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Magnesium in the lattice of calcite-shelled brachiopods
Chemical Geology 257 (2008) 59–64
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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
Magnesium in the lattice of calcite-shelled brachiopods Maggie Cusack a,⁎, Alberto Pérez-Huerta a, Markus Janousch b, Adrian A. Finch c a b c
Department of Geographical & Earth Sciences, University of Glasgow, G12 8QQ Glasgow, UK Swiss Light Source, Paul Scherrer Institute, Switzerland School of Geography & Geosciences, University of St. Andrews, KY16 9AL, UK
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Article history: Received 8 May 2008 Received in revised form 31 July 2008 Accepted 9 August 2008 Editor: D. Rickard Keywords: XANES at Mg K-edge Synchrotron Magnesium Calcite
a b s t r a c t Palaeoclimate information is often extracted from Rhynchonelliform brachiopod shell calcite, in particular the inner secondary layer, via the δ18O composition, which is a proxy for seawater temperature. Compared to δ18O, the potential for Mg/Ca ratio, as a brachiopod seawater temperature proxy, has been neglected. The use of Mg/Ca ratio as a temperature proxy assumes that, with increasing temperature, more Mg substitutes for Ca in the calcite lattice. Brachiopod shells, like all biominerals, are composites of organic and inorganic components. This raises the possibility that magnesium is hosted by the organic components. Alternatively, magnesium may be present as a separate mineral phase, rather than a true component of the calcite lattice, or incorporated into calcite in non-ideal or variable coordination. Here we use synchrotron X-ray absorption Near Edge Spectroscopy (XANES) at the Mg K-edge to determine the local environment of magnesium in two species of brachiopod with low Mg-calcite shells, Terebratulina retusa and Notosaria nigricans and one species with a high Mg-calcite shell, Novocrania anomala. XANES at the Mg K-edge of a suite of Mg-bearing standards fingerprints the local environment of magnesium in the brachiopod shell powders as well as in situ analyses. In all cases, it is evident that magnesium is not hosted by organic components but is within the inorganic component of the shell. These data support the possibility of using brachiopod Mg/Ca ratios as a temperature proxy. © 2008 Published by Elsevier B.V.
1. Introduction 1.1. Brachiopods as palaeothermometers It is well established that the δ18O of brachiopod shell calcite is a source of environmental information (Lowenstam, 1961; Carpenter and Lohmann, 1995; Brand and Gao, 2003). Specifically, the inner part of the secondary layer of the shell is in oxygen isotope equilibrium with ambient seawater (Carpenter and Lohmann, 1995; Auclair et al., 2003a; Parkinson et al., 2005). Thus, brachiopods are used extensively as palaeothermometers (Popp et al., 1986; Adlis et al., 1988; Grossman et al., 1991; Auclair et al., 2003b; Korte et al., 2005; Azmy et al., 2006). Lowenstam's pioneering demonstration of the suitability of low Mgcalcite brachiopods (Rhynchonelliformea) as recorders of seawater temperature via δ18O (Lowenstam, 1961) also addressed Mg concentration. Lowenstam concluded that preliminary analyses indicated that the Mg concentration of low Mg-calcite brachiopods is out of equilibrium with seawater while the high Mg-calcite of the Craniiformea is in equilibrium with seawater Mg concentrations. Although trace and minor elements have been characterized in terms of ontogeny (Buening and Carlson, 1992; Lee et al., 2004), little has
⁎ Corresponding author. Tel.: +44 141 330 5491; fax: +44 141 330 4817. E-mail address: [email protected] (M. Cusack). 0009-2541/$ – see front matter © 2008 Published by Elsevier B.V. doi:10.1016/j.chemgeo.2008.08.007
been done to assess brachiopod Mg content as a proxy for seawater temperature until a recent demonstration that the magnesium concentration of the innermost secondary layer is an effective proxy for seawater temperature (Pérez-Huerta et al., 2008). 1.2. Mg/Ca ratio of brachiopod shells The advantage of using the Mg content as a seawater temperature proxy is that, unlike δ18O, the Mg concentration is not influenced by salinity (Klein et al., 1996) or (on geological timescales) the fluctuations in polar ice volumes. The Mg/Ca ratio of many carbonate-producing organisms such as foraminifera (Elderfield and Ganssen, 2000; Lear et al., 2002; Bentov and Erez, 2005), coccoliths (Stoll et al., 2001) and bivalves (Klein et al., 1996) record ambient temperature without the influence of salinity (Klein et al., 1996). If the Mg concentration of brachiopod shells can be used as a proxy for seawater temperature then the long brachiopod lineage (Cambrian to Recent) with diagenetically stable low Mg-calcite of rhynchonelliform brachiopods, would make this a very attractive proxy that could be applied over geological timescales. Electron probe microanalysis (EPMA) reveals that the distribution of magnesium in the shells of brachiopods from the sub-phylum with low Mg-calcite shells (Rhynchonelliformea) is heterogeneous with significantly higher magnesium concentrations in the outer (primary) layer than the inner (secondary) layer (England et al., 2007).
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Fig. 1. Back scatter electron (BSE) scanning electron microscopy (SEM) image of etched sections of (a) T. retusa, (b) N. nigricans and (c) N. anomala, in the regions where Mg XANES had been determined on polished surfaces. The outer primary layer (P) of acicular calcite is underlain by the secondary layer (S) which, in T. retusa and N. nigricans is comprised of calcite fibres while in N. anomala it is calcite semi-nacre. Scale bars = 100 µm.
