Possible controls on Li, Na, and Mg incorporation into aragonite coral skeletons

Chemical Geology 396 (2015) 98–111

Contents lists available at ScienceDirect

Chemical Geology journal homepage: www.elsevier.com/locate/chemgeo

Possible controls on Li, Na, and Mg incorporation into aragonite coral skeletons Claire Rollion-Bard a,⁎, Dominique Blamart b a b

Institut de Physique du Globe de Paris (IPGP), UMR CNRS 7154, Université Paris Diderot, 1 Rue Jussieu, F-75238 Paris Cedex 05, France Laboratoire des Sciences du Climat et de l'Environnement, Avenue de la Terrasse, F-91198 Gif-sur-Yvette Cédex, France

a r t i c l e

i n f o

Article history: Received 11 December 2013 Received in revised form 15 December 2014 Accepted 16 December 2014 Available online 7 January 2015 Editor: Michael E. Böttcher Keywords: Corals Mg/Ca Li/Ca Na/Ca Incorporation processes Biomineralisation

a b s t r a c t We present ion probe measurements of Li/Ca, Na/Ca and Mg/Ca ratios of three scleractinian corals (Lophelia pertusa, Desmophyllum cristagalli, Porites lutea). These ratios are systematically enriched in Rapid Accretion Deposits (RADs) compared to surrounding fibres, or Thickening Deposits (TDs), and present huge variations that cannot be ascribed to any environmental parameter change. Moreover, these elemental ratios are positively correlated in the three coral species. We explore different mechanisms to explain these observations: (1) mixing between different carrier phases, (2) influence of specific ion pumps, (3) precipitation rate effects, (4) Rayleigh fractionation, and (5) pH change in the calcifying fluid. Of these possibilities, the most likely proposal seems to be kinetic effects that have influence on the number of defects (i.e., modification of the crystallographic structure), which are linked to the precipitation rate of the skeleton, and the partition coefficients are the cause of the positive correlation between Li, Na, and Mg in the coral skeleton. Temperature has an indirect influence on the skeletal concentration of these elements through its effect on the skeletal growth rate. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Aragonitic coral skeleton chemical and isotopic compositions are widely used as proxies of marine palaeoenvironmental conditions (see Corrège, 2006, for a review). Physico-chemical parameters of water masses, such as temperature, salinity or pH, are sought, reconstructed through proxies involving the isotopic and/or trace-elemental composition of skeletons, for example e.g., δ18O, δ11B, clumped isotopes Δ47, Mg/Ca, and Sr/Ca (e.g., Smith et al., 1979; Beck et al., 1992; Mitsuguchi et al., 2001; Corrège, 2006; Ghosh et al., 2006). In practice, each proxy is complicated by the existence of biological processes, so-called ‘vital effects’, which more or less overprint thermodynamic relationships or perturb simple inorganic precipitation processes. For example, dramatic variations in Mg/Ca ratios and δ18O (up to 10‰) are recorded in coral skeleton (e.g., Adkins et al., 2003; Rollion-Bard et al., 2003a,b; Meibom et al., 2004; Lutringer et al., 2005; Meibom et al., 2008; Allison et al., 2010), which cannot be ascribed to change in environmental parameters (e.g., Rollion-Bard and Blamart, 2014). At the sub-micrometre level, the scleractinian coral skeleton is composed primarily of two microstructural components. The dominant component is the cyclically produced Thickening Deposits (TDs) that were traditionally referred to as ‘fibres’ (Partz, 1882; Ogilvie, 1896). Much less abundant are the Rapid Accretion Deposits (RADs) (Stolarski, 2003) or ⁎ Corresponding author. Tel.: +33 1 83 95 76 93. E-mail address: [email protected] (C. Rollion-Bard).

http://dx.doi.org/10.1016/j.chemgeo.2014.12.011 0009-2541/© 2014 Elsevier B.V. All rights reserved.

Early Mineralization Zones (EMZ) (Cuif et al., 2003a), traditionally referred to as Centers of Calcification (CoCs) (Wells, 1956). For consistency, we adopt here the term RAD. RAD structures are visible as optically dark regions in polished thin sections (Ogilvie, 1896; Cuif and Dauphin, 1998; Stolarski, 2003; Brahmi et al., 2012). The size (typically 2–10 μm in diameter) and distribution of RADs relative to the TDs, as well as the arrangement pattern of TDs, are strongly taxonomically dependent (Cuif et al., 2003b; Stolarski et al., 2011). RAD can have dramatically different compositions compared with the adjacent TD (e.g., Robinson et al., 2014; Rollion-Bard and Blamart, 2014). From these observations, several models have been proposed to explain these vital effects: (1) pH variations in the calcifying fluid (Adkins et al., 2003; Holcomb et al., 2009), (2) Rayleigh fractionation in a closed or semi-closed reservoir (Cohen et al., 2006; Gagnon et al., 2007), (3) kinetic fractionation (McConnaughey, 1989; Sinclair et al., 2006), (4) a mixing between direct seawater transport and ionic pumping (Gagnon et al., 2012), and (5) compartmentalized precipitation (Meibom et al., 2004, 2008; Rollion-Bard et al., 2010; Rollion-Bard and Blamart, 2014) with the possible role of amorphous calcium carbonate (ACC) precursors in the precipitation of RAD (Rollion-Bard et al., 2010). All these biomineralization models are generally based on behaviours of elements in inorganic carbonate and from the general view that the composition of the calcifying fluid is similar or close to seawater composition. In that view, to try to decipher biological effects from inorganic behaviour, inorganic experiments are conducted and results are

C. Rollion-Bard, D. Blamart / Chemical Geology 396 (2015) 98–111

99

Table 1 Geographic coordinates, depth sampling and seawater environmental parameters for the three species studied. Species

Sampling location

Depth (m)

Temperature (°C)

Salinity (p.s.u.)

Age

Lophelia pertusa Desmophyllum cristagalli Porites lutea

55°31′N, 15°39 W 52°18′N, 13°03′W 166°3′E, 22°3′S

747 610 2.5

8.5 ± 0.5 9.0 ± 1.5 a 23.2 ± 2.3

35.7 nd 35.55

Modern Between 8765 ± 190 and 8520 ± 100 yearsa Modern

a

Data from Lutringer et al. (2005).

compared with biocarbonates. For example, it was shown that Li/Ca ratio decreases with increasing temperature in inorganic aragonite experiments (Marriott et al., 2004a,b). This trend was confirmed in corals (Marriott et al., 2004a,b), as well as in brachiopods (Delaney et al., 1989). This decrease was ascribed to an increase of the solubility of Li2CO3 relative to CaCO3 at higher temperature (Lea, 1999; Marriott et al., 2004a,b). Contrary to Li/Ca ratios, Mg/Ca increases with increasing temperature (e.g., Chave, 1954; Mitsuguchi et al., 1996; Reynaud et al., 2007). However, Gaetini and Cohen (2006) showed from aragonite precipitation experiments that Mg/Ca decreases with increasing temperature, whereas Mg/Ca measurements in Diploria labyrinthiformis increase with temperature. They explained this discrepancy by ‘vital effects’ modifications of precipitating fluid composition. Few studies explore the behaviour of Na/Ca in calcium carbonate. This is probably due to the fact that potential applications of Na/Ca as environmental proxy seem limited. To our knowledge, Na/Ca was only explored as proxy of salinity. It was not conclusive as there is only a trend between these two parameters (Swart, 1980). Moreover, Na content is not related to the Na/Ca of the solution (Swart, 1979, 1981). Complicating this general view, it seems that all the cations do not simply replace Ca2+ in the aragonite lattice, as can be the case in an ideal solid solution model. As an example, Mg2+ was proposed to be in a disordered Mg-bearing material (organic material or highly disordered inorganic phase like ACC) (Finch and Allison, 2008; Meibom et al., 2008). The Li/Mg ratio seems to have apparently the advantage that vital effects appear to be minimal and, recently, it was proposed to use it as proxy of temperature (Case et al., 2010). Indeed, Li/Mg ratio is more or less constant in the coral skeletons investigated so far, whatever the microstructure analysed, and the same Li/Mg vs temperature calibration is applicable for deep-sea and tropical corals (Case et al., 2010; Hathorne et al., 2013; Raddatz et al., 2013). Different mechanisms have been proposed to explain the link between Li/Ca and Mg/Ca ratios: Rayleigh fractionation during the precipitation phase (Case et al., 2010), or pH variation in the fluid of calcification (Raddatz et al., 2013). In this study, we investigate Li/Ca, Na/Ca, and Mg/Ca ratios in three scleractinian coral species (Lophelia pertusa, Desmophyllum cristagalli, and Porites lutea). We measured the different microstructures with SIMS and NanoSIMS to evaluate and to discuss the possible control mechanisms on these ratios, and the relationship between Li/Mg and water temperature. 2. Samples Three scleractinian corals were studied, including two deep-sea corals (L. pertusa and D. cristagalli), and one tropical coral (P. lutea). The samples were selected for their different habitats (Table 1) and different skeleton structures. The two chosen deep-sea corals, L. pertusa and D. cristagalli, lived in stable environments with minimal seasonal variation of temperature and salinity. L. pertusa and D. cristagalli are also characterized by well-defined ultra-structural organization (see Adkins et al., 2003; Blamart et al., 2007; Rollion-Bard et al., 2010 for more details). The L. pertusa and D. cristagalli samples were collected during the MD 123 Geomound cruise in 2001. L. pertusa comes from the top core MD 01-2454G located at 55°31′N and 15°39 W (Southwest Rockall Bank). The L. pertusa sample was collected alive at a water depth of 747 m, where the mean annual temperature is 8.5 ± 0.5 °C, and the

