support from the LASSO project, IFM-GEOMAR, Germany. This work was completed as part of a PhD for LF, which was supported by the Lapsed bursary scheme, University of St. Andrews, U.K. The specimens were kindly provided by the University of Wales, UK. This article has benefited greatly from the constructive reviews of two anonymous reviewers. References Addadi, L., Raz, S., Weiner, S., 2003. Taking advantage of disorder: amorphous calcium carbonate and its roles in biomineralization. Advanced Materials 15 (12), 959–970. Anand, P., Elderfield, H., Contre, M.H., 2003. Calibration of Mg/Ca thermometry in planktonic foraminifera from a sediment trap time series. Paleoceanography 18 (2), 1050. doi:10.1029/2002PA000846. Carré, M., Bentaleb, I., Bruguier, O., Ordinola, E., Barrett, N.T., Fontugne, M., 2006. Calcification rate influence on trace element concentrations in aragonitic bivalve shells: evidences and mechanisms. Geochimica et Cosmochimica Acta 70 (19), 4906–4920. Cuif, J.-P., Dauphin, Y., Doucet, J., Salome, M., Susini, J., 2003. XANES mapping of organic sulfate in three scleractinian coral skeletons. Geochimica et Cosmochimica Acta 67 (1), 75–83. Dauphin, Y., Cuif, J.-P., Salome, M., Susini, J., 2005. Speciation and distribution of sulfur in a mollusk shell as revealed by in situ maps using X-ray absorption near-edge structure (XANES) spectroscopy at the S K-edge. American Mineralogist 90 (11–12), 1748–1758. Dietzel, M., Gussone, N., Eisenhauer, A., 2004. Co-precipitation of Sr2+ and Ba2+ with aragonite by membrane diffusion of CO2 between 10 and 50 °C. Chemical Geology 203 (1–2), 139–151.
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