Conversely, the magnesium distribution in the sub-phylum with high Mg-calcite (Craniiformea) is uniform with no significant difference between the primary and secondary layers (England et al., 2007). In rhynchonelliform brachiopods, the distinction between primary and secondary layer calcite in terms of magnesium concentration is akin to
that of δ18O in the sense that the primary layer is isotopically light and the secondary layer is in equilibrium with seawater (Carpenter and Lohmann, 1995; Auclair et al., 2003a; Parkinson et al., 2005; Parkinson and Cusack, 2007). Using an equation developed for bivalve molluscs (Vander Putten et al., 2000), the Mg/Ca ratio of the innermost
Fig. 2. XANES spectra at Mg k-edge of powdered Mg- bearing standards. (A) brucite (Mg(OH)2), dolomite (CaMg(CO3)2) and Mg associated with organic material (B) magnesium carbonate (MgCO3), Pozalagua limestone and aragonite (CaCO3). Spectra generated by scanning 1300 to 1364 eV for each scan. Number of scans averaged was dependent on the magnesium concentration such that — an average of 2 scans was required for brucite and magnesium carbonate while 8 scans were averaged for the Pozalagua calcite standard and 12 for the aragonite standard.
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secondary layer of three species of rhynchonelliform brachiopods can record the mean seawater temperature (Pérez-Huerta et al., 2008). This opens up the possibility of using Mg/Ca ratios of brachiopod shells to determine seawater palaeotemperatures. Accurate use of the Mg/Ca ratio as a temperature proxy depends on consistent substitution of Ca within the lattice by Mg in correlation to temperature based on laboratory experiments using inorganic calcite e.g. (Burton and Walter, 1991). However, biominerals are nm-scale composites of mineral and organic phases e.g. (Dauphin et al., 2003; Marin et al., 2005; Nudelman et al., 2006; Cusack et al., in press). Thus, it is essential to determine whether magnesium is indeed present as a true lattice component of the calcite. Alternatively magnesium may be bound to organic components, present as other mineral phases such as dolomite or huntite, or substituted non-ideally or inconsistently into calcite. In other marine carbonate biominerals such as coral skeletons, the use of the Sr/Ca ratio as a temperature proxy has been strengthened by the confirmation of the location of strontium within the aragonite lattice using synchrotron XAFS analyses (Finch and Allison, 2003; Finch et al., 2003; Allison et al., 2005). The suitability of X-Ray absorption near edge spectroscopy (XANES) for fingerprinting magnesium and strontium in calcite and aragonite has been demonstrated (Finch and Allison, 2007). Here we apply Mg K-edge XANES to three species of brachiopod to determine the local environment of Mg in the shells. This powerful analytical technique determines whether magnesium is a true component of the calcite lattice or associated with organic components in these natural bio-composites. The technique has been applied successfully to coral aragonite (Finch and Allison, 2008).
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materials studied by Finch and Allison (2007) but we have repeated the XANES as part of the present study since their data were collected on a different beamline and there may be systematic differences. For analyses of magnesium associated with organic components, which comprises mainly proteins, the soft tissue of the bivalve mollusc, Mytilus edulis was lyophilized and the dry powder used as a source of organic-associated magnesium in the absence of any mineral. This is similar to the organic standard used by Finch and Allison (2007, 2008). 2.3. XANES — analysis conditions XANES analyses were carried out at the Lucia beamline of the Swiss Light Source at the Paul Scherrer Institute, Switzerland (Flank et al., 2006). XANES data were collected by scanning X-rays between 1300 and 1364 eV in a beam of width 4.5 µm and height 10 µm, recording the fluorescence yield of the Mg Kα secondary radiation using a silicon drift diode detector. The active area of the detector is 10 mm2 and has an energy resolution of about 120 eV at the Mg K-edge at a maximum count rate of about 105 per second. The samples were glued onto a copper plate, which was mounted perpendicular to the incoming beam. The fluorescence detector made an angle of 12° with respect to the sample surface. This grazing-exit set-up allows minimizing the socalled self-absorption effect for concentrated samples (Grolimund
2. Materials and methods 2.1. Brachiopod samples Two species of rhynchonelliform brachiopod, Terebratulina retusa and Notosaria nigricans and one craniid species, Novocrania anomala were analysed. Specimens of T. retusa and N. anomala were collected from the Firth of Lorn, Oban, NW Scotland (56° 24'N, 5°38'W) at a depth of 200 m. Specimens were transported in seawater to the University of Glasgow where all soft tissues was removed using dental tools. N. nigricans was from Otago Shelf, South Island, New Zealand (45°S, 170°E). Valves were cleaned in an ultrasonic bath using an aqueous solution of sodium hypochlorite (1% v/v) for 2 min and thoroughly rinsed in Milli Q™ water. 2.2. XANES — sample preparation XANES was performed on powders and polished blocks. Several specimens of each species were powdered together for XANES analysis. For in situ XANES, shells were cut longitudinally along the plane of symmetry and polished to display the shell thickness through outer primary to inner secondary layers. Cut shells were embedded in epoxy resin in 1 cm diameter cylindrical blocks of 0.5 cm thickness and the shell sections polished through a series of grinding and polishing discs. Initially the sample surface is ground down using diamond impregnated papers at 74 µm and then 20 µm, diamond slurry at 8 µm then 6 µm are followed by a compound diamond pad at 6 µm then 3 µm. The polishing stages are performed with alpha aluminium oxide at 1 µm and 0.3 µm with a final polish with 0.06 µm colloidal silica on a short nap disc before etching for 12 min with a 1% (v/v) aqueous solution of ethanoic acid to remove any surface contamination. A suite of Mg-bearing powdered standards including brucite, magnesium carbonate (magnesite), dolomite, aragonite, Pozalagua calcite (Finch and Allison, 2008) and Mg hosted within organic material were included. The inorganic standards are the same
Fig. 3. XANES spectra at Mg k-edge of powdered shells of two brachiopod species, T. retusa, and N. nigricans have low Mg-calcite while N. anomala has a high Mg-calcite shell.
