A simple biomineralization model to explain Li, Mg, and Sr incorporation into aragonitic foraminifera and corals

doi:10.1016/j.epsl.2017.10.022

Earth and Planetary Science Letters

Volume 481, 1 January 2018, Pages 20-29

https://doi.org/10.1016/j.epsl.2017.10.022 Get rights and content

Highlights

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Li/Mg is well correlated to temperature in foraminiferal and coral aragonite.
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A conceptual model is proposed to explain why Li/Mg is immune to ‘vital effects’.
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Li/Mg is hypothetically unaffected by Ca²⁺ pumping and Rayleigh fractionation.
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Precipitation rate may play a role via surface entrapment.
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Sr/Ca is consistent with this model.

Abstract

In contrast to Li/Ca and Mg/Ca, Li/Mg is strongly anticorrelated with temperature in aragonites precipitated by the benthic foraminifer Hoeglundina elegans and a wide range of scleractinian coral taxa. We propose a simple conceptual model of biomineralization that explains this pattern and is consistent with available abiotic aragonite partition coefficients. Under this model the organism actively modifies seawater within its calcification pool by raising its [Ca²⁺], using a pump that strongly discriminates against both Li⁺ and Mg²⁺. Rayleigh fractionation during calcification effectively reverses this process, removing Ca²⁺ while leaving most Li⁺ and Mg²⁺ behind in the calcifying fluid. The net effect of these two processes is that Li/Mg in the calcifying fluid remains very close to the seawater value, and temperature-dependent abiotic partition coefficients are expressed in the biogenic aragonite Li/Mg ratio. We further show that coral Sr/Ca is consistent with this model if the Ca²⁺ pump barely discriminates against Sr²⁺. In H. elegans the covariation of Sr/Ca and Mg/Ca requires either that the pump more strongly discriminates against Sr²⁺, or that cation incorporation is affected by aragonite precipitation rate via the mechanism of surface entrapment. In either case Li/Mg is minimally affected by such ‘vital effects’ which plague other elemental ratio paleotemperature proxies.

Introduction

Dissolved Li, Mg, Sr, and Ca all behave nearly conservatively in seawater, meaning that their ratios are approximately constant throughout the oceans. The oceanic residence times of these four elements are relatively long, on the order of 1 to 10 Ma, so that oceanic metal/Ca ratios are also relatively constant through time during the late Quaternary. Hence any changes in the metal/Ca of biogenic CaCO₃ may potentially be attributed to variations in the environmental parameter(s) that affect metal partitioning into the mineral, such as temperature. Mg/Ca has been widely applied as a paleotemperature proxy in calcitic foraminifera (Nürnberg, 1995), while Sr/Ca has been similarly used in aragonitic corals (Beck et al., 1992). In both cases ancillary environmental parameters such as carbonate saturation state, and/or physiological parameters such as growth rate, often appear to overprint the temperature signal. For the elemental ratios that are not widely used as paleotemperature proxies, such as Sr/Ca in foraminifera and Mg/Ca in corals, such ancillary effects can obscure any temperature dependence. Improved characterization of the various influences on metal partitioning is therefore a crucial goal of paleoceanographic proxy development, with an eye toward greater understanding of the biomineralization process.

Following the pioneering work of Delaney et al. (1985), Li/Ca has received renewed attention in both foraminifera and corals, but has not yet seen widespread application as a paleoceanographic proxy. Several studies have demonstrated a negative correlation between biogenic Li/Ca and temperature, but significant ancillary influences such as calcification rate have also been suggested (e.g. Hall and Chan, 2004, Hathorne et al., 2013; Marriott et al., 2004a, Marriott et al., 2004b). Benthic foraminiferal Li/Ca from a holothermal depth transect was found to be positively correlated with seawater saturation state with respect to calcite (Lear and Rosenthal, 2006), leading to the suggestion that Mg/Ca and Li/Ca can be used in linear combination to solve for both paleotemperature and saturation state (Lear et al., 2010). Bryan and Marchitto (2008) showed that Mg/Li in several taxa of benthic foraminifera is better correlated to temperature than either Mg/Ca or Li/Ca alone, especially for the aragonitic Hoeglundina elegans ( $r^{2} = 0.49$ for Mg/Ca, 0.90 for Mg/Li). They proposed that both Mg/Ca and Li/Ca reflect, in part, modification of the internal calcification pool, and that the ratio Mg/Li effectively corrects for physiological and/or saturation state influences, thereby isolating the temperature effect. A similar improvement using Mg/Li (or Li/Mg) has since been demonstrated in a diverse range of aragonitic corals, including deep sea taxa (Case et al., 2010, Montagna et al., 2014, Raddatz et al., 2013).

Here we further explore the relationship between Li/Ca and Mg/Ca in biogenic aragonites, and use it to construct a simple model of biomineralization. We then discuss the implications of that model for the coral Sr/Ca paleotemperature proxy.

