Boron Proxies: From Calcification Site pH to Cenozoic pCO2

 1811-5209/25/0021-0098$2.50 DOI: 10.2138/gselements.21.2.98

Keywords: pH proxy; boron isotopes; foraminifera; corals; pCO2

INTRODUCTION

The elemental composition of the atmosphere has evolved through geological time, with its carbon dioxide (CO2) content over the Cenozoic of particular interest for climate studies, as CO2 is a greenhouse (or heat-trapping) gas. Carbon dioxide is the greenhouse gas with the highest current atmospheric concentration (after water vapour), and anthropogenic emissions are causing the atmospheric partial pressure of CO2 (pCO2) to rise to ever higher levels. These anthropogenic emissions of CO2 lead to climate changes like global warming and ocean acidification. To take stock of this anthropogenic increase in atmospheric CO2, it is necessary to understand the natural phenomena that control carbon partitioning between reservoirs other than the atmosphere and thus regulate atmospheric pCO2 on both geological and human timescales. Seawater pH (acidity) is closely related to atmospheric pCO2 and is one of the important and measurable parameters of the carbonate system in the ocean. Therefore, the oceanic paleo-pH value is scientifically desirable, both for its own value, but also to indirectly understand the movement of carbon between oceans and atmosphere. The pCO2 of the past atmosphere can be measured directly in ice cores, but its time record is limited to around the last one million years. Thus, to reconstruct pCO2 over longer geological times, it is necessary to use indirect in aqueous solution, boric acid and borate ion. The combination of acid–base speciation and the boron isotopic fractionation between the two dissolved species of boron leads to a variation in the isotopic composition of each species as the pH of the solution changes. Furthermore, if only one aqueous species is incorporated, or selectively incorporated, both the isotopic composition of marine calcium carbonate is currently and by far the most commonly applied proxy for oceanic pH and, hence, pCO2 in the past.

Boron is present in two forms in aqueous solution, boric acid and borate ion. The combination of acid–base speciation and the boron isotopic fractionation between the two dissolved species of boron leads to a variation in the isotopic composition of each species as the pH of the solution changes. Furthermore, if only one aqueous species is incorporated, or selectively incorporated, both the isotopic composition and boron concentration of the CaCO3 mineral will depend on pH (Hemming and Hanson 1992). Therefore, it is possible to access past oceanic pH via the analysis of these carbonate minerals using either their boron isotope ratios or boron concentrations. In combination with knowledge of a second parameter of the carbonate system (commonly dissolved inorganic carbon, alkalinity or CaCO3 saturation state), it is possible to then calculate the dissolved CO2 concentration, and thereby, the CO2 concentration of the overlying atmosphere. However, numerous studies have shown that the compositions of biogenic carbonates do not simply reflect the pH of the surrounding seawater, requiring empirical calibrations of the relationship between the boron isotopic composition of shells/skeletons and the boron chemistry of the seawater from which they grew. Such biological processes of calcification are commonly given the catch-all term “vital effects.” Indeed, during biomineralisation—the physiological process that enables living organisms to develop a mineral structure—a common strategy of carbonate organisms is to increase the pH of the local solution to enhance the precipitation potential. As well as being directly observed with careful studies of living organisms, this was confirmed with the help of in situ boron isotope measurements, such as by laser ablation and ion microprobe analysis, which have provided a wealth of information on how organisms regulate their calcification pH. Among other things, thanks to their high spatial resolution (on the order of µm), these in situ techniques have shown that calcification pH can differ during the deposition of the different microstructures present in carbonate shells or skeletons. Despite the apparent complications associated with these fine-scale details, the techniques enable calcification site pH to be reconstructed and, given sufficient understanding of how this relates to their environment, ocean pH as well. Here, we review the principle of using boron isotopes as a pH proxy. We then discuss the link between calcification pH and seawater pH and present a compilation of pCO2 reconstructions for the last 70 million years from the δ11B–pH proxy.

