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Geochimica et Cosmochimica Acta 236 (2018) 315–335 www.elsevier.com/locate/gca
The Li isotope composition of marine biogenic carbonates: Patterns and mechanisms
Mathieu Dellinger a,b,⇑, A. Joshua West a, Guillaume Paris c,d, Jess F. Adkins c, Philip A.E. Pogge von Strandmann e, Clemens V. Ullmann f, Robert A. Eagle g,h,i, Pedro Freitas j,1, Marie-Laure Bagard k, Justin B. Ries l, Frank A. Corsetti a, Alberto Perez-Huerta m, Anthony R. Kampf n
a Department of Earth Sciences, University of Southern California, Los Angeles, USA b Department of Geography, Durham University, Durham, DH1 3LE, UK c Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, USA d Centre de Recherches Pe´trographiques et Ge´ochimiques (CRPG), UMR 7358, CNRS-Universite´ de Lorraine, France e London Geochemistry and Isotope Centre, Institute of Earth and Planetary Sciences, University College London and Birkbeck, University of London, Gower Street, London WC1E 6BT, UK f University of Exeter, Camborne School of Mines & Environment and Sustainability, Institute, Penryn Campus, Penryn TR10 9FE, UK g Institute of the Environment and Sustainability, University of California, Los Angeles, LaKretz Hall, 619 Charles E Young Dr. E #300, Los Angeles, CA 90024, USA h Atmospheric and Oceanic Sciences Department, University of California – Los Angeles, Math Science Building, 520 Portola Plaza, Los Angeles, CA 90095, USA i Universite´ de Brest, UBO, CNRS, IRD, Ifremer, Institut Universitaire Europe´en de la Mer, LEMAR, Rue Dumont d’Urville, 29280 Plouzane´, France j Divisao de Geologia e Georecursos Marinhos, Instituto Portugues do Mar e da Atmosfera (IPMA), Av. de Brasilia s/n, 1449-006 Lisbon, Portugal k Institut des Sciences de la Terre d’Orle´ans (ISTO), UMR 7327, CNRS, Universite´ d’Orle´ans, BRGM, 1A, rue de la Fe´rollerie, 45071 Orle´ans Cedex 2, France l Department of Marine and Environmental Sciences, Marine Science Center, Northeastern University, Nahant, MA 01908, USA m Department of Geological Sciences, The University of Alabama, Tuscaloosa, AL 35487, USA n Mineral Sciences Department, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, CA 90007, USA
Received 30 August 2017; accepted in revised form 10 March 2018; available online 17 March 2018
Abstract
Little is known about the fractionation of Li isotopes during formation of biogenic carbonates, which form the most promising geological archives of past seawater composition. Here we investigated the Li isotope composition (d7Li) and Li/Ca ratios of organisms that are abundant in the Phanerozoic record: mollusks (mostly bivalves), echinoderms, and bra- chiopods. The measured samples include (i) modern calcite and aragonite shells from various species and natural environ- ments (13 mollusk samples, 5 brachiopods and 3 echinoderms), and (ii) shells from mollusks grown under controlled conditions at various temperatures. When possible, the mollusk shell ultrastructure was micro-sampled in order to assess intra-shell heterogeneity. In this paper, we systematically characterize the influence of mineralogy, temperature, and biological
⇑ Corresponding author at: Durham University, Geography Department, South Road, Durham, UK. E-mail address: [email protected] (M. Dellinger). 1 Present address: Danish Shellfish Centre, National Institute of Aquatic Resources, Danish Technical University, DK-7900, Nykøbing Mors, Denmark. https://doi.org/10.1016/j.gca.2018.03.014 0016-7037/Ó 2018 Elsevier Ltd. All rights reserved. 316 M. Dellinger et al. / Geochimica et Cosmochimica Acta 236 (2018) 315–335 processes on the d7Li and Li/Ca of these shells and compare with published data for other taxa (foraminifera and corals). Aragonitic mollusks have the lowest d7Li, ranging from +16 to +22‰, echinoderms have constant d7Li of about +24‰, brachiopods have d7Li of +25 to +28‰, and finally calcitic mollusks have the largest range and highest d7Li values, ranging from +25‰ to +40‰. Measured brachiopods have similar d7Li compared to inorganic calcite precipitated from seawater (d7Li of +27 to +29‰), indicating minimum influence of vital effects, as also observed for other isotope systems and making them a potentially viable proxy of past seawater composition. Calcitic mollusks, on the contrary, are not a good archive for seawater paleo–d7Li because many samples have significantly higher d7Li values than inorganic calcite and display large inter- species variability, which suggests large vital effects. In addition, we observe very large intra-shell variability, in particular for mixed calcite-aragonite shells (over 20‰ variability), but also in mono-mineralic shells (up to 12‰ variability). Aragonitic bivalves have less variable d7Li (7‰ variability) compared to calcitic mollusks, but with significantly lower d7Li compared to inorganic aragonite, indicating the existence of vital effects. Bivalves grown at various temperatures show that temperature has only a minor influence on fractionation of Li isotopes during shell precipitation. Interestingly, we observe a strong cor- relation (R2 = 0.83) between the Li/Mg ratio in bivalve Mytilus edulis and temperature, with potential implications for paleo- temperature reconstructions. Finally, we observe a negative correlation between the d7Li and both the Li/Ca and Mg/Ca ratio of calcite mollusks, which we relate to biomineralization processes. To explain this correlation, we propose preferential removal of 6Li from the calci- fication site of calcite mollusks by physiological processes corresponding to the regulation of the amount of Mg in the calci- fying medium. We calculate that up to 80% of the initial Li within the calcification site is removed by this process, leading to high d7Li and low Li/Ca in some calcite mollusk specimens. Collectively, these results suggest that Mg (and thus [Li]) is strongly biologically controlled within the calcifying medium of calcite mollusks. Overall, the results of this study show that brachiopods are likely to be suitable targets for future work on the determina- tion of paleo-seawater Li isotope composition—an emerging proxy for past weathering and hydrothermal processes. Ó 2018 Elsevier Ltd. All rights reserved.
Keywords: Lithium isotopes; Biogenic carbonates; Brachiopods; Mollusks; Biomineralization; Li/Mg ratio
1. INTRODUCTION carbonate rocks over geologic timescales (>10–100 kyrs). Li isotopes are strongly fractionated during water-rock A growing body of evidence suggests that the Li isotope interaction, with 6Li being preferentially incorporated into composition of seawater may be a promising proxy for trac- clay minerals while 7Li is concentrated in the dissolved ing past weathering and hydrothermal conditions at the phase (Chan et al., 1992; Huh et al., 1998; Pistiner and Earth’s surface, because the primary inputs of Li to the Henderson, 2003). As a result, dissolved riverine d7Li varies oceans are from rivers and the high-temperature hydrother- as a function of the ratio of primary mineral dissolution to mal flux from ocean ridges (Chan et al., 1992; Huh et al., secondary mineral formation (e.g. Pogge von Strandmann 1998; Hathorne and James, 2006; Misra and Froelich, and Henderson, 2015), and the evolution of d7Li and 2012). Furthermore, the residence time of Li in the ocean Li/Ca ratios of the ocean may provide information about is about 1–3 Ma, and the marine Li isotopic composition paleo-weathering regimes. 7 7 6 7 6 (d Li = [( Li/ Li)/( Li/ Li)L-SVEC 1] 1000; expressed in Reconstructing the Li isotopic composition of seawater ‰) and concentration are spatially uniform (Angino and requires a sedimentary archive, and carbonates have been Billings 1966). Published Li isotope records in foraminifera a preferred target so far (e.g. Vigier et al., 2007; Misra (Misra and Froelich, 2012; Hathorne and James, 2006) and and Froelich, 2012; Pogge von Strandmann et al., 2013). bulk carbonates (Pogge von Strandmann et al., 2013; Laboratory experiments inform general understanding of Lechler et al., 2015; Pogge von Strandmann et al., 2017) Li incorporation into inorganic carbonates. In aragonite, are characterized by large (several per mil) d7Li variations Li+ is thought to substitute for Ca2+ in the mineral lattice, in the geological past. These changes have been attributed whereas in calcite, Li+ occupies an interstitial location to past changes in weathering congruency, intensity, or (Okumura and Kitano, 1986). The Li/Ca ratio of inorganic rates (Bouchez et al., 2013; Froelich and Misra, 2014; Li carbonates is influenced by the Li/Ca ratio and/or the Li and West, 2014; Wanner et al., 2014). concentration of the fluid from which it precipitates The relationship between Li isotope fractionation and (Marriott et al., 2004b,a; Gabitov et al., 2011). The Li/Ca chemical weathering on the continents has been well- ratio of inorganic calcite decreases with increasing temper- studied, and although details are still debated, general ature (Marriott et al., 2004a,b). An increase in Li/Ca with trends are understood (Huh et al., 2001; Wanner et al., salinity was also observed for calcite but not for aragonite 2014; Bagard et al., 2015; Dellinger et al., 2015; Pogge (Marriott et al., 2004b), but the Li/Ca ratio of inorganic von Strandmann and Henderson, 2015; Dellinger et al., aragonite increases with precipitation rate (Gabitov et al., 2017). Dissolved Li transported to the oceans is primarily 2011). In addition, the isotopic fractionation factor between derived from the weathering of silicate rocks (Huh et al., inorganic calcium carbonate and solution is strongly 2001; Kısakurek} et al., 2005), which generates alkalinity dependent upon the carbonate mineralogy, with the frac- and, unlike carbonate weathering, sequesters CO2 in tionation factor between inorganic aragonite and seawater M. Dellinger et al. / Geochimica et Cosmochimica Acta 236 (2018) 315–335 317
