IN SITU STABLE ISOTOPE MEASUREMENTS IN FORAMINIFERAL TESTS BY SIMS

Foraminifera are a successful group of marine protists that pervaded most marginal to fully marine environments during the Phanerozoic. In modern oceans, they are the most diverse group of marine calcifiers. Most modern planktic foraminiferal species live in the surface to thermocline layer of the open ocean, and in the deep marginal seas such as the Mediterranean, Caribbean, South China Sea, and Red Sea. However, planktic foraminifera are mostly absent from shallow marginal seas, such as the North Sea where reproduction is impeded (e.g., Schiebel & Hemleben, 2017). Symbiont-bearing planktic foraminiferal species depend on light and are therefore restricted to the relatively shallow euphotic zone, whereas some symbiont-barren species have been sampled from water depths below 4000 m (Schiebel & Hemleben, 2017). Benthic foraminifera inhabit all marine environments, living above, at, or below the sediment water interface in water depths ranging from the intertidal zone to the deep ocean (Corliss, 1985; Pawlowski & Holzmann, 2009). Most planktic foraminiferal species live for only about one month (e.g., Schiebel & Hemleben, 2005), whereas some benthic species have a life span of up to several years (e.g., Purton & Brasier, 1999). The fossilized calcite tests of these unicellular organisms deposited in seafloor sediments provide an extensive paleoclimate archive dating back hundreds of millions of years. Combined with their ubiquity in the marine environment, foraminifera are one of the most important recorders of past environmental conditions.

Since the 1940s, various analytical methods have been developed to deduce paleoenvironmental information from these microfossils. Beginning with the pioneering work of Urey (1947), McCrea (1950), Epstein et al. (1951, 1953), and the landmark paper published by Emiliani (1955), measurements of the oxygen isotope composition (δ¹⁸O) of fossil foraminiferal tests have revolutionized our understanding of the Earth’s past climate. It is remarkable that many of these early methodologies and techniques to analyze the δ¹⁸O (and δ¹³C) composition of foraminiferal tests are still being used today. However, advances in instrumentation now allow for significantly smaller sample masses and faster analysis while, at the same time, providing higher precision and accuracy.

Typically, the oxygen and carbon isotope composition of foraminiferal tests (and other carbonate samples) is measured by gas source mass spectrometry (GSMS). Thereby, the sample (single or multiple pooled foraminiferal tests) is reacted with phosphoric acid, and the resulting CO₂ gas is subsequently ionized and analyzed for the mass 44 (¹²C¹⁶O¹⁶O), mass 45 (¹³C¹⁶O¹⁶O as well as ¹²C¹⁷O¹⁶O where the ¹⁷O contribution can be corrected using the Craig (1957) algorithm), and mass 46 (¹²C¹⁸O¹⁶O). From these measurements, the δ¹⁸O and δ¹³C composition of the sample is calculated and calibrated relative to the Vienna Pee-Dee Belemnite (V-PDB) carbonate standard. Minimum sample weights for modern GSMS systems are typically ∼10 µg, facilitating the analysis of individual amputated chambers of larger foraminiferal tests. However, latest methodological developments have demonstrated that accurate measurements of δ¹⁸O and δ¹³C by GSMS from just 3 µg of carbonate are possible (Vonhof et al., 2020).

Although the technique to analyze foraminiferal tests by GSMS was developed in the 1940s, it is still the best choice for the vast majority of paleoclimate studies, and in most scenarios, the isotopic measurements of multiple pooled tests provide a faithful picture of the Earth’s past climate. However, depending on the scientific objectives, conventional approaches for the analysis of the δ¹⁸O and δ¹³C composition of foraminiferal tests may be limited in their capability to provide optimal results due to several reasons. First, both planktic and benthic foraminiferal tests are heterogeneous on micrometer scales and therefore provide a wealth of additional information that cannot be assessed by dissolving and homogenizing their tests for analysis. For example, information about past water column stratification may be preserved as geochemical signatures in the micrometer-thin calcite layers of a planktic foraminifer as the test migrates vertically through the water column as part of the organisms’ ontogenetic development (e.g., Kozdon et al., 2009), and tests of benthic species with a long lifespan may provide a record of seasonality (e.g., Evans et al., 2013). Second, fossil foraminifera tests may be affected by diagenetic alteration, a process that changes their initial isotopic and chemical composition on micrometer scales. Using conventional approaches, it is not possible to separate the diagenetic phases prior to analysis, which may introduce a significant bias in the resulting paleorecord (e.g., Kozdon et al., 2011; Wycech et al., 2016; Raymo et al., 2018; Poirier et al., 2021). Third, conventional approaches struggle to resolve δ¹⁸O and δ¹³C signals captured by live-collected foraminifera in laboratory culture where they precipitate a very small fraction of their tests under controlled conditions. The ultimate goal of such studies is to improve our understanding of how environmental parameters are recorded in test calcite, which is difficult to resolve on fine scales with the bulk conventional measurement technique.