mean salinity is 35.7 p.s.u. This specimen was extendedly studied for lithium, oxygen, boron and carbon isotopes (Rollion-Bard et al., 2003b; Lutringer et al., 2005; Blamart et al., 2007; Rollion-Bard et al., 2009, 2010). Two pieces of this specimen were analysed: one by SIMS (Lophelia-1) and the other one by NanoSIMS (Lophelia-2). In both cases, the L. pertusa sections exhibit clearly defined classical RAD zones and, in addition, a zone further outwards in the wall which is structurally similar to TDs but geochemically similar to RADs (Blamart et al., 2007) (Fig. 1a). The D. cristagalli sample comes from core MD 01-2459G located at 52°18′N 13°03′W (Northern Porcupine Seabight) at a water depth of 610 m. The coral was at 117–120 cm depth in the sediment core. Some corals found in this core have been dated either by the U/Th method or by 14C measurements (Lutringer et al., 2005; Frank et al., 2009) leading to a Holocene age estimated to be in the range of 8765 ± 190 and 8520 ± 100 years (Lutringer et al., 2005; Frank et al., 2009). The water temperature at this location during the Holocene was probably quite similar and estimated to be 9 °C ± 1.5 °C (Lutringer et al., 2005). As for L. pertusa, the D. cristagalli coral shows a clear RAD zone surrounded by TDs (Lazier et al., 2007). The tropical P. lutea sample is a fragment collected at the Boulari Reef in New Caledonia in 1994 (166°3′E, 22°3′S) at a water depth of 2.5 m. The mean annual temperature, based on record at Amédée Islet, is 23.2 °C, with a mean annual amplitude of 4.7 °C. The mean annual salinity is 35.55 p.s.u., with an annual amplitude of 0.5. More details on this sample are in Rollion-Bard et al. (2003a). Contrary to L. pertusa and D. cristagalli, RADs are not present in distinct zones, but are distributed in the coral skeleton. Observations under an optical microscope lead to a RAD diameter estimation of less than 5 μm, as described by Allison (1996). 3. Methods 3.1. NanoSIMS Magnesium/Ca and lithium/Ca analyses were carried out on a polished (1/4 micron diamond paste) and Au-coated (20 nm) surface using a NanoSIMS ion microprobe. With a primary beam focused to a spot-size of about 1 μm, the sample surface was analysed in spot mode. Secondary ions of 7Li+, 24Mg+, and 44Ca+ were simultaneously collected in electron multipliers at a mass resolving power of 5000. Each analysis consisted of 120 s of pre-sputtering and 100 s of data acquisition. The primary beam was stepped across the sample surface to obtain transects with a step size of about 15 μm. Measured 7Li+/44Ca+ and 24Mg+/44Ca+ were converted into molar ratios using the CAL-HTP standard ([Li] = 2 ppm, Vigier et al., 2007) and the OKA-C standard (Mg/Ca = 4.55 mmol/mol, Bice et al., 2005), respectively, analysed under identical conditions. Errors are estimated from multiple measurements of the standards and are 15% for Li/Ca and 5% for Mg/ Ca ratios (1σ). 3.2. SIMS Li/Ca, Na/Ca and Mg/Ca were measured using a Cameca ims 3f ion microprobe at CRPG (Nancy, France). The analytical method is the same as described in Hart and Cohen (1996). We used a focused O− primary beam of about 10 nA. The pre-sputtering time was 2 min. The

100

C. Rollion-Bard, D. Blamart / Chemical Geology 396 (2015) 98–111

C. Rollion-Bard, D. Blamart / Chemical Geology 396 (2015) 98–111

masses 7 (7Li+), 23.5 (background), 23 (Na+), 24 (24Mg+) and 44 (44Ca+) were measured using a − 70 eV energy filtering, by peak jumping on an electron multiplier, for 20 s, 2 s, 8 s, 15 s, and 4 s, respectively. No matrix effect (Rollion-Bard and Marin-Carbonne, 2011) was observed for the measurements of elemental ratios. OKA-C was used to determine the Na/Ca and Mg/Ca ion yields (Na/Ca = 1.94 mmol/mol, Mg/Ca = 4.55 mmol/mol, Bice et al., 2005), and CAL-HTP (Vigier et al., 2007) was used to calibrate the Li/Ca. The external reproducibility was determined by multiple measurements of the reference materials, and for Li/Ca measurements it was ± 10% (1σ), and for Na/Ca and Mg/Ca ±0.6% (1σ). 4. Results All the measured ratios are reported in Table 2. In L. pertusa, Li/Ca, Na/Ca and Mg/Ca ratios show a large change associated with the microstructure of the coral, i.e., RAD and RAD-like versus surrounding fibres (Fig. 1a). In Lophelia-1, Li/Ca ranges from 10.3 μmol/mol to 22.2 μmol/mol, Na/Ca values are between 21.94 mmol/mol and 28.11 mmol/mol and Mg/Ca ranges from 2.16 mmol/mol to 4.60 mmol/mol. In Lophelia-2, Li/Ca ranges from 9.3 μmol/mol to 18.9 μmol/mol, Na/Ca between 19.55 mmol/mol and 28.88 mmol/mol, and Mg/Ca from 1.66 mmol/mol to 3.93 mmol/mol. In the sample measured by NanoSIMS, i.e., at higher resolution, trace element variations are characterized by larger amplitudes, as expected. Li/Ca varies between 7.9 and 25.3 μmol/mol, and Mg/Ca between 1.49 mmol/mol and 4.29 mmol/mol. Whatever the sample, Li/Ca and Mg/Ca are higher in RAD and RAD-like by a factor of more than 2 relative to fibres, and for Na/Ca, by a factor of ≈1.5 (Fig. 1b, c). After micromilling, the different microstructures of this coral were also measured for Mg/Ca ratio by ICP-AES (see Greaves et al., 2008, for the experimental procedure). The RAD zone gives a value of 3.6 ± 0.25 mmol/mol, the aragonitic fibres between the centre of the calyx and the RAD zone have a Mg/Ca value of 2.6 ± 0.34 mmol/mol, whereas the fibres after the RAD zone have a value of 3.2 ± 0.22 mmol/mol. The more external part of the L. pertusa specimen has a Mg/Ca ratio of 3.0 ± 0.25 mmol/mol. All these values are in agreement with the SIMS and NanoSIMS measurements. In D. cristagalli, only the TD part was analysed. The Li/Ca values are between 7.7 and 13.8 μmol/mol, Na/Ca between 19.72 and 25.00 mmol/mol, and Mg/Ca between 2.04 and 3.71 mmol/mol (Fig. 2). The P. lutea sample was only analysed for Li/Ca and Mg/Ca in 4 different zones (Fig. 3a). Li/Ca ratios range between 6.1 and 21.6 μmol/mol, and Mg/Ca values range between 3.05 and 8.10 mmol/mol. Before the analyses, it was not possible to distinguish the RAD, but we can assume their presence by the high Mg/Ca values (Fig. 3b) (Meibom et al., 2007). The range of Li/Ca measured in this study is in agreement with those measured by Marriott et al. (2004a), Rollion-Bard et al. (2009), Case et al. (2010), Raddatz et al. (2013), and Hathorne et al. (2013). The Mg/Ca values are in agreement with all the previous studies (e.g., Weber, 1974; Mitsuguchi et al., 1996, 2001; Sinclair, 2005; Sinclair et al., 2006; Reynaud et al., 2007, among many others). Na/Ca measurements are also in agreement with the range determined in previous studies (e.g., Amiel et al., 1973; Polyakov and Krasnov, 1975; Swart, 1981; Oomori et al., 1982; Bar-Matthews et al., 1993; Mitsuguchi et al., 2001, 2010). The three ratios measured in this study show a dependence to the structure of the coral skeleton, all being enriched in RAD and RAD-like compared to TD (Figs. 1b, c; S1). To our knowledge, it is the first time that Na/Ca ratio was investigated with the different microstructures of the coral. This distinction between RAD and the surrounding fibre signatures is a common feature for almost all the elemental and isotopic

101

ratios measured so far (e.g., Allison, 1996; Adkins et al., 2003; Sinclair et al., 2006; Blamart et al., 2007; Gagnon et al., 2007; Juillet-Leclerc et al., 2009; Case et al., 2010; Raddatz et al., 2013, among others), except δ7Li (Rollion-Bard et al., 2009). However, it should be noted that L. pertusa measurements show also an area enriched in Li/Ca and Mg/Ca independent of RAD and RAD-like zones (Fig. 1c, zone around 1500–1800 μm). 5. Discussion The co-variation of Mg, Na and Li is at two different scales: (1) at the millimetre scale where a dependency of Mg/Li with temperature has been documented (Case et al., 2010; Hathorne et al., 2013; Raddatz et al., 2013), and (2) at microscale where the positive correlations are observed even in deep-sea corals for which the temperature is essentially constant (Fig. 4). 5.1. Distribution coefficient of Li/Ca, Na/Ca and Mg/Ca: temperature dependency? To allow a better comparison with published data, the averages of the corals measured in this study are reported in Fig. 5 with the data of Marriott et al. (2004a,b), Case et al. (2010), and Raddatz et al. (2013). If an inverse relationship between the Li/Ca ratio and the temperature is clearly expressed for the inorganic aragonite experiments and for the data of Porites lobata (Marriott et al., 2004a) (Fig. 5a), it is blurred for temperature less than 15 °C. The data used to cover the range between 2 and 15 °C correspond to two different deep-sea corals. The lack of correlation between the two parameters is perhaps related to some species effects or to the microstructures of the skeleton. In these conditions, it is difficult to assess any decrease of Li/Ca with increasing temperature for the T range between 2 and 30 °C with some consequence on the Li/Mg ratio temperature proxy (see the following section). White (1977) investigated the precipitation of Na into aragonite and observed that Na/Ca ratio decreases with temperature ranging from 25 to 75 °C. This relationship was also observed by Kinsman (1970) for inorganic aragonite in the range of temperature between 15 and 96 °C. This decrease with increasing temperature is also detected in our samples with the Na/Ca ratios of deep-sea corals (average of 24.5 mmol/mol for L. pertusa) being higher than the Na/Ca of tropical coral (average of ≈ 20 mmol/mol for Porites species, Mitsuguchi et al., 2010). Nevertheless, we cannot draw strong conclusions for the temperature dependency of Na/Ca in corals because of the scarcity of data. From Fig. 5b, it is clear that, even if there is a broad trend for an increase of Mg/Ca with increasing temperature, there are other mechanisms that are superimposed to this trend and that prevent the use of Mg/Ca in coral skeleton as an accurate temperature proxy. Despite a lack of strong temperature dependency of Li/Ca and Mg/Ca partition, there is an increase of Mg/Li ratio with temperature and this relationship seems to be independent of the coral species (Fig. 5c). However, in the few data available, Li/Mg ratios reported by Case et al. (2010) at a given temperature are systematically lower to those measured by Raddatz et al. (2013) on L. pertusa. Moreover, despite this global trend, it should be noted that L. pertusa and D. cristagalli show a range of Li/Mg between 2.96 and 7.35 mmol/mol, and 3.44 and 4.37 mmol/mol, respectively. This corresponds to a variation of temperature between −7.2 and 11.3 °C for L. pertusa and between 3.4 and 8.2 °C for D. cristagalli, using the relation determined by Hathorne et al. (2013), whereas these two corals grew under quasi-constant temperature.

