# Coccoliths as Recorders of Paleoceanography and Paleoclimate over the Past 66 Million Years

Clara T Bolton, Heather M Stoll

► To cite this version:

Clara T Bolton, Heather M Stoll. Coccoliths as Recorders of Paleoceanography and Paleoclimate over the Past 66 Million Years. Annual Review of Earth and Planetary Sciences, 2025, 53, pp.169-194. 10.1146/annurev-earth-040623-103211. hal-04878665v1

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Submitted on 10 Jan 2025 (v1), last revised 26 Nov 2025 (v2)

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# Coccoliths as Recorders of Paleoceanography and Paleoclimate over the Past 66 Million Years

Clara T. Bolton¹,*, and Heather M. Stoll²,.*

¹Climate Research Group, Aix-Marseille Université, CNRS, IRD, CEREGE UM34, 13545 Aix en Provence, France; email: [bolton@cerege.fr](mailto:bolton@cerege.fr)

²Department of Earth Sciences, ETH Zürich, Zürich, Switzerland

These authors contributed equally to this work.

## Keywords

coccolithophores, calcification, calcareous nannofossils, paleoceanography, proxies

## Abstract

Coccolithophores are a major group of oceanic calcifying phytoplankton, and their calcite skeletal remains, termed calcareous nannofossils, are a major component of deep-sea sediments accumulating since the Jurassic. Coccolithophores play a role in both the biological pump and the carbonate pump, exporting organic and inorganic carbon, respectively, out of the surface ocean. This means that they are key responders to and recorders of ocean carbon cycle and climate changes over geological and shorter timescales, and studying these responses can help elucidate the uncertain fate of calcifying phytoplankton under projected climate change scenarios. Here, we review established and emerging approaches for reconstructing (a) mixed-layer ocean temperature, (b) marine productivity, and (c) aspects of the ocean carbon cycle, using calcareous nannofossils from deep-sea sediments. For each parameter, we discuss the different proxies that have been proposed, based on abundance or species composition, inorganic geochemistry, and/or coccolith morphology, and explore their applications and limitations in Cenozoic paleoceanography.

Coccolithophores in Paleoceanography
1. Calcareous nannofossils can be used to reconstruct upper ocean conditions and changes over centennial to million-year timescales.

2. Key coccolith-based proxies for temperature, productivity, and the carbon cycle are reviewed.

3. Approaches based on assemblages, geochemistry, and morphology provide novel insights into the evolution and adaptation of coccolithophores and past climate.

# 1. INTRODUCTION

Coccolithophores are a group of unicellular, calcifying algae (phylum Haptophyta, class Prymnesiophyceae) that are ubiquitous and abundant in the upper layers of the ocean, inhabiting a wide variety of ecological niches (Young et al. 2003). The ability of coccolithophores to produce coccoliths, calcite plates precipitated intracellularly and extruded to form a cell covering called a coccosphere, means that they interact with and record their surface ocean environment via calcification as well as photosynthesis, making them uniquely useful in paleoceanography (Figure 1). Coccolithophores produce two distinct types of calcium carbonate coccoliths during different life-cycle phases and via distinct biomineralization modes, namely heterococcoliths (~1 to 20 µm in length and formed of a radial array of crystal units) and holococcoliths (tiny euhedral crystals less than 0.1 µm) (Young & Henriksen 2003). Heterococcoliths have greater preservation potential and higher morphological diversity than holococcoliths; thus, they have a complete fossil record and form the basis of all paleoceanographic and biostratigraphic studies alongside nannoliths, a heterogeneous group of calcareous nannofossils generally thought to originate from haptophytes (Young 1998). For the purpose of this review on paleoceanographic proxies, the term coccolith refers to heterococcoliths, and the term calcareous nannofossils refers to coccoliths and nannoliths considered together.
<figure><img src="image_1.png" /><figcaption>**Figure 1** Schematic illustration of coccolithophore depth habitats, cellular interactions with the environment, and commonly applied coccolith-based proxies. (a) The living assemblage is composed of UPZ (~0–100 m depth, depending on oceanographic regime) and DPZ (~100–200 m depth) communities, dominated by different species. Upon death or consumption, organic and inorganic components of coccolithophore cells sink and are exported out of the photic zone as marine snow, often as part of aggregates or fecal pellets, leading to a fossil assemblage (primarily composed of individual coccoliths rather than intact coccospheres) in sediments that has undergone selective dissolution and displays reduced diversity. Panel a adapted with permission from a graphic by Antonin Brousse based on coccolithophore scanning electron microscope images by Luc Beaufort. (b) Coccolithophore cells are surrounded by a set of interlocking calcite plates called coccoliths. Coccolithophores interact with the external environment via photosynthesis and calcification. The main morphological and geochemical proxies based on fossil coccoliths are detailed in the boxes. Abbreviations: DPZ, deep photic zone; UPZ, upper photic zone.</figcaption></figure>

Coccolithophore calcification is estimated to contribute on average 1–10% (>20% in oligotrophic environments) to total carbon fixation (calcification plus photosynthesis) (Poulton et al. 2007). Coccoliths produced in the surface ocean sink out of the photic zone, contributing directly to the carbonate pump and indirectly (via ballasting) to the biological pump (Balch 2018, Monteiro et al. 2016) (Figure 1). Most coccoliths dissolve in the water column during settling or *Coccolithophores in Paleoceanography*
on the sea floor, buffering the ocean (Sulpis et al. 2021). Nevertheless, coccoliths make up
around half of total biogenic CaCO₃ in Holocene deep-sea sediments (Broecker & Clark 2009),
and the rain of coccoliths to the sea floor since the Upper Triassic (~215 Ma) has contributed to
the formation of the largest geological carbon sink on Earth. The sensitivity of sea floor
carbonate dissolution to global carbon cycle fluctuations constitutes a crucial stabilizing
feedback in Earth's climate system (Broecker & Peng 1987). Although only a fraction of
coccoliths produced in the surface ocean are preserved in sediments, fossil coccoliths record the
rapid evolutionary turnover of coccolithophores (see review in Young et al. 2005) and encode
information on surface ocean or climate parameters during past geological periods, so they are
ideal for reconstructing the biotic response to both abrupt and gradual climate changes (e.g.,
Gibbs et al. 2020, Hannisdal et al. 2012). Many different approaches are used to decipher
paleoceanographic and paleoclimatic information encoded in calcareous nannofossils, and these
are discussed in the following sections, grouped by target parameter.

KEY CONTRIBUTIONS OF COCCOLITHOPHORES TO PALEOCLIMATE
RESEARCH

* Calcareous nannofossils are an unparalleled tool in biostratigraphy and a key component of the geologic timescale, allowing dating and cross correlation of different marine sedimentary sections.

* The abundance and species composition of (modern) coccolithophore communities and (fossil) calcareous nannofossil assemblages provide unique insight into frontal movements, water mass characteristics, and vertical ocean stratification, in particular revealing the cyclicity of tropical productivity variations over the past several million years.

* Coccolithophore responses to nutrient-stimulated growth are imprinted in the Sr/Ca ratio of calcite coccoliths, revealing important productivity changes from Paleogene extreme warm periods to late Quaternary orbitally paced cycles.

* Culture studies of coccolithophore strains under controlled conditions have revealed strong sensitivities to carbonate chemistry, and coccolith carbon isotope vital effects have revealed changes in carbon limitation that indicate decreases in atmospheric CO₂ during key climate transitions.

* Long-term changes in coccolithophore size and calcification over the Cenozoic manifest adaptations and/or evolutionary responses to climate and carbon cycle drivers, with implications for understanding the response of marine calcifiers to climate change scenarios.