In addition to the application of SIMS to measure and study heterogeneity in the δ¹⁸O and δ¹³C composition of foraminifera on micrometer scales, several other SIMS applications such as the analysis of boron and lithium isotopes in <30-µm-sized subdomains within foraminiferal tests are being explored presently. Thus, SIMS approaches have opened the door to a wealth of new information that is inaccessible by conventional GSMS measurements and thus established an entirely new field of curiosity-driven paleoproxy and biomineralization research.

Since the 1990s, ‘in situ’ (measurement in the ‘original place’) analytical approaches revolutionized data acquisition for paleoclimate research as well as for many other fields in the Earth sciences. Compared to conventional analytical methodologies, in situ approaches allow for the determination of the isotopic and chemical composition of a sample on micrometer scales.

The most commonly used in situ analytical approaches in the field of proxy research and paleoclimatology are electron probe microanalysis (EPMA), secondary ion mass spectrometry (SIMS, or ion microprobe), and laser-ablation inductively coupled plasma mass spectrometry (LA-ICP-MS). Among these three different approaches, the electron microprobe, which captures the elemental composition on micrometer scales, is the oldest in situ technique (commercially available since the late 1950s; de Chambost, 2011) and was first utilized to analyze planktic foraminiferal tests for the distribution and concentration of a suite of trace elements in a remarkable study by Hooper (1964) that established the entirely new field of in situ analysis of biominerals. In more recent studies, EPMA systems were successfully employed to measure Mg/Ca and Sr/Ca ratios in foraminiferal tests on micrometer scales and to compile elemental maps from chamber wall cross-sections of cultured or fossil foraminiferal tests to better understand their compositional heterogeneity or the processes of biocalcification (e.g., Eggins et al., 2004; Fehrenbacher & Martin, 2011; Branson et al., 2013; Fehrenbacher et al.; this issue).

Laser-ablation inductively coupled plasma mass spectrometry, which was developed in the 1980s (Gray, 1985), provides much higher sensitivities than EPMA approaches and is primarily used for the chemical characterization of the sample on small spatial scales, although certain isotope ratios can also be measured. The LA-ICP-MS spots are typically 50 µm or less for depth profiling with a stationary laser or elemental mapping with a laser rastering over the sample. Foraminiferal tests were first analyzed by LA-ICP-MS in the mid-1990s to assess the impact of contaminant Fe-Mn coatings on other trace elements incorporated into benthic test calcite (Wu & Hillaire-Marcel, 1995). The development of laser systems with short wavelengths (213 nm and 193 nm) in the late 1990s, in combination with better protocols for standardization and data processing, greatly improved the analytical precision and accuracy of trace element measurements in carbonates. Today, LA-ICP-MS is by far the most widely used in situ approach for the analysis of fossil foraminiferal tests (see also Fehrenbacher at al.; this issue).