7 aaragonite-seawater = 0.988 – 0.993 (corresponding to a In this study, we focus mainly on characterizing the d Li Daragonite-seawater of 7to 12‰) and the fractionation and Li/Ca of carbonate-forming organisms, particularly factor between inorganic calcite and seawater bivalves and brachiopods, since these may be some of the acalcite-seawater = 0.998 – 0.995 (Dcalcite-seawater of 2to most important Phanerozoic paleoenvironmental bioarc- 5‰; Marriott et al., 2004a,b; Gabitov et al., 2011). hives. We also present a few measurements of echinoderms. A number of studies have investigated the Li/Ca ratio of Bivalves, brachiopods, and echinoderms are present in biogenic carbonates, showing that the incorporation of widely distributed habitats in the modern-day ocean, are lithium depends upon various parameters that include tem- often well-preserved during diagenesis, and are abundant perature, salinity, growth rate, carbonate ion concentra- in the Phanerozoic record (Wilkinson, 1979; Veizer et al., tion, dissolved Li concentration, and biology (also called 1999; Immenhauser et al., 2016). Prior studies have reported ‘‘vital effects”). Temperature appears to be a major control Li isotope data on Ordovician brachiopods (Pogge von on the Li/Ca ratio of brachiopods, which show increasing Strandmann et al., 2017), and Li/Ca values of modern Li/Ca with decreasing temperature (Delaney et al., 1989), bivalves and brachiopods (Delaney et al., 1989; The´bault similar to that observed for inorganic calcite. However, et al., 2009; The´bault and Chauvaud, 2013; Fu¨llenbach no systematic trend between Li/Ca and temperature has et al., 2015), but no Li isotope data on modern bivalves been observed for other biogenic carbonates. Instead, cul- and brachiopods. Here we test the influence of temperature, ture experiments and core top studies have shown that mineralogy and biology on Li isotopic composition and the Li/Ca ratio of foraminifera is influenced by the solution Li/Ca ratio using a set of mollusk, brachiopod and echino- Li/Ca ratio, DIC concentration, and possibly the growth derm samples from various environments, in order to evaluate 7 rate (Delaney et al., 1985; Hall and Chan, 2004; Hathorne the suitability of these taxa for reconstructing past d Liseawater. and James, 2006; Lear and Rosenthal, 2006; Vigier et al., 2015). In contrast, the Li/Mg ratio of corals and foramini- 2. ORIGIN OF THE SAMPLES AND SAMPLING fera is more strongly related to temperature than Li/Ca and STRATEGY has been recently proposed as being a reliable proxy for ocean temperature (Bryan and Marchitto, 2008; Case Two types of samples have been investigated: (i) shells et al., 2010; Montagna et al., 2014; Rollion-Bard and from modern marine organisms corresponding to a wide Blamart, 2015; Fowell et al., 2016). The Li/Ca ratio of mol- range of mineralogy, species, and locations; and (ii) shells lusks might be controlled by a combination of vital effects, grown in controlled culture experiments at various growth rate, changes in ocean productivity, and/or dissolu- temperatures. tion of riverine fine sediments within the ocean (The´bault et al., 2009; The´bault and Chauvaud, 2013; Fu¨llenbach 2.1. Field-collected modern shells et al., 2015). In contrast to the wide range of organisms studied for Li Modern shell samples were retrieved from the Natural elemental ratios, Li isotope ratios have been investigated History Museum of Los Angeles County collections, sup- mostly in modern foraminifera and corals. Modern corals plemented with miscellaneous other specimens. All mollusk have Li isotopic composition ranging from +17 to +25‰ samples from this study, except the gastropod Turritella, (Marriott et al., 2004a,b; Rollion-Bard et al., 2009), signif- are bivalves (n = 17 specimens). They come from 13 species icantly fractionated relative to seawater but with an average comprising oysters, clams, mussels, and scallops. We also d7Li similar to inorganic aragonite (around +19‰). The analyzed 5 brachiopod and 3 echinoderm specimens, each intra-specimen variability for corals is relatively low, less from different species. These shells come from a wide range than ±2‰, but small systematic differences exist between of marine environments from cold to warm sea surface tem- species (Rollion-Bard et al., 2009). Present-day planktic for- perature ( 1to30°C). The location and characteristics of aminifera d7Li range between +27 and +31‰ (Hall et al., the specimens are summarized in Table 1 and Fig. 1.We 2005; Hathorne and James, 2006; Misra and Froelich, extracted the main seawater parameters (sea surface tem- 2012) with a median value of 30‰, very close to modern perature – SST, salinity, alkalinity), including annual aver- seawater (31‰), making them targets for past work recon- ages and, when possible, specifically sampling the growth structing the Li isotope composition of the Cenozoic ocean interval of the shells (average of the 3 months having the (Hathorne and James, 2006; Misra and Froelich, 2012). highest SST). We used the World Ocean Atlas 2013 for However, Li isotopic fractionation in foraminifera may SST and salinity (Locarnini et al., 2013) and GLODAPv2 depend upon seawater dissolved inorganic carbon (DIC) database for alkalinity (Olsen et al., 2016), or specified ref- concentration (Vigier et al., 2015), and/or on pH (Roberts erences when more accurate data were available. Because of et al., 2018). In addition, well-preserved planktic foramini- uncertainty regarding the sampling location, we attribute a fera are not very abundant in the geological record prior to relatively large uncertainty to these ocean parameters. the Cenozoic (Wilkinson, 1979). Considering other calcify- Field-collected shells were cleaned in an ultrasonic bath ing organisms, Ullmann et al. (2013b) for belemnites and with distilled water, cut, and drilled. The sampling strategy Pogge von Strandmann et al., (2017) for brachiopods have was intended to simultaneously sample a large (20–30 mg), shown that the hard parts of these organisms show promise representative ‘‘bulk” sample in the middle of the shell for preserving the Li isotope composition of the ocean over while also targeting some micro-scale samples, using a geological timescales, but detailed studies of modern speci- micro-mill, in order to investigate possible intra-shell vari- mens remain lacking. ability (Fig. 2). Table 1 315–335 (2018) 236 Acta Cosmochimica et Geochimica / al. et Dellinger M. 318 Data for modern field-collected and growth experiment biogenic carbonates from this study. Sample Sample type Phylum Species Specimen Common Sampling location Dominant d7Li Aragonite Calcite Li/Ca Mg/Ca Al/Ca Sr/Ca d18 O Growth Annual name # name mineralogya temperatureb temperaturec (‰)(%) (%) (lmol/mol) (mmol/mol) (lmol/mol) (mmol/mol) (‰)(°C) (°C) Field-collected Mollusk samples 57-12 Mixed Mollusk Chlamys cheritata Scallops Alaska (Kachemak Bay) USA C 39.3 0 100 19.5 5.7 Mixed Sea Urchin Strongylocentrotus Urchins Leo Carillo, CA, USA HMC 24.4 69.2 88.2 Fig. 1. Map representing the location and name of all the field-collected samples from this study. (A) America, (B) East Asia, Oceania and Antarctica, and (C) Europe. We studied four different specimens of oysters (Cras- colbecki from Antarctica (partly described in Eagle et al., sostrea gigas) from four different localities spanning a wide 2013). One sample of 20 mg for each of these species was range of ocean temperature (12–27 °C). The shell of Cras- collected by milling the middle of the shell, and these sam- sostrea gigas is predominantly composed of calcite with ples thus correspond to a mix of the prismatic and nacreous two types of mineralogical structure, the ‘‘chalky structure” layers. and ‘‘foliate layers” (Carriker and Palmer, 1979; Carriker Two Mytilus californianus mussel specimens from differ- et al., 1980; Ullmann et al., 2010, 2013a). The chalky struc- ent locations, the USA (Washington State) and Mexico, ture is composed of a 3D network while foliate layers are were also studied. The shell of Mytilus californianus is com- elongated calcite crystals. ‘‘Bulk” samples of about 20 mg posed of a calcite prismatic outer layer and an aragonite of mixed calcite were sampled in the middle and outer layer nacreous inner layer. Because of this mineralogical hetero- of specimens collected in Washington and California (USA) geneity, both specimens were micro-drilled at various loca- and Ecuador. The fourth specimen was collected in the tions on the shell in order to sample the inner or outer layer North Sea in the List basin and has been previously inves- separately. tigated at small scale for other chemical proxies (Ullmann Clam specimens studied here comprise three genera et al., 2013a, 2010). Specific foliate layers and chalky struc- (Chione, Tridacna and Laternula). Chione specimens ture were micro-sampled (see Ullmann et al., 2010 for (mostly composed of aragonite) are from three different details about the sampling protocol). We also determined species: Chione californiensis (California), Chione subimbri- the growth temperature for this North Sea oyster sample cata (Costa Rica), and Chione subrugosa (Peru). The two using calcite d18O, following Ullmann et al. (2010; 2013a) Tridacna species studied were Tridacna gigas (Costa Rica) using an average d18O value for the List basin seawater of and Tridacna maxima (Mariana island), both with a shell 1.3‰ (V-SMOW). of pure aragonite. One shell sample of 20 mg from each Scallop samples are from two distinct genera (Chlamys of these species was collected by milling the middle of the and Adamussium). Three different Chlamys species were shell, and specific inner and outer layers were also sampled investigated: Chlamys cheritata (Alaska), Chlamys hastata to test for intra-shell variability. (California), and Laevichlamys squamosa (Philippines). Five specimens each from different species of calcitic For Adamussium, we studied one specimen of Adamussium brachiopods were investigated in this study. These samples M. Dellinger et al. / Geochimica et Cosmochimica Acta 236 (2018) 315–335 321 was grown at temperatures between 15 and 30 °C, Mytilus edulis between 10.7 and 20.2 °C and Pecten maximus between 10.8 and 20.2 °C. Only the outer layer of the shells was sampled. The thin inner layer of Mytilus edulis was milled out when present (from the pallial line towards the umbo) before sampling from the outer surface. For Pecten maximus, the shell was sampled from the outer cross- lamellar layer, close to the margin and away from the inner layer and myostracum. Surface features like growth distur- bances and the striae that tend to show a disturbed arrange- ment of crystals and high Mg/Ca, Sr/Ca and Mn/Ca ratios (Freitas et al., 2006) were included in the sampling. 