BORON ISOTOPIC COMPOSITION OF CaCO3 AS A pH PROXY

Boron is a minor component of seawater on Earth, with a concentration of ~4 µg/g in the oceans. The fluxes of boron to and from the oceans are relatively small, and thus the residence time of boron is very long, on the order of millions of years. This means that neither the concentration of boron nor the ratio of its two stable isotopes (10B and 11B) change very quickly even if the fluxes of the source or sinks change, although some changes are thought to have taken place on timescales of 10s of millions of years. One natural sink of boron is its incorporation into marine biocarbonates (including shells), that can then be deposited and buried on the seafloor, and are subsequently uplifted onto continents, or subducted into the mantle. Analysis of recovered carbonates from rock sections or (pre-subduction) sediment cores can then reveal the history of boron and its isotopes through geological time. Carbon dioxide in contact with water undergoes the following set of equilibrium reactions, which are tightly related to (and somewhat influence) the pH of the fluid:

CO2 + H2O ⇋ HCO3– + H+ ⇋ CO3 2– + 2H+

Boron in aqueous solution acts similarly to the dissolved carbonate species; it is this similarity that renders boron a useful tracer of carbon in fluid systems. Dissolved boron has two chemical species: one with a trigonal (flattrian gular) form, boric acid B(OH)3; and the other with a tetra hedral (3-dimensional pyramidal) charged form, borate ion B(OH)4−. These two species arise from an acid–base reaction (Fig. 1), whereby dissolved boron is mainly in the form of B(OH)3 at low pH, and as B(OH)4– at high pH:

B(OH)3 + H2O ⇋ B(OH)4– + H+

The heavy isotope of boron, 11B, preferentially partitions into B(OH)3, whereas the light isotope, 10B, preferentially partitions into B(OH)4 −. This results in a difference in isotopic composition between the two dissolved species, with a fractionation factor of 27.2 ± 0.6‰ (Klochko et al. 2006; Fig. 1). If the boron isotopic composition of the bulk solution is fixed, or nearly so, then the boron isotopic composition of either species closely relates to the pH of the solution (although B(OH)4– is the predominant form incorporated into carbonates).

Starting from the pioneering works of Vengosh et al. (1991) and Hemming and Hanson (1992), many studies have conducted laboratory experiments precipitating inorganic carbonates under controlled conditions to better under stand the mechanisms and factors controlling boron incorporation (e.g., Noireaux et al. 2015; Uchikawa et al. 2023 and references therein). All of these studies show a strong dependence of carbonate δ11B on pH. The key reason is that boron substitutes for CO3 2– in the carbonate lattice, possibly as BO2(OH)2− (Hemming and Hanson 1992) predominantly derived from the charged borate ion:

CaCO3 + B(OH)4– ⇋ Ca(HBO3) + HCO3– + H2O

In detail, nuclear magnetic resonance (NMR), X-ray spectroscopy, and electronic and energy-loss spectroscopy (EELS) studies on both inorganic and biocarbonates (i.e., those forming under biological control) show that most calcium carbonates contain boron in both tetrahedral and trigonal forms (e.g., Klochko et al. 2009; Rollion-Bard et al. 2011; Noireaux et al. 2015; Philips et al. 2023). However, the measured δ11B values are incompatible with carbonates having incorporated high amount of the aqueous trigonal form B(OH)3 (e.g., Noireaux et al. 2015). Thus, the isotopic composition and coordination can be reconciled through a change in the coordination of the borate ion from tetrahedral to trigonal in the crystal lattice after incorporation (Klochko et al. 2009; Branson et al. 2015). This recoordination must occur without significant isotopic fractionation and could be a rate-limiting factor controlling the incorporation of boron into calcite (e.g., Ruiz-Agudo et al. 2012). However, some studies have suggested that some aqueous B(OH)3 is incorporated, even though this is not the main form in which boron is added to the carbonate lattice (e.g., Noireaux et al. 2015). It is also unclear to what extent the rate of crystal growth affects boron incorporation and fractionation, with experimental studies reporting contrasting findings (Mavromatis et al. 2015; Uchikawa et al. 2023 and references therein) potentially related to interactions with other ions present in seawater. For these and other reasons, it is not fully clear how to apply the laboratory experimental findings directly to biocarbonates.

Boron Incorporation into Biocarbonates— The Vital Effects

Biocarbonates have a large range of boron isotopic compositions (Fig. 2). These values are distributed both above and below those expected for the isotopic composition of B(OH)4– of the seawater in which they grew, such that few biologically produced marine carbonates have δ11B values matching that of the source borate ion of their host seawater. Moreover, it is possible that the ranges shown in Figure 2 for certain organisms do not reflect the full natural amplitude due to the small number of studies carried out. This is the case, for example, for coccoliths and sea urchins. The isotopic compilation shown in Figure 2 suggests two “end member” organisms (excluding algae) in terms of boron incorporation: scleractinian corals (whether cold-water or shallow-water corals), and benthic and planktonic foraminifera.