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et al., 2004). Magnesium fluorescence maps were obtained from delivering primary X-rays of 1350 eV with the same experimental setup. Resulting spectra were obtained throughout averaging 4–6 scans in each analysis with about 8 h of acquisition time per 4 scans. Data were processed using Athena software version 0.5.084 [http://cars9. uchicago.edu/~ifeffit] (Ravel and Newville, 2005). 2.4. Scanning Electron Microscopy (SEM) — sample preparation After XANES analyses of the polished brachiopod shell sections, the sections were etched, to reveal structural detail, by 10 s incubation in
an aqueous solution of HCl (5% v/v) before rinsing in MilliQ™ water. Dried uncoated samples were viewed in an FEI-Quanta 200 SEM in low vacuum mode with an accelerating voltage of 20 kV. 3. Results Back scatter electron (BSE) scanning electron microscopy (SEM) images of etched sections in the regions of the Mg-XANES analyses for the three brachiopod species are presented in Fig. 1. The secondary layer accounts for the majority of shell thickness in all cases. In the low Mg-calcite brachiopods T. retusa (Fig. 1a) and N.
Fig. 4. Maps of magnesium distribution throughout shell thickness in (A) T. retusa, (B) N. nigricans and (C) N. anomala. Magnesium distribution maps generated by magnesium fluorescence as a result of X-ray absorption. In each map, the outermost shell is to the top with the extent of the primary layer (P) outlined with black hashed lines. (D) Colour scale indicates fluorescence count rate (counts s− 1). All three maps have the same colour scale. Points 1–3 on each map indicate location of 3 XANES spectra at Mg K-edge below each magnesium map with TR1-3 for the locations in T. retusa, NN1-3 for N. nigricans and NA1-3 for N. anomala.
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nigricans (Fig. 1b) the secondary layer is composed of calcite fibres while in the high Mg-calcite craniid, N. anomala (Fig. 1c) the secondary layer comprises calcite semi-nacre. The XANES of the standards and brachiopod samples are presented in Fig. 2. The XANES are identical to those of Finch and Allison (2007) showing no systematic differences resulting from the use of a different beamline between those data and ours. Peaks in XANES spectra result from transition of the 1 s electron to p empty states and the multiple scattering of the photoelectron with the surrounding atoms of the Mg. Presence or absence of specific peaks is characteristic for each standard (Fig. 2). Thus the sensitivity of the Mg-K XANES as a fingerprinting tool is demonstrated by the strikingly diverse spectra of the standards reflecting the different Mg local coordination states of magnesium in each standard (Fig. 2). Importantly, the spectrum for organic-associated magnesium is distinct from any of the mineral standards by being somewhat featureless after the edge. This lack of features results from the fact that the elements that are predominant in organic components such as carbon and hydrogen, have poor electron backscattering and thus lack XANES resonances (Finch and Allison, 2007). The resultant, fairly featureless XANES is readily distinguished from XANES obtained from all the inorganic standards, notably those of the calcite standards. XANES spectra of the shell powders are uniform for all three brachiopod species (Fig. 3). The spectra in Fig. 3 are very similar to those obtained from Pozalagua calcite, suggesting that magnesium is hosted in the brachiopod calcite in a similar structural state to that in Pozalagua calcite. The XANES is quite different to that of the organic standard and we therefore infer that Mg is indeed hosted within the inorganic (calcite) component of the shell. In situ analyses were carried out to determine the distribution of magnesium throughout the shell and to then inform the in situ XANES analyses. XANES spectra were obtained from particular locations within the shell rather than simply obtaining spectra from the overall composition as in Fig. 3. X-ray absorption generates secondary X-ray fluorescence that enables the distribution of magnesium to be determined. Maps of Mg Kα-fluorescence through the thickness of the three brachiopod species indicate the common pattern among rhynchonelliform brachiopods of higher magnesium concentration in the primary layer (Fig. 4A,B) that has been described previously (England et al., 2007; Pérez-Huerta et al., 2008; Cusack et al., 2008b). Conversely, while the magnesium concentration in the craniid, N. anomala is fairly uniform with no significant difference between primary and secondary layers (England et al., 2007), the map of secondary fluorescence indicates that the outermost layer is a little depleted in magnesium as indicated by the Mg map (Fig. 4C). Small differences in the spectra of the different shells and across the different layers can be explained by the angular dependence of the absorption (Pérez-Huerta et al., in press). The shells are composed of small calcite crystallites that are oriented for each species (Cusack et al., 2007, 2008c; Pérez-Huerta and Cusack, 2008; Cusack et al., in press). Since calcite shows a strong X-ray dichroism, the absorption spectrum will depend on the orientation of those crystallites. This is not the case for the powder spectra where one averages over all angles. 4. Discussion The Mg/Ca ratio of the innermost half of the secondary layer of brachiopod shells corresponds with ambient seawater temperature when the equation developed for M. edulis (Vander Putten et al., 2000) is applied (Pérez-Huerta et al., 2008). This relationship between magnesium concentration and seawater temperature may simply be coincidental if merely based on the assumption that magnesium is present in the calcite lattice. The data here confirm that magnesium is not associated with the organic components of the shell in both rhynchonelliform and craniid brachiopods. This confirmation sup-
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Fig. 5. Mean concentration and range of magnesium concentration in primary (■) and secondary (●) layer of T. retusa and the entire shell of N. anomala (▲) where there is no significant difference in Mg concentration between primary and secondary layers. Data from (England et al., 2007).