3. ANALYTICAL METHODS 3.1. Mineralogy The proportion of aragonite versus calcite for the major- ity of the powdered samples was measured at the Natural History Museum of Los Angeles County with a R-AXIS RAPID II X-ray diffraction system. Whole-pattern-fitting, implemented in JADE 2010 (Materials Data, Inc.), was used to analyze the X-ray powder diffraction patterns. The precision for this method is about ±5%. Fig. 2. Schematic showing the various types of sampling used in this study (bulk and specific layers) for mussels, clams, oysters, and 3.2. Leaching and dissolution of the samples brachiopods. Since Li concentrations in carbonates are generally very low (< 1 ppm), carbonate samples are sensitive to contam- include the species Campages mariae (Aliguay Island, ination by other phases during dissolution, particularly Philippines), Laqueus rubellus (Sagami Bay, Japan), Tere- from silicate minerals (Vigier et al., 2007). All samples were bratalia transversa (Friday Harbor, Washington State, therefore subjected to a pre-leach following a method USA), Notosaria nigricans (South Island, New Zealand), modified from Saenger and Wang (2014), to remove and Frenulina sanguinolenta (Mactan Island, Philippines). exchangeable ions using 1 N ammonium acetate followed These brachiopods have primary and secondary shell layers by 3 rinses with milliQ (Millipore) water. The samples were (both calcite, with different ultrastructure). Unlike the pri- then digested in dilute hydrochloric acid (HCl 0.05 N) for mary layer and the outer part of the secondary layer, the 1 h. The volume of acid used for digestion was calculated innermost part of the secondary layer is characterized by to dissolve about 95% of the sample in order to minimize negligible vital effects for C and O isotopes (Auclair et al., the leaching of non-carbonate phases. After 1 h, the super- 2003; Cusack and Huerta, 2012; Penman et al., 2013; natant was collected while the sample residue was weighed Ullmann et al., 2017). We primarily sampled bulk mixed in order to determine the yield of the digestion. For the layer samples (corresponding mostly to the secondary layer) great majority of samples, the yield for the digestion was in this study. Approximately 20 mg of bulk powder was col- between 90 and 100%. As discussed below, Al/Ca ratios lected from each species except for Terebratulina retusa, were measured in order to confirm the absence of which was sampled from various portions of the shell to test aluminosilicate-derived solutes in the leachate. for intra-shell variability of Li isotope composition. Three species of sea urchins (high-Mg calcite) were col- 3.3. Trace element measurements lected from California waters: Strongylocentrotus fransis- canus, Strongylocentrotus purpuratus and Dendraster sp. A Ratios of trace elements Li, Mg, Sr, Al, Mn, and Fe rel- large 30 mg bulk powder was collected for each of the ative to Ca were measured using a Thermo Scientic Element samples. 2 inductively coupled plasma mass spectrometer (ICP-MS) at the University of Southern California (USC) following a 2.2. Cultured shells method adapted from Misra et al. (2014). All samples and standards were measured at a Ca concentration of 50 ppm. Two calcite bivalve species, Mytilus edulis and Pecten Li, Mg, Sr, and Al concentrations were measured at low maximus (Freitas et al., 2008), and one aragonite bivalve mass resolution whereas Fe and Mn were measured at (Mercenaria mercenaria) were experimentally grown at var- medium mass resolution. The instrument was first condi- ious temperatures. Details about the culture experiments tioned for 1 h with a solution of 50 ppm Ca. A set of 10 for Mytilus edulis and Pecten maximus are available in multi-elemental calibration standards was measured at the Freitas et al. (2006, 2008, 2012). Mercenaria mercenaria beginning of the run, and a bracketing standard solution 322 M. Dellinger et al. / Geochimica et Cosmochimica Acta 236 (2018) 315–335 was measured every 5–10 samples to correct for the drift of standard) and rock (BCR-2 and SGR-1) standards are the signal. Accuracy and precision of analyses were checked reported in Pogge von Strandmann et al. (2013, 2017). using the aragonite reference material FEBS-1 (NRC) and The total procedural blank for Li isotopes is effectively in-house prepared standard solutions matching typical cal- undetectable (<0.005 ng Li). cium carbonate chemical composition. Analytical precision was 6% for Mg/Ca and Sr/Ca ratio, 8% for Li/Ca and 15% 4. RESULTS for Al/Ca ratios. 4.1. Sample mineralogy 3.4. Lithium isotopes The sample set from this study included shells composed Lithium was separated from the matrix by ion-exchange of pure calcite, aragonite, and high-Mg calcite, as well as chromatography using a method modified from James and mixtures of these minerals. Mineralogy was measured when Palmer (2000). The dissolved calcium carbonate fraction possible on the same powder used for Li isotope analysis was passed through a column containing 4 mL of Biorad (see table 1). Pure calcite specimens (over 95% calcite) AG50W X-12 (200–400 mesh) resin. The Li fraction was included oysters (C. gigas), scallops (P. maximus, C. cheritata eluted with 0.5 N HCl (elution volume of about 13.5 mL) and C. hastata), and brachiopod samples. Pure aragonitic and evaporated to dryness at a temperature of 90–100 °C. skeletal material from this study included clams (T. gigas Purified samples were kept until measurement as solid salts and T. maxima) and gastropods (Turritella). All other in Teflon beakers and subsequently dissolved in 5% HNO3 measured specimens had a mixed mineralogy, and, for this for mass spectrometry analysis. Lithium isotope ratios were reason, were micro-sampled at specific locations on the measured on a Thermo Neptune MC ICP-MS at Caltech, shells to obtain mineralogically pure phases. The drilled using a Cetac Aridus desolvator as an introduction system. C. squamosa sample contained about 30% aragonite. Samples were measured following a standard-sample brack- Chione samples were primarly composed of aragonite, with eting method with the commonly used L-SVEC standard a lesser proportion of calcite (1–46%). The mineralogy of (Flesch et al., 1973). The method comprised 50 cycles of Mytilus californianus shell samples ranged from pure calcite 4 s for both standards and samples. Typical sensitivity to pure aragonite. The mineralogy of experimentally cul- was 30 pA (about 3 V) for 10 ng/g Li solution. Most of tured samples was not measured but inferred from previous the samples were measured at concentrations ranging from studies (e.g., Ries, 2011; Freitas et al., 2006, 2008; Ries 5 to 10 ng/g, with the smallest samples measured at 1 or et al., 2009) to be either pure calcite (Mytilus edulis, Pecten 2 ng/g. Clean acid was measured before and after each sam- maximus) or pure aragonite (Mercenaria mercenaria). The ple and standard, and the signal subtracted to correct for mineralogy for specific layers of the oyster sample was the background contribution. Each sample was typically not measured either but is assumed to be pure calcite measured twice in a row. Accuracy and reproducibility of (Ullmann et al., 2010). In the following, we refer to the isotopic measurements were checked through repeated ‘‘calcite” or ‘‘aragonite” for samples having more than analyses of seawater, with long-term average d7Li = 95% calcite and aragonite, respectively, with other samples +30.9 ± 0.8‰ (2r, n = 63 separations and measurements) being classified as ‘‘mixed”. and L-SVEC solutions passed through columns giving d7Li = 0.1 ± 0.8‰ (2r, n = 25 separations and measure- 4.2. Major and trace element ratios ments). We therefore consider that the external measure- ment precision is ±1‰. More information about the We use minor and major element ratios, along with min- analytical method is available in the supplementary eralogical data, to characterize the samples from this study. materials. In general, aragonite has higher Sr and lower Mg concen- The samples of the oyster Crassostrea gigas from the trations than calcite (Dodd, 1967; Milliman et al., 1974). List Basin were purified using a similar technique (Pogge Our dataset is consistent with these observations. The von Strandmann et