* The organic remains of coccolithophores (including alkenones) form the basis of a robust sea surface temperature proxy and also provide insight into past carbonate chemistry and cell physiology.
## 2. TEMPERATURE

### 2.1. Clumped Isotopes

Clumped isotope thermometry measures the abundance of bonds between the rare isotopes ¹⁸O and ¹³C in the CaCO₃ molecule, reported as Δ₄₇. The abundance of such bonds, or clumping of the rare isotopes, is thermodynamically favored at cold temperatures (for a review, see Huntington & Petersen 2023). Because large sample sizes are typically required for the mass spectrometric measurement of Δ₄₇, and because the abundance of coccoliths is much higher than that of planktic foraminifera in sediments deposited before the Plio-Pleistocene (the past 5.33 million years), there has been interest in evaluating the potential for coccolith clumped isotope thermometry. Laboratory calibrations of coccoliths cultured at known temperatures confirm a strong temperature control on Δ₄₇ in coccoliths (Clark et al. 2024, Katz et al. 2017), and the calibration is similar to published calibrations for planktic foraminifera. Unlike other surface ocean temperature proxies, which are deliberately regressed against and calibrated to sea surface (0 m depth) temperature (SST), coccolith Δ₄₇ calibrations yield the actual calcification temperature. In globally distributed late Holocene sediments, coccolith Δ₄₇ exhibits a strong correlation with SST (Mejía et al. 2023). In low latitude oceans with a steep thermocline, Holocene sediment data suggest that production of most coccoliths occurs at depths of 80–120 m (Mejía et al. 2023), consistent with observations of maximum coccolithophore cell density at these depths in tropical, oligotrophic regions sampled during cruises (Beaufort et al. 2008, Poulton et al. 2017).

Coccolith Δ₄₇ has been measured in Miocene (23.03 to 5.33 Ma) to Recent samples in a few settings. One study examined Δ₄₇ in different coccolith-dominated size fractions from a core in the deep equatorial Pacific [Integrated Ocean Drilling Program (IODP) Site U1338] spanning the late Miocene to early Pliocene and highlighted the importance of isolating coccolith carbonate from authigenic carbonate and fragments in the measured fraction (Drury & John 2016). Due to differing standardization approaches, these measurements cannot be converted to the modern I-CDES scale for application of coccolith or foraminifera temperature calibrations. Recent protocols for narrow (coccolith-dominated) fine-fraction sediment analysis additionally include oxidation steps to limit potential interference from other molecules derived from organic matter or sulfides in the measurement of the minor abundance mass 47 clumped peak (Clark et al. 2024, Coccolithophores in Paleoceanography)
Mejía et al. 2023). At a western tropical Atlantic core site [Ocean Drilling Program (ODP) Site 926), late Miocene Δ47 coccolith temperatures are in the range 26 °C to 31°C, consistent with estimates of SST greater than 28 °C based on alkenone unsaturation ratios (Tanner et al. 2024). In contrast, subpolar North Atlantic Δ47 coccolith temperatures are significantly colder than alkenone-derived temperatures during the mid- to late Miocene, suggesting steeper latitudinal temperature gradients than those inferred from alkenones (Mejía et al. 2020).

Clumped isotope thermometry of coccoliths has the advantage that the estimation of temperature does not require any assumptions about the oxygen isotopic composition (δ¹⁸O) of seawater at the time of calcification; thus, it is independent from changes in ice volume and local hydrology. Coccolith δ¹⁸O composition is, like all carbonates, sensitive to temperature (Candelier et al. 2013, Dudley et al. 1986); however, its application for relative paleothermometry is robust only for time periods without significant ice volume variations in locations where the local hydrological regime is thought to have been relatively stable over time, and absolute paleothermometry requires a constraint on the δ¹⁸O of seawater. Laboratory culture studies suggest relative insensitivity of coccolith δ¹⁸O to salinity changes at constant temperature and δ¹⁸O of growth medium (Hermoso & Lecasble 2018). However, on long timescales, seawater δ¹⁸O changes are not a sole direct result of salinity changes, ice volume/sea level changes do not scale linearly with seawater δ¹⁸O composition, and quantifying the relative contribution of seawater δ¹⁸O versus temperature to calcite δ¹⁸O under differing boundary conditions is complex. Mg/Ca ratios in planktic and benthic foraminiferal calcite are routinely used to reconstruct calcification temperature or SST. In coccoliths, although Mg/Ca may also be controlled by temperature, the challenge of removing noncarbonate sources of Mg from coccolith fractions has so far limited the application of coccolith Mg/Ca (Stoll et al. 2001).

## 2.2. Assemblages

Calcareous nannofossil assemblages are sensitive to temperature changes on short and longer timescales, although temperature responses can be difficult to decouple from concurrent nutrient-related responses. For example, major cooling during the middle Miocene is thought to have forced macroevolutionary changes including increased abundance and diversification of
reticulofenestrid coccoliths<fnref n="1" /> at all latitudes (Henderiks et al. 2020). During glacial-interglacial climate shifts in the Pleistocene, certain species show clear covariance with temperature (Marino et al. 2009). Thus, in addition to the geochemical methods described above, coccolith assemblage-based calibrations or transfer functions to reconstruct SST have been proposed. These include statistical model approaches to reconstruct mean annual SST from assemblage counts in the eastern Pacific Ocean (Saavedra-Pellitero et al. 2013, 2022) and a global paleothermometer based on the relative abundance of *Gephyrocapsa* morphotypes (Bollmann et al. 2002, Henderiks & Bollmann 2004).

# 3. PRODUCTIVITY

## 3.1. Coccolith Accumulation and Dissolution

One of the most direct indicators of past primary production is the sedimentary accumulation rate of biominerals from primary producers such as diatoms and coccolithophores. Coccolithophores are a fundamental component of oceanic primary production, and their abundance has been shown to increase in concert with other phytoplankton groups (Barber & Hiscock 2006, Bolton et al. 2010b). In the case of coccoliths, the accumulation rate in sediments depends not only on the balance between production in the surface ocean and export efficiency but also on the intensity of carbonate dissolution that varies with time, core depth, and past deep-ocean circulation. The accumulation of coccoliths can be used to provide a first order indication of paleoproductivity fluctuations over time in oceanographic settings well above the carbonate compensation depth where dissolution intensity is inferred to have remained constant over time. Beyond numerical counts of coccolith fluxes and accumulation rates, techniques for estimating individual coccolith size and mass (see Section 4.2) now allow for estimating past cell size and biovolume, as well as quantitative estimates of total and species- or group-specific coccolith CaCO₃ fluxes and mass accumulation rates (MARs) (Beaufort et al. 2021, Suchéras-Marx & Henderiks 2014, Valença et al. 2024).