ports the potential of this climate proxy in low Mg-calcite-shelled brachiopods. The pattern of high magnesium concentration in the primary layer and lower in secondary layer (Fig. 5) of rhynchonelliform brachiopods is well established (Cusack and Williams, 2007; England et al., 2007; Pérez-Huerta et al., 2008; Cusack et al., 2008a)}. Likewise, it has been noted that the transition from high to low magnesium concentrations is not always as abrupt as the switch from acicular calcite of the primary layer to the calcite fibres of the secondary layer (England et al., 2007; Cusack et al., 2008a). An example of higher magnesium concentrations persisting into the secondary layer is evident in Fig. 4A. This distribution pattern suggests that magnesium may be associated with organic components. Maps of magnesium distribution are therefore important to inform the selection of locations of in situ XANES spectroscopy. Thus, this area with a higher magnesium concentration than the surrounding secondary layer (Area 2 in Fig. 4A) was included in the in situ XANES spectroscopy and it was determined that, even here, despite appearance, magnesium is not associated with organic components. Craniid brachiopods have high concentrations of magnesium throughout the shell thickness (Fig. 5) although here we reveal that the primary layer of N. anomala is somewhat depleted in magnesium relative to the semi-nacreous secondary layer. Although these data confirm that magnesium is located within the lattice throughout the thickness of N. anomala the fact that the shell contains higher Mg/Ca ratios than seawater indicates that, unlike rhynchonelliform brachiopods, the Mg concentration in craniid shells will not determine seawater temperature via the equation developed for M. edulis by (Vander Putten et al., 2000). Further work is required to measure magnesium concentration in craniids from different water temperatures in order to either develop an equation that relates craniid shell magnesium concentration to seawater temperature or conclude that, despite being a lattice component, craniid shell magnesium concentration cannot be used as a proxy for seawater temperature. This situation where magnesium is hosted within the mineral component of brachiopod shells differs from that of magnesium within coral aragonite where magnesium is hosted within a disordered phase (Finch and Allison, 2008). This emphasizes the requirement to test the assumption that magnesium is a lattice component in individual systems that are employed in palaeoproxy studies. Acknowledgments MC, APH & AF gratefully acknowledge the funding for this work from the Swiss Light source (ID 20070868) and from the European Commission under the 6th Framework Programme through the Key Action: Strengthening the European Research Area, Research
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Infrastructures (Contract n°: RII3-CT-2004-506008). MC and APH acknowledge financial support from the BBSRC (BB/E003265/1). We are grateful to the Scottish Association for Marine Science, (SAMS), Dunstaffnage Marine Laboratory, Oban Scotland, especially Jim Watson and the Captain and crew of RV Calanus, for their considerable assistance in brachiopod collection in the Firth of Lorn. J. Gilleece is thanked for his help in the preparation of polished blocks and Les Hill and Mike Shand are thanked for their help with the preparation of Fig. 4. This work is in-keeping with Theme 3 (Atmosphere, Oceans and Climate) of SAGES (Scottish Alliance for Geoscience, Environment and Society). References Adlis, D.S., Grossman, E.L., Yancey, T.E., McLerran, R.D., 1988. Isotope stratigraphy and paleodepth changes of Pennsylvanian cyclical sedimentary deposits. Palaios 3, 487–506. Allison, N., Finch, A.A., Newville, M., Sutton, S.R., 2005. Strontium in coral aragonite: 3. Sr coordination and geochemistry in relation to skeletal architecture. Geochimica et Cosmochimica Acta 69, 3801–3811. Auclair, A.-C., Joachimski, M.M., Lécuyer, C., 2003a. Deciphering kinetic, metabolic and environmental controls on stable isotope fractions between seawater and the shell of Terebratalia transversa (Brachiopoda). Chemical Geology 202, 59–78. Auclair, A.C., Joachimski, M.M., Lecuyer, C., 2003b. Stable isotope composition of modern and fossil brachiopod shell calcite: physiological and environmental controls. Geophysical Research Abstracts 5, 13334. Azmy, K., Veizer, J., Jin, J., Copper, P., Brand, U., 2006. Paleobathymetry of a Silurian shelf based on brachiopod assemblages: an oxygen isotope test. Canadian Journal Of Earth Sciences 43, 281–293. Bentov, S., Erez, J., 2005. Novel observations on biomineralization processes in foraminifera and implications for Mg/Ca ratio in the shells. Geology 33, 841–844. Brand, U., Gao, Y.W., 2003. Chemostratigraphy and correlation of the Late Pennsylvanian Madera Formation, Canon de San Diego, New Mexico, USA. Carbonates And Evaporites 18, 151–170. Buening, N., Carlson, S.J., 1992. Geochemical investigation of growth in selected Recent articulate brachiopods. Lethaia 25, 331–345. Burton, E.A., Walter, L.M., 1991. The effects of pCO2 and temperature on magnesium incorporation in calcite in seawater and MgCl2–CaCl2 solutions. Geochimica et Cosmochimica Acta 55, 777–785. Carpenter, S.J., Lohmann, K.C., 1995. δ18 O and δ13 C values of modern brachiopod shells. Geochimica et Cosmochimica Acta 59, 3748–3764. Cusack, M., Williams, A., 2007. Biochemistry & diversity of brachiopod shells. In: Kaesler, R. (Ed.), Treatise on Invertebrate Paleontology Part H, Brachiopoda. Geol. Soc. Am. & Univ. Kansas, New York, pp. 2373–2395. Cusack, M., Dauphin, Y., Chung, P., Pérez-Huerta, A. and Cuif, J.P., in press. Multiscale structure of calcite fibres of the shell of the brachiopod Terebratulina retusa. Journal of Structural Biology. Cusack, M., Perez-Huerta, A., Dalbeck, P., 2007. Common crystallographic control in calcite biomineralization of bivalved shells. Crystengcomm 9, 1215–1218. Cusack, M., et al., 2008a. Micro-XANES mapping of sulphur and its association with magnesium and phosphorus in the shell of the brachiopod, Terebratulina retusa. Chemical Geology 253, 172–179. Cusack, M., et al., 2008b. Oxygen isotope composition, magnesium distribution and crystallography of Terebratulina retusa. Fossils & Strata 54, 259–267. Cusack, M., Pérez-Huerta, A., Dalbeck, P., Chung, P., Lee, M.R., 2008c. Comparison of calcite crystallographic texture in the shells of the rhynchonelliform brachiopod, Terebratulina retusa and the bivalve mollusc, Mytilus edulis. Proceedings of the 15th International Conference on Textures of Materials., USA. Dauphin, Y., Guzman, N., Denis, A., Cuif, J.P., Ortlieb, L., 2003. Microstructure, nanostructure and composition of the shell of Concholepas concholepas (Gastropoda, Muricidae). Aquatic Living Resources 16, 95–103. Elderfield, H., Ganssen, G., 2000. Past temperature and δ18 0 of surface ocean waters inferred from foraminiferal Mg/Ca ratios. Nature 405, 442–445. England, J., Cusack, M., Lee, M.R., 2007. Magnesium and sulphur in the calcite shells of two brachiopods, Terebratulina retusa and Novocrania anomala. Lethaia 40, 2–10.