Fig. 1. Localisation of SIMS spots in Lophelia pertusa (L. pertusa-2) sample. b) SIMS Mg/Ca (mmol/mol), Na/Ca (mmol/mol) and Li/Ca (μmol/mol) ratios versus the distance in μm. c) NanoSIMS measurements of Mg/Ca (mmol/mol) and Li/Ca (μmol/mol) versus distance in μm. Note that there is a systematic increase of these ratios in RAD zone and RAD zone ‘like’ (see text for definition). The ‘?’ indicates an increase that seems not linked to the microstructure of the coral skeleton.

102

C. Rollion-Bard, D. Blamart / Chemical Geology 396 (2015) 98–111

Table 2 Li/Ca (μmol/mol), Na/Ca (mmol/mol), and Mg/Ca (mmol/mol) measured by SIMS and NanoSIMS in 3 coral species. Point 1 is arbitrary taken at a distance of 0 μm. Sample

Distance (μm)

Li/Ca (μmol/mol)

Na/Ca (mmol/mol)

Mg/Ca (mmol/mol)

Lophelia-1

0 80 160 240 320 400 480 560 640 720 800 880 960 1040 1120 1200 1280 1360 1440 1520 1600 1680 1760 1840 1920 2000 2080 2160 2240 2320 2400 2480 2560 2640 0 120 240 360 480 600 720 840 960 1080 1200 1320 1440 1560 1680 1800 1920 2040 2160 2280 2400 2520 2640 2760 2880 20 40 60 80 100 120 140 160 180 200 220 240 260 280

19.52 20.26 22.17 20.74 20.57 19.61 10.99 14.71 11.15 15.59 11.69 15.33 16.12 21.67 13.34 12.71 12.27 12.76 12.40 12.31 11.60 13.53 13.27 12.76 13.15 11.77 11.46 14.34 10.27 12.39 14.92 13.48 12.98 14.63 12.51 11.73 12.45 15.91 14.66 12.19 13.95 15.83 13.32 12.40 15.69 12.04 13.85 18.51 14.05 13.33 13.44 15.04 14.43 18.93 9.34 10.61 11.07 9.48 10.24 17.03 12.66 13.45 13.67 9.49 8.30 9.10 7.95 11.06 14.88 18.67 19.98 18.23 18.68

26.03 26.07 27.18 25.83 25.90 25.97 23.73 25.73 23.45 25.72 23.36 26.25 25.62 28.11 24.01 23.55 22.92 23.01 24.65 23.38 23.83 25.56 25.04 24.79 23.73 23.77 22.11 24.46 21.94 23.02 24.86 24.81 24.11 25.33 24.14 23.19 24.80 27.37 25.24 23.81 25.31 25.54 24.62 23.35 26.01 23.56 25.90 28.88 25.34 25.40 24.56 25.63 25.39 24.90 19.55 20.82 21.48 20.31 20.46 n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d.

4.17 4.40 4.55 4.02 4.12 4.60 3.05 3.57 2.90 3.38 2.72 3.38 3.20 4.26 2.72 2.64 2.54 2.55 2.92 2.57 2.75 3.14 3.00 2.87 2.68 2.60 2.27 2.89 2.16 2.28 2.83 2.58 2.66 2.66 2.64 2.42 2.71 3.25 2.91 2.45 2.83 2.15 2.68 2.44 3.03 2.38 3.02 3.93 2.93 2.90 2.86 3.34 3.10 3.59 1.77 2.05 2.19 1.66 1.70 2.73 2.55 2.79 2.99 1.61 1.67 1.67 1.49 2.06 3.85 4.03 4.16 4.28 4.29

Lophelia-2

Lophelia-NanoSIMS

Table 2 (continued) Sample

Distance (μm)

Li/Ca (μmol/mol)

Na/Ca (mmol/mol)

Mg/Ca (mmol/mol)

Lophelia-NanoSIMS

300 320 340 360 380 400 420 440 460 480 500 520 540 560 580 600 620 640 660 680 700 720 740 760 780 800 820 840 860 880 900 920 940 960 980 1000 1020 1040 1060 1080 1100 1120 1140 1160 1180 1200 1220 1240 1260 1280 1300 1320 1340 1360 1380 1400 1420 1440 1460 1480 1500 1520 1540 1560 1580 1600 1620 1640 1660 1680 1700 1720 1740 1760 1780

19.07 16.53 14.65 12.53 13.21 14.20 13.19 14.60 14.51 11.06 11.88 11.59 10.67 10.77 9.78 9.56 8.17 9.60 12.87 14.49 14.77 13.87 11.39 11.05 12.74 11.63 11.76 12.00 14.27 13.79 13.30 14.94 16.45 19.95 19.93 16.19 17.98 16.09 16.02 16.04 16.62 16.50 16.16 16.07 16.31 15.59 15.75 16.37 12.09 12.09 11.93 9.98 10.68 11.01 13.13 10.71 16.73 17.39 15.86 15.49 18.34 17.74 17.68 16.21 21.16 25.27 18.98 17.90 17.47 16.40 16.26 15.70 15.56 14.63 13.53

n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d.

3.90 3.56 3.91 3.93 3.95 3.87 3.54 3.18 3.71 2.85 3.07 3.10 3.01 2.90 2.80 2.47 2.76 2.56 2.70 2.89 2.85 2.77 2.16 2.08 2.49 2.24 2.26 2.32 2.95 2.75 2.70 2.74 3.72 3.79 3.92 3.36 3.65 3.58 3.54 3.40 3.68 3.56 3.29 3.28 3.37 3.44 3.39 3.25 2.49 2.46 2.41 2.23 2.35 2.22 2.74 2.23 2.53 2.85 2.49 2.41 2.85 2.71 2.69 2.47 2.89 3.72 2.69 2.54 2.44 2.53 2.54 2.36 2.39 2.27 2.07 (continue on next page)

C. Rollion-Bard, D. Blamart / Chemical Geology 396 (2015) 98–111 Table 2 (continued) Sample

Distance (μm)

Li/Ca (μmol/mol)

Na/Ca (mmol/mol)

Mg/Ca (mmol/mol)

Lophelia-NanoSIMS

1800 1820 1840 1860 1880 1900 0 120 240 360 480 720 840 960 1080 1200 1320 1440 1560 1680 1800 1920 2040 2160 2280 2400 2520 2640 2760 2880

15.54 17.62 17.19 15.16 18.61 16.56 13.10 13.34 11.41 13.48 12.71 10.84 9.52 12.47 8.94 13.60 10.96 10.25 13.53 9.98 11.67 8.45 12.14 13.77 13.25 13.83 7.71 13.57 11.58 13.46

n.d. n.d. n.d. n.d. n.d. n.d. 25.00 23.08 22.53 24.00 23.76 22.55 21.47 23.05 21.01 23.18 22.15 22.18 22.93 21.64 22.81 20.16 23.13 23.01 22.23 24.72 19.72 22.69 21.51 22.34

2.39 2.74 2.65 2.25 2.64 2.72 3.46 3.10 2.91 3.36 3.28 3.07 2.56 3.34 2.32 3.53 2.95 2.98 3.69 2.81 3.32 2.09 3.40 3.71 3.35 3.65 2.04 3.35 2.74 3.08

11.16 11.79 18.10 21.64 13.63 18.80 10.03 11.07 18.44 12.01 10.58 9.63 8.71 8.68 9.95 10.29 9.82 10.92 10.57 11.70 12.04 14.47 17.65 n.d. 15.53 12.56 10.80 6.38 7.96 6.11 7.16 7.75 7.99 7.66 7.73 9.15 12.80 20.05 9.71 13.38 10.95 n.d.

n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d.