The most commonly used in situ technique for stable isotope analysis, however, is secondary ion mass spectrometry (SIMS) which is based on the bombardment of the sample with a focused ion beam. In many modern instruments, two ion sources are utilized for the analysis of geological samples: ¹⁶O^– is used to enhance ionization of metallic elements, and ¹³³Cs⁺ for nonmetallic elements. The impact of the primary ions with the sample surface displaces atoms on the sample, thereby creating a ‘collision cascade’ that is ionizing a small portion of the targeted material which is subsequently accelerated by an electrostatic field into a mass spectrometer for analysis. Although SIMS has been used in Earth and material sciences for the measurement of elemental compositions and elemental distributions on small spatial scales for more than half a century (e.g., Herzog et al., 1967), the analysis of carbonate minerals by SIMS has been virtually nonexistent until the late 1980s (Veizer et al., 1987). The first study exploring the suitability of SIMS for the analysis of foraminiferal tests was published by Allison & Austin (2003). One motivation of this study was to use SIMS as an alternative to EPMA to measure the concentration of a suite of trace elements in benthic foraminifera tests on micrometer scales and to evaluate the potential of SIMS approaches for Mg/Ca paleothermometry.

In situ measurements of the oxygen isotope ratio in geologic samples by SIMS was first demonstrated by Giletti et al. (1978), however, it took more than two decades and many improvements in instrumentation including optimizations of the operating parameters such as instrument tuning, improved sample preparation, and the establishment of robust standardization until sub-permille precision for in situ analysis of δ¹⁸O in carbonates could be achieved (Rollion-Bard et al., 2003; Valley & Kita, 2009). After a period of rapid development spanning from the late 1990s to the early 2000s, the precision of <0.3‰ (±2 SD) reported by Valley & Kita (2009) has approached a physical limit defined by the number of atoms in spots of 10 µm and below. As the oxygen isotope composition of foraminiferal tests is one of the longest established, best understood, and most widely used of all paleoclimate proxies, the ability to measure δ¹⁸O (and δ¹³C) on small spatial scales with sub-permille precision has the potential to revolutionize paleoproxy research.

The preparation of foraminiferal tests for stable isotope analysis by SIMS requires expertise and diligence. Typically, the selected tests are cast together with standard grains in a 1-inch diameter epoxy round, ground to the level of best exposure, and polished (Fig. 1). The epoxy must be compatible with high vacuum, and a sub-micrometer polishing relief is required to facilitate high precision and accuracy (Kita et al., 2011).

Although very time consuming, this sample preparation technique provides the unique opportunity to image the cross-sectioned foraminiferal chamber walls prior to analysis which allows for the identification of the domains of interest and/or the areas to avoid. For example, cross-sections of the mounted foraminiferal tests can be imaged by a scanning electron microscope (SEM) or EPMA equipped with a cathodoluminescence (CL) detector which provides the opportunity to quickly assess the general preservation quality of the fossil tests (Fig. 2). Under CL, unaltered domains of the chamber wall feature a blue luminescence, whereas altered areas are characterized by an orange luminescence linked to the incorporation of Mn²⁺ into the test material (e.g. Wendler et al., 2012). Other suitable imaging approaches employ the use of backscattered electron microscopy (BSE) to investigate the texture of the foraminiferal chamber walls (Fig. 3). Using this methodology, Kozdon et al. (2011) reported that a microgranular chamber wall texture similar to that found in modern or cultured planktic foraminiferal tests is still preserved in subdomains within fossil tests from the Paleocene-Eocene transition (∼56 Ma), whereas the outer regions of the tests are composed out of much coarser crystals. Subsequent in situ δ¹⁸O analysis of the microgranular domains within the chamber walls confirmed their better preservation, whereas the coarser outer crystals are of diagenetic origin.

After data acquisition, a second session of sample imaging should be performed to verify that contaminant phases or epoxy are not included in the analysis pit. Furthermore, the correlation of the precise location of the SIMS analysis pit with information obtained by high-resolution imaging facilitates the interpretation of the data within the context of a complex and much larger sample.

In situ δ¹⁸O measurements of foraminiferal tests by SIMS were first published in a seminal study by Rollion-Bard et al. (2007). The researchers used SIMS with 15 µm spots to document the δ¹⁸O variation in cross-sections of the knob area of live-collected and cultured specimens of a long-lived (∼ 2 years), symbiont-bearing benthic foraminifera. They reported an intratest range in δ¹⁸O that, when converted to temperature, exceeds the seasonal temperature variation at collection site and it was postulated that ‘vital effects’ in combination with different generations of calcite may contribute to the relatively large range in intratest δ¹⁸O values.