al., 2013, Pogge von Strandmann Mg/Ca ratios of the current dataset span over two orders and Henderson, 2015), where the dissolved calcium car- of magnitude, ranging from 0.3 to 109 mmol mol 1 bonate fraction was passed through a 2-stage cation (Fig. 3). Aragonite and mixed shell samples have lower exchange procedure with columns containing Biorad Mg/Ca values (0.3–8.0 mmol mol 1) compared to low- AG50W X-12 (200–400 mesh) resin. The first column con- magnesium calcite (LMC; with Mg/Ca of 1.0–20.0 mmol tained 2.4 ml resin, and the second column 0.5 ml. In both mol 1). The sea urchin samples (HMC) have the highest cases the Li fraction was eluted using 0.2 M HCl. Analyses Mg/Ca ratios within this dataset, ranging from 80 to 109 were performed on a Nu Instruments HR MC-ICP-MS at mmol mol 1. The Mg/Ca values of the shells of Pecten Oxford, with a 7Li sensitivity of 18 pA for a 20 ng/ml maximus and Mytilus edulis agree well with previously pub- solution at an uptake rate of 75 ll/min. Analyses consisted lished values from the literature (Freitas et al., 2009, 2008, of three separate repeats of 10 ratios (10 s total integration 2006). The Sr/Ca values range from 0.5 to 2.5 mmol mol 1, time), for a total duration of 300 s/sample during each with aragonite and high-magnesium calcite (HMC) samples analytical session. Precision and accuracy were assessed from this study having higher Sr/Ca compared to LMC. by multiple analyses of N. Atlantic seawater, with a The Mg/Ca and Sr/Ca values of our samples are in the long-term value and reproducibility of +31.2 ± 0.6‰ range of previously published values for modern mollusks (2r, n = 61). Other carbonate (JLs-1 and in-house marl (Steuber, 1999), brachiopods (Delaney et al., 1989; M. Dellinger et al. / Geochimica et Cosmochimica Acta 236 (2018) 315–335 323 Fig. 3. (A) Sr/Ca of the biogenic carbonates from this study and from literature sources as a function of Mg/Ca. Corals (Sr/Ca > 8) are not plotted on this figure. Data collected in this study are consistent with expectations based on mineralogy (higher Sr/Ca and lower Mg/Ca for aragonite compared to calcite). The three points surrounded by a circle have very high Sr/Ca compared to other samples and are excluded from further discussion because the exact mineralogical composition of these samples is not known. (B) Li/Ca of the biogenic carbonates as a function of Mg/Ca. Carpenter and Lohmann, 1992; Brand et al., 2003; Ullmann 4.3. Lithium isotopes et al., 2017) and sea urchins (LaVigne et al., 2013). The Li/Ca ratios of bivalve mollusks from this study For the entire dataset (Table 1), the Li isotope composi- range between 3.7 and 52.0 lmol mol 1, while the only gas- tion ranges between +14.9 and +40.7‰, indicating that tropod, Turritella, has the lowest Li/Ca value (1.7 lmol these biogenic carbonates have both lower and higher mol 1) of all the samples. Brachiopods have Li/Ca ratios d7Li compared to modern seawater (+31‰). For the mod- ranging from 20 to 43 lmol mol 1, while the high-Mg cal- ern biogenic carbonates, the pure aragonitic mollusks have cite echinoderm specimens have the highest Li/Ca of this the lowest d7Li values, ranging from +14.9 to +21.7‰, dataset, ranging from 60 to 81 lmol mol 1. The Li/Ca whereas the pure calcitic mollusks have higher d7Li, ranging values of our samples are within the range of previously from +20.5 to +40.7‰ (Fig. 4). Mixed aragonite-calcite published Li/Ca from the literature (see Fig. 4). If we con- samples have intermediate values. For the extensively sider all reported measurements (including measurements micro-sampled North Sea oyster sample, the d7Li ranges made at various parts on a single shell), the range of Li/Ca from 20.5 to 37.8‰ with no significant systematic differ- ratio of biogenic calcite is very high with values up to ences between the chalky and foliate layers. The 8 bra- 250 lmol mol 1 measured on some parts of the bivalve chiopod and 3 echinoderm samples have relatively Pecten maximus (The´bault and Chauvaud, 2013). However, uniform d7Li, ranging respectively from +24.7 to +27.8‰ if we consider only the average value for each specimen, the and from +24.1 to +24.4‰ (Fig. 4). The field-collected Li/Ca ratio ranges from 10 to 50 lmol mol 1 for LMC specimens from this study come from various locations that organisms, between 1 and 30 lmol mol 1 for aragonitic span a wide range of ocean temperatures ( 1to30°C). speciments, and between 60 and 90 lmol mol 1 for high- Because the location of most of the samples is not known Mg calcite biogenic carbonates, showing that there is a precisely, and natural temperatures may vary seasonally, mineralogical control on the Li/Ca of biogenic carbonate we assign a 2 °C uncertainty to estimated growth tempera- (Fig. 4B). Furthermore, there is an overall correlation tures and only look to identify any large first order relation- between Li/Ca and Mg/Ca (Fig. 3) for all biogenic carbon- ships. We find no effect of temperature on the measured ates, suggesting that these two elements are impacted by d7Li using this approach (Fig. 5B). This lack of correlation one or more common processes during biomineralization. is particularly clear for the four specimens of Crassostrea The elemental compositions of cultured samples (for gigas, with temperatures ranging from +10 to +22 °C which the mineralogy was not measured) are in agreement (points labelled C.G.1 to C.G.4 in Fig. 5B). In addition, with other samples and plot inside the field defined by each we can also consider the influence of short timescale polymorph mineral (Fig. 4). For the oyster sample from (weekly to monthly) temperature variation on the Li iso- List Tidal Basin (assumed to be pure calcite), we observe tope composition of the Crassostrea gigas specimen from that 3 samples have much higher Sr/Ca ratio and lower the North Sea. For this specimen, we establish time series Li/Ca than surrounding samples and plot well outside the along the foliate layers and chalky using growth strata, trend defined by the mixture between aragonite and calcite. and calcification temperatures were calculated using the Whether these samples contain some aragonite or high-Mg d18O of each sample (Ullmann et al., 2013a, 2010). No cor- calcite, or perhaps have been altered, has not be deter- relation was observed between the calcification temperature mined. In the absence of additional information, these sam- and d7Li for either the chalky substance or foliate layers, ples will not be further considered in our interpretation. despite the large range of d7Li values. 324 M. Dellinger et al. / Geochimica et Cosmochimica Acta 236 (2018) 315–335 45 AB300 200 40 100 35 Seawater 40 30 30 Inorganic calcite 20 Li (‰) 25 Inorganic aragonite Li/Ca 7 (µmol/mol) 10 20 4 3 15 2 High-Mg High-Mg Aragonite Calcite Mixed Aragonite Calcite calcite calcite 10 1 Corals Corals (mixed) Mollusks Mollusks (Calcite) Mollusks Benthic Benthic Mollusks Planktic Mollusks Benthic Planktic (Aragonite) Red algae foraminifera foraminifera foraminifera foraminifera foraminifera Brachiopods Brachiopods Echinoderms Echinoderms Fig. 4. (A) Li isotope composition of modern carbonates, organized by phylum and mineralogy. Small transparent points (for mollusks and corals) correspond to all data for each phylum. Each large data marker corresponds to the average value for one specimen. Data from corals (Marriott et al., 2004a; Rollion-Bard et al., 2009), planktic foraminifera (Hathorne and James, 2006; Marriott et al., 2004a; Misra and Froelich, 2009; Rollion-Bard et al., 2009), and benthic foraminifera (Marriott et al., 2004b) are from previously published literature. (B) Li/Ca ratio of modern carbonates, organized by phylum and mineralogy. Each large data marker corresponds to the average value for one specimen. Each small data marker corresponds to an individual measurement. Horizontal bars correspond to the maximum and minimum value for all data for each phylum. Data for corals (Hathorne et al., 2013; Marriott et al., 2004b; Montagna et al., 2014; Rollion-Bard et al., 2009; Rollion- Bard and Blamart, 2015), planktic and benthic foraminifera (Hall et al., 2005; Hall and Chan, 2004; Hathorne and James, 2006; Misra and Froelich, 2012), and red algae (Darrenougue et al., 2014) are from previous studies. Data from mollusks and brachiopods also include previously published data in addition to results from this study (Delaney et al., 1989; Fu¨llenbach et al., 2015; The´bault et al., 2009; The´bault and Chauvaud, 2013). Skeletal organisms with the highest Li/Ca ratios are high-Mg calcite like red algae (60–110 lmol mol 1; Darrenougue et al., 2014), low-Mg calcitic mollusks (20–250 lmol mol 1; Fu¨llenbach et al., 2015; The´bault and Chauvaud, 2013), and brachiopods (20–50 lmol mol 1; Delaney et al., 1989). Aragonitic mollusks and benthic foraminifera have the lowest reported Li/Ca ratios among skeletal organisms, between 2 and 11 lmol mol 1 (Hall and Chan, 2004; The´bault et al., 2009). For the samples from growth experiments at various biological processes significantly influence the Li isotope temperatures, the d7Li ranges from +32.1 to +35.2‰ for composition and Li/Ca ratio of mollusk shells, but not Pecten maximus samples, from +33.3 to +39.7‰ for Myti- the compositions of the secondary layer (the only one lus edulis, and from +17.2 to +19.2‰ for Mercenaria measured in this study) of brachiopods. mercenaria. For the two calcitic calcifiers (Mytilus edulis and Pecten maximus), we observe a weak positive correla- 5.1. Influence of mineralogy tion between measured d7Li and temperature for the stud- ied range (r2 = 0.3; Fig. 5A). The Li isotope composition