<footnote n="1">1 Reticulofenestrid coccoliths is a term applied to coccoliths of the Noelaerhabdaceae family that all have the same basic structure as *Reticulofenestra*; it includes the *Cyclicargolithus-Reticulofenestra-Pseudoemiliania-Gephyrocapsa-Emiliania* lineage.</footnote>
Although some studies have sought to investigate coccolith accumulation in settings where dissolution is inferred to be constant, it is ideal to evaluate indicators of changing coccolith dissolution intensity (e.g., Flores et al. 2003). In the deep-sea fossil record, dissolution indices are crucial for isolating a potential dissolution signal from ecological ones and for assessing spatial or temporal trends in CaCO₃ preservation that may bias productivity reconstructions based on nannofossil assemblage composition, abundances and MARs, or geochemical records. Closely located sediment cores, presumed to feature similar coccolithophore assemblages and fluxes but recovered from different sea floor depths exposed to different dissolution intensities, provide the opportunity to evaluate the effect of varying dissolution on coccoliths. Examination of Pliocene-aged sediments across a depth transect of sites in the tropical Atlantic showed that nannofossil assemblages in deeper sites differed significantly from those of shallow sites, without obvious visual signs of poor preservation, and permitted an updated comprehensive dissolution susceptibility ranking of species (Gibbs et al. 2004b). Several indices are based on variations in the ratio between dissolution-resistant and dissolution-susceptible species. The CEX index and its variants use the different susceptibilities of fragile *Emiliania huxleyi* and other small *Gephyrocapsa* versus robust *Calcidiscus leptoporus* coccoliths (Boeckel & Baumann 2004, Bordiga et al. 2013, Dittert et al. 1999). Other studies have demonstrated the usefulness of an index based on a single species (reducing the potential interference of ecological changes), including the abundance of disarticulated (i.e., isolated distal or proximal shields) versus complete *Calcidiscus* placoliths<fnref n="2" /> (Bordiga et al. 2013, Marino et al. 2009, Matsuoka 1990, McIntyre & McIntyre 1971) and fragmented versus whole *Discoaster* specimens (Bolton et al. 2010a). Dissolution is not the only factor altering coccoliths after their production. In sediments, overgrowth of calcareous nannofossils with diagenetic calcite can also hinder species recognition and alter original geochemical signatures, and a thorough assessment of overgrowth—for example, using scanning electron microscope images and/or geochemical approaches (Dedert et al. 2014; Prentice et al. 2014; Suchéras-Marx et al. 2016, 2021a)—can be important for the interpretation of paleoproductivity records.

<footnote n="2">² A placolith is a heterococcolith type with a rim that has two or more well-developed shields.</footnote>
## 3.2. Assemblage-Based Reconstructions of Productivity and Nutricline Depth

Most of the diversity in living coccolithophore populations is made up of small, rare species with low preservation potential (Young et al. 2005), and coccolith diversity in surface sediments is significantly reduced compared to that of living coccolithophore populations in the overlying water column because of selective dissolution of fragile species (Andruleit et al. 2004, Saavedra-Pellitero & Baumann 2015). However, species with good preservation potential, representing around a quarter of living species (Young et al. 2005), still show distinct biogeographical distributions, depth stratification [i.e., upper photic zone and deep photic zone (DPZ) communities], and sensitivity to physical and chemical environmental conditions; thus, sediment assemblages or ratios between species are a powerful tool for reconstructing past oceanography, in particular nutrient conditions, ocean currents, and frontal movements (Baumann et al. 2005, Beaufort & Aubry 1990, Wells & Okada 1997) (Figure 1).

The use of assemblage composition to reconstruct past productivity is one of the broadest and most powerful applications of calcareous nannofossils in paleoceanography, from the Mesozoic (252 to 66 Ma) (e.g., Lees et al. 2005) to the Cenozoic (66 to 0 Ma) (e.g., Bolton et al. 2010a, Flores et al. 2012, Gibbs et al. 2006). Various species groups or ratios have been used to infer productivity regimes over the Plio-Pleistocene (5.33 to 0 Ma), including total *Discoaster* and *Sphenolithus* abundances (in numbers/mm²) (Gibbs et al. 2004a), *Discoaster* relative abundance (Imai et al. 2015), the ratio between *Reticulofenestra* and *Florisphaera profunda* coccoliths (Flores et al. 2000), or the relative abundance of cool-water mesotrophic species (Bolton et al. 2010a). Measurements on intact fossil coccospheres (cell size, coccolith size, and number of coccoliths per cell), exceptionally preserved in some clay-rich locations, have also been suggested to provide information on species-specific growth responses to oceanographic change in the past (Gibbs et al. 2013).

The existence of a DPZ coccolithophore community (Figure 1) in tropical to temperate regions has proven extremely useful in reconstructing past productivity and water column stratification. The abundance of coccoliths belonging to the species *F. profunda* relative to the total assemblage was first proposed as an indicator of nutricline depth in the equatorial Atlantic Ocean (Molfino & McIntyre 1990) and later as an indicator of turbidity (primarily controlled by productivity) in the northwest Pacific Ocean (Ahagon et al. 1993). In the modern ocean, *F. profunda*
*profunda* is a tropical-subtropical species most abundant in the DPZ (Hernández-Almeida et al. 2019a, Okada & Honjo 1973), and low relative abundances are associated with a shallow nutricline and higher overall productivity and turbidity, and vice versa. Although the extant DPZ community is quite diverse, *F. profunda* is essentially the only DPZ species preserved continuously in sediments, and its relative abundance is a robust indicator of past tropical-subtropical productivity fluctuations since it became abundant in the late Miocene–early Pliocene (e.g., Beaufort et al. 2001, McIntyre & Molfino 1996). The exact timing of the origination of *F. profunda* is unclear, although significant *F. profunda* relative abundances are documented back to 8–10 million years ago, or Ma (Šupraha & Henderiks 2020), and a gradual increase in *F. profunda* contribution to tropical-subtropical nannofossil assemblages from the late Miocene toward the Modern is observed (Boscolo-Galazzo et al. 2022). Regional and global calibrations of *F. profunda* relative abundance to satellite-derived net primary productivity (NPP) estimates have been proposed (Beaufort et al. 1997, Hernández-Almeida et al. 2019b, Saavedra-Pellitero et al. 2022) (Figure 2). Modern ocean NPP correlates positively with the seasonality of NPP, and recent data-model comparisons suggest that the relative abundance of *F. profunda* might actually represent the amplitude of the annual NPP cycle rather than total NPP per unit time because the former is more sensitive to precession (Beaufort & Sarr 2024). *F. profunda*'s thermal tolerance (>10°C) limits its use for productivity reconstructions to low and mid-latitudes, with the strongest relationship between ~30°N and 40°S, and its biogeographical range is likely restricted during glacial coolings. In some regions, *F. profunda* percent can be dominantly controlled by temperature or water column stratification (sometimes decoupled from productivity), and potential dissolution effects must also be considered (Hernández-Almeida et al. 2019b).
<figure><img src="image_2.png" /></figure>

Figure 2 NPP reconstructions based on the relative abundance of coccoliths belonging to the deep photic zone species *Florisphaera profunda*. (a) Percent *F. profunda* regressed with modern satellite-derived NPP. Original Indian Ocean surface sediment calibration is in green (Beaufort et al. 1997), and updated global 30°N to 30°S surface sediment calibration is in gray (Hernández-Almeida et al. 2019b). (b) An example of NPP reconstructed using *F. profunda* relative abundance over the past 150,000 years from a Banda Sea (western tropical Pacific Ocean) sediment core (Beaufort et al. 2010). See Supplemental Figure 1 for a map with site locations. Abbreviation: NPP, net primary productivity.

Identification of fossil coccoliths belonging to the extant DPZ genera *Gladiolithus*, *Algirosphaera*, and *Solisphaera* in exceptionally preserved late Paleocene to early Oligocene sediments from coastal Tanzania suggests that the DPZ ecological niche was already established at this time (Bown et al. 2009). However, coccoliths belonging to these DPZ genera are rare or easily overlooked in the fossil record because they tend to be small and fragile with low fossilization potential; thus, they have not been used in paleoceanographic studies.