Kozdon et al. (2009) were the first to measure the δ¹⁸O composition in planktic foraminiferal tests by SIMS. Using 3 µm spots, they reported an intratest δ¹⁸O range of more than 3‰ between the early-formed lamellar calcite and the later-formed crust calcite in the polar to subpolar planktic foraminifera Neogloboquadrina pachyderma from a North Atlantic core top. Such heterogeneity was interpreted to result from changes in habitat depth during ontogeny (Fig. 4). Similar to the findings of Rollion-Bard et al. (2008), the intratest-δ¹⁸O range of N. pachyderma exceeds the range of ‘equilibrium δ¹⁸O’ in the specimens’ habitat, presumably due to vital effects linked to the mechanisms of biocalcification.

A migration to greater water depth during ontogenetic development is also well documented for the planktic foraminifera Trilobatus sacculifer, a commonly selected species for paleoclimate reconstructions. Due to this depth migration, the test composition of T. sacculifer is basically an aggregate mixture of two phases, early-formed pregametogenic calcite that precipitates in relatively shallow waters, and a thick gametogenic crust that is secreted at the end of the specimens’ life cycle in colder, deeper waters (e.g., Bé, 1980). The addition of the gametogenic crust to the exterior of T. sacculifer tests may bias temperature reconstructions inferred from conventional whole-test GSMS analysis towards the colder, deeper waters. New ideas that may provide a solution for the long-standing challenge of a cold-bias were presented in a seminal study by Wycech et al. (2018a). By carefully examining cross-sections of Holocene T. sacculifer tests using SEM imaging, it was found that the amount of pregametogenic calcite in many tests is greatly reduced due to varying degrees of dissolution. It is important to note that this type of dissolution is not visible on the outside of the tests, therefore, it may remain entirely undetected when selecting specimen for analysis by traditional (reflected light) microscopy. After SEM imaging, Wycech et al. (2018a) used SIMS to analyze the δ¹⁸O composition of both the pregametogenic and the gametogenic calcite on micrometer scales and reported that this approach provides a new solution to enhance the fidelity of records of past surface ocean conditions as environmental information for the upper water column can be extracted from the pregametogenic calcite layers. In light of these results, future studies should consider SIMS for paleoceanographic reconstructions from other planktic foraminiferal species that form a thick outer crust in deeper waters at the end of their life cycle.

The capability of SIMS to analyze the oxygen and carbon isotope composition in foraminiferal tests on micrometer scales has also opened the door to experiments that will help to improve our understanding of the complex processes of biomineralization and how changing environmental parameters are recorded in the isotopic composition of the laboratory-grown calcite. In a novel study, Vetter et al. (2013) used SIMS with 3 µm spots to measure the variation in δ¹⁸O across the wall of the final chamber of Orbulina universa that was transferred every 12 h between ambient seawater and seawater enriched with barium and ¹⁸O to produce multiple chemically and isotopically distinct layers (Fig. 5). Depth profiling by LA-ICP-MS on fragments of the same final chambers delineated the regions within the chamber wall precipitated in ambient and barium-labeled seawater that were subsequently cross-correlated to the areas enriched in ¹⁸O as identified by SIMS. This study reveals that barium and ¹⁸O tracers are incorporated into the foraminiferal chamber wall with no measurable offset, demonstrating for the first time that cation and stable isotope tracers in seawater are synchronously incorporated during test calcification. Furthermore, it was shown that SIMS allows for the measurement of test calcite δ¹⁸O that was precipitated within a time span as short as 12 h, facilitating applications such as the quantification of daily or diurnal events in the planktic foraminifer test chemistry from the fossil record.

A related experiment conducted by Vetter et al. (2014) using a ¹³C tracer combined with barium similarly documented synchronous incorporation of isotopic and cation tracers into test calcite. With this study, it was demonstrated that the δ¹³C of test calcite precipitated within 24 h in ¹³C-labeled seawater can be resolved and accurately measured by SIMS using 8-µm spots, highlighting the potential of this technique for addressing questions about ecology, biomineralization, and paleoceanography.