Experimental inorganic calcium carbonate precipitates is slightly higher at high temperature than at lower temper- have lower d7Li values compared to the solution from ature with a d7Li-temperature relationship of about which they precipitate (Marriott et al., 2004a,b; Gabitov +0.2‰/°C. For the aragonitic bivalve (Mercenaria merce- et al., 2011), with aragonite more fractionated 7 naria), the opposite relation is observed, with slightly (D Liaragonite-solution = 7to 12‰) than calcite 7 7 higher d Li at low temperature than at high temperature (D Licalcite-solution = 2to 5‰). Biogenic carbonates also (d7Li-temperature relationship of 0.1‰/°C). are fractionated differently according to their mineralogy with d7Li of calcite shells from +25 to +40‰ (excluding 5. DISCUSSION samples ofl04, 05, and 06 which we remove as noted above), whereas aragonitic shells have d7Li from +15 to +24‰ The d7Li range for biogenic carbonates from this study (Fig. 4A). Bi-mineralic shells exhibit intermediate d7Li. (+14.9 to +40.7‰) is much larger than the range of These observations are consistent with other types of bio- previously-reported Li isotope compositions for both inor- genic carbonates: the d7Li of modern calcitic planktic fora- ganic carbonates and modern seawater (Marriott et al., minifera is systematically higher than 26‰ (Hathorne and 2004a,b; Misra and Froelich, 2012). This suggests an James, 2006; Misra and Froelich, 2009) whereas corals environmental and/or biological control on the Li isotope (aragonite) have d7Li consistently lower than +25‰ composition of these biogenic carbonates. In this discus- (Rollion-Bard et al., 2009). Interestingly, the three high- sion, we explore the influence of mineralogy, temperature, Mg calcite samples (echinoderms) from this study have an and biology (taxonomic differences, inter-species, and intermediate d7Li of +24‰. We also note systematic differ- intra-specimen variability) on the Li isotope fractionation ences in Li/Ca ratio amongst aragonite, calcite and high- in mollusks, brachiopods and echinoderms. We show that Mg calcite samples. The inorganic partition coefficient for M. Dellinger et al. / Geochimica et Cosmochimica Acta 236 (2018) 315–335 325 Fig. 5. (A) Li isotope composition as a function of temperature for mollusks grown at various temperatures. The small black squares correspond to inorganic calcite precipitation experiments at various temperature while the small filled red squares represent abiogenic precipitation experiments at varying salinity (Marriott et al., 2004a). (B) Li isotope composition as a function of the growth temperature for modern field-collected biogenic mollusks, brachiopods, and echinoderms from this study. All data correspond to the mean of all the measurements of a single specimen. The initials correspond to the genera and species name. (C) Li/Ca ratio (in lmol mol 1) of brachiopods as a function of the annual temperature. Data from Delaney et al. (1989) for brachiopods and inorganic experimental data from Marriott et al. (2004a,b) are also represented. (D) Li/Mg ratio (in lmol mmol 1) as a function of the growth temperature for mollusk species Mytilus edulis. Li (relative to Ca) between inorganic carbonates and solu- the interstitial position in calcite compared to substitution tion (referred here as KdLi), determined in abiogenic exper- of Li+ for Ca2+ in aragonite (Okumura and Kitano, 1986; iments, is slightly higher for aragonite compared to calcite Tomascak et al., 2016). Additionally, because of their sim- (Marriott et al., 2004a,b). However, the Li/Ca ratio of arag- ilar ionic radii, Li often substitutes for Mg in silicate miner- onitic skeletons is generally lower than biogenic calcite (see als (Tomascak et al., 2016). Hence, differences in Mg the compilation by Hathorne et al., 2013), a difference con- binding environment between calcite and aragonite could firmed by this study (Fig. 4B). also potentially explain the different Li isotope composition The reasons for the differential incorporation of Li and between these minerals. its isotopes between the various inorganic carbonate miner- als are not clear. Previous studies have proposed that Li+ 5.2. Influence of temperature substitutes for the Ca2+ site in aragonite, whereas in calcite, Li is incorporated interstitially (Marriott et al., 2004a,b). The three bivalve species (Pecten maximus, Mytilus edu- The larger isotope fractionation observed in inorganic arag- lis and Mercenaria mercenaria) grown at different tempera- onite compared to calcite could be due to the fact that there tures, keeping other parameters constant, show only weak is less fractionation of Li isotopes during incorporation in correlation (r2 = 0.3–0.5) between d7Li and temperature 326 M. Dellinger et al. / Geochimica et Cosmochimica Acta 236 (2018) 315–335 (Fig. 5A). The d7Li of field-collected specimens from vari- appears difficult to use mollusk Li/Mg to estimate water ous locations shows no relationship with temperature. Col- temperature unless targeting specific species (like Mytilus lectively, these data indicate that temperature has minor edulis). influences on d7Li within mollusk species but is not the first order control on d7Li variability across the species investi- 5.3. Intra-shell variability gated in this study. This conclusion is consistent with results from inorganic carbonate precipitation experiments A large intra-shell Li isotope variability (up to 25‰)is (see Fig. 5A) that show no temperature-dependence of car- observed for bi-mineralic mollusk shells. This is best exem- bonate d7Li (Marriott et al., 2004a). The same observation plified by Mytilus californianus, for which the inner arago- was made for experimentally-grown foraminifera Amphiste- nitic nacreous layer has a d7Li as low as 15‰, while the gina lessonnii (Vigier et al., 2015). We note that field- d7Li of the outer calcite prismatic layer is about 40‰. All collected coral samples also showed no correlation between Mytilus californianus samples plot on the same negative temperature and d7Li (Marriott et al., 2004a; Rollion-Bard regression between d7Li and the proportion of aragonite et al., 2009). measured by XRD (Fig. 6). Interestingly, no variation is In contrast to d7Li values, relationships between carbon- observed across the horizontal length of the outer layer ate Li/Mg, and to a lesser extent Li/Ca, and temperature (rectangles in Fig. 6). This result indicates that the Li iso- have been reported in other studies (Marriott et al., tope composition of the calcite part of the shell of Mytilus 2004a; Bryan and Marchitto 2008; Case et al., 2010; californianus is relatively homogenous and independent of Hathorne et al., 2013; Montagna et al., 2014; Fowell shell growth rate or age. In contrast, for the Chione shells, et al., 2016). For inorganic calcite (Marriott et al., 2004a) dominantly composed of aragonite with a small proportion and brachiopods (Delaney et al., 1989), Li/Ca ratios exhibit of calcite (in general < 20%, one sample at 55%), the a negative relationship with temperature. For corals and observed intra-shell variability is much lower (less than foraminifera, very good correlations have been observed 3‰), although the samples with the highest proportion of between temperature and Li/Mg ratio, suggesting that the calcite have systematically highest d7Li for each species. latter might be a promising proxy for reconstructing past Intra-shell variability was also investigated on a calcitic ocean temperature. We observe that although some samples oyster (Crassostrea gigas) and aragonitic clam (Tridacna from this study plot close to the inorganic trend, most sam- maxima). The observed intra-shell variability of the arago- ples have higher Li/Ca than inorganic carbonate for a given nitic clam is small, less than 2‰ between the outer and temperature (not shown). Similar to the case for Li iso- inner layer. In contrast, relatively large d7Li variability topes, temperature does not seem to be the first-order con- (about 12‰; excluding the anomalous Mg/Ca and Sr/Ca trol on Li/Ca of mollusks across species, although it does samples) was observed for Crassostrea gigas in at least 3 influence Li/Ca within individual mollusk species. On the specimens. However, no significant differences were noticed other hand, the brachiopods from this study plot on the between the chalky and foliate layers, indicating that Li iso- same Li/Ca vs. temperature regression as the samples from tope variability in this oyster is not controlled by the chalky Delaney et al. (1989) confirming the temperature control of vs. foliate nature of the calcite shell. Finally, intra-shell Li/Ca for brachiopods (Fig. 5C). variability was also tested for a brachiopod shell (Terebrat- Considering the relationship between the Li/Mg ratio in ulina transversa), for which we observe a limited variability mollusks and water temperature, several observations can of 2.5‰ between anterior and posterior valves. However, be made. First, for the growth experiments, for which the we did not attempt to determine whether the secondary temperature has been monitored, we observe a strong cor- and primary layers of brachiopod shells have similar d7Li, relation between Li/Mg and T for the species Mytilus edulis as has been done for others isotope proxies (Auclair (r2 = 0.83; Fig. 5D) but no correlation for Pecten maximus et al., 2003; Cusack and Huerta, 2012; Penman et al., and Mercenaria mercenaria. This is the first time that a cor- 2013; Ullmann et al., 2017), and this question remains to relation between the Li/Mg in a marine bivalve and temper- be investigated. ature is reported. This suggests