### 3.3. Coccolith Sr/Ca ratios

Across productivity gradients in the ocean such as upwelling zones, the Sr/Ca ratio of coccoliths is observed to be higher in zones of highest export production, and the ratio has therefore been proposed as a productivity indicator (Stoll & Schrag 2000). Culture experiments show the Sr/Ca *Coccolithophores in Paleooceanography*
ratio to be relatively insensitive when increased light stimulates higher growth rates (Stoll et al. 2002a), and another culture study suggests that nutrient stimulation of productivity may be the dominant process contributing to variations across natural productivity gradients (Stoll et al. 2007c). Potential mechanisms for the variation in Sr/Ca ratios have been explored in cellular models additionally constrained by stable Ca isotopes, confirming that increased calcification rates promote higher coccolith Sr/Ca (Mejía et al. 2018). There is a significant difference in the range of Sr partitioning coefficients among different species, with extreme high values in the coccolithophore *Scyphosphaera apsteinii* (Guerreiro et al. 2024, Hermoso et al. 2017, Meyer et al. 2020) and partitioning about 50% higher in larger taxa such as *C. leptoporus* or *Helicosphara carteri* compared to *Gephyrocapsa* species and *E. huxleyi* (Stoll et al. 2002a). Consequently, the interpretation of fine-fraction Sr/Ca needs to account for the potential effects of changing assemblage composition (e.g., Guerreiro et al. 2024, Mejía et al. 2014, Tangunan et al. 2017). Additionally, Sr partitioning in cultures increases by ~0.03 mmol/mol per °C (Müller et al. 2014; Stoll et al. 2002a,b), which may need to be accounted for in some studies where temperature changes are significant, for example, in reconstructions spanning glacial-interglacial cycles or large climate transitions. For records spanning timescales longer than a few million years, potential changes in seawater Sr/Ca ratio also warrant consideration (Langer et al. 2006, Sosdian et al. 2012).

In the Holocene Mediterranean Sea, coccolith Sr/Ca indicates a significant increase in productivity in the eastern Mediterranean in an array of species during the time interval coinciding with deposition of sapropel S1, whereas coccolith Sr/Ca confirms stable productivity during the same interval in the western Mediterranean (Figure 3). Over the late Pleistocene, coccolith Sr/Ca has been employed to characterize changes in Arabian Sea upwelling (Stoll et al. 2007c), the upwelling response to Southern Hemisphere westerlies migration (Mejía et al. 2014), coccolithophore growth rates in the western tropical Pacific (Jin et al. 2018), and productivity in the equatorial Indian Ocean (Tangunan et al. 2017) and in the Pacific sector of the Southern Ocean (Saavedra-Pellitero et al. 2017). On longer timescales, coccolith fraction Sr/Ca has been used to infer changes in the production of bloom species (defined as *E. huxleyi*, *Gephyrocapsa caribbeanica*, and *Gephyrocapsa ericsonii* in the cited study) on 400 kyr timescales (Rickaby et al. 2007). Pliocene orbitally driven productivity cycles in the western tropical Atlantic have also *Coccolithophores in Paleooceanography*
been characterized with Sr/Ca (Waite et al. 2008). Sr/Ca has also been employed to evaluate productivity in deeper time. Because diagenetic carbonates typically have an order of magnitude lower Sr content than pristine coccoliths, appreciable diagenetic overgrowth may bias estimation of the primary Sr/Ca signal (Dedert et al. 2014). Separation of placolith-dominated fractions generally less susceptible to overgrowth than nannoliths such as *Discoaster* and *Sphenolithus*, or picking of individual placolith coccoliths for analysis by secondary ion mass spectrometry (SIMS), has been used to limit the influence of strongly overgrown nannofossils and coccoliths in older sediments (Stoll & Shimizu 2009, Stoll et al. 2007b). Sr/Ca records from SIMS suggest decreased tropical ocean productivity across the Paleocene–Eocene Thermal Maximum but elevated productivity in the southern high latitudes (Gibbs et al. 2010, Stoll et al. 2007a). Recent studies using synchrotron-based nanoXRF (X-ray fluorescence spectroscopy) mapping provide insight into Sr incorporation into coccoliths in relation to crystallography (Suchéras-Marx et al. 2021b).

<figure><img src="image_3.png" /><figcaption>Coccolithophores in Paleooceanography</figcaption></figure>
**Figure 3** Coccolith Sr/Ca as a productivity indicator in the eastern (a, Core BC07) and western (b, Core 274G) Mediterranean Sea in the Holocene spanning the time period of sapropel S1. Elevated Sr/Ca ratios indicate enhanced productivity in all examined species in the eastern Mediterranean during the time of sapropel deposition but constant productivity in the western Mediterranean. The contrasting absolute Sr/Ca ratios of different species are evident in monospecific picked populations (points, ion probe measurements, from Stoll et al. 2007b) as well as coccolith size fractions (points with lines, solution ICP-AES measurements, from Dedert et al. 2012). (a, inset) A scanning electron microscope image of populations of picked *Helicosphaera carteri* before ion probe analysis. Ba/Al is shown as an independent productivity indicator illustrating the time of sapropel deposition (gray shading). Ba/Al data in BC07 from Freydier et al. (2001) and in 274G from Martínez-Ruiz et al. (2003). See **Supplemental Figure 1** for a map with site locations. Abbreviation: ICP-AES, inductively coupled plasma-atomic emission spectroscopy.

**3.4. Other Trace Elements**

The application of other trace element ratios in coccoliths from marine sediments is currently more limited because most techniques are not able to physically separate coccoliths from co-occurring clays and Mn-Fe oxides. Compared to carbonate, these other phases are not as significant a source of Sr as they are for Mg or B, and SIMS is not yet sufficiently sensitive for reliable measurements of B in small populations of individually picked coccoliths (Diez Fernández et al. 2015). Consequently, these elements are useful for constraining biomineralization and ion transport processes in pure coccoliths grown in laboratory culture (Liu et al. 2021, Müller et al. 2011, Stoll et al. 2012) but currently have limited application for paleo-studies.

**4. OCEAN CARBON CYCLE PROCESSES**

Long-term adaptation of coccolithophores to decreasing $pCO_2$ over the Cenozoic has resulted in modern cells capable of actively enhancing $CO_2$ at the site of photosynthesis via carbon concentration mechanisms (CCMs), resulting in higher photosynthetic rates than those achievable if cells were solely reliant on passive $CO_2$ diffusion (Raven et al. 2012). This adaptation can be imprinted in the stable oxygen and carbon isotopic composition ($\delta^{18}$O, $\delta^{13}$C) of coccoliths during calcification. In addition, cell and coccolith size, degree of cellular calcification [cellular particulate inorganic carbon (PIC) to particulate organic carbon (POC) ratio, or PIC:POC], and coccolith $CaCO_3$ accumulation are thought to have responded to climate and carbon cycle drivers on various timescales. Thus, rather than allowing a direct reconstruction of past specific growth parameters, these isotopic and morphological coccolith proxies can reveal information on large-scale physiological adaptations to changes in ocean carbonate chemistry *Coccolithophores in Paleooceanography*
including aqueous CO₂ concentration ([CO₂]) in the geological past, permitting indirect inferences on climate evolution (e.g., Bolton & Stoll 2013).

**4.1. Manifestation of Coccolithophore Physiology in Coccolith δ¹³C**

Coccolithophore calcification occurs in dedicated intracellular vesicles, and coccolithophores are known to use CCMs, including pumping bicarbonate into the cell or into cellular compartments. As a result, biologically mediated processes lead to variable degrees of apparent isotopic disequilibria between coccolith calcite and external seawater, described as vital effects, which differ among species and cell sizes (Dudley et al. 1986, Ziveri et al. 2003). Laboratory culture studies and cellular models suggest that coccolith δ¹³C is an indicator of the processes of acquisition and allocation of dissolved inorganic carbon (DIC) by the cell, which is very sensitive to carbon availability (Bolton & Stoll 2013, Chauhan & Rickaby 2024, Holtz et al. 2017, McClelland et al. 2017, Stoll et al. 2019). The cell's intensity of bicarbonate pumping and allocation of carbon between calcification and photosynthesis influences the intracellular δ¹³C of DIC. When CO₂ is less available—either due to its lower external concentration or due to large cells having low surface area to volume ratios—the significance of CCMs increases. These biologically driven carbon uptake and transport processes give rise to significant differences in coccolith δ¹³C among modern species of different sizes and PIC:POC, which are of variable magnitude depending on [CO₂]. In low [CO₂] cultures, there is an up to 5‰ (Ziveri et al. 2003) range in δ¹³C among different species, but in culture experiments with high [CO₂], a much smaller range in δ¹³C in coccoliths from small versus large cells is measured (Hermoso et al. 2016, Le Guevel et al. 2024, Rickaby et al. 2010).