It is often assumed that benthic and planktic foraminiferal tests showing no visible signs of dissolution or diagenetic overprinting under the optical microscope are well-preserved and that their original δ¹⁸O composition has not changed over time. However, this assumption has been questioned on the grounds that diagenetic calcite can replace primary foraminiferal test structures with little or no change to such delicate structures as wall pores, internal wall layering, or surface ornamentation (Pearson et al., 2001; Sexton et al., 2006; Pearson et al., 2007; Sexton & Wilson, 2009; Poirier et al., 2021). Consequently, failure to recognize and quantify diagenetic alteration is a potential source of error in climate reconstructions based on the δ¹⁸O composition of benthic and planktic foraminiferal tests.

Over the last two decades, it has come to light that foraminiferal tests can be differentiated on the basis of their state of preservation (e.g., Sexton et al., 2006; Sexton & Wilson, 2009; Poirier et al., 2021). The tests of living foraminifera are typically translucent and appear glassy under the optical microscope. This kind of preservation is generally rare among foraminiferal assemblages preserved in deep-sea sediments. The vast majority of fossil tests feature a frosty appearance that likely indicates a modest degree of diagenetic alteration (e.g., Pearson et al., 2001; Sexton et al., 2006). However, depending on the degree of diagenesis, some portions of the chamber wall may still largely retain their original chemical and isotopic composition. Kozdon et al. (2011) used SIMS to measure the δ¹⁸O composition of both the microgranular calcite on the inside and the coarser crystalline phase on the outside (Fig. 3) of chamber walls of the planktic foraminifera Morozovella velascoensis recovered from Early Paleogene sediments. It was found that the microgranular calcite, which features a texture similar to that reported from modern, live-collected planktic foraminiferal tests, appears to have largely retained its original δ¹⁸O composition. In contrast, in situ δ¹⁸O measurements of the coarser crystalline outer domains reveal a diagenetic origin of these phases, suggesting formation at the seafloor or in the upper sediment column. As it is not possible to separate the diagenetic from the biogenic phases, conventional whole-test GSMS analyses of these tests represent a mixture of sea surface and bottom water conditions which introduces a significant cold-bias in the paleoclimate record. By analyzing the δ¹⁸O of the better-preserved microcrystalline calcite by SIMS, Kozdon et al. (2011) reported δ¹⁸O values that are -0.6‰ to -2.7‰ lower than previously published conventional ‘whole-test’-δ¹⁸O values for age equivalent samples from a late Paleocene to early Eocene (56–49 Ma) section recovered at ODP Site 865 in the central Pacific (Fig. 6). The SSTs calculated by Kozdon et al. (2011) from the in situ δ¹⁸O measurements are 4°C to 8°C higher than those previously reported by GSMS analysis and are generally consistent with climate model predictions and published SSTs derived from rare and exceptionally well-preserved foraminiferal tests, whereas the cooler temperatures inferred from previous conventional GSMS measurements cannot be replicated by model simulations. These results demonstrate that in situ measurements of δ¹⁸O can greatly improve the fidelity of paleoclimate records, especially from foraminiferal tests that are not well preserved.

The offset in δ¹⁸O and δ¹³C between SIMS and GSMS measurements of fossil foraminiferal tests from the same core samples can further be used to quantify the degree of diagenetic alteration by mass balance (Fig. 7). However, it is important to note that the offset in δ¹⁸O between SIMS and GSMS analysis is not necessarily constant. SIMS and GSMS measurements of both planktic and benthic foraminiferal tests from the Campbell Plateau (DSDP Site 277) feature the largest offset in δ¹⁸O during the early Eocene Climate Optimum (EECO, Fig. 8). This offset is gradually decreasing during the following Eocene cooling suggesting that either diagenesis at the site is most pronounced during hot climates or the offset in δ¹⁸O between biogenic and diagenetic phases within individual foraminiferal tests is not constant as the difference between sea surface and bottom water temperatures varies over time.