5.21 6.16 6.35 7.11 5.75 5.96 4.67 5.59 6.49 5.45 6.01 4.84 3.96 3.05 4.86 5.48 5.30 6.22 6.37 6.43 6.13 5.80 6.16 5.29 7.36 6.39 6.31 4.48 4.12 4.50 4.87 4.29 3.79 4.17 4.63 4.35 6.30 7.16 5.85 8.10 4.43 3.76

D. cristagalli

P. lutea Zone 1

Zone 2

Zone 3

Zone 4

103

In the following, different mechanisms that can affect the Li, Na and Mg incorporation into the coral skeleton are investigated: (1) mixing of various carrier phases, (2) specific pumping of cations to sites of calcification, (3) precipitation rate, via direct influence on the partition coefficient or via modification of the crystal structure, (4) Rayleigh fractionation, and (5) pH variation in the calcifying fluid. 5.2. Possible controls for Li, Na and Mg incorporation 5.2.1. Carrier phase of Li, Na, and Mg? As shown by Finch and Allison (2008) in Porites coral skeleton, it seems that Mg is not in the aragonite structure, but is present in organic matter or a highly disordered inorganic phase, like possibly Amorphous Calcium Carbonate (ACC). Thus it could explain the higher Mg/Ca ratio of RADs compared to fibres, as organic matter is more present in RAD (Cuif et al., 2003b) and as it was also proposed that ACC could be precursors of RAD formation (Rollion-Bard et al., 2010), ACC having higher Mg content than carbonate phase (Jacob et al., 2008). Few studies have dealt with Na compositions in scleractinian corals. An early study of Amiel et al. (1973) concluded that about 90% of Na is in the aragonite skeleton, the rest being in the organic compounds. Moreover, it seems that Na/Ca in coral is not directly related to the concentration of Na in seawater (Amiel et al., 1973; Swart, 1981). For the moment, it is not possible to conclude if Na has the same carrier phase as Mg, but its link with the organic matter could also explain the similar behaviour of Mg and Na, and its enrichment in RAD compared to fibres. To our knowledge, the exact carrier phase of Li is not yet determined. As described above, it is not clear if Li+ substitutes Ca2+, as it is thought for aragonite, or if it is trapped into interstitial spaces, as it seems to be the case for calcite (Okumura and Kitano, 1986; Marriott et al., 2004a,b). It is not known, also, if Li is associated with the organic matter of coral. Moreover, knowing that the isotopic composition of lithium is the same between RAD and fibres (Rollion-Bard et al., 2009), it seems unlikely that the enrichment of Li content in RAD would be due to an increase in organic matter content. The various possible carriers for Mg and Na could explain the different behaviours in trace element compositions of RAD compared to fibres, and the enrichment of Mg/Ca and Na/Ca in RAD but it cannot explain the positive correlation between these ratios. Indeed, it cannot be related to some mixing between fibres and RAD structures as in L. pertusa and in D. cristagalli fibre zones, the positive correlation between Li/Ca, Na/Ca and Mg/Ca still exists. Nevertheless the enrichment of Na, Mg and Li in RAD could be related to some link with organic matter trapped in them. Moreover, it is then difficult to explain the Mg/Li relationship with temperature if the link between Mg and Li is only due to the presence of organic matter. 5.2.2. Biomineralization processes via ion pump The way by which cations present in seawater reach the sites of precipitation is still a matter of debate. In a general point of view, it is thought that Ca2+ is brought to sites of calcifications by direct seawater supply (Tambutté et al., 2011; Gagnon et al., 2012), ion channels (Tambutté et al., 1996) and/or Ca-ATPase enzyme (Isa et al., 1980). For some authors, this enzyme is specific to Ca2+ (Ip and Krishnaveni, 1991; Ip and Lim, 1991), whereas for some others, Sr2+ (Ferrier-Pagès et al., 2002) or Mg2 + (Isa et al., 1980) could be incorporated by this pathway too. The advantages of Ca-ATPase are (1) to increase the Ca2+ concentrations at sites of calcification, and (2) perhaps more importantly, by the exchange of Ca2+ with 2H+, to increase pH, enhancing carbonate precipitation (McConnaughey, 1989). If the Ca-ATPase enzyme is specific to Ca2+ ions, the increase of calcification rate will favour the supply of Ca2+ in the fluid, and by consequence will decrease the trace element content relative to calcium. As Me/Ca ratios are in general positively correlated with growth rate of coral, this scenario seems unlikely. On the other hand, Ca-ATPase is not the only pathway to supply

104

C. Rollion-Bard, D. Blamart / Chemical Geology 396 (2015) 98–111

Fig. 2. SIMS measurements of Mg/Ca (mmol/mol), Na/Ca (mmol/mol) and Li/Ca (μmol/mol) in Desmophyllum cristagalli versus distance in μm. All the measurements were only performed in fibres.

Ca2+ to sites of calcification, and this effect can be blurred by direct supply of seawater. Concerning the other cations, Mg-ATPase and Na+/K+-ATPase enzymes were detected in the tropical coral Galaxea fascicularis (Ip and Lim, 1991), as well as Na2 +/Ca2 + ion pumps (Marshall, 1996).

Na+/H+ pumps were also found in foraminifera (Erez, 2003), but not yet in corals. To our knowledge, no ion pump or enzyme implicating Li+ was found in coral tissue. So, at this state, it would be speculative to conclude about the role of ion pumps and enzymes for the co-variations of Mg2+, Na+ and Li+.

Fig. 3. a) Localisation of the zones of measurements in the Porites lutea sample. b) NanoSIMS measurements of Mg/Ca (mmol/mol) and Li/Ca (μmol/mol) in the 4 zones analysed.

C. Rollion-Bard, D. Blamart / Chemical Geology 396 (2015) 98–111

105

Fig. 4. a) Li/Ca (μmol/mol) versus Mg/Ca (mmol/mol). Open blue squares and open red diamonds represent the measurements performed in this study in L. pertusa. Open orange triangles are data measured in D. cristagalli (this study). For comparison, data from literature are reported. All are performed with LA-ICP-MS technique. Open black circles are measurements in Balanophyllia malouensis (Case et al., 2010), open purple circles are measurements in D. dianthus (Case et al., 2010) and open green circles are data performed in L. pertusa (Raddatz et al., 2013). b) Na/Ca (mmol/mol) versus Mg/Ca (mmol/mol). Same symbols as in a) are used for measurements from this study. Data from literature are plotted for comparison. 1: data from Mitsuguchi et al. (2010). 2: data from Bar-Matthews et al. (1993). c) Li/Ca (μmol/mol) versus Na/Ca (mol/mol). Symbols are the same as described in a). Measurements are plotted along a line with a slope corresponding to Li/Na ≈ 1 mmol/mol. Note that RAD and RAD ‘like’ zone data are off this line. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

106

C. Rollion-Bard, D. Blamart / Chemical Geology 396 (2015) 98–111

5.2.3. Precipitation rate dependency 5.2.3.1. Effect on the partition coefficients. Precipitation rate was shown to influence Mg/Ca, Li/Ca and Na/Ca partition in inorganic calcium carbonate experiments. Gabitov et al. (2011) observed a positive correlation between Mg and Li partition coefficients and growth rates of inorganic aragonites. This dependency with growth rate was explained with a growth entrapment model (Watson, 1996; Gabitov et al., 2008). In this scenario, a layer enriched in these elements by a factor f relative to the equilibrium with the surrounding seawater is present at the growing surface and is incorporated in the newly precipitated calcite crystal layer. Increasing growth rate leads to the entrapment of this crystal surface composition by the newly formed aragonite before the excess of Li, Na and Mg is redistributed by diffusion into the aragonite. It results in an increase of Li/Ca and Mg/Ca ratios. Busenberg and Plummer (1985) observed the same tendency in inorganic calcite, with an increase of the Na partition coefficient with growth rate. To our knowledge, no data are available for growth rate influence of Na partition coefficient into inorganically precipitated aragonite. In this perspective, the observed correlation of Na/Ca, Mg/Ca and Li/ Ca with coral microstructure might be ascribed to a growth rate effect (or kinetic effects). Recently, Brahmi et al. (2012) showed that there is a difference in Mg/Ca ratios by a factor of ≈3 between TDs and RADs due to a large difference in growth rate (1–3 μm/day versus 50–60 μm/day, respectively). This growth rate difference seems to have no effect on Sr/Ca ratios. The ranges observed in Li/Ca, Mg/Ca and Na/Ca within a single coral skeleton might be related to local growth rate variations during skeleton formation, with difference between RAD and TD growth rates, but also certainly during the growth period of TD where variations can be driven by food supply (Mortensen, 2000). This could explain the enrichment of Li and Mg in L. pertusa in the zone between 1500 and 1800 μm (Fig. 1c). It should also be noted that RADs certainly experienced another mechanism during their precipitation, like ACC precursors (Rollion-Bard et al., 2010). Indeed, as seen in Fig. 4c, RAD and RAD-like zones are enriched in Li compared to the global trend defined by TDs. 5.2.3.2. Modification of the crystallographic structure. Ionic size is one of the major factors controlling trace element substitution in crystals. To allow uninhibited substitution, cations must have similar or slightly different ionic radii (at most 15% difference) (Goldschmidt, 1954; Kretz, 1982). Mg2 + is a small cation compared to Ca2 + (Shannon, 1976) and it is unlikely that there is a simple substitution between these two cations in aragonite lattice (Speer, 1983). The same is true for Na+ and Li+ since they have different charges that hinder simple substitution to the Ca2 + crystal site, and the unbalanced charge has then to be filled by other charges in the lattice or by adsorbed cations (Billings and Ragland, 1967). Instead, Mg2+, Na+, and Li+ cations are thought to be trapped into defect sites (Amiel et al., 1973; White, 1977; Cross and Cross, 1983; Busenberg and Plummer, 1985; Watanabe et al., 2001; Mitsuguchi et al., 2010). Moreover, the number of defect sites increases with precipitation rate. It leads to the increase of Mg/Ca, Li/Ca and Na/Ca with growth rate, in principle consistent with the enrichment of these ratios in RAD. It was also shown that the presence of Na+ increases the unit cell dimensions of calcite (Busenberg and Plummer, 1985) and hence the number of defects. If this is also true for aragonite, it could explain the positive correlation between Na and other trace elements. Mitsuguchi et al. (2001) described a positive correlation between Na, Mg and S in corals, and are trapped in lattice defects they proposed that Na+, Mg2+ and SO2− 4 and distortions, which are more important in RAD due to the higher precipitation rate (Brahmi et al., 2012) and the irregular shape of the crystals (Gladfelter, 1982). Moreover, based on synchrotron data, Pokroy et al. (2006) showed that biogenic aragonite are distorted compared to inorganic aragonite and that these distortions are probably due