In stony corals, skeletal boron isotope values are well above those expected for the borate ion in seawater, suggesting that the pH at the corals’ calcification sites is higher than the ambient seawater (e.g., Rollion-Bard et al. 2003; McCulloch et al. 2018). The magnitude of this increase is greater at low pH than at high pH (Venn et al. 2013; McCulloch et al. 2018), suggesting that the corals require elevated pH to calcify effectively. Such control of pH by corals is known as pH up-regulation. This up-regulation can raise the pH of the calcification site ~0.5 to 1 pH units higher than the seawater pH. By raising pH at the calcification site, the corals increase the saturation state of aragonite (a polymorph of calcium carbonate) of their calcifying fluid, thus fostering the precipitation of their aragonitic skeletons. This ability to up-regulate may also insulate the calcification site pH somewhat against the effects of anthropogenic ocean acidification (from human-induced increases of atmospheric pCO2), but maintaining this offset may come at an energetic cost to the coral organism. The magnitude of the pH up-regulation recorded by coral boron isotopes agrees well with the few studies that have directly measured calcification fluid pH with either microelectrodes or pH-sensitive dyes (Venn et al. 2013). The agreement between these techniques indicates that 1) in corals, the involvement of B(OH)3 and the other effects discussed above are probably very minimal; and 2) the δ11B of the calcification fluid is similar to the δ11B of original seawater—the δ11B of the fluid from which the carbonates precipitate is one of the parameters taken into account when calculating its pH (Fig. 1). To complicate this picture, however, δ11B values in corals have been shown to vary in a single polyp or through the skeletal microstructures by several per mille, implying that different components of coral precipitate under different pH regimes or via different mechanistic pathways from the initial seawater, with implications for the ability and resilience of corals to deal with on-going anthropogenic climate change (e.g., Chalk et al. 2021).

Foraminifera, in contrast, are characterised by only a small difference between the pH of their calcifying fluid and that of seawater (as indicated by boron isotopes), such that foraminifera record the pH conditions of seawater more closely and directly than corals. One cause for the difference could be that foraminifera raise the pH of their calcifying fluids more variably than the consistent up-regulation of pH exercised by corals. The foraminiferal range in calcifying pH has been observed both via pH-sensitive fluorescent dyes and the δ11B values measured at a microscale. An additional contributing mechanism may be the rapid diffusion of boric acid into the calcifying space, thereby keeping the δ11B of the marine carbonate similar to the seawater borate ion, although this possibility requires further investigation. The observed small offset between δ11B values of foraminiferal shells and ambient seawater, combined with the widespread presence of foraminiferal shells in marine sediments across long spans of Earth history, have led these microfossils to become the most widely used target for reconstructing pH/pCO2. Due to their small size, few studies have explored the inter- or intra-shell heterogeneity of δ11B in foraminifera, with one of the first studies performed on Amphistegina (Rollion-Bard and Erez 2010), a large symbiont-bearing epibenthic foraminifer. This species shows a large amplitude of variations in δ11B, but is perhaps not representative of all foraminifera. It would therefore be useful to generate spatially resolved boron isotopic and concentration measurements from more species, particularly the planktic foraminifera routinely studied in palaeoceanography. In this case, however, we face the difficulty of performing sufficiently precise in situ measurements given the small sizes of the target foraminifera. The development of more precise in situ measurements could help to overcome this and other difficulties, thus enabling greater insights into the biomineralisation processes in foraminifera, as well as in even smaller organisms such as coccolithophores where few data are currently available (see Fig. 2).

Biological Fingerprint

Most calcifying organisms grow their skeletons or shells within privileged (i.e., isolated or semi-isolated) spaces, either vacuoles and/or spaces between existing carbonate and tissue. As summarised above, most, but not all, organisms increase their calcification pH in these privileged spaces to promote shell or skeleton growth. One of the simplest and least energy-intensive ways to raise pH is to expel protons in exchange for other cations (positively charged ions) present in seawater. Many carbonate organisms gain their Ca2+ from seawater as they release H+ from the privileged space (possibly via Ca2+-ATPase; Fig. 3). This exchange has the dual advantage of raising the pH and increasing the concentration of Ca2+, one of the essential constituents of carbonates, thus also raising the saturation state of calcium carbonate in the calcification space.