For paleoceanographic applications using coccoliths from sediments, isotopic analyses can be performed on bulk coccolith fractions (e.g., <20 µm); however, these results need to be interpreted in the context of changing species contributions to total calcite mass (with large assemblage changes often associated with major climate or carbon cycle transitions). Repeated decanting, microfiltration, and centrifugation methods have been developed to separate narrow size fractions of coccoliths containing concentrated species/groups (Bolton et al. 2012; Minoletti et al. 2001, 2009; Stoll & Ziveri 2002; Zhang et al. 2018, 2021). Therefore, for paleo-proxy applications, coccolith δ¹³C measurements are generally performed on restricted size fractions
inferred to reflect a limited range of cell sizes and potentially a limited range of species or genera.

The need for efficient CCMs is greater for large cells than small cells due to their smaller surface area to volume ratio. Thus, comparing coccolith δ¹³C among coeval sediment fractions dominated by large and small coccoliths, assumed to be precipitated from seawater of identical δ¹³C DIC, isolates the differential physiological effects. The range of δ¹³C vital effects, measured as the difference between the δ¹³C of coccoliths precipitated by small versus large cells (or Δ¹³Csmall-large), increased significantly in the late Miocene (Figure 4). This was interpreted to reflect increased intensity of CCMs for photosynthesis, especially in larger coccolithophores, with declining [CO₂] (Bolton & Stoll 2013, Bolton et al. 2016). Smaller increases in Δ¹³Csmall-large from the latest Eocene to the earliest Oligocene (Tremblin et al. 2016) and during the Miocene Climatic Transition (~14 Ma) (Hermoso et al. 2020) were also interpreted to reflect decreasing [CO₂] (Figure 4).

<figure><img src="image_4.png" /></figure>

Figure 4 The range of coccolith δ¹³C vital effects over the past 60 Ma, expressed as the difference between the δ¹³C of small (~2–5 µm) and large (~8–12 µm) coccoliths (Δ¹³Csmall-large). The error bar represents the propagated analytical uncertainty, assuming analytical uncertainty of 0.08‰ for δ¹³C measurements. See Supplemental Table 1 for data, sources, and exact coccolith size fractions used to calculate Δ¹³Csmall-large for each dataset. Age models are as in original publications. See Supplemental Figure 1 for a map with site locations. Abbreviation: ODP, Ocean Drilling Program.
Where a species of planktic foraminifera can be inferred to have a similar habitat depth and seasonality as coeval coccoliths and its species-specific vital effects are known (i.e., δ¹³C of DIC can be estimated), the absolute carbon isotopic fractionation of different coccolith fractions can be calculated as Δ¹³C_coccolith-DIC (= δ¹³C_coccolith fraction – δ¹³C_DIC). Over the past 10 Ma, the Δ¹³C_coccolith-DIC of large coccoliths (~8–12 µm) decreased by nearly 2‰ in a tropical Atlantic core, interpreted to reflect the increasing carbon limitation experienced by large cells (Bolton et al. 2016). The Δ¹³C_coccolith-DIC for the large coccolith fraction shows a large (nearly 2‰) transient decline over the latest Eocene with a partial recovery in the early Oligocene, similarly interpreted to reflect CO₂ limitation of larger cells (calculated in Stoll et al. 2019 using data from Tremblin et al. 2016). In the past 10 million years, the Δ¹³C_coccolith-DIC for smaller (~2–5 µm) coccoliths remained more stable than for large coccoliths, varying only ~0.75‰. The long-term comparable stability of the Δ¹³C_coccolith-DIC of the small coccolith fraction is consistent with culture studies of *Gephyrocapsa oceanica* under variable [CO₂] (Le Guevel et al. 2024, Rickaby et al. 2010).

These results support the practice of using the δ¹³C of small coccoliths to estimate δ¹³C of DIC to calculate the fractionation into photosynthetically fixed organic matter (εₚ) for pCO₂ proxy reconstructions because in culture δ¹³C_coccoliths-organic matter is highly correlated with δ¹³C_DIC-organic matter (Torres Romero et al. 2024).

Nonetheless, over Pleistocene glacial-interglacial cycles, variation in the Δ¹³C_coccolith-DIC of small coccolith fractions has been detected in studies employing higher-resolution sampling. In cores MD95-2037 (Atlantic) and IODP Site U1443 (Indian), Δ¹³C_coccolith-DIC is around 1‰ higher during glacial periods when [CO₂] was reduced (Bolton et al. 2018, Godbillot et al. 2022). However, at ODP Site 925 (Atlantic), the up to 1.5‰ variation in Δ¹³C_coccolith-DIC of *Gephyrocapsa* coccoliths is unrelated to [CO₂] over glacial cycles (González-Lanchas et al. 2021). In the western tropical Pacific, precession-paced maxima in Δ¹³C_coccolith-DIC of small reticulofenestrid coccoliths (2‰ range) coincide with maxima in coccolith PIC export (Jin et al. 2024). In addition to reflecting varying coccolithophore fractionation, this variation in the Δ¹³C_coccolith-DIC of small coccolith fractions may also be in part a product of variation in foraminiferal vital effects over glacial-interglacial cycles due to changes in surface ocean carbonate ion concentration (Spero et al. 1999).
**4.2. Manifestation of Evolution or Adaptation in Coccolith Morphology**

Calcareous nannofossils have been an unparalleled tool in biostratigraphy since the 1950s, thanks to their fast evolutionary turnover, their abundance, and the synchronous nature of origination, extinction, and size-change events across most oceans (e.g., Bown 1998, Martini 1971, Raffi et al. 2006). The evolution and diversity of calcareous nannofossils have responded to both abrupt and gradual climate changes in the geological past, with higher diversity generally occurring during warmer climates of the Cenozoic (Bown et al. 2004, de Vargas et al. 2007). Some groups or species, e.g., *Coccolithus pelagicus* (Henderiks & Rickaby 2007) and *Calcidiscus* (Knappertsbusch 2000), show highly conservative morphologies over time. Others, notably the reticulofenestrids, display large temporal size and mass shifts and a high diversity of coccolith morphotypes, sizes, and masses within living communities and single-sample fossil populations. The development of different techniques (microscopy or coulter-counter based; some automated) to accurately measure size or mass of coccoliths now allows the generation of large datasets spanning long time periods at high resolution (Beaufort et al. 2021, Valença et al. 2024), providing new insights into morphological changes and their drivers.

**4.2.1. Coccolith size.**

The Noelaerhabdaceae, or reticulofenestrids, are a cosmopolitan and long-lived family that evolved in the Eocene, and their coccoliths dominate most Neogene nannofossil assemblages. Reticulofenestrid coccoliths have been the focus of most studies of coccolith size evolution and are thought to correlate with mean cell size changes at the population level (Sheward 2016, Suchéras-Marx et al. 2022). Reticulofenestrid size changes can act as biostratigraphic markers due to their global synchronicity (Beaufort et al. 2022, Kameo & Takayama 1999) and can provide clues on evolving climatic conditions that constitute selective pressures on cell size (Hannisdal et al. 2012, Henderiks & Pagani 2008, Herrmann & Thierstein 2012).