that the Li/Mg ratio in In summary, there is significant but not systematic intra- Mytilus edulis has potential for paleo-temperature recon- shell variability for some skeletons. The largest intra-shell struction in the ocean. However, more data testing the d7Li variability (>25‰) is controlled by mineralogical mix- influence of other parameters are necessary to definitely val- ing between calcite and aragonite, but up to 12‰ variability idate such a calibration. Secondly, the relationship between is also observed in some mineralogically pure species (e.g., Li/Mg and T for Mytilus edulis is different from the rela- the oyster C. gigas) while intra-shell variability of less than tionships defined by other organisms (e.g. Bryan and 2.5‰ is observed in other taxa (Chione, Tridacna, Marchitto 2008; Case et al., 2010; Montagna et al., 2014; Terebratulina). Fowell et al., 2016), indicating that the relationship between Li/Mg and temperature is taxon-dependent. Finally, if we 5.4. Influence of biological processes report also field-collected organisms on the Li/Mg temper- ature plot (not shown), we observe that although there is a 5.4.1. Evidence for vital effects global trend of decreasing Li/Mg with temperature, the cor- Here, we compare our biogenic samples to inorganic relation between these two parameters is highly scattered. carbonates. Precipitation experiments have shown that the Thus, contrary to corals, the relationship between Li/Mg carbonate phase is enriched in 6Li compared to the fluid and temperature is overall quite weak and therefore it from which it precipitates (Marriott et al., 2004a,b). M. Dellinger et al. / Geochimica et Cosmochimica Acta 236 (2018) 315–335 327 Fig. 6. Example of intra-shell Li isotope variability for the species Mytilus californianus. (A) Sampling locations shown by the red dots on left figure. (B) d7Li varies as a function of aragonite percentage in the shell. Following Planchon et al. (2013), we can define the deviation In order to remove variability arising from differences 7 7 from inorganic values as D Liphysio = d Licarbonate biogenic between the partition coefficients of inorganic calcite and 7 7 d Licarbonate inorganic with ‘‘d Licarbonate inorganic” being aragonite, we normalize the observed partition coefficient the d7Li value of the corresponding inorganic carbonate of Li between biogenic carbonate and seawater 7 Li precipitated from modern seawater (d Liseawater =31‰), [D = (Li/Ca)biogenic carb./(Li/Ca)seawater] to the partition as derived from the experiments by Marriott et al., coefficient between inorganic carbonates and seawater 7 Li (2004a,b). We use a D Licalcite-solution value of 3‰ for [Kd = (Li/Ca)inorganic carb./(Li/Ca)seawater]. We define this 7 7 Li Li Li the d Li of inorganic calcite and a D Liaragonite-solution value parameter as b =D /Kd to express the enrichment or of 12‰ for inorganic aragonite (Marriott et al., 2004b,a). depletion in Li (relative to Ca) in the biogenic carbonate 7 The D Liphysio values of mollusk shells range from 4to relative to inorganic carbonate, i.e., the enrichment or +14‰ (Fig. 7). This suggests a strong vital effect on the depletion of Li in shells due to physiological processes only. incorporation of Li isotopes in mollusk shells. The As discussed previously, inorganic experiments have shown 7 Li Li D Liphysio of brachiopods ranges between 0 and 3‰ (aver- that Kd (defined as ‘‘D ” in Marriott et al. (2004a,b) but age of 1.4‰, n = 8 measurements), suggesting a limited referred to here as ‘‘KdLi”) for calcite is a function of tem- influence of vital effects for this group of organisms. Inter- perature. Hence for each sample, the bLi value should be 7 Li estingly, the D Liphysio values are larger and more positive calculated with the Kd corresponding to the growing tem- for calcitic mollusk shells (i.e. they preferentially incorpo- perature of the shell. However, as discussed before, there is rate the heavy isotope 7Li) compared to aragonitic shells. a large uncertainty on the growth temperature of field- This result indicates that physiological processes favor the collected shells from this study. In addition, the relationship utilization of the light isotope for aragonitic mollusks and between KdLi and temperature for aragonite has yet to be the heavy isotope for calcitic mollusks. The influence of experimentally investigated. Therefore, we consider both vital effects on Li isotope composition have also been iden- (i) bLi values normalized to the KdLi determined at 25 °C, Li Li tified for benthic foraminifera by Vigier et al. (2015) who which we will refer to as ‘‘b 25°C” and (ii) bT calculated showed that the d7Li of cultured Amphistegina benthic for- with the KdLi value corresponding to the associated growth aminifera can be as low as 21‰ and as high as 38‰, temperature and applied to aragonite using the same rela- depending upon the DIC concentration of seawater. tionship to temperature as determined for calcite. Consider- Regarding the Li/Ca values, as observed by Hathorne ing the data from both this study and from the literature et al. (2013) and described in Section 5.2., biogenic calcite (on other biogenic carbonates), the calculated bLi values has higher average Li/Ca than biogenic aragonite, the are between 0.2 and 3 for aragonite skeletons and between opposite of what is observed for inorganic carbonates 2 and more than 10 for calcite skeletons (Fig. 7). Hence, cal- (Marriott et al., 2004a,b). This apparent conundrum may cite organisms are systematically enriched in Li relative to be explained by the influence of physiological processes that inorganic calcite, likely as a result of biologically- either favor Li incorporation in calcite relative to aragonite controlled processes. through the involvement of specific cellular processes, or if there is a strong influence of pH and/or calcification rate on 5.4.2. Taxonomic differences in d7Li and Li/Ca the inorganic equilibrium partition coefficients (as sug- Comparison of our results with published data reveals gested by Gabitov et al., 2011). This stresses the need for important differences in the d7Li and Li/Ca ratios between more experiments looking at the controls on the inorganic various species, genera and phyla. At the phylum level, the partition coefficients and specifically the role of pH and cal- largest differences in Li isotope composition are observed cification rates. within the group of calcite organisms for which each 328 M. Dellinger et al. / Geochimica et Cosmochimica Acta 236 (2018) 315–335 7 Li Li Fig. 7. D Liphysio values as a function of (A) b 25°C values (Li/Ca ratio normalized to Li/Ca of inorganic carbonate at 25 °C) and (B) bT values (Li/Ca ratio normalized to Li/Ca of inorganic carbonate at the corresponding growth temperature). The hand-drawn dotted circles correspond to each taxonomic group. (C) Also shown for comparison, the d7Li as a function of the Li/Ca (in lmol mol 1) for biogenic, inorganic and cultured experiment carbonates. The empty blue diamond symbols corresponds to coral growth experiments from Rollion-Bard et al. (2009). 7 Li phylum has a distinct pair of D Liphysio and b values Shells of mollusk species Mytilus edulis and Pecten max- 7 (Fig. 7). The range of D Liphysio of modern field-collected imus, grown at various temperature, all other parameters calcitic mollusks ( 2 to +13‰) is significantly larger com- constant, exhibit systematic Li isotope differences of 4– pared to modern planktic foraminifera ( 2to+4‰), bra- 5‰ for seawater temperatures ranging from 10 to 20 °C chiopods ( 3to0‰), and benthic foraminifera ( 7to (Fig. 5B). Furthermore, we observe that the two species 7 7 1‰). Aragonitic calcifiers, including corals (D Liphysio = of Chlamys have higher d Li compared to species of other 0to+4‰), and aragonitic bivalves ( 4to+1‰), have a mollusk genera grown at similar temperature. Up to 7‰ 7 smaller range of D Liphysio. We also observe that for a given variability between species of equivalent mineralogy is 7 D Liphysio value, sea urchins, brachiopods, and mollusks observed at a given temperature (Fig. 5B). have the highest bLi, followed by planktic and benthic for- aminifera, followed by aragonite calcifiers. This shows that 5.4.3. Origin of the vital effect for calcite mollusks 7 Li physiological processes significantly influence the propor- When D Liphysio values are compared to b25°C for mol- tion of Li incorporated into the shell of various types of lusks (Fig. 7), we observe a negative correlation between 7 Li calcifiers. D Liphysiol and b25°C for Mytilus edulis specimens grown In addition, we also investigated the importance of inter- at various temperature (r2 = 0.85). Interestingly, this rela- genera and inter-species variability by comparing the d7Li tionship is also observed for all calcitic mollusks (r2 = of shells from various species grown in similar thermal envi- 0.63) from this study. For the temperature-normalized inor- Li ronments. Our dataset reveals large inter-species differences ganic Li/Ca ratios (bT ), the correlation is less good but still in Li isotope composition of mollusk shells (for a given holds for calcite mollusks (r2 = 0.45) but not for Mytilus mineralogy), in contrast to foraminifera and brachiopods. edulis specimens (r2 = 0.21). For aragonite mollusks, we M. Dellinger et al. / Geochimica et Cosmochimica Acta 236 (2018) 315–335 329 7 also observe a negative correlation between D Liphysio and vacuoles and transports Na (and Li) inside the vacuoles Li 2 Li b25°C (r = 0.47) but no correlation is observed with bT . (Erez, 2003; Bentov et al., 2009). These vacuoles are then In this section, we