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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
Magnesium in the lattice of calcite-shelled brachiopods Maggie Cusack a,⁎, Alberto Pérez-Huerta a, Markus Janousch b, Adrian A. Finch c a b c
Department of Geographical & Earth Sciences, University of Glasgow, G12 8QQ Glasgow, UK Swiss Light Source, Paul Scherrer Institute, Switzerland School of Geography & Geosciences, University of St. Andrews, KY16 9AL, UK
a r t i c l e
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Article history: Received 8 May 2008 Received in revised form 31 July 2008 Accepted 9 August 2008 Editor: D. Rickard Keywords: XANES at Mg K-edge Synchrotron Magnesium Calcite
a b s t r a c t Palaeoclimate information is often extracted from Rhynchonelliform brachiopod shell calcite, in particular the inner secondary layer, via the δ18O composition, which is a proxy for seawater temperature. Compared to δ18O, the potential for Mg/Ca ratio, as a brachiopod seawater temperature proxy, has been neglected. The use of Mg/Ca ratio as a temperature proxy assumes that, with increasing temperature, more Mg substitutes for Ca in the calcite lattice. Brachiopod shells, like all biominerals, are composites of organic and inorganic components. This raises the possibility that magnesium is hosted by the organic components. Alternatively, magnesium may be present as a separate mineral phase, rather than a true component of the calcite lattice, or incorporated into calcite in non-ideal or variable coordination. Here we use synchrotron X-ray absorption Near Edge Spectroscopy (XANES) at the Mg K-edge to determine the local environment of magnesium in two species of brachiopod with low Mg-calcite shells, Terebratulina retusa and Notosaria nigricans and one species with a high Mg-calcite shell, Novocrania anomala. XANES at the Mg K-edge of a suite of Mg-bearing standards fingerprints the local environment of magnesium in the brachiopod shell powders as well as in situ analyses. In all cases, it is evident that magnesium is not hosted by organic components but is within the inorganic component of the shell. These data support the possibility of using brachiopod Mg/Ca ratios as a temperature proxy. © 2008 Published by Elsevier B.V.
1. Introduction 1.1. Brachiopods as palaeothermometers It is well established that the δ18O of brachiopod shell calcite is a source of environmental information (Lowenstam, 1961; Carpenter and Lohmann, 1995; Brand and Gao, 2003). Specifically, the inner part of the secondary layer of the shell is in oxygen isotope equilibrium with ambient seawater (Carpenter and Lohmann, 1995; Auclair et al., 2003a; Parkinson et al., 2005). Thus, brachiopods are used extensively as palaeothermometers (Popp et al., 1986; Adlis et al., 1988; Grossman et al., 1991; Auclair et al., 2003b; Korte et al., 2005; Azmy et al., 2006). Lowenstam's pioneering demonstration of the suitability of low Mgcalcite brachiopods (Rhynchonelliformea) as recorders of seawater temperature via δ18O (Lowenstam, 1961) also addressed Mg concentration. Lowenstam concluded that preliminary analyses indicated that the Mg concentration of low Mg-calcite brachiopods is out of equilibrium with seawater while the high Mg-calcite of the Craniiformea is in equilibrium with seawater Mg concentrations. Although trace and minor elements have been characterized in terms of ontogeny (Buening and Carlson, 1992; Lee et al., 2004), little has
⁎ Corresponding author. Tel.: +44 141 330 5491; fax: +44 141 330 4817. E-mail address: [email protected] (M. Cusack). 0009-2541/$ – see front matter © 2008 Published by Elsevier B.V. doi:10.1016/j.chemgeo.2008.08.007
been done to assess brachiopod Mg content as a proxy for seawater temperature until a recent demonstration that the magnesium concentration of the innermost secondary layer is an effective proxy for seawater temperature (Pérez-Huerta et al., 2008). 1.2. Mg/Ca ratio of brachiopod shells The advantage of using the Mg content as a seawater temperature proxy is that, unlike δ18O, the Mg concentration is not influenced by salinity (Klein et al., 1996) or (on geological timescales) the fluctuations in polar ice volumes. The Mg/Ca ratio of many carbonate-producing organisms such as foraminifera (Elderfield and Ganssen, 2000; Lear et al., 2002; Bentov and Erez, 2005), coccoliths (Stoll et al., 2001) and bivalves (Klein et al., 1996) record ambient temperature without the influence of salinity (Klein et al., 1996). If the Mg concentration of brachiopod shells can be used as a proxy for seawater temperature then the long brachiopod lineage (Cambrian to Recent) with diagenetically stable low Mg-calcite of rhynchonelliform brachiopods, would make this a very attractive proxy that could be applied over geological timescales. Electron probe microanalysis (EPMA) reveals that the distribution of magnesium in the shells of brachiopods from the sub-phylum with low Mg-calcite shells (Rhynchonelliformea) is heterogeneous with significantly higher magnesium concentrations in the outer (primary) layer than the inner (secondary) layer (England et al., 2007).
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Fig. 1. Back scatter electron (BSE) scanning electron microscopy (SEM) image of etched sections of (a) T. retusa, (b) N. nigricans and (c) N. anomala, in the regions where Mg XANES had been determined on polished surfaces. The outer primary layer (P) of acicular calcite is underlain by the secondary layer (S) which, in T. retusa and N. nigricans is comprised of calcite fibres while in N. anomala it is calcite semi-nacre. Scale bars = 100 µm.