From the early Cenozoic to the present, coccolith size generally decreases at the whole-assemblage level (Herrmann & Thierstein 2012). In our new global compilation of reticulofenestrid coccolith size spanning the past 40 million years (Figure 5; Supplemental Table 2), we resolve shorter-term size changes that are superimposed on the long-term decrease in mean size and size range (Beaufort et al. 2022, Bolton et al. 2016, Guitián et al. 2020,
Henderiks & Pagani 2008, Imai et al. 2015, Ma et al. 2024, Pagani et al. 2011, Tanner et al. 2024, Young 1990). Major size decreases are seen at the Eocene–Oligocene transition, in the middle Oligocene, in the late Miocene (~9 Ma), and in the early Pliocene (~5 Ma). On the other hand, clear size increases occur in the early Miocene (~20–24 Ma), the mid-Miocene (~15–9 Ma), the late Miocene–early Pliocene (~8–5 Ma), and the last ~2 Ma that are less clearly correlated with global climate (pCO₂ or deep-sea δ¹⁸O) trends (Figure 5). Significant gaps in the record occur during the middle Miocene and the Eocene, where to our knowledge whole-population reticulofenestrid size measurements have not yet been published. Although limited data are available for other coccolith groups, over the past 15 million years, a small decrease in the size and volume of *Helicosphaera* coccoliths has also been documented (Šupraha & Henderiks 2020). Size trends in *Calcidiscus* coccoliths since the early Miocene show relatively constant values and a size maximum occurring in the late Miocene (Knappertsbusch 2000). For near-spherical cells such as coccolithophores, smaller cell sizes provide a higher surface area to volume ratio, so a small cell size can be advantageous for assimilation when aqueous CO₂ or nutrients are at low concentrations (Marañón et al. 2013). Yet, the role of resource scarcity (e.g., declining Cenozoic CO₂ concentration or changes in nutrient availability) as a selective pressure on cell size and macroevolutionary changes remains a question of much discussion in the community and warrants further investigation (Bolton et al. 2016, Guitián et al. 2020, Henderiks & Pagani 2008, Ma et al. 2024, Marañón 2015, Young 1990).
<figure><img src="image_5.png" /><figcaption>**Figure 5** Long-term changes in coccolith size over the past 40 Ma in relation to climate. (a) Cenozoic global reference benthic foraminiferal oxygen isotope dataset (Westerhold et al. 2020). (b) 500-thousand-year smoothed multi-proxy atmospheric pCO₂ reconstruction (Hönisch et al. 2023). (c) Reticulofenestrid coccolith length. Points represent mean length values, and bars represent the ninety-fifth and fifth percentiles of the size distribution for each sample, where available. Age models and adopted species concepts are as in original publications. See **Supplemental Table 2** for coccolith size data compilation and sources. See **Supplemental Figure 1** for a map with site locations. Abbreviations: DSDP, Deep Sea Drilling Project; IODP, International Ocean Discovery Program; ODP, Ocean Drilling Program.</figcaption></figure>

*Coccolithophores in Paleooceanography*
In the Plio-Pleistocene, the alternating dominance of reticulofenestrid coccoliths with smaller versus larger coccoliths appears to be a global signal (captured in the morphological divergence index), and has been linked to climate cycles driven by eccentricity (100 and 400 kyr timescales). This alternating dominance of morphotypes impacts the carbon cycle via modulation of coccolith MARs—which are highest when coccolithophores producing smaller coccoliths proliferate (Beaufort et al. 2022). These fossil morphological changes have been linked to rapid species radiation events in the reticulofenestrids based on genomic analyses (Bendif et al. 2019, 2023).

### 4.2.2. Coccolith calcification.

Coccolith calcite production is estimated to contribute around 50% of pelagic calcite production in the modern ocean; thus, coccolithophores are a major player in the ocean carbonate pump (Neukermans et al. 2023). Unlike the larger tests of planktic foraminifera that often sink independently, small coccoliths have been proposed to be a significant source of mineral ballast in aggregates in the global ocean, enhancing the efficiency of organic carbon export from the surface ocean and hence the biological pump (Le Moigne et al. 2014, Ziveri et al. 2007). There has also been concern that coccolithophore calcification may be affected by ocean acidification (Beaufort et al. 2011, Meyer & Riebesell 2015). These observations have motivated interest in evaluating the degree of cellular calcification of coccolithophorids over time and its response to ocean [CO₂] and other oceanographic parameters. Estimating calcification, either as the calcite per cell surface area or the PIC:POC ratio, requires estimating the thickness of coccoliths that would have covered the living cell. The first study to estimate coccolith mass based on morphology used coccolith dimensions, species-specific correction factors, and calcite density (Beaufort & Heussner 1999). Subsequently, Young & Ziveri (2000) developed the dimensionless parameter *k*<sub>s</sub> as a measure of coccolith volume using a similar method with *k*<sub>s</sub> being the fraction of volume of a cube that is occupied by the volume of a coccolith, where the cube length is given by the coccolith length. Among coccoliths of similar length, *k*<sub>s</sub> will covary with coccolith thickness, but it cannot predict PIC:POC ratios when coccolith length is also evolving.

The use of birefringence of coccolith calcite under polarized light microscopy provided a method to efficiently quantify individual coccolith mass on large numbers of coccoliths, to study
the variations of population mean mass over time and space (Beaufort 2005). The subsequent
development of circular polarized light microscopy has improved the precision of coccolith area
and therefore thickness and mass estimates (Beaufort et al. 2021, Bollmann 2014, Fuertes et al.
2014). Earlier birefringence-based techniques were applicable only to coccoliths in the thickness
range 0 to 1.55 µm, and characterizing the thicker coccoliths prevalent in the earlier Neogene
and Paleocene (up to 4 µm) required additional method development and calibration (Beaufort et
al. 2014, González-Lemos et al. 2018, Guitián et al. 2022). Bidirectional circular polarization,
which presents the advantage of not requiring calibration or constancy of microscope light
parameters, allows for the measurements of coccoliths of up to 2.2 µm thickness with the use of
red light during image acquisition (Beaufort et al. 2021).

Reticulofenestrids are well-suited to estimates of degree of calcification because the c-axis of
the majority of the coccoliths has a radial orientation. Calcification cannot be as effectively
quantified for other lineages with significant calcite with a vertically oriented c-axis (e.g.,
*Calcidiscus*, *Helicosphaera*), although relative changes in morphology and mass over time for
these genera have been quantified (Cubillos et al. 2012, Šupraha & Henderiks 2020).

The first study of long-term changes in calcification focused on reticulofenestrids smaller
than 5 µm and showed that, for a given coccolith size, coccolith thickness and *k*<sub>s</sub> decreased
significantly over the past 14 million years, concomitant with declining atmospheric CO<sub>2</sub> (Bolton
et al. 2016). This decline was attributed to progressive CO<sub>2</sub> limitation and reallocation of
resources to pump bicarbonate into the cell for photosynthesis rather than calcification. Using
culture calibrations of the relationship between calcite carbon per cell surface area and coccolith
thickness (Bolton et al. 2016), recent quantifications of coccolith thickness for the full size range
of reticulofenestrid coccoliths allow estimation of the PIC:POC ratio of this lineage over the past
28 million years (Guitián et al. 2022, Tanner et al. 2024) (Figure 6). PIC:POC ratios exhibit
substantial variability within a given population, as well as both short-term and long-term
variation. Given the presence of short-term variation where data resolution is higher, it is
possible that long-term trends may not be robustly estimated where data density is low.
Nonetheless, for this culture calibration, the data suggest that the average reticulofenestrid
PIC:POC ratio was around 0.9 to 1 in the Oligocene to early Miocene, similar to values of the
past 3 million years (Figure 6). PIC:POC extending to significantly higher values (up to 1.5)