discuss several hypotheses for explaining transported into the calcification site of foraminifera where this correlation and relate these observations to potential the organic matrix is present (Erez, 2003; Bentov et al., mechanisms of Li isotope fractionation during 2009). At low DIC concentration, the activity of the Na/ biomineralization. proton exchanger would be more intense and more Li Most skeletal organisms calcify in a reservoir isolated would be transported into the calcification site (Vigier from external seawater. They favor calcification by either et al., 2015). Assuming this process fractionates Li isotopes (i) increasing saturation state (by increasing their internal (for example by kinetic or enzymatic isotope fractionation), pH, DIC and/or internal Ca concentration), (ii) reducing the result would be an increase in the Li/Ca ratio and a their internal fluid Mg/Ca ratio (in particular for modern decrease in the d7Li of the calcification reservoir relative 7 calcite organisms), or (iii) using a complex organic template to seawater (i.e. negative D Liphysio values). This is what to control orientation and distribution of crystals during we observe for aragonite mollusks as most of the samples 7 nucleation (Ries, 2010; Immenhauser et al., 2016). These have negative D Liphysio values. Moreover, benthic forami- pathways are not mutually exclusive. Mollusks have an nifera and some calcite mollusks and brachiopods also have 7 extracellular-type process of biomineralization (Weiner slightly negative D Liphysio values (Fig. 7). Hence, this pro- and Dove, 2003; Weiner and Addadi, 2011; Immenhauser cess could potentially explain their variability in Li isotope et al., 2016). Precipitation of the inner layer is inferred to and Li/Ca ratios. However, the great majority of calcitic 7 take place somewhere in the extrapallial space (which con- mollusks and foraminifera have positive D Liphysio values, tains extrapallial fluid or EPF), located between the inner which implies the need for a different explanation. shell surface and the outer mantle epithelium. For the outer Another possibility is that Li is actively removed from layer, the EPF is located between the prismatic layer and the calcification site, with an isotope fractionation resulting the mantle epithelium. The EPF contains inorganic ions from preferential removal of 6Li (Vigier et al., 2015). This 7 7 and various organic molecules that interact to form the process would lead to high d Li (high D Liphysio) and low biominerals. Precipitation is controlled by specialized cells Li/Ca (low bLi) of carbonates. Removal of Mg from the cal- of the outer mantle epithelium that release complex organic cification reservoir through Mg specific channels has previ- macromolecules that are used as organic templates for con- ously been suggested for foraminifera (Zeebe and Sanyal, trolling the morphology of precipitated crystals. Usually, a 2002; Bentov and Erez, 2006) to explain their low Mg/Ca precursor amorphous carbonate phase (ACC) is first pre- value relative to seawater. Although the relevance of this cipitated and then transformed to calcite or aragonite process is debated (Wombacher et al., 2011; Pogge von (Baronnet et al., 2008; Weiner and Addadi, 2011). It has Strandmann et al., 2014), high Mg content in fluids inhibits been suggested that precursor amorphous phases are also calcite precipitation (e.g. Berner, 1975), so removal of Mg is used by echinoderms (Beniash et al., 1997). one possible strategy to favor calcite precipitation (Zeebe 7 Li The negative relationship between D Liphysio and b for and Sanyal, 2002; Bentov and Erez, 2006; Ries, 2010; calcite mollusks cannot be produced by carbonate precipi- Wang et al., 2013). As Li is often associated with Mg, we tation alone (e.g., by varying proportions of Li incorpo- suggest that similarly to Mg, Li could be transported out rated into carbonates) because (i) the partitioning of Li of the calcification site by specific channels and/or pumps between the carbonates and the fluid strongly favors the (Bentov and Erez, 2006). This hypothesis is supported by fluid (KdLi 1), hence a very small amount of Li is incor- the negative correlation between d7Li and Mg/Ca for cal- porated into carbonate minerals and therefore carbonate citic mollusks (Fig. 8B), indicating that, indeed, mollusks precipitation does not change the d7Li of the fluid and (ii) having the highest d7Li also have the lowest Mg/Ca ratio. carbonates would have d7Li lower than seawater, not The process of Li removal from the calcification site can higher as observed for most of the mollusk samples, be modeled in a simple way as either (i) an open system at because 6Li is preferentially incorporated into inorganic steady-state (input fluxes are balanced by output fluxes) or carbonates. Furthermore, it has been argued that in (ii) a closed or semi-enclosed system, corresponding to non- bivalves, passive ion transport through ion channels to steady-state conditions with output fluxes being higher than the calcification site results in similar composition in the input fluxes (requiring periodic ‘batch’ replenishment of the extrapallial space as in the seawater (Immenhauser et al., calcifying medium). For the latter, the Li/Ca and Li isotope 2016). Hence, the most likely explanation for the observed composition of the fluid inside the calcification reservoir trends is that the d7Li and Li concentration of the calcifica- evolves following a Rayleigh distillation as a function of tion fluid is modified prior to carbonate precipitation by the proportion of Ca and Li removed. physiological processes leading to addition or removal of The corresponding equation for the open system at Li in the internal calcification medium and that this process steady-state is: also fractionates Li isotopes. Li D ¼ D 1 c ð1Þ This type of mechanism was recently proposed by Vigier physio pump fluid fluid et al. (2015) for explaining the range of Li/Ca and d7Li of and for the closed system: cultured foraminifera of the genus Amphistegina at low Li D ¼ D ln c ð2Þ and high DIC concentrations. In this conceptual model, ele- physio pump fluid fluid 7 vation of pH within the seawater vacuoles is achieved by a with D Lipump-fluid being the fractionation factor 7 Na/proton exchanger that removes protons from the (D Lipump-fluid = 1000 ln(apump-fluid)) between the Li 330 M. Dellinger et al. / Geochimica et Cosmochimica Acta 236 (2018) 315–335 7 Li Fig. 8. (A) D Liphysio values as a function of b25°C values (Li/Ca ratio normalized to Li/Ca of inorganic carbonate at 25 °C) for mollusks. Calcite mollusks define a negative trend in this space, and this trend can be fitted with either a steady-state open system fractionation (black 2 Li line) or a Rayleigh fractionation model (grey line), both with an r = 0.64 (excluding the sample having the highest b25°C value). The numbers along the model curves correspond to the proportion of Li remaining in the calcification reservoir before precipitation of the shell. (B) 7 7 Negative relationship between D Liphysio and Mg/Ca in calcitic mollusks. Shells having the highest D Liphysio values also have the lowest Mg/ Ca ratio. cLi bLi removed and the Li within the calcification site, and fluid at a 25 C value of 7 ± 1 for the open system and at being the proportion of Li remaining in the fluid in the cal- 7.5 ± 1.0 for the closed system (Fig. 8A). Hence, the initial cification reservoir after Li extrusion, calculated as the ratio Li/Ca ratio of the mollusks, in the absence of Li extrusion, between the concentration of Li remaining in the reservoir is about 7 times higher than the Li/Ca ratio of inorganic after extrusion divided by the initial concentration of Li bLi calcite. Investigation of the reasons for such high 25 C before extrusion. Assuming that there is no Ca removal values for mollusks is beyond the scope of this study, cLi by this process, then we can express fluid as: but preferential incorporation of Ca in carbonates ðLi=CaÞ ðLi=CaÞ bLi (e.g. Elderfield et al., 1996) and/or specific Ca input or cLi ¼ fluid ¼ carb ¼ ð3Þ removal from the calcification site through channel pump fluid ðLi=CaÞ ðLi=CaÞ bLi 0 carb 0 0 or exchange enzyme transporter (Carre´ et al., 2006) could Li ” b With the subscript ‘‘fluid corresponding to the fluid in potentially explain 25 C higher than 1. Regarding the ” 7 the calcification reservoir, ‘‘0 to initial fluid in the calcifica- fractionation factor, we obtain a D Lipump-fluid value of ” tion reservoir before Li removal, ‘‘carb to carbonate and 15‰ (apump-fluid = 0.985) for the open system and 9‰ ‘‘carb-0” to the composition of the carbonate formed in (apump-fluid = 0.991) for the closed system model. We the absence of Li extrusion (i.e. when (Li/Ca)res =(Li/Ca)0). hypothesize that this fractionation corresponds to a kinetic Hence, for the open system at steady-state, Eqs. (1) isotope fractionation where the 6Li is preferentially and (3) can be combined to give: extruded from the calcification site by diffusion or active ! transport through membranes. For diffusion in water at bLi D ¼ D 1 ð4Þ low temperature, the Li isotope fractionation is relatively physio pump fluid bLi 0 small (about 0.997; Richter et al., 2006) whereas the frac- tionation factor through a membrane at 22 °C was deter- and for the closed system, Eqs. (2) and (3) can be combined mined to be 0.989 by Fritz (1992). The latter value is to give: ! close to the fractionation factor corresponding to closed bLi system (Rayleigh) fractionation inferred in our model. As D ¼ D ln ð5Þ physio pump fluid bLi represented in Fig. 8, we calculate that up to 80% of