Another influence biology may have is in the precipitation pathways of shells or skeletons. Amorphous calcium carbonates (ACC) appear to be ubiquitous in biocarbonates as are other forms of stable or meta-stable carbonate solids. ACCs have been discovered in bivalves, brachiopods, sea urchins, and corals. Very recently, calcium carbonate hemihydrate was also detected as a precursor of aragonite in corals and molluscnacre (e.g., the pearlescent organic inorganic composite material found in oysters; Schmidt et al. 2024). Such precursors forming prior to the final calcite or aragonite biomineral could influence the incorporation of elements and isotopic fractionations. Numerous laboratory experimental studies have started to explore these aspects (see Jantschke and Scholz 2025 this issue), but the probable diversity of structural and/or chemical forms of ACC (Cartwright et al. 2012) cautions against simple and broad applications of the experimental results to natural biocarbonates. Despite these and other biological influences (the “vital effects”), the δ11B of biocarbonates universally increases with seawater pH; thus, with the use of suitable calibrations, their isotope compositions enable reconstructions of the pH of seawater in the geological past.

CaCO3 BORON CALCIUM RATIOS: A MORE COMPLICATED PROXY

As the charged borate ion is considered to be the predominant form of boron incorporated by marine carbonates, and pH controls its concentration in seawater relative to boric acid, one would expect the B/Ca ratio of biocarbonates to also track the pH of seawater, much as with boron isotopes. However, it seems that there are additional carbonate system controls on B/Ca ratios that are either not straightforward, or suggest other influences on the calcification site B(OH)4−. For example, the relationships to pH, borate:carbonate and borate:DIC (dissolved inorganic carbon), are all weaker in planktic foraminifera than the relationship between B/ Ca and ΔCO3 2– in the case of benthic foraminifera (where ΔCO3 2– is the difference between [CO3 2–] and saturation; Yu and Elderfield 2007; Henehan et al. 2015). As the precise competition between carbon species and B(OH)4− at the calcification site remains unclear, uncertainty persists concerning to which environmental parameter B/Ca should be related. Thus, it is currently difficult to apply B/Ca as a straightforward proxy for seawater carbonate chemistry outside of benthic foraminifera, where the relationship with ΔCO3 2– seems clear.

However, given that B/Ca is typically much easier to deter mine than δ11B, and given its potential to provide a non-pH carbonate system variable which, when used together with pH, allows the entire carbonate system to be constrained, the B/Ca ratio proxy warrants further investigation. For example, using δ11B as a pH proxy and B/Ca as a carbonate ion proxy (as in foraminifera or in corals) enables the whole carbonate system to be constrained (Zeebe and Wolf-Gladrow 2001). In corals, this has been used with some degree of success (e.g., DeCarlo et al. 2018; Chalk et al. 2021), and it has been used to infer that the dissolved organic carbon content and saturation states inside coral calcification spaces are elevated and can vary with time, temperature, and calcification mechanism. However, the approach is complicated due to the close relationship between pH and carbonate ion concentration in most natural systems, such that small uncertainties in the inputs become large uncertainties in the outputs. Despite this and other uncertainties around B/Ca as a proxy, it has been used to give carbonate system information, including the evolution of the carbonate system through time, in both modern and palaeoceanographic settings.

THE CENOZOIC pH–pCO2 RECORD

The most widespread and influential use of the boron proxies has been to reconstruct past ocean pH, and from this to determine the CO2 concentration of Earth’s past atmosphere (Hain et al. 2018). To date, the most complete pH–pCO2 record comes from surface dwelling planktic foraminifera (Fig. 4), which have exceptional fossil preservation stretching back hundreds of millions of years (to the Jurassic Period). Recent compilations of past atmospheric CO2 concentrations (e.g., CenCO2PIP) rely heavily on boron isotope reconstructions (from principally, but not only, foraminifera) to derive atmospheric CO2 concentrations that overlap with direct measurements derived from ice cores (~800,000 years). These rely primarily on extant taxa in the recent past (<6 Ma), with the advantage that these species can be calibrated and tested directly in laboratory environments. Extinct forms, further back in the geological record, require extensive knowledge of the ocean chemistry and habitat predictions, and are thus less well constrained. However, the general trend is very clear and robust, with pCO2 declining throughout most of the Cenozoic. Figure 4 is a Cenozoic compilation of δ11B-derived atmospheric CO2 concentrations, which shows some major features: the late Pleistocene orbital cycles (far right), which agree well with ice core derived estimates of pCO2 (see inset), evidence for pCO2 cycles with the same pacing as climate cycles (i.e., 41,000 y) prior to ~1.5 Ma, and pCO2 levels roughly equivalent to today in the Pliocene and late Miocene (middle panel), but up to 2000 µatm CO2 in the Eocene and Palaeocene atmosphere (left panel). Along the base of the figure is a representation of global mean annual surface temperature for the same time periods. Periods of high pCO2 are clearly associated with elevated temperatures of up to 13 °C above the pre-industrial value during the Palaeogene.