Coccolithophores in Paleoceanography
characterized the early late Miocene, followed by a decline in average PIC:POC between about 7 and 5 Ma. PIC:POC averaged over the past 3 million years was potentially 25% lower than during the 6.5 to 8.5 Ma period. The late Miocene reticulofenestrid PIC:POC decline coincides with the decline in $k_s$ of small (<5 µm) coccoliths observed across tropical sites (Bolton et al. 2016). In contrast to reticulofenestrid coccoliths, estimated PIC:POC in *Helicosphaera* was relatively stable over the past 15 million years, despite decreasing coccolith sizes (Šupraha & Henderiks 2020).
<figure><img src="image_6.png" /><figcaption>Coccolithophores in Paleooceanography</figcaption></figure>
**Figure 6** Coccolith calcification indices over the past 30 Ma and nannofossil CaCO₃ flux to sediments since 15 Ma. (a) Average coccolith length, (b) average coccolith thickness, (c) average $k_s$ value, and (d) average estimated PIC:POC ratio, all from the same reticulofenestrid coccolith populations from three sites. Error bars show ±1 standard deviation. Diamond symbols show data for coccoliths in the 3.5-µm to 4.5-µm range only. Data from Bolton et al. (2016) [ODP Site 925 Miocene to Pleistocene, remeasured with calibration using calcite wedge as presented in Tanner et al. (2024), González-Lanchas et al. (2021) (ODP Site 925 Pleistocene), Tanner et al. (2024) (ODP Site 926), and Guitián et al. (2022) (IODP Site 1406)]. PIC:POC ratios are calculated from the thickness versus PIC/cell surface area relationship presented by Bolton et al. (2016), recalculated using a sigmoidal calibration with a calcite wedge as reported by González-Lemos et al. (2018). (e) Nannofossil CaCO₃ flux estimates from various sites where records are not thought to be significantly biased by dissolution. Data from Si & Rosenthal (2019) (lines) and Suchéras-Marx & Henderiks (2014) (points with error bars representing propagated ±95% confidence interval). (e, inset) The relationship between estimated PIC:POC and coccolith length as a function of age. See Supplemental Figure 1 for a map with site locations. Abbreviations: IODP, Integrated Ocean Drilling Program; ODP, Ocean Drilling Program; PIC, particulate inorganic carbon; POC, particulate organic carbon.

The overall production of coccolithophorid cells is likely limited by nutrients such as nitrogen, phosphorus, and trace nutrients essential to growth. The variations in reconstructed PIC:POC indicate that for a given supply of nutrients to generate coccolithophorid biomass, there may be modest variations in the amount of calcite generated. This is in addition to ecosystem-level variations in the relative abundance of coccolithophores and other calcifying plankton (foraminifera, pteropods) to noncalcifying phytoplankton.

### 4.3. Impact of Changing Coccolith Production Through the Cenozoic

Records of deep-sea CaCO₃ MARs indicate a decline in the rates of total carbonate accumulation since the mid-Miocene. In the mid-Miocene, open ocean carbonate burial was dominated by coccoliths and nannoliths (60–85%) (Si & Rosenthal 2019), but today carbonate is approximately equally split between coccoliths and planktic foraminifera (Baumann et al. 2004, Broecker & Clark 2009, Frenz et al. 2005). Burial fluxes of planktic foraminifera are comparably stable since the Miocene (Si & Rosenthal 2019), whereas across a range of sites, the nannofossil CaCO₃ flux decreased nearly an order of magnitude since the mid-Miocene (Si & Rosenthal 2019, Suchéras-Marx & Henderiks 2014) (Figure 6e). Reduced foraminiferal fragmentation since the late Miocene suggests that carbonate preservation has overall improved (Si & Rosenthal 2019) and that decreased coccolith carbonate production is the main cause of reduced carbonate accumulation in sediments. The steepest decline in coccolith CaCO₃ flux occurred in the past 4–5 million years (Si & Rosenthal 2019, Suchéras-Marx & Henderiks 2014). Because the coccolith CaCO₃ production depends both on the PIC:POC ratio of each cell and on the total
coccolithophore biomass, increased overall biomass production in some regions during the late Miocene biogenic bloom (Pillot et al. 2023) may have sustained coccolith CaCO₃ production between 8 and 4 Ma despite decreasing PIC:POC ratios in the dominant reticulofenestrids. At the same time, an order of magnitude decrease in coccolith CaCO₃ MARs after 5 Ma, compared to an only 25% decrease in coccolith PIC:POC ratio, suggests that decreasing coccolith CaCO₃ accumulation cannot be due only to changes in the degree of cellular calcification but must additionally reflect decreases in coccolithophore cell production.

## 5. CONCLUSIONS

Calcareous nannofossils endure as a key tool in paleoceanography by providing accurate biostratigraphic age constraints that underpin the interpretation of other proxies and by sensitively recording past oceanographic conditions on short and long timescales. Calcareous nannofossils have proven particularly useful in reconstructing past productivity regimes, via both assemblage-based and geochemical (Sr/Ca) methods. Recent and ongoing development of the coccolith clumped isotope paleothermometer also shows promise for directly deriving ocean mixed-layer temperature at the time of calcification. Ocean carbonate chemistry is another key area in which geochemical and morphological coccolith-based proxies can reveal important information. Coccolith stable isotopes in size-restricted fractions can provide indirect evidence for cellular physiological adaptation to changing [CO₂] over geological time. Although culture studies on single strains under controlled conditions are invaluable for a mechanistic understanding of coccolith stable isotopes in the fossil record, field data from coccoliths sampled in the modern ocean would also contribute to a clearer interpretation of fossil coccolith δ¹⁸O and δ¹³C, the coupling between them, and the relative importance of [CO₂] versus other parameters (e.g., light, nutrients). Changes in individual coccolith size and calcification (PIC:POC) over time can now be accurately measured with advanced microscope techniques, and new automated methods permit the generation of large, high-resolution datasets. These datasets will open new avenues of research that will contribute to a better understanding of the drivers of size and calcification changes in the fossil record on different timescales (e.g., evolution, temperature, resource limitation including nutrients and [CO₂]). The role of coccolith carbonate production
and export in the geological carbon cycle is still poorly quantified; however, evolving methods combining accurate coccolith mass and abundance determination with other sedimentological data will provide a clearer picture in the future.

## DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.

## ACKNOWLEDGMENTS

We thank Jorijntje Henderiks, Jeremy Young, Baptiste Suchéras-Marx, Harry McClelland, Louis Claxton, Weimin Si, Iván Hernández-Almeida, and Luc Beaufort for providing published data, digitizing their data, or clarifying certain aspects of their datasets. We thank Baptiste Suchéras-Marx and Luc Beaufort for comments on a draft of the manuscript. This review benefited from financial support from IODP France (to C.T.B.), ANR (Project ANR-22-EDIR-0003-01 to C.T.B.), and SNF (Award 200021_182070 to H.M.S.). This review uses data from sediment samples provided by the International Ocean Discovery Program and its predecessor programs (DSDP, ODP, IODP). This manuscript is a contribution of the Climate Research Group at CEREGE (C.T.B.).