to organic molecules imbricated into the crystal structure. Van de Locht et al. (2013) studied RAD and fibre zones by transmission electron microscopy (TEM) in a P. lobata coral sample. They found that RADs are composed of randomly oriented crystals between 10 and 100 nm in size and with a porous texture, whereas fibres are composed of dense acicular crystals. They interpreted this difference of structure by some variations of growth rate, RAD being the result of rapid growth compared to fibres. Concerning the RAD-like zone, it could be a previous RAD zone corresponding to an anterior period of life of the coral. They could have been incorporated into the fibre zone during the thickening of the coral skeleton. They kept the geochemical signature of RAD, but their morphology was changed during the thickening. This has to be confirmed by further study on the RAD-like zones. Nevertheless, it should be noted that based on inorganic calcium carbonate precipitations, Okumura and Kitano (1986) inferred alkali metal ion (Li+, Na+, K+ and Rb+) substitution for Ca2+ in aragonite, whereas they are in interstitial positions in calcite, that the presence of Mg2+ in solution decreases the incorporation of alkali metal ions in aragonite and that the presence of Na+ in aragonite decreases the precipitation of the other alkali metal ions in aragonite. These observations do not corroborate the positive co-variations of Mg, Na and Li in aragonitic corals (Fig. 4) and could suggest that alkali metal ions do not have the same behaviour during biomineralisation processes, perhaps due to the influence of organic matter on the formation of the coral skeleton (Addadi et al., 1987; Cuif et al., 2013). 5.2.4. Rayleigh fractionation Rayleigh fractionation has been proposed as the main mechanism responsible for large variations of isotopic and elemental ratios in coral skeletons (Cohen et al., 2006; Gagnon et al., 2007; Case et al., 2010). In this model, precipitation occurs from an extracytoplasmic calcifying fluid (ECF), a semi-closed reservoir with fluid initially similar in composition to seawater. As the partition coefficient of trace elements between coral and seawater is different from unity, the ECF composition evolves. Following Elderfield et al. (1996) and Gagnon et al. (2007), the Me/Ca value of aragonite precipitated following a Rayleigh process is expressed as:

 Me Me ðD −1Þ ¼ DMe   F Me Ca coral Ca 0

ð1Þ

where Me is the concentration of Li, Na or Mg, DMe is the partition coefficient between aragonitic coral and seawater of element Me, F = (Ca/Ca0) is the fraction of Ca in the fluid relative to the initial content of Ca (Ca0), and (Me/Ca)0 is the initial Me/Ca ratio of the fluid. Here, we apply this model to study the positive relations between Na/Ca and Mg/ Ca and between Li/Ca and Na/Ca. Fig. 6a shows three models of closed system Rayleigh fractionation, all the modelling parameters being reported in Table 3. In two simulations, we begin with the Li/Ca and Na/Ca values of seawater as the initial ratios of ECF (Li/Ca = 2.5 mmol/mol, and Na/Ca = 45.9 mol/mol). The partition coefficients of model 1 are those for inorganic aragonite (DNa = 0.0004 (Kinsman, 1970) and DLi = 0.003 (Marriott et al., 2004a,b)). The partition coefficients in the second model are determined in order to obtain the least fractionated ratios measured in this study (Li/Ca = 9.35 μmol/mol and Na/Ca = 19.55 mmol/mol). In that case, DNa is calculated at 4.2 × 10−4 and DLi at 3.74 × 10−3, which are values close to the inorganic aragonite partition coefficients, and for DLi in the range of previous lithium partition coefficients determined in Case et al. (2010) on deep-sea corals. These first two Rayleigh fractionation simulations do not account for all the data and the trend determined in this study. We then play with the different parameters to determine the ‘best fit’ model. The partition coefficients of Na and Li were fixed at the values obtained in the inorganic aragonite precipitation experiment and the initial ratios of the ECF were adjusted to (Li/Ca)0 = 3 mmol/mol and (Na/Ca)0 = 40 mol/mol. This implies that Li would be enriched in the ECF and that Na would be depleted in ECF relative to seawater.

C. Rollion-Bard, D. Blamart / Chemical Geology 396 (2015) 98–111

107

Fig. 5. a) Li/Ca (μmol/mol) versus temperature (°C). Black squares represent the average of the measurements in fibres performed in this study. Data from literature are plotted for comparison. Grey squares are data in L. pertusa from Raddatz et al. (2013), grey circles are data in various deep-sea corals from Case et al. (2010), and white circles are data in Porites coral from Marriott et al. (2004a,b). The decrease of Li/Ca ratio with temperature in inorganic aragonite is also represented (black diamonds, Marriott et al., 2004a,b). b) Mg/Ca (mmol/mol) versus temperature (°C) for different coral species. Black squares correspond to averages of measurements from this study. Grey squares are data from Raddatz et al. (2013), grey circles are data from Case et al. (2010), and triangles are data from Hathorne et al. (2013). White circles represent data from cultured corals (Reynaud et al., 2007). The black line is the empirical calibration determined by Mitsuguchi et al. (1996). c) Mg/Li (mol/mmol) versus temperature (°C). Black squares represent measurement averages from this study. Data from literature are plotted for comparison (Case et al., 2010; Hathorne et al., 2013; Raddatz et al., 2013). All the data fit the exponential calibration line defined by Hathorne et al. (2013) (dotted line).

108

C. Rollion-Bard, D. Blamart / Chemical Geology 396 (2015) 98–111

parameters for Rayleigh fractionation. By combining Eq. (1) for Na and Mg, it comes that:

ln


 Na ¼ Ca

!
 DNa −1 Mg ln DMg −1 Ca "
 !
 # Na DNa −1 Mg : ln − þ ln Ca 0 DMg −1 Ca 0

ð2Þ

In a log–log plot, Na/Ca is correlated to Mg/Ca (Fig. 6b) with a R2 = 0.79. Using Eq. (2), it comes that the slope of this relation is related to the partition coefficients of Na/Ca and Mg/Ca. To calculate DNa, we assume that the ECF has the same composition in Mg than seawater (i.e., (Mg/Ca)sw = 5.1 mol/mol), and we calculate D Mg by considering the smallest value of Mg/Ca measured in L. pertusa (Mg/Ca = 1.66 mmol/mol). It gives a value of 3.25 × 10− 4, which is about one order of magnitude lower than the inorganic DMg determined by Gaetini and Cohen (2006). Using the slope of Eq. (2), it comes that DNa = 6.22(± 0.60) × 10− 1. This value is very different from the value determined for inorganic aragonite (Kinsman, 1970). Combining the calculated partition coefficients of Na and Mg and the intercept of Eq. (2), we estimated the ratio of Na/Ca of the ECF to be 32.45+3.50 −2.50 mmol/mol, value a little lower than seawater. We repeat the same method in log–log plot of Na/Ca versus Li/Ca (Fig. 6c) and using the values of DNa and (Na/Ca)ECF determined previously. It gives DLi = 3.4(± 1.0) × 10− 1 and (Li/Ca)ECF = 27.5+14 −16 μmol/mol (Table 3). We can note that if we first plot Li/Ca versus Mg/Ca and then Na/Ca vs Mg/Ca, we obtain the same values within errors. In a first step, the models based on inorganic coefficients or ECF values of Na/Ca, Li/Ca, and Mg/Ca close to seawater are not able to reproduce the trend between Li/Ca and Na/Ca ratios (Fig. 6a). In a second step, we used the slopes determined between Na/Ca vs Mg/Ca and Li/Ca vs Na/Ca (Fig. 6b, c). This gives partition coefficients that are very different from the ones determined for inorganic aragonite and ECF values distinct from seawater (Table 3, model 4), especially for Li/Ca ratio. Li+ is perhaps discriminated because no ion pump implicating this element exists in coral tissue, contrary to Na+ and Mg2+. ECF composition close or similar to seawater is one of the main assumptions for palaeo-reconstruction of environmental parameters (e.g., Corrège, 2006) and this is contradicted by the results shown here. If the Rayleigh fractionation reflects the processes responsible for the correlation between Li/Ca, Mg/Ca and Na/Ca, then the ECF has a composition, at least in these elements, different from seawater. It could also question the fact that calcium carbonate is the main carrier of these elements as the partition coefficients are far from the ones determined from inorganic precipitation experiments. The simplest solution is that Rayleigh fractionation is not the main mechanism responsible for the co-variation of Li/Ca, Mg/Ca and Na/Ca. We could note that it is difficult to apply a Rayleigh model for both lithium and sodium as their concentrations are drastically different (in seawater, Li/Ca =

But again, this ‘best fit’ model does not account for all the data (Fig. 6a, model 3). As it seems that partition coefficients and the initial compositions of the fluid are different from inorganic aragonite and seawater, we applied the method used in Gagnon et al. (2007) to decipher the

Fig. 6. In the graphs, RAD data are not considered. a) Same data as in Fig. 4c with the addition of calculated Rayleigh fractionation evolution models. The lines correspond to different parameters for the calculation (Table 3). The star represents the initial composition of the fluid in model 2 (see text for more details). 1. DLi = 3 × 10−3 (Marriott et al., 2004a,b) and DNa = 4 × 10−4 (Kinsman, 1970); initial values correspond to seawater ratios. 2. Partition coefficients are calculated for the least fractionated Li/Ca and Na/Ca values, i.e., DLi = 3.74 × 10−3 and DNa = 4.2 × 10−4; initial values correspond to seawater ratios. 3. ‘Best fit’ model with D Li = 3 × 10 − 3 and D Na = 4 × 10 − 4 , and (Li/Ca)ECF = 3 mmol/mol, and (Na/Ca)ECF = 40 mol/mol. 4. Model calculated according to the method of Gagnon et al. (2007). In this model, DLi = 3.4 × 10−1 and DNa = 6.22 × 10−1, and (Li/Ca)ECF = 0.0275 mmol/mol, and (Na/Ca)ECF = 32.45 mol/mol. Note that, in this case, partition coefficients of Li and Na are completely different from those of inorganic aragonite, and that initial compositions of the ECF are distinct from seawater. ECF: extracytoplasmic calcifying fluid. b) Log–log plot of Na/Ca (mmol/mol) versus Mg/Ca (mmol/mol) in the L. pertusa sample. The slope of the linear correlation between the data is indicated (R2 = 0.79). c) Log–log plot of Li/Ca (μmol/mol) versus Na/Ca (μmol/mol) in the L. pertusa sample. The slope of the linear correlation between the data is indicated (R2 = 0.84).