Boron Proxies Reveal Ocean Dynamics

Beyond using boron proxies to reconstruct atmospheric pCO2, they can also be used to trace the distribution of carbon in the global ocean and, thus, inform on the spatial f lux of CO2 to and from the atmosphere from different ocean environments, as well as the storage or sequestration of carbon in the deep ocean away from the atmosphere. For example, B/Ca and δ11B of benthic foraminifera have been used to reconstruct deep ocean pH and carbonate ion in the Atlantic during Pleistocene glacial–interglacial cycles (e.g., Chalk et al. 2019). During the warm interglacials with higher atmospheric pCO2 (including our current one), the Atlantic is characterised by relatively minor gradients in pH and carbonate ion down to ~4000 m. In contrast, in full glacial stages (cold periods with lower atmospheric pCO2), a sharp pH and carbonate ion gradient to lower values in the deep Atlantic is located at a water depth of ~2500 m, reflecting increased oceanic carbon storage. Periods of rapid climate change, including glacial–interglacial transitions, are associated with rapid fluctuations in the magnitude of this pH/carbonate ion gradient. A compilation of high latitude surface foraminiferal δ11B data adds to this picture by showing the highly dynamic nature of ocean–atmosphere carbon fluxes during these time intervals. High-resolution sediment cores show short periods of low surface ocean pH consistent with the shoaling of the carbon-rich deep waters to the surface during deglaciations where they return their dissolved CO2 back to the atmosphere (Shuttleworth et al. 2021). This allows us to identify the high-latitude areas as being important for driving fluctuations in atmospheric pCO2 on short to medium timescales. Together, these two proxy archives, alongside knowledge of atmospheric pCO2, can reveal the nature and mechanisms of oceanic CO2 storage and its sensitivity to perturbations. This is knowledge that is crucial to determine the effectiveness of the ocean at modulating anthropogenic change on timescales of a few hundred to tens of thousands of years.

CONCLUSION

Boron isotopes of biogenic carbonates are one of our sharpest tools for determining a key parameter of Earth’s climate—the atmospheric concentration of CO2 in the geological past. Recent studies have improved our under standing of vital effects, thereby enabling much clearer conversions from boron isotope records to climate recon structions. Room for improvement nevertheless remains, with forefront challenges being to understand the mechanisms and influences of biocarbonate mineralisation and how to calibrate extinct species. Studies of biomineralisation processes, mainly using boron proxies, show that most or many calcifying marine organisms raise their internal pH and/or increase their dissolved organic carbon to enhance CaCO3 precipitation. However, it appears that different organisms employ different mechanisms for raising pH, and in situ studies have shown that such mechanisms can differ even within a single organism, requiring further species-specific and calcification-site-specific investigations to understand the biology and biochemistry involved. Nevertheless, even though the organisms manipulate the solution from which they precipitate, this solution is derived from seawater and tracks important changes in seawater characteristics. These changes are then preserved in the boron isotopes and boron concentrations of the resulting biocarbonates, and this proxy record reveals variations in environmental conditions over great expanses of time. The Cenozoic record of atmospheric pCO2 change is still incomplete, and orbitally resolved records from multiple sites will take decades to complete, but are readily achievable. It is however crucial for this endeavour that routine and precise analyses of boron isotopes become faster, cheaper, and more abundant. Eventual expansion deeper into Earth’s history (i.e., across the Phanerozoic) will require reliable estimates of boron fractionation from other calcifying groups and tighter controls on ocean chemistry and diagenesis, in particular, improved knowledge of how the boron isotopic composition of seawater has changed over geologic time, which is arguably the single greatest source of uncertainty.

ACKNOWLEDGMENTS

We would like to thank the guest editors of this issue for their invitation to contribute an article. Additionally, we would like to thank M. Pesnin, R. Brown, and M. Buisson for their proof reading and suggestions, and A. Bard for the illustrations in Figure 2. Oscar Branson and one anonymous reviewer are thanked for their thoughtful comments. We also thank Thomas W. Sisson, Gavin Foster, and David Evans for the editing of this manuscript.

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