Conversely, the magnesium distribution in the sub-phylum with high Mg-calcite (Craniiformea) is uniform with no significant difference between the primary and secondary layers (England et al., 2007). In rhynchonelliform brachiopods, the distinction between primary and secondary layer calcite in terms of magnesium concentration is akin to
that of δ18O in the sense that the primary layer is isotopically light and the secondary layer is in equilibrium with seawater (Carpenter and Lohmann, 1995; Auclair et al., 2003a; Parkinson et al., 2005; Parkinson and Cusack, 2007). Using an equation developed for bivalve molluscs (Vander Putten et al., 2000), the Mg/Ca ratio of the innermost
Fig. 2. XANES spectra at Mg k-edge of powdered Mg- bearing standards. (A) brucite (Mg(OH)2), dolomite (CaMg(CO3)2) and Mg associated with organic material (B) magnesium carbonate (MgCO3), Pozalagua limestone and aragonite (CaCO3). Spectra generated by scanning 1300 to 1364 eV for each scan. Number of scans averaged was dependent on the magnesium concentration such that — an average of 2 scans was required for brucite and magnesium carbonate while 8 scans were averaged for the Pozalagua calcite standard and 12 for the aragonite standard.
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secondary layer of three species of rhynchonelliform brachiopods can record the mean seawater temperature (Pérez-Huerta et al., 2008). This opens up the possibility of using Mg/Ca ratios of brachiopod shells to determine seawater palaeotemperatures. Accurate use of the Mg/Ca ratio as a temperature proxy depends on consistent substitution of Ca within the lattice by Mg in correlation to temperature based on laboratory experiments using inorganic calcite e.g. (Burton and Walter, 1991). However, biominerals are nm-scale composites of mineral and organic phases e.g. (Dauphin et al., 2003; Marin et al., 2005; Nudelman et al., 2006; Cusack et al., in press). Thus, it is essential to determine whether magnesium is indeed present as a true lattice component of the calcite. Alternatively magnesium may be bound to organic components, present as other mineral phases such as dolomite or huntite, or substituted non-ideally or inconsistently into calcite. In other marine carbonate biominerals such as coral skeletons, the use of the Sr/Ca ratio as a temperature proxy has been strengthened by the confirmation of the location of strontium within the aragonite lattice using synchrotron XAFS analyses (Finch and Allison, 2003; Finch et al., 2003; Allison et al., 2005). The suitability of X-Ray absorption near edge spectroscopy (XANES) for fingerprinting magnesium and strontium in calcite and aragonite has been demonstrated (Finch and Allison, 2007). Here we apply Mg K-edge XANES to three species of brachiopod to determine the local environment of Mg in the shells. This powerful analytical technique determines whether magnesium is a true component of the calcite lattice or associated with organic components in these natural bio-composites. The technique has been applied successfully to coral aragonite (Finch and Allison, 2008).
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materials studied by Finch and Allison (2007) but we have repeated the XANES as part of the present study since their data were collected on a different beamline and there may be systematic differences. For analyses of magnesium associated with organic components, which comprises mainly proteins, the soft tissue of the bivalve mollusc, Mytilus edulis was lyophilized and the dry powder used as a source of organic-associated magnesium in the absence of any mineral. This is similar to the organic standard used by Finch and Allison (2007, 2008). 2.3. XANES — analysis conditions XANES analyses were carried out at the Lucia beamline of the Swiss Light Source at the Paul Scherrer Institute, Switzerland (Flank et al., 2006). XANES data were collected by scanning X-rays between 1300 and 1364 eV in a beam of width 4.5 µm and height 10 µm, recording the fluorescence yield of the Mg Kα secondary radiation using a silicon drift diode detector. The active area of the detector is 10 mm2 and has an energy resolution of about 120 eV at the Mg K-edge at a maximum count rate of about 105 per second. The samples were glued onto a copper plate, which was mounted perpendicular to the incoming beam. The fluorescence detector made an angle of 12° with respect to the sample surface. This grazing-exit set-up allows minimizing the socalled self-absorption effect for concentrated samples (Grolimund
2. Materials and methods 2.1. Brachiopod samples Two species of rhynchonelliform brachiopod, Terebratulina retusa and Notosaria nigricans and one craniid species, Novocrania anomala were analysed. Specimens of T. retusa and N. anomala were collected from the Firth of Lorn, Oban, NW Scotland (56° 24'N, 5°38'W) at a depth of 200 m. Specimens were transported in seawater to the University of Glasgow where all soft tissues was removed using dental tools. N. nigricans was from Otago Shelf, South Island, New Zealand (45°S, 170°E). Valves were cleaned in an ultrasonic bath using an aqueous solution of sodium hypochlorite (1% v/v) for 2 min and thoroughly rinsed in Milli Q™ water. 2.2. XANES — sample preparation XANES was performed on powders and polished blocks. Several specimens of each species were powdered together for XANES analysis. For in situ XANES, shells were cut longitudinally along the plane of symmetry and polished to display the shell thickness through outer primary to inner secondary layers. Cut shells were embedded in epoxy resin in 1 cm diameter cylindrical blocks of 0.5 cm thickness and the shell sections polished through a series of grinding and polishing discs. Initially the sample surface is ground down using diamond impregnated papers at 74 µm and then 20 µm, diamond slurry at 8 µm then 6 µm are followed by a compound diamond pad at 6 µm then 3 µm. The polishing stages are performed with alpha aluminium oxide at 1 µm and 0.3 µm with a final polish with 0.06 µm colloidal silica on a short nap disc before etching for 12 min with a 1% (v/v) aqueous solution of ethanoic acid to remove any surface contamination. A suite of Mg-bearing powdered standards including brucite, magnesium carbonate (magnesite), dolomite, aragonite, Pozalagua calcite (Finch and Allison, 2008) and Mg hosted within organic material were included. The inorganic standards are the same
Fig. 3. XANES spectra at Mg k-edge of powdered shells of two brachiopod species, T. retusa, and N. nigricans have low Mg-calcite while N. anomala has a high Mg-calcite shell.
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et al., 2004). Magnesium fluorescence maps were obtained from delivering primary X-rays of 1350 eV with the same experimental setup. Resulting spectra were obtained throughout averaging 4–6 scans in each analysis with about 8 h of acquisition time per 4 scans. Data were processed using Athena software version 0.5.084 [http://cars9. uchicago.edu/~ifeffit] (Ravel and Newville, 2005). 2.4. Scanning Electron Microscopy (SEM) — sample preparation After XANES analyses of the polished brachiopod shell sections, the sections were etched, to reveal structural detail, by 10 s incubation in
an aqueous solution of HCl (5% v/v) before rinsing in MilliQ™ water. Dried uncoated samples were viewed in an FEI-Quanta 200 SEM in low vacuum mode with an accelerating voltage of 20 kV. 3. Results Back scatter electron (BSE) scanning electron microscopy (SEM) images of etched sections in the regions of the Mg-XANES analyses for the three brachiopod species are presented in Fig. 1. The secondary layer accounts for the majority of shell thickness in all cases. In the low Mg-calcite brachiopods T. retusa (Fig. 1a) and N.