Section snippets

Materials and methods

We present 11 new metal/Ca measurements in H. elegans from nine Holocene core tops (Table 1). Each sample contained ∼5–10 individuals >250 μm, which were crushed and reductively and oxidatively cleaned following the methods of Boyle and Rosenthal (1996). Samples were analyzed for a suite of trace and minor elemental ratios by high-resolution sector field ICP-MS, as described by Marchitto (2006). Long-term 1σ precision is 0.9% for Li/Ca, 0.5% for Mg/Ca, and 0.6% for Sr/Ca. Concentrations of

Li/Ca, Mg/Ca, and Li/Mg versus temperature

With the addition of new measurements from the deep sea, the weak negative correlation between Li/Ca and temperature reported for H. elegans (Bryan and Marchitto, 2008, Hall and Chan, 2004) becomes even weaker ( $r^{2} = 0.01$ , Fig. 1a). Aragonitic coral Li/Ca exhibits a considerably stronger negative correlation to temperature ( $r^{2} = 0.52$ across multiple taxa, Fig. 1a), as has been noted previously (Case et al., 2010, Montagna et al., 2014). For Mg/Ca in H. elegans the correlation to temperature

Conclusions

We present a simple conceptual model that explains the remarkably similar behavior of Li/Mg between the aragonitic foraminifer H. elegans and various aragonitic coral taxa. We suggest that Li/Mg reflects the ratio between the abiotic partition coefficients $K_{Li / Ca}$ and $K_{Mg / Ca}$ because neither Ca²⁺ pumping nor Rayleigh fractionation significantly alters the Li/Mg ratio of the calcifying fluid. This model is consistent with coral Sr/Ca if the Ca²⁺ pump barely discriminates against Sr²⁺. In contrast

Acknowledgments

We are grateful to Matthias López Correa and Andres Rüggeberg for providing access to the cold-water coral samples listed in Table S2, as well as to Riccardo Rodolfo-Metalpa for the Cladocora caespitosa samples. We thank Derek Weller for laboratory assistance. Ed Hathorne and an anonymous reviewer provided comments that improved this paper. This work was supported in part by US NSF grants OCE-0425522 and OCE-0648215 to Marchitto. McCulloch is supported by an ARC Laureate Fellowship (LF120100049

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Citation Excerpt :
To further evaluate the growth rate effects in cation incorporation, it is instructive to compare the deep-sea coral data to inorganic experiments as well as other marine calcifying organisms, especially those that make aragonite. Recently it was discovered that the aragonitic benthic foraminifera Hoeglundina elegans shares the same Li/Mg–temperature relation with different coral species (Marchitto et al., 2018; Stewart et al., 2020). However, the Li/Ca, Mg/Ca and Sr/Ca ratios of H.elegans are lower than those of corals and closer to those of other calcitic foraminifera (Rosenthal et al., 2006; Bryan and Marchitto, 2008; Marchitto et al., 2018).
Deep-sea corals are a useful archive of thermocline, intermediate, and deep waters in past oceans. However, application of traditional oceanographic tracers to deep-sea corals remains a challenge due to our insufficient understanding of their “vital effects”. Deep-sea corals are ideal test organisms to study the mechanism underlying vital effects generally, due to the large tracer gradients in individual corals living under relatively constant environmental conditions. Lessons learned from these corals might apply to other scleractinia and to marine calcifiers more generally. Here we present stable isotope, minor and trace metal (Me/Ca ratios) data in a suite of modern Desmophyllum dianthus specimens, collected over multiple spatial scales in individual corals (bulk, micromill, SIMS, NanoSIMS), with multi-proxy analyses made on the same material whenever possible. Spatially coherent Me/Ca correlations are observed in the fibrous aragonite of individual corals, including positive correlations between Mg/Ca, Li/Ca and B/Ca, as well as negative correlations between Mg/Ca and Sr/Ca, consistent with previous studies. We also for the first time document strong correlations between the isotopic (δ¹⁸O and δ¹³C) and elemental compositions of the skeletons, most notably a negative correlation between δ¹⁸O and Mg/Ca. The centers of calcification (COCs) in the coral skeletons show distinct tracer correlations from the aragonite fibers that possibly reflect a more complicated formation mechanism. We interpret the spatially coherent tracer correlations in deep-sea corals with a numerical model of coral calcification previously developed for stable isotopes that considers the role of the enzyme carbonic anhydrase in the calcification processs. With the carbonate chemistry in the model constrained by the stable isotope data, we are able to explain the observed Me/Ca correlations as well as their range of variability, as a result of internal pH elevation in the extracellular calcifying fluid (ECF) of the corals with limited Ca-pumping through the calicoblastic membrane. In particular, the positive Mg/Ca–B/Ca correlation in the fibrous aragonite suggests a borate (B(OH)₄^–) substitution for carbonate ion (CO₃^2–) incorporation mechanism in biogenic aragonite. We also suggest the growth rate dependence of the incorporation of minor and trace elements based conceptually on an ion-by-ion growth model may help explain the absolute Me/Ca values in biogenic aragonites. Finally, we generally find more limited tracer variability in corals from undersaturated seawater compared to their counterparts from supersaturated conditions, suggesting a limit to their internal pH elevation in response to this environmental stress. Understanding the biomineralization mechanisms underlying the vital effects is important for better use of these tracers for paleoceanographic applications, and may shed light on the response of marine calcification to future ocean acidification.

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A simple biomineralization model to explain Li, Mg, and Sr incorporation into aragonitic foraminifera and corals

Highlights

Abstract

Introduction

Section snippets

Materials and methods

Li/Ca, Mg/Ca, and Li/Mg versus temperature

Conclusions

Acknowledgments

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