C. Rollion-Bard, D. Blamart / Chemical Geology 396 (2015) 98–111

109

Table 3 Parameters used in the various Rayleigh fractionation modellings. Model #

Description

(Mg/Ca)0 mol/mol

(Na/Ca)0 mmol/mol

(Li/Ca)0 mmol/mol

DNa

DLi

DMg

1 2 3 4

sw values inorganic partition coefficients sw values best fit partition coefficients Best fit values inorganic partition coefficients Calculation based on log-log plots (Fig. 6b,c) (see text for more details)

– – – 5.1

45.9 45.9 40 32.45

2.5 2.5 3 0.0275

4 × 10−4 4.2 × 10−4 4 × 10−4 6.22 × 10−1

3 × 10−3 3.74 × 10−3 3 × 10−3 3.4 × 10−1

– – – 3.32 × 10−4

2.5 mmol/mol, and Na/Ca = 45.9 mol/mol). Moreover, there is no variation of the Li isotope compositions along the L. pertusa skeleton (Rollion-Bard et al., 2009), ruling out a Rayleigh fractionation for this element. It is also consistent with the conclusions of Hathorne et al. (2013) (as well as Allison et al. (2011) and Brahmi et al. (2012) for Sr/Ca and Mg/Ca). 5.2.5. Modification of the calcifying fluid pH Holcomb et al. (2009) precipitated inorganic aragonite from seawater with morphology and Mg, Sr, and Ba compositions that mimic the RAD and fibre behaviours of coral. In their experiments, the granular centres are linked to high aragonite saturation index, whereas surrounded fibres are due to a decrease of saturation state. This variation in saturation state (pH) of the ECF could then explain the enrichment in Li, Mg and Na in RADs relative to fibres in corals. However, based on the data of Blamart et al. (2007) in L. pertusa, Rollion-Bard et al. (2010) rules out this ‘pH model’. In these studies, boron isotopic compositions (δ11B) were measured in RAD and in TD: the δ11B of RAD is ≈ 10‰ smaller than that of TD. If the δ11B of bicarbonate is a pH proxy of seawater (Hemming and Hanson, 1992), it implies that the pH at which calcify the RADs is smaller than the pH at which precipitates the TD. Besides pH variation, the difference in δ11B between RAD and TD could also reflect a kinetic effect. However, Gabitov et al. (2014), based on laboratory calcite precipitation experiments, showed that precipitation rate has no discernible effect on δ11B (within measurement uncertainty, ≈2‰, 2σ). Thus the δ11B difference of ≈10‰ between RAD and TD predominantly reflects difference in pH, with RAD pH being smaller than TD pH. This is exactly contrary to the proposition of Holcomb et al. (2009). 6. Conclusions In this study, Li/Ca, Na/Ca and Mg/Ca ratios are measured in deepsea and tropical scleractinian corals at micrometre scale. Large variations were found in each individual, and these variations cannot be explained by changes of environmental parameters. The three elemental ratios are strongly correlated to microstructures of the coral skeleton, all of them being enriched in RAD compared to surrounding fibres, as already established for O, C and B isotopic compositions. This implies that the inter-individual variations are the result of some vital effects. These vital effects seem to affect in the same way the studied cations because of the strong positive correlations between Li/Ca, Na/Ca and Mg/Ca. The observed microscale distribution and co-variations imply that growth rate effect is one of the main controlling factors. This factor can play by kinetic effects in two ways: (1) the entrapment of crystal surface composition by the new formed aragonite, as proposed from inorganic aragonite precipitation experiments (e.g., Gabitov et al., 2011) and/or (2) the increase of defect sites that allow Mg2 +, Na+ and Li+ to be trapped. Thus, the Li/Mg correlation with temperature would not be due to direct inorganic thermodynamic effect, but to the influence of temperature to some biological processes impacting the growth rate (Shinn, 1966). The measurements of isotopic composition of Mg could give us more information about the incorporation processes of Mg2+ into coral aragonite and the possible influence of kinetic effect on vital effects (Immenhauser et al., 2010; Yoshimura et al., 2011; Saulnier et al., 2012; Mavromatis et al., 2013). In these conditions, the use of

Li/Mg ratio as palaeothermometer, based on data derived from different deep-sea and tropical corals, is risky because biomineralisation and biological processes including growth rate are strongly species dependent. This study opens also the potential use of Na/Mg or Li/Na ratios as possible proxy of temperature. But this has to be tested in corals grown at different environmental conditions (temperature, salinity, pH …) before any validation. Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.chemgeo.2014.12.011. Acknowledgements This work was supported by the CNRS INSU programme (INTERRVIE). DB thanks Commissariat à l’Energie Atomique et aux Energies Alternatives for financial support and IPSL (Institut Pierre Simon Laplace) as a part of the project BIOMAC. Anders Meibom is thanked for the NanoSIMS analyses and for comments on the manuscript. We thank three anonymous reviewers, and the editor Michael Böttcher for insightful comments, which contributed to improve the manuscript. This is IPGP contribution no. 3591. References Addadi, L., Moradian, J., Shay, E., Maroudas, N.G., Weiner, S., 1987. A chemical model for the cooperation of sulfates and carboxylates in calcite crystal nucleation: relevance to biomineralization. Proc. Natl. Acad. Sci. U. S. A. 84, 2732–2736. Adkins, J., Boyle, E.A., Curry, W.B., 2003. Stable isotopes in deep-sea corals and a new mechanism for “vital effects”. Geochim. Cosmochim. Acta 67, 1129–1143. Allison, N., 1996. Geochemical anomalies in coral skeletons and their possible implications for paleoenvironmental analyses. Mar. Chem. 55, 367–379. Allison, N., Finch, A.A., EIMF, 2010. The potential origins and paleoenvironmental implications of high temporal resolution d18O heterogeneity in coral skeletons. Geochim. Cosmochim. Acta 74, 5537–5548. Allison, N., Cohen, I., Finch, A.A., Erez, J., EMIF, 2011. Controls on Sr/Ca and Mg/Ca in scleractinian corals: the effects of Ca-ATPase and transcellular Ca channels on skeletal chemistry. Geochim. Cosmochim. Acta 75, 6350–6360. Amiel, A.J., Friedman, G.M., Miller, D.S., 1973. Distribution and nature of trace elements in modern aragonitic corals. Sedimentology 20, 47–64. Bar-Matthews, M., Wasserburg, G.J., Chen, J.H., 1993. Diagenesis of coral skeletons: correlation between trace elements, textures, and 234U/238U. Geochim. Cosmochim. Acta 57, 257–276. Beck, J.W., Edwards, L., Ito, E., Taylor, F.W., Recy, J., Rougerie, F., Joannot, P., Henin, C., 1992. Sea-surface temperature from coral skeletal strontium/calcium ratios. Science 257, 644–647. Bice, K.L., Layne, G.D., Dahl, K., 2005. Application of secondary ion mass spectrometry to the determination of Mg/Ca in rare, delicate, or altered planktonic foraminifera: examples from the Holocene, Paleogene, and Cretaceous. Geochem. Geophys. Geosyst. 6, Q12P07. http://dx.doi.org/10.1029/2005GC000974. Billings, G.K., Ragland, P.C., 1967. Geochemistry and mineralogy of the recent reef and lagoonal sediments south of Belize (British Honduras). Chem. Geol. 3, 135–153. Blamart, D., Rollion-Bard, C., Meibom, A., Cuif, J.-P., Juillet-Leclerc, A., Dauphin, Y., 2007. Correlation of boron isotopic composition with ultrastructure in the deep-sea coral Lophelia pertusa: implications for biomineralization and paleo-pH. Geochem. Geophys. Geosyst. 8, Q12001. http://dx.doi.org/10.1029/2007GC001686. Brahmi, C., Kopp, C., Domart-Coulon, I., Stolarski, J., Meibom, A., 2012. Skeletal growth dynamics linked to trace-element composition in the scleractinian coral Pocillipora damicornis. Geochim. Cosmochim. Acta 99, 146–158. Busenberg, E., Plummer, L.N., 1985. Kinetic and thermodynamic factors controlling the and Na+ in calcites and selected aragonites. Geochim. distribution of SO2− 4 Cosmochim. Acta 49, 713–725. Case, D.H., Robinson, L.F., Auro, M.E., Gagnon, A.C., 2010. Environmental and biological controls on Mg and Li in deep-sea scleractinian corals. Earth Planet. Sci. Lett. 300, 215–225. Chave, K.E., 1954. Aspects of the biogeochemistry of magnesium. 1. Calcareous marine organisms. J. Geol. 62, 266–283.