the 0 Li initially present at the calcification site is removed before 7 Li The D Liphysio and b25°C data for calcite mollusks can be precipitation of calcite for mollusks. We note that this 7 fitted by Eqs. (4) and (5) assuming that (i) all the mollusks mechanism could also explain the high D Liphysio and low Li Li b b25°C values of Amphistegina benthic foraminifera grown have a relatively similar initial 0 at the calcification site and (ii) there is a unique associated isotope fractionation at high DIC concentration from Vigier et al. (2015). Indeed, 7 we can speculate that in foraminifera both addition of Li factor (D Lipump-fluid) for all mollusks. The best fits (both + + giving r2 = 0.64) corresponding to both the closed and open (through the Na /H transporter) and removal of Li system isotope fractionation for calcite mollusks are repre- (coincident with Mg removal) exist. At high DIC + + sented on Fig. 8. The trends intercept the grey line corre- concentration, the activity of the Na /H transporter 7 (leading to low D7Li ) is lowered, so removal of Li sponding to the absence of vital effects (D Liphysio =0) physio M. Dellinger et al. / Geochimica et Cosmochimica Acta 236 (2018) 315–335 331 7 becomes dominant with resulting D Liphysio value being therefore it is likely that the Li/Ca and Li isotope variabil- higher. Ultimately, the Li isotope composition of biogenic ity of bulk carbonates can be controlled to some extent by carbonates is probably controlled by the balance between the relative contributions of different taxonomic groups processes removing and adding dissolved Li to the calcifica- (Fig. 7C). This effect may be most pronounced at times tion medium. of major change in ecosystem structure, for example, dur- ing extinction events. There is also evidence that the over- 6. IMPLICATIONS FOR RECONSTRUCTING PAST all pattern of biomineralization has significantly changed SEAWATER COMPOSITION during the Phanerozoic Eon with an increase in the pro- portion of skeletal to non-skeletal carbonates over time, One goal of this study is to test whether and how differ- together with large changes in the type of skeletal carbon- ent biocalcifying organisms may be used to reconstruct the ates (Wilkinson, 1979; Milliman, 1993; Kiessling et al., past d7Li of seawater. The secondary layers of brachiopods 2003). Additionally, any global change of the main car- analyzed here have homogeneous d7Li, with little apparent bonate mineralogy over time (e.g. calcite and aragonite influence from vital effects, temperature, and inter-species seas during the Phanerozoic; Stanley and Hardie, 1999) differences. In addition, as previously observed by would likely have influenced bulk carbonate d7Li because Delaney et al. (1989), the Li/Ca of brachiopods may be a calcite has higher d7Li than aragonite for both inorganic reliable proxy for tracing past ocean temperature if Li/Ca and biogenic carbonates. Hence, any long-term recon- of the ocean is known or, conversely, determining past struction of past d7Li of seawater using bulk carbonates Li/Ca of the ocean if the calcification temperature is known should take into account the influence of secular changes through other proxies. Collectively, these observations sug- in mineralogy and taxonomic origin of the carbonate that gest that brachiopods are promising candidates as archives is preserved. of past Li isotope composition and potentially also temper- ature of seawater. However, as we only analyzed 5 different 7. CONCLUSIONS specimens from 5 different species, we suggest caution in interpreting these results and urge more analyses of In this study, we measured for the first time the Li iso- present-day brachiopods (including considering intra-shell tope composition of modern mollusks, brachiopods, and variability) to confirm these conclusions. echinoderms in order to test whether these samples are Unlike brachiopods, the range of d7Li and Li/Ca val- viable targets for determining the past d7Li of the ocean ues of modern calcitic mollusks is large and significantly and to provide further insight into the geochemistry of influenced by physiological processes, including inter- biomineralization. We investigated both modern field- species and inter-specimen differences. Therefore, fossil collected shells from various environments and shells exper- shells of calcitic mollusks are probably not good targets imentally grown at varying temperatures. We considered for inferring the past Li isotope composition or tempera- the influence of mineralogy, temperature, taxonomy, and ture of the oceans, unless the reconstructions are limited vital effects on the Li isotope and Li/Ca composition of bio- to single species. As mollusks can constitute a significant genic carbonates. The major conclusions are: component of bulk carbonates (Wilkinson, 1979), it is important to take them into account to understand the (1) Brachiopods are promising targets for tracing past Li Li isotope composition of bulk carbonates (Pogge von isotope composition of the ocean because they have Strandmann et al., 2013; Lechler et al., 2015), at least similar d7Li compared to inorganic calcite precipi- when these are fossiliferous. The d7Li and Li/Ca values tated from seawater (i.e. not significantly affected of aragonitic mollusks are similar to inorganic aragonite by vital effects) and exist since the Cambrian (i.e. composition. Therefore, they are likely to be better available for study in deep time). archives for marine d7Li that calcitic mollusks. However, (2) There is a strong mineralogical control on the d7Li of aragonite mollusks are also more prone to diagenetic biogenic carbonates. Calcite shells have d7Li between transformation and, at this stage, it is not known how dia- +25 and +40‰ while aragonitic organisms have d7Li genesis affects primary d7Li signatures. The small subset of systematically lower than 25‰. High-Mg calcite echinoderm skeletons analyzed here point to a relatively echinoderm shells have intermediate d7Li of +24‰. narrow range of values, but more work would need to (3) Only a small influence of temperature is observed in be done to establish whether these observations are sys- mollusks from growth experiments, and no relation tematic and the extent to which the signal in high-Mg cal- between temperature and d7Li is observed for mod- cite is preserved during diagenesis. ern field-collected mollusks. The results of this study have important implications (4) There is strong physiological control on the d7Li of for the interpretation of Li isotope and Li/Ca data from mollusks. When normalized to inorganic fractionation d7 7 7 7 bulk Phanerozoic carbonates. Over time, the Li of bulk (D Liphysio = d Licarbonate biogenic d Licarbonate inorganic), carbonates is potentially influenced by several parameters calcite mollusks display positive and widely ranging 7 including seawater Li isotope composition, carbonate min- D Liphysio values, between 1 and +14‰, which indi- eralogy, diagenesis, the proportion of skeletal to non- cates the influence of physiological effects. Aragonite skeletal carbonates, taxonomy, and temperature. We have mollusks exhibit less variability than calcite mollusks, d7 7 found that different genera have distinct Li (ranging by with D Liphysio ranging from +1 to 4‰, with most several tens of per mil) and distinct Li/Ca ratio, and of the values being negative. 332 M. Dellinger et al. / Geochimica et Cosmochimica Acta 236 (2018) 315–335 (5) Different species collected from similar temperatures sea urchin larval spicule growth. Proc. Roy. Soc. London B: vary by up to 7‰ in d7Li, indicating substantial Biol. 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This is best explained by a simple fractionation Bouchez J., von Blanckenburg F. and Schuessler J. A. (2013) model driven by Li removal from the calcification site Modeling novel stable isotope ratios in the weathering zone. and an associated single isotope fractionation. We Am. J. Sci. 313, 267–308. https://doi.org/10.2475/04.2013.01. propose that this process is related to combined Mg Brand U., Logan A., Hiller N. and Richardson J. (2003) and Li removal from the calcification site of calcite Geochemistry of modern brachiopods: applications and impli- cations for oceanography and paleoceanography. Chem. Geol. mollusk in order to lower Mg/Ca of the calcifying 198(3–4), 305–334. medium in support of calcite precipitation. Bryan S. P. and Marchitto T. M. (2008) Mg/Ca-temperature proxy in benthic foraminifera: new calibrations from the Florida ACKNOWLEDGEMENTS Straits and a hypothesis regarding Mg/Li. Paleoceanography 23. https://doi.org/10.1029/2007PA001553, n/a-n/a. This work was primarily supported by the American Chemical Carpenter S. J. and Lohmann K. C. (1992) Sr/Mg ratios of modern Society Petroleum Research Fund (award 53418-DNI2 to AJW). marine calcite: empirical indicators of ocean chemistry and We thank the Natural History Museum of Los Angeles County precipitation rate. Geochim. Cosmochim. Acta 56, 1837–1849. for providing bivalve samples. We thank Jonathan Erez and an https://doi.org/10.1016/0016-7037(92)90314-9. anonymous reviewer for their constructive comments on the manu- Carre´ M., Bentaleb I., Bruguier O., Ordinola E., Barrett N. T. and script. MD acknowledges financial support from Durham Univer- Fontugne M. (2006) Calcification rate influence on trace sity and a Marie Curie COFUND International Junior research element concentrations in aragonitic bivalve shells: evidences Fellowship held at Durham University. RAE and JBR acknowl- and mechanisms. Geochim. Cosmochim. 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