Fig. 4. Maps of magnesium distribution throughout shell thickness in (A) T. retusa, (B) N. nigricans and (C) N. anomala. Magnesium distribution maps generated by magnesium fluorescence as a result of X-ray absorption. In each map, the outermost shell is to the top with the extent of the primary layer (P) outlined with black hashed lines. (D) Colour scale indicates fluorescence count rate (counts s− 1). All three maps have the same colour scale. Points 1–3 on each map indicate location of 3 XANES spectra at Mg K-edge below each magnesium map with TR1-3 for the locations in T. retusa, NN1-3 for N. nigricans and NA1-3 for N. anomala.
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nigricans (Fig. 1b) the secondary layer is composed of calcite fibres while in the high Mg-calcite craniid, N. anomala (Fig. 1c) the secondary layer comprises calcite semi-nacre. The XANES of the standards and brachiopod samples are presented in Fig. 2. The XANES are identical to those of Finch and Allison (2007) showing no systematic differences resulting from the use of a different beamline between those data and ours. Peaks in XANES spectra result from transition of the 1 s electron to p empty states and the multiple scattering of the photoelectron with the surrounding atoms of the Mg. Presence or absence of specific peaks is characteristic for each standard (Fig. 2). Thus the sensitivity of the Mg-K XANES as a fingerprinting tool is demonstrated by the strikingly diverse spectra of the standards reflecting the different Mg local coordination states of magnesium in each standard (Fig. 2). Importantly, the spectrum for organic-associated magnesium is distinct from any of the mineral standards by being somewhat featureless after the edge. This lack of features results from the fact that the elements that are predominant in organic components such as carbon and hydrogen, have poor electron backscattering and thus lack XANES resonances (Finch and Allison, 2007). The resultant, fairly featureless XANES is readily distinguished from XANES obtained from all the inorganic standards, notably those of the calcite standards. XANES spectra of the shell powders are uniform for all three brachiopod species (Fig. 3). The spectra in Fig. 3 are very similar to those obtained from Pozalagua calcite, suggesting that magnesium is hosted in the brachiopod calcite in a similar structural state to that in Pozalagua calcite. The XANES is quite different to that of the organic standard and we therefore infer that Mg is indeed hosted within the inorganic (calcite) component of the shell. In situ analyses were carried out to determine the distribution of magnesium throughout the shell and to then inform the in situ XANES analyses. XANES spectra were obtained from particular locations within the shell rather than simply obtaining spectra from the overall composition as in Fig. 3. X-ray absorption generates secondary X-ray fluorescence that enables the distribution of magnesium to be determined. Maps of Mg Kα-fluorescence through the thickness of the three brachiopod species indicate the common pattern among rhynchonelliform brachiopods of higher magnesium concentration in the primary layer (Fig. 4A,B) that has been described previously (England et al., 2007; Pérez-Huerta et al., 2008; Cusack et al., 2008b). Conversely, while the magnesium concentration in the craniid, N. anomala is fairly uniform with no significant difference between primary and secondary layers (England et al., 2007), the map of secondary fluorescence indicates that the outermost layer is a little depleted in magnesium as indicated by the Mg map (Fig. 4C). Small differences in the spectra of the different shells and across the different layers can be explained by the angular dependence of the absorption (Pérez-Huerta et al., in press). The shells are composed of small calcite crystallites that are oriented for each species (Cusack et al., 2007, 2008c; Pérez-Huerta and Cusack, 2008; Cusack et al., in press). Since calcite shows a strong X-ray dichroism, the absorption spectrum will depend on the orientation of those crystallites. This is not the case for the powder spectra where one averages over all angles. 4. Discussion The Mg/Ca ratio of the innermost half of the secondary layer of brachiopod shells corresponds with ambient seawater temperature when the equation developed for M. edulis (Vander Putten et al., 2000) is applied (Pérez-Huerta et al., 2008). This relationship between magnesium concentration and seawater temperature may simply be coincidental if merely based on the assumption that magnesium is present in the calcite lattice. The data here confirm that magnesium is not associated with the organic components of the shell in both rhynchonelliform and craniid brachiopods. This confirmation sup-
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Fig. 5. Mean concentration and range of magnesium concentration in primary (■) and secondary (●) layer of T. retusa and the entire shell of N. anomala (▲) where there is no significant difference in Mg concentration between primary and secondary layers. Data from (England et al., 2007).