110

C. Rollion-Bard, D. Blamart / Chemical Geology 396 (2015) 98–111

Cohen, A.L., Gaetani, G.A., Lundälv, T., Corliss, B.H., George, R.Y., 2006. Compositional variability in a cold-water scleractinian, Lophelia pertusa: new insights into “vital effects”. Geochem. Geophys. Geosyst. 7. http://dx.doi.org/10.1029/2006GC001354. Corrège, T., 2006. Sea surface temperature and salinity reconstruction from geochemical tracers. Palaeogeogr. Palaeoclimatol. Palaeoecol. 232, 408–428. Cross, T.S., Cross, B.W., 1983. U, Sr, and Mg in Holocene and Pleistocene corals A. palmata and M. annuleris. J. Sedimentol. Petrol. 53, 587–594. Cuif, J.-P., Dauphin, Y., 1998. Microstructural and physico-chemical characterization of ‘centers of calcification’ in septa of some recent scleractinian corals. Paläontol. Z. 72, 257–270. Cuif, J.-P., Lecointre, G., Perrin, C., Tillier, A., Tillier, S., 2003a. Patterns of septal biomineralization in Scleractinia compared with their rRNA phylogeny: a dual approach for a new taxonomic framework. Zool. Scr. 32, 459–473. Cuif, J.-P., Dauphin, Y., Doucet, J., Salome, M., Susini, J., 2003b. XANES mapping of organic sulfate in three scleractinian coral skeletons. Geochim. Cosmochim. Acta 67, 75–83. Cuif, J.-P., Bendounan, A., Dauphin, Y., Nouet, J., Sirotti, F., 2013. Synchrotron-based photoelectron spectroscopy provides evidence for a molecular bond between calcium and mineralizing organic phases in invertebrate calcareous skeletons. Anal. Bioanal. Chem. http://dx.doi.org/10.1007/s00216-013-7312-4. Delaney, M.L., Popp, B.N., Lepzelter, C.G., Anderson, F., 1989. Lithium-to-calcium ratios in Modern, Cenozoic, and Paleozoic articulate brachiopod shells. Paleoceanography 4, 681–691. Elderfield, H., Bentram, C., Erez, J., 1996. A biomineralization model for the incorporation of trace elements into foraminiferal calcium carbonate. Earth Planet. Sci. Lett. 142, 409–423. Erez, J., 2003. The source of ions for biomineralization in foraminifera and their implication for paleoceanographic proxies. Rev. Mineral. Geochem. 54, 115–149. Ferrier-Pagès, C., Boisson, F., Allemand, D., Tambutté, E., 2002. Kinetics of strontium uptake in the scleractinian coral Styllophora pistillata. Mar. Ecol. Prog. Ser. 245, 93–100. Finch, A.A., Allison, N., 2008. Mg structural state in coral aragonite and implications for the paleoenvironmental proxy. Geophys. Res. Lett. 35, L08704. http://dx.doi.org/10.1029/ 2008GL033543. Frank, N., Ricard, E., Lutringer-Paquet, A., van der Land, C., Colin, C., Blamart, D., Foubert, A., Van Rooij, D., Henriet, J.-P., de Haas, H., van Weering, T., 2009. The Holocene occurrence of cold water corals in the NE Atlantic: implications for coral carbonate mound evolution. Mar. Geol. 266, 129–142. Gabitov, R.I., Gaetini, G.A., Watson, E.B., Cohen, A.L., Ehrlich, H.L., 2008. Experimental determination of growth rate effect on U6+ and Mg2+ partitioning between aragonite and fluid at elevated U6+ concentration. Geochim. Cosmochim. Acta 72, 4058–4068. Gabitov, R.I., Schmitt, A.K., Rosner, M., McKeegan, K.D., Gaetini, G.A., Cohen, A.L., Watson, E.B., Harrison, T.M., 2011. In situ d7Li, Li/Ca, and Mg/Ca analyses of synthetic aragonites. Geochem. Geophys. Geosyst. 12. http://dx.doi.org/10.1029/2010GC003322. Gabitov, R.I., Rollion-Bard, C., Tripati, A., Sadekov, A., 2014. In situ study of boron partitioning between calcite and fluid at different crystal growth rates. Geochim. Cosmochim. Acta 137, 81–92. Gaetini, G.A., Cohen, A.L., 2006. Element partitioning during precipitation of aragonite from seawater: a framework for understanding paleoproxies. Geochim. Cosmochim. Acta 70, 4617–4634. Gagnon, A.C., Adkins, J.F., Fernandez, D.P., Robinson, L.F., 2007. Sr/Ca and Mg/Ca vital effects correlated with skeletal architecture in a scleractinian deep-sea coral and the role of Rayleigh fractionation. Earth Planet. Sci. Lett. 261, 280–295. Gagnon, A.C., Adkins, J.F., Erez, J., 2012. Seawater transport during coral biomineralization. Earth Planet. Sci. Lett. 329–330, 150–161. Ghosh, P., Adkins, J., Affek, H., Balta, B., Guo, W.F., Schauble, E.A., Schrag, D., Eiler, J.M., 2006. C13O18 bonds in carbonate minerals: a new kind of paleothermometer. Geochim. Cosmochim. Acta 70, 1439–1456. Gladfelter, E.H., 1982. Skeletal development in Acropora cervicornis: I. Patterns of calcium carbonate accretion in the axial corallite. Coral Reefs 1, 45–51. Goldschmidt, V.M., 1954. Geochemistry. In: Muir, A. (Ed.), Oxford University Press, Fair Lawn, N. J. (730 pp.). Greaves, M., Caillon, N., Rebaubier, H., Bartoli, G., Bohaty, S., Cacho, I., Clarke, L., Cooper, M., Daunt, C., Delaney, M., et al., 2008. Interlaboratory comparison study of calibration standards for foraminiferal Mg/Ca thermometry. Geochem. Geophys. Geosyst. 9. http://dx.doi.org/10.1029/2008GC001974. Hart, S.R., Cohen, A.L., 1996. Sr/Ca in corals: an ion probe study of annual cycles and microscale coherence with other trace elements. Geochim. Cosmochim. Acta 60, 3075–3084. Hathorne, E.C., Felis, T., Suzuki, A., Kawahata, H., Cabioch, G., 2013. Lithium in the aragonite skeletons of massive Porites corals: a new tool to reconstruct tropical sea surface temperatures. Paleoceanography 28, 143–152. Hemming, N.G., Hanson, G.N., 1992. Boron isotopic composition and concentration in modern marine carbonates. Geochim. Cosmochim. Acta 56, 537–543. Holcomb, M., Cohen, A.L., Gabitov, R.I., Hutter, J.L., 2009. Compositional and morphological features of aragonite precipitated experimentally from seawater and biogenically by corals. Geochim. Cosmochim. Acta 73, 4166–4179. Immenhauser, A., Buhl, D., Richter, D., Niedermayr, A., Riechelmann, D., Dietzel, M., Schulte, U., 2010. Magnesium-isotope fractionation during low-Mg calcite precipitation in a limestone cave — field study and experiments. Geochim. Cosmochim. Acta 74, 4346–4364. Ip, Y.K., Krishnaveni, P., 1991. The incorporation of strontium (Sr2+) into the skeleton of the hermatypic coral Galaxea fascicularis. J. Exp. Zool. 258, 273–276. Ip, Y.K., Lim A.L.L., 1991. Are calcium and strontium transported by the same mechanism in the hermatypic coral Galaxea fascicularis? J. Exp. Biol. 159, 507–513. Isa, Y., Ikehara, N., Yamazato, K., 1980. Evidence for the occurrence of Ca2+-dependent adenosine triphosphatase in a hermatypic coral, Acropora hebes (DANA). Sesoko Mar. Sci. Lab. Tech. Rep. 7, 19–25.