In one of the first studies using SIMS to measure δ¹³C on fossil foraminifera, Kozdon et al. (2018) reassessed the magnitude of the Carbon Isotope Excursion (CIE) marking the onset of the Paleocene-Eocene Thermal Maximum (PETM). The CIE signals the release of massive amounts of ¹³C-depleted carbon into the ocean-atmosphere system, creating conditions that are widely regarded as the best ancient analogue for our future climate. The CIE is the most widely used parameter to constrain the mass of carbon input, however, the size of this excursion differs depending upon the material being analyzed, which introduces significant uncertainty into carbon input estimates (e.g., Bains et al., 2003). Such discrepancies are most evident between terrestrial and marine records that yield mean CIE magnitudes of ∼4.7‰ and ∼2.8‰, respectively (McInerney & Wing, 2011). Using the same methodology previously developed for in situ δ¹⁸O measurements in foraminiferal tests, Kozdon et al. (2018) analyzed the δ¹³C composition in minute (∼7 µm) subdomains within planktic foraminifera of the genus Morozovella velascoensis from ODP Site 865 in the central Pacific and reported a CIE magnitude of ∼4.6‰. This CIE is 2‰ larger than that registered by conventional whole-test GSMS measurements of the same planktic foraminifer species and is in agreement with the mean CIE magnitude reported from the terrestrial realm (McInerney & Wing, 2011; Fig. 9). In a subsequent study applying the same methodology on planktic foraminiferal tests of the genus Acarinina spp. from the Kerguelen Plateau (ODP Site 1135), Hupp et al. (2023) reported a CIE magnitude of 5.3‰, which is comparable to the CIE magnitude found in many terrestrial PETM records and consistent with earlier results from ODP Site 865.

The aforementioned studies indicate that the use of SIMS to perform δ¹⁸O and δ¹³C analyses on micrometer-scales represents a fundamental advance for enhancing the fidelity of paleoclimate reconstructions in certain scenarios, and new information about the processes of biomineralization can be obtained by analyzing micrometer-sized portions of foraminiferal tests precipitated in a controlled laboratory environment. However, in order to fully assess the potential of this technique, it is critical to perform comparisons of δ¹⁸O and δ¹³C analyses on foraminiferal tests by SIMS and GSMS. Wycech et al. (2018b) measured the δ¹⁸O composition of the final chamber of the planktic foraminifer species Orbulina universa from laboratory culture and core top sediments by SIMS and GSMS and reported that δ¹⁸O values measured by SIMS are, on average, 0.9‰ lower than values derived by conventional GSMS measurements. This offset was not eliminated by sample treatment and it was postulated that it likely stems from a combination of factors such as SIMS measurements of oxygen in chemically-bound water and refractory organic matter, sample treatment, and conditions during GSMS analysis, differences in minor element concentration of samples vs. standards, and/or a change in the SIMS instrumental mass fractionation due to the different crystalline microstructures of the foraminiferal tests in comparison to the coarse crystals of the calcite standard. However, more research is required to fully assess the origin of this offset. It is important to emphasize that the SIMS-GSMS offset may not be the same on foraminifer taxa with substantially different compositions, test microstructures, porosities, and/or burial histories. For example, SIMS δ¹⁸O measurements of the massive (coarse crystalline) outer crust of the planktic foraminiferal species Neogloboquadrina pachyderma approach values determined by conventional analysis (Kozdon et al., 2009; Fig. 4). Furthermore, mass balances published by Kozdon et al. (2011, 2018; Fig. 7) estimating the ratio of biogenic and diagenetic calcite in planktic foraminiferal tests from the Paleocene-Eocene transition could not have been computed if the 0.9‰ offset in δ¹⁸O between SIMS and GSMS analysis is applied to SIMS measurements of these fossil tests.

A related experiment comparing δ¹³C analyses by SIMS and GSMS on O. universa tests grown in the laboratory and from core top samples performed by Wycech et al. (2024) revealed more complex results. Cultured tests cleaned with hydrogen peroxide feature no difference between SIMS and GSMS δ¹³C measurements, however fossil test fragments from core top samples cleaned with hydrogen peroxide yield a SIMS – GSMS offset of 0.6‰, while vacuum roasting of fossil test fragments removes the SIMS – GSMS difference. These studies motivate future research to investigate the origin of the intermethod offset between SIMS and GSMS analyses of δ¹⁸O and δ¹³C of modern planktic foraminiferal tests, as a better understanding of this offset will further enhance the robustness of SIMS-based paleoclimate records.