ports the potential of this climate proxy in low Mg-calcite-shelled brachiopods. The pattern of high magnesium concentration in the primary layer and lower in secondary layer (Fig. 5) of rhynchonelliform brachiopods is well established (Cusack and Williams, 2007; England et al., 2007; Pérez-Huerta et al., 2008; Cusack et al., 2008a)}. Likewise, it has been noted that the transition from high to low magnesium concentrations is not always as abrupt as the switch from acicular calcite of the primary layer to the calcite fibres of the secondary layer (England et al., 2007; Cusack et al., 2008a). An example of higher magnesium concentrations persisting into the secondary layer is evident in Fig. 4A. This distribution pattern suggests that magnesium may be associated with organic components. Maps of magnesium distribution are therefore important to inform the selection of locations of in situ XANES spectroscopy. Thus, this area with a higher magnesium concentration than the surrounding secondary layer (Area 2 in Fig. 4A) was included in the in situ XANES spectroscopy and it was determined that, even here, despite appearance, magnesium is not associated with organic components. Craniid brachiopods have high concentrations of magnesium throughout the shell thickness (Fig. 5) although here we reveal that the primary layer of N. anomala is somewhat depleted in magnesium relative to the semi-nacreous secondary layer. Although these data confirm that magnesium is located within the lattice throughout the thickness of N. anomala the fact that the shell contains higher Mg/Ca ratios than seawater indicates that, unlike rhynchonelliform brachiopods, the Mg concentration in craniid shells will not determine seawater temperature via the equation developed for M. edulis by (Vander Putten et al., 2000). Further work is required to measure magnesium concentration in craniids from different water temperatures in order to either develop an equation that relates craniid shell magnesium concentration to seawater temperature or conclude that, despite being a lattice component, craniid shell magnesium concentration cannot be used as a proxy for seawater temperature. This situation where magnesium is hosted within the mineral component of brachiopod shells differs from that of magnesium within coral aragonite where magnesium is hosted within a disordered phase (Finch and Allison, 2008). This emphasizes the requirement to test the assumption that magnesium is a lattice component in individual systems that are employed in palaeoproxy studies. Acknowledgments MC, APH & AF gratefully acknowledge the funding for this work from the Swiss Light source (ID 20070868) and from the European Commission under the 6th Framework Programme through the Key Action: Strengthening the European Research Area, Research
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Infrastructures (Contract n°: RII3-CT-2004-506008). MC and APH acknowledge financial support from the BBSRC (BB/E003265/1). We are grateful to the Scottish Association for Marine Science, (SAMS), Dunstaffnage Marine Laboratory, Oban Scotland, especially Jim Watson and the Captain and crew of RV Calanus, for their considerable assistance in brachiopod collection in the Firth of Lorn. J. Gilleece is thanked for his help in the preparation of polished blocks and Les Hill and Mike Shand are thanked for their help with the preparation of Fig. 4. This work is in-keeping with Theme 3 (Atmosphere, Oceans and Climate) of SAGES (Scottish Alliance for Geoscience, Environment and Society). References Adlis, D.S., Grossman, E.L., Yancey, T.E., McLerran, R.D., 1988. Isotope stratigraphy and paleodepth changes of Pennsylvanian cyclical sedimentary deposits. Palaios 3, 487–506. Allison, N., Finch, A.A., Newville, M., Sutton, S.R., 2005. Strontium in coral aragonite: 3. Sr coordination and geochemistry in relation to skeletal architecture. Geochimica et Cosmochimica Acta 69, 3801–3811. Auclair, A.-C., Joachimski, M.M., Lécuyer, C., 2003a. Deciphering kinetic, metabolic and environmental controls on stable isotope fractions between seawater and the shell of Terebratalia transversa (Brachiopoda). Chemical Geology 202, 59–78. Auclair, A.C., Joachimski, M.M., Lecuyer, C., 2003b. Stable isotope composition of modern and fossil brachiopod shell calcite: physiological and environmental controls. Geophysical Research Abstracts 5, 13334. Azmy, K., Veizer, J., Jin, J., Copper, P., Brand, U., 2006. Paleobathymetry of a Silurian shelf based on brachiopod assemblages: an oxygen isotope test. Canadian Journal Of Earth Sciences 43, 281–293. Bentov, S., Erez, J., 2005. Novel observations on biomineralization processes in foraminifera and implications for Mg/Ca ratio in the shells. Geology 33, 841–844. Brand, U., Gao, Y.W., 2003. Chemostratigraphy and correlation of the Late Pennsylvanian Madera Formation, Canon de San Diego, New Mexico, USA. Carbonates And Evaporites 18, 151–170. Buening, N., Carlson, S.J., 1992. Geochemical investigation of growth in selected Recent articulate brachiopods. Lethaia 25, 331–345. Burton, E.A., Walter, L.M., 1991. The effects of pCO2 and temperature on magnesium incorporation in calcite in seawater and MgCl2–CaCl2 solutions. Geochimica et Cosmochimica Acta 55, 777–785. Carpenter, S.J., Lohmann, K.C., 1995. δ18 O and δ13 C values of modern brachiopod shells. Geochimica et Cosmochimica Acta 59, 3748–3764. Cusack, M., Williams, A., 2007. Biochemistry & diversity of brachiopod shells. In: Kaesler, R. (Ed.), Treatise on Invertebrate Paleontology Part H, Brachiopoda. Geol. Soc. Am. & Univ. Kansas, New York, pp. 2373–2395. Cusack, M., Dauphin, Y., Chung, P., Pérez-Huerta, A. and Cuif, J.P., in press. Multiscale structure of calcite fibres of the shell of the brachiopod Terebratulina retusa. Journal of Structural Biology. Cusack, M., Perez-Huerta, A., Dalbeck, P., 2007. Common crystallographic control in calcite biomineralization of bivalved shells. Crystengcomm 9, 1215–1218. Cusack, M., et al., 2008a. Micro-XANES mapping of sulphur and its association with magnesium and phosphorus in the shell of the brachiopod, Terebratulina retusa. Chemical Geology 253, 172–179. Cusack, M., et al., 2008b. Oxygen isotope composition, magnesium distribution and crystallography of Terebratulina retusa. Fossils & Strata 54, 259–267. Cusack, M., Pérez-Huerta, A., Dalbeck, P., Chung, P., Lee, M.R., 2008c. Comparison of calcite crystallographic texture in the shells of the rhynchonelliform brachiopod, Terebratulina retusa and the bivalve mollusc, Mytilus edulis. Proceedings of the 15th International Conference on Textures of Materials., USA. Dauphin, Y., Guzman, N., Denis, A., Cuif, J.P., Ortlieb, L., 2003. Microstructure, nanostructure and composition of the shell of Concholepas concholepas (Gastropoda, Muricidae). Aquatic Living Resources 16, 95–103. Elderfield, H., Ganssen, G., 2000. Past temperature and δ18 0 of surface ocean waters inferred from foraminiferal Mg/Ca ratios. Nature 405, 442–445. England, J., Cusack, M., Lee, M.R., 2007. Magnesium and sulphur in the calcite shells of two brachiopods, Terebratulina retusa and Novocrania anomala. Lethaia 40, 2–10.
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