Jacob, D.E., Soldati, A.L., Wirth, R., Huth, J., Wehrmeister, U., Hofmeister, W., 2008. Nanostructure, composition and mechanisms of bivalve shell growth. Geochim. Cosmochim. Acta 72, 5401–5415. Juillet-Leclerc, A., Reynaud, S., Rollion-Bard, C., Cuif, J.-P., Dauphin, Y., Blamart, D., FerrierPagès, C., Allemand, D., 2009. Oxygen isotopic signature of the skeletal microstructures in cultured corals: identification of vital effects. Geochim. Cosmochim. Acta 73, 5320–5332. Kinsman, D.J.J., 1970. Trace cations in aragonite. Abstr. Geol. Soc. Am. 2, 596–597. Kretz, R., 1982. A model for the distribution of trace elements between calcite and dolomite. Geochim. Cosmochim. Acta 46, 1979–1981. Lazier, A.V., Smith, J.E., Risk, M.J., Schwarcz, H.P., 2007. The skeletal structure of Desmophyllum cristagalli: the use of deep-water corals in sclerochronology. Lethaia 32, 119–130. Lea, D.W., 1999. Trace elements in foraminiferal calcite. In: Sen Gupta, Barun K. (Ed.), Modern Foraminifera. Klumer Academic Publishers, Great Britain, pp. 259–277. Lutringer, A., Blamart, D., Frank, N., Labeyrie, L., 2005. Paleotemperatures from deep-sea corals: scale effects. In: Freiwald, A., Roberts, J.M. (Eds.), Cold Water Corals and Ecosystems. Springer, Berlin, pp. 1081–1096. Marriott, C.S., Henderson, G.M., Belshaw, N.S., Tudhope, A.W., 2004a. Temperature dependence of δ7Li, δ44Ca and Li/Ca during growth of calcium carbonate. Earth Planet. Sci. Lett. 222, 615–624. Marriott, C.S., Henderson, G.M., Crompton, R., Staubwasser, M., Shaw, S., 2004b. Effect of mineralogy, salinity, and temperature on Li/Ca and Li isotope composition of calcium carbonate. Chem. Geol. 212, 5–15. Marshall, A.T., 1996. Calcification in hermatypic and ahermatypic corals. Science 271, 637–639. Mavromatis, V., Gautier, Q., Bosc, O., Schott, J., 2013. Kinetics of Mg partition and Mg stable isotope fractionation during its incorporation in calcite. Geochim. Cosmochim. Acta 114, 188–203. McConnaughey, T., 1989. 13C and 18O isotopic disequilibrium in biological carbonates: II. In vitro simulation of kinetic isotope effects. Geochim. Cosmochim. Acta 53, 163–171. Meibom, A., Cuif, J.-P., Hillion, F., Constantz, B.R., Juillet-Leclerc, A., Dauphin, Y., Watanabe, T., Dunbar, R.B., 2004. Distribution of magnesium in coral skeleton. Geophys. Res. Lett. 31, L23306. Meibom, A., Mostefaoui, S., Cuif, J.-P., Dauphin, Y., Houlbreque, F., Dunbar, R., Constantz, B., 2007. Biological forcing controls the chemistry of reef-building coral skeleton. Geophys. Res. Lett. 34, L02601. http://dx.doi.org/10.1029/2006GL028657. Meibom, A., Cuif, J.-P., Houlbreque, F., Mostefaoui, S., Dauphin, Y., Meibom, K.L., Dunbar, R., 2008. Compositional variations at ultra-structure length scales in coral skeleton. Geochim. Cosmochim. Acta 72, 1555–1569. Mitsuguchi, T., Matsumoto, E., Abe, O., Uchida, T., Isdale, P.J., 1996. Mg/Ca thermometry in coral skeletons. Science 274, 961–964. Mitsuguchi, T., Uchida, T., Matsumoto, E., Isdale, P.J., Kawana, T., 2001. Variations in Mg/Ca, Na/Ca, and Sr/Ca ratios of coral skeletons with chemical treatments: Implications for carbonate geochemistry. Geochim. Cosmochim. Acta 65, 2865–2874. Mitsuguchi, T., Uchida, T., Matsumoto, E., 2010. Na/Ca variability in coral skeletons. Geochem. J. 44, 261–273. Mortensen, P.B., 2000. Lophelia pertusa (Scleractinia) in Norwegian waters. Distribution, growth, and associated fauna. (PhD thesis). Department of Fisheries and Marine Biology, University of Bergen, Norway. Ogilvie, M.M., 1896. Microscopic study of Madreprarian types of corals. Philos. Trans. R. Soc. Lond. 187B, 83–345. Okumura, M., Kitano, Y., 1986. Coprecipitation of alkali metal ions with calcium carbonate. Geochim. Cosmochim. Acta 50, 49–58. Oomori, T., Kaneshima, K., Nakamura, Y., Kitano, Y., 1982. Seasonal variation of minor elements in coral skeletons. Galaxea 1, 77–86. Partz, E., 1882. Uber die verawandschaftlichen Beziehungen einige Korallengattungen. Paleontographica 29, 81–123. Pokroy, B., Fitch, A.N., Lee, P.L., Quintana, J.P., Caspi, E.N., Zolotoyabko, E., 2006. Anisotropic lattice distortions in the mollusk-made aragonite: a widespread phenomenon. J. Struct. Biol. 153, 145–150. Polyakov, D.M., Krasnov, E.V., 1975. Determination of the growth rate and age of corals Porites by the strontium and sodium content in their skeletons. Biol. Morya 6, 55–60. Raddatz, J., Liebetrau, V., Rüggeberg, A., Hathorne, E., Krabbenhöft, A., Eisenhauer, A., Böhm, F., Vollstaedt, H., Fietzke, J., Lopez Correa, M., Freiwald, A., Dullo, W.-Ch., 2013. Stable Sr-isotope, Sr/Ca, Mg/Ca, Li/Ca, and Mg/Li ratios in the scleractinian cold-water coral Lophelia pertusa. Chem. Geol. 352, 143–152. Reynaud, S., Ferrier-Pagès, C., Meibom, A., Mostefaoui, S., Mortlock, R., Fairbanks, R., Allemand, D., 2007. Light and temperature effects on Sr/Ca and Mg/Ca ratios in the scleractinian coral Acropora sp. Geochim. Cosmochim. Acta 71, 354–362. Robinson, L., Adkins, J.F., Gagnon, A., Prouty, N., Roark, B., van der Flierdt, T., 2014. The geochemistry of deep-sea coral skeletons: applications for paleoceanography. DeepSea Res. II 99, 184–198. Rollion-Bard, C., Blamart, D., 2014. SIMS method and examples of applications in coral biomineralization. In: Gower, L.B., DiMasi, E. (Eds.), Biomineralization Handbook. Characterization of Biominerals and Biomimetic Materials. Taylor & Francis, United Kingdom, pp. 249–260. Rollion-Bard, C., Marin-Carbonne, M., 2011. Determination of SIMS matrix effects on oxygen isotopic compositions in carbonates. J. Anal. At. Spectrom. 26, 1285–1289. Rollion-Bard, C., Chaussidon, M., France-Lanord, C., 2003a. pH control on oxygen isotopic composition of symbiotic corals. Earth Planet. Sci. Lett. 215, 275–288. Rollion-Bard, C., Blamart, D., Cuif, J.-P., Juillet-Leclerc, A., 2003b. Microanalysis of C and O isotopes of azooxanthellate and zooxanthellate corals by ion microprobe. Coral Reefs 22, 405–415. Rollion-Bard, C., Vigier, N., Meibom, A., Blamart, D., Reynaud, S., Rodolfo-Metalpa, R., Martin, S., Gattuso, J.-P., 2009. Effects of environmental conditions and skeletal

C. Rollion-Bard, D. Blamart / Chemical Geology 396 (2015) 98–111 ultrastructure on the Li isotopic compositions of scleractinian corals. Earth Planet. Sci. Lett. 286, 63–70. Rollion-Bard, C., Blamart, D., Cuif, J.-P., Dauphin, Y., 2010. In situ measurements of oxygen isotopic composition in deep-sea coral, Lophelia pertusa: re-examination of the current geochemical models of biomineralization. Geochim. Cosmochim. Acta 74, 1338–1349. Saulnier, S., Rollion-Bard, C., Vigier, N., Chaussidon, M., 2012. Mg isotope fractionation during calcite precipitation: an experimental study. Geochim. Cosmochim. Acta 91, 75–91. Shannon, R.D., 1976. Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides. Acta Crystallogr. A32, 751–767. Shinn, E.A., 1966. Coral growth rate, an environmental indicator. J. Paleontol. 40, 233–240. Sinclair, D.J., 2005. Correlated trace element “vital effects” in tropical corals: a new geochemical tool for probing biomineralization. Geochim. Cosmochim. Acta 69, 3265–3284. Sinclair, D.J., Williams, B., Risk, M., 2006. A biological origin for climate signals in corals — trace element “vital effects” are ubiquitous in scleractinian coral skeletons. Geophys. Res. Lett. 33, L17707. http://dx.doi.org/10.1029/2006GL027183. Smith, S., Buddemeier, R., Redalje, R., Houck, J., 1979. Strontium–calcium thermometry in coral skeletons. Science 204, 404–407. Speer, J.A., 1983. Crystal chemistry and phase relations of the orthorhombic carbonates. Rev. Mineral. Geochem. 11, 145–190. Stolarski, J., 2003. Three-dimensional micro- and nanostructural characteristics of the scleractinian coral skeleton: a biocalcification proxy. Acta Palaeontol. Pol. 48, 497–530. Stolarski, J., Kitahara, V.M., Miller, D., Cairns, S.D., Mazur, M., Meibom, A., 2011. The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals. BMC Evol. Biol. 11, 316–325. Swart, P.K., 1979. The effect of increased calcium concentrations on the growth and skeletal composition of a scleractinian coral: Acropora squamosa. J. Sediment. Petrol. 49, 951–954.

111

Swart, P.K., 1980. The environmental geochemistry of scleractinian coral skeletons. (PhD thesis). University of London. Swart, P.K., 1981. The strontium, magnesium and sodium composition of recent scleractinian coral skeletons as standards for paleoenvironmental analysis. Palaeogeogr. Palaeoclimatol. Palaeoecol. 34, 115–136. Tambutté, E., Allemand, D., Mueller, E., Jaubert, J., 1996. A compartmental approach to the mechanism of calcification in hermatypic corals. J. Exp. Biol. 199, 1029–1041. Tambutté, S., Holcomb, M., Ferrier-Pagès, C., Reynaud, S., Tambutté, E., Zoccola, D., Allemand, D., 2011. Coral biomineralization: from the gene to the environment. J. Exp. Mar. Biol. Ecol. 408, 58–78. van de Locht, R., Verch, A., Saunders, M., Dissard, D., Rixen, T., Moya, A., Kröger, R., 2013. Microstructural evolution and nanoscale crystallography in scleractinian coral spherulites. J. Struct. Biol. 183, 57–65. Vigier, N., Rollion-Bard, C., Spezzaferri, S., 2007. In situ measurements of Li isotopes in foraminifera. Geochem. Geophys. Geosyst. 8, Q01003. http://dx.doi.org/10.1029/ 2006GC001432. Watanabe, T., Minagawa, M., Oba, T., Winter, A., 2001. Pretreatment of coral aragonite for Mg and Sr analysis: implications for coral thermometers. Geochem. J. 35, 265–269. Watson, B.E., 1996. Surface enrichment and trace-element uptake during crystal growth. Geochim. Cosmochim. Acta 60, 5013–5020. Weber, J.N., 1974. Skeletal chemistry of scleractinian reef corals: uptake of magnesium from seawater. Am. J. Sci. 274, 84–93. Wells, J.W., 1956. Scleractinia. In: Moore, R.C. (Ed.), Treatrise on Invertabrate Paleontology, Part F, Scleractinia. Geological Society of America and University of Kansas Press, New York and Lawrence/Kansas, pp. F328–F344. White, A.F., 1977. Sodium and potassium coprecipitation in aragonite. Geochim. Cosmochim. Acta 41, 613–625. Yoshimura, T., Tanimizu, M., Inoue, M., Suzuki, A., Iwasaki, N., Kawahata, H., 2011. Mg isotope fractionation in biogenic carbonates of deep-sea coral, benthic foraminifera, and hermatypic coral. Anal. Bioanal. Chem. 401, 2755–2769.