Researchers are also exploring the suitability of SIMS for microchemical analysis of the boron and lithium isotope composition (δ¹¹B and δ⁷Li, respectively) in foraminiferal tests. The δ¹¹B composition of foraminifera has been established as an empirical paleo-pH proxy (e.g., Spivack et al., 1993; Sanyal et al., 1995). However, the use of planktic foraminiferal tests for paleo-pH reconstruction provides some complications: Due to their depth migration, chambers precipitate at different water depth and hence at different pH conditions, and conventional analysis only provides a single δ¹¹B value representing the average composition. Furthermore, conventional δ¹¹B measurements of foraminifera require a large number of individual tests (typically >50, Guillermic et al., 2020), which may pose a challenge for sediments with a relatively low abundance of planktic foraminiferal tests. In order to provide a new solution to these challenges, Kasemann et al. (2009) was the first to evaluate the suitability of SIMS to measure the δ¹¹B composition in foraminiferal tests. Using spots of ∼15 µm, they analyzed O. universa whose final chambers were precipitated in a controlled laboratory environment and reported that in situ SIMS δ¹¹B measurements and conventional pooled-test data agree to within 1.3‰ and are thus sufficiently accurate for geochemical applications. They concluded that this technique is a useful tool to distinguish between the biological and environmental control on the boron isotope composition of biogenic carbonates and may thus improve our understanding of biological factors affecting the boron isotope fractionation.

Foraminiferal δ⁷Li can be used to reconstruct long-term changes in the Li isotope composition of seawater resulting from imbalances in weathering and hydrothermal inputs and sedimentary outputs (e.g., Hathorne & James, 2006). Therefore, the foraminiferal δ⁷Li record may be a potential proxy for past changes in silicate weathering intensity if the effect of other environmental parameters on the Li isotope composition of foraminiferal tests is known. The effect of secondary factors on foraminiferal δ⁷Li was assessed in a seminal study by Vigier et al. (2015) that pioneered in situ δ⁷Li analysis in foraminiferal test by SIMS. The authors demonstrated that a reproducibility of 1‰ (1σ) or better for in situ δ⁷Li measurements can be achieved using 20–30-µm spots. Using this technique, Vigier et al. (2015) were able to demonstrate that δ⁷Li in cultured benthic foraminifera is insensitive to temperature and pH variations but features a strong positive correlation with the Dissolved Inorganic Carbon (DIC) content of seawater. Thus, in addition to providing useful information about long-term variations in silicate weathering, the lithium isotopic composition of foraminifera may serve as a new proxy for past ocean DIC. When combined with other paleo-proxies of the carbonate system such as boron isotopes, δ⁷Li may therefore be a powerful tool for reconstructing rapid variations in the past oceanic carbon cycle.

These seminal studies may serve as a blueprint for future research, centered on newly designed culture experiments to assess how fast-changing environmental parameters are recorded in micrometer-thin layers within foraminiferal calcite, or on the acquisition of multiple isotopic measurements from the same individual foraminiferal tests to compile records with extremely high temporal resolution. As SIMS analyses are minimally destructive and preserve the vast majority of the foraminiferal test, future studies may also explore new pathways in combining multiple analytical approaches on the same individual foraminiferal test as the fidelity of paleoclimate records can be greatly improved by integrating different proxy-information from the same archive (‘multiproxy approach’).

Since the 2000s, in situ δ¹⁸O and δ¹³C measurements of foraminiferal test on micrometer scales by SIMS have revolutionized data acquisition for paleoclimate records and for paleoproxy research. Previous studies have demonstrated that SIMS analysis of planktic foraminiferal tests allows for the reconstruction of past water column stratification, that daily events recorded in micrometer-thin bands within foraminiferal chamber walls can be registered, and that better-preserved domains can be identified and analyzed to significantly enhance the fidelity of paleoclimate records. Furthermore, SIMS analyses that target the early-formed pregametogenic calcite and exclude the later-formed gametogenic crust offer new and groundbreaking opportunities to reconstruct past near-surface temperatures from the fossil foraminiferal record. Future directions will likely be centered on multiproxy approaches using a combination of SIMS-EPMA or SIMS-LA-ICP-MS to improve the fidelity of paleoclimate reconstructions as well as on newly-designed culturing experiments for micron-scale in situ analysis of laboratory-grown calcite to enhance our understanding of foraminiferal ecology and biocalcification.