## LITERATURE CITED

* Ahagon N, Tanaka Y, Ujiie H. 1993. *Florisphaera profunda*, a possible nannoplankton indicator of late Quaternary changes in sea-water turbidity at the northwestern margin of the Pacific. *Mar. Micropaleontol.* 22:255-73

* Andruleit H, Rogalla U, Stäger S. 2004. From living communities to fossil assemblages: origin and fate of coccolithophores in the northern Arabian Sea. *Micropaleontology* 50:5-21

* Archer DE. 1996. An atlas of the distribution of calcium carbonate in sediments of the deep sea. *Glob. Biogeochem. Cycles* 10:159-74

* Balch WM. 2018. The ecology, biogeochemistry, and optical properties of coccolithophores. *Annu. Rev. Mar. Sci.* 10:71-98

*Coccolithophores in Paleoceanography*
Barber R, Hiscock M. 2006. A rising tide lifts all phytoplankton: growth response of other phytoplankton taxa in diatom-dominated blooms. *Glob. Biogeochem. Cycles* 20:GB4S03

Baumann K-H, Andruleit H, Böckel B, Geisen M, Kinkel H. 2005. The significance of extant coccolithophores as indicators of ocean water masses, surface water temperature, and palaeoproductivity: a review. *Paläontol. Z.* 79:93–112

Baumann K-H, Böckel B, Frenz M. 2004. Coccolith contribution to South Atlantic carbonate sedimentation. In *Coccolithophores: From Molecular Processes to Global Impact*, ed. HR Thierstein, JR Young, pp. 367–402. Berlin: Springer

Beaufort L. 2005. Weight estimates of coccoliths using the optical properties (birefringence) of calcite. *Micropaleontology* 51:289–97

Beaufort L, Aubry MP. 1990. Fluctuations in the composition of late Miocene calcareous nannofossil assemblages as a response to orbital forcing. *Paleoceanography* 5:845–65

Beaufort L, Barbarin N, Gally Y. 2014. Optical measurements to determine the thickness of calcite crystals and the mass of thin carbonate particles such as coccoliths. *Nat. Protoc.* 9:633–42

Beaufort L, Bolton CT, Sarr A-C, Suchéras-Marx B, Rosenthal Y, et al. 2022. Cyclic evolution of phytoplankton forced by changes in tropical seasonality. *Nature* 601:79–84

Beaufort L, Couapel M, Buchet N, Claustre H, Goyet C. 2008. Calcite production by coccolithophores in the south east Pacific Ocean. *Biogeosciences* 5:1101–17

Beaufort L, de Garidel-Thoron T, Mix AC, Pisias NG. 2001. ENSO-like forcing on oceanic primary production during the late Pleistocene. *Science* 293:2440–44

Beaufort L, Gally Y, Suchéras-Marx B, Ferrand P, Duboisset J. 2021. A universal method for measuring the thickness of microscopic calcite crystals, based on bidirectional circular polarization. *Biogeosciences* 18:775–85

Beaufort L, Heussner S. 1999. Coccolithophorids on the continental slope of the Bay of Biscay—production, transport and contribution to mass fluxes. *Deep-Sea Res. II* 46:2147–74

Beaufort L, Kaars S, Bassinot F, Moron V. 2010. Past dynamics of the Australian monsoon: precession, phase and links to the global monsoon concept. *Clim. Past* 6:695–706

Beaufort L, Lancelot Y, Camberlin P, Cayre O, Vincent E, et al. 1997. Insolation cycles as a major control of equatorial Indian Ocean primary production. *Science* 278:1451–54

*Coccolithophores in Paleoceanography*
Beaufort L, Probert I, de Garidel-Thoron T, Bendif E, Ruiz-Pino D, et al. 2011. Sensitivity of coccolithophores to carbonate chemistry and ocean acidification. *Nature* 476:80–83

Beaufort L, Sarr A-C. 2024. Eccentricity forcing on tropical ocean seasonality. *Clim. Past* 20:1283–301

Bendif EM, Nevado B, Wong EL, Hagino K, Probert I, et al. 2019. Repeated species radiations in the recent evolution of the key marine phytoplankton lineage *Gephyrocapsa*. *Nat. Commun.* 10:4234

Bendif EM, Probert I, Archontikis OA, Young JR, Beaufort L, et al. 2023. Rapid diversification underlying the global dominance of a cosmopolitan phytoplankton. *ISME J.* 17:630–40

Boeckel B, Baumann K-H. 2004. Distribution of coccoliths in surface sediments of the south-eastern South Atlantic Ocean: ecology, preservation and carbonate contribution. *Mar. Micropaleontol.* 51:301–20

Bollmann J. 2014. Weight approximation of coccoliths using a circular polarizer and interference colour derived retardation estimates—(the CPR Method). *Biogeosciences* 11:1899–910

Bollmann J, Henderiks J, Brabec B. 2002. Global calibration of *Gephyrocapsa* coccolith abundance in Holocene sediments for paleotemperature assessment. *Paleoceanography* 17:7–1–7–9

Bolton CT, Gibbs SJ, Wilson PA. 2010a. Evolution of nutricline dynamics in the equatorial Pacific during the late Pliocene. *Paleoceanography* 25:PA1207

Bolton CT, Hernández-Sánchez MT, Fuertes M-A, González-Lemos S, Abrevaya L, et al. 2016. Decrease in coccolithophore calcification and CO₂ since the middle Miocene. *Nat. Commun.* 7:10284

Bolton CT, Lawrence KT, Gibbs SJ, Wilson PA, Cleaveland LC, Herbert TD. 2010b. Glacial–interglacial productivity changes recorded by alkenones and microfossils in late Pliocene eastern equatorial Pacific and Atlantic upwelling zones. *Earth Planet. Sci. Lett.* 295:401–11

Bolton CT, Stoll HM. 2013. Late Miocene threshold response of marine algae to carbon dioxide limitation. *Nature* 500:558–62

Bolton CT, Stoll HM, Mendez Vicente A. 2012. Vital effects in coccolith calcite: Cenozoic climate-$p$CO$_2$ drove the diversity of carbon acquisition strategies in coccolithophores? *Paleoceanography* 27:PA4204
Bolton CT, Yamamoto M, Seki O, Stoll HM, Phelps SR, et al. 2018. *Carbon trading in a low CO₂ world: understanding carbon isotopic fractionation in coccolithophores over glacial-interglacial cycles*. Presented at Am. Geophys. Union Fall Meeting, Washington, DC, Dec. 10–14

Bordiga M, Beaufort L, Cobianchi M, Lupi C, Mancin N, et al. 2013. Calcareous plankton and geochemistry from the ODP site 1209B in the NW Pacific Ocean (Shatsky Rise): new data to interpret calcite dissolution and paleoproductivity changes of the last 450 ka. *Palaeogeogr. Palaeoclimatol. Palaeoecol.* 371:93–108

Boscolo-Galazzo F, Jones A, Dunkley Jones T, Crichton KA, Wade BS, Pearson PN. 2022. Late Neogene evolution of modern deep-dwelling plankton. *Biogeosciences* 19:743–62

Bown PR, ed. 1998. *Calcareous Nannofossil Biostratigraphy*. Dordrecht, Neth.: Springer

Bown PR, Dunkley Jones T, Young J, Randell R. 2009. A Palaeogene record of extant lower photic zone calcareous nannoplankton. *Palaeontology* 52:457–69

Bown PR, Lees JA, Young JR. 2004. Calcareous nannoplankton evolution and diversity through time. In *Coccolithophores: From Molecular Processes to Global Impact*, ed. HR Thierstein, JR Young, pp. 481–508. Berlin: Springer

Broecker W, Clark E. 2009. Ratio of coccolith CaCO₃ to foraminifera CaCO₃ in late Holocene deep sea sediments. *Paleoceanography* 24:PA3205

Broecker WS, Peng TH. 1987. The role of CaCO₃ compensation in the glacial to interglacial atmospheric CO₂ change. *Glob. Biogeochem. Cycles* 1:15–29

Candelier Y, Minoletti F, Probert I, Hermoso M. 2013. Temperature dependence of oxygen isotope fractionation in coccolith calcite: a culture and core top calibration of the genus *Calcidiscus*. *Geochim. Cosmochim. Acta* 100:264–81

Chauhan N, Rickaby RE. 2024. Size-dependent dynamics of the internal carbon pool drive isotopic vital effects in calcifying phytoplankton. *Geochim. Cosmochim. Acta* 373:35–51

Clark AJ, Torres-Romero I, Jaggi M, Bernasconi SM, Stoll HM. 2024. A clumped isotope calibration of coccoliths at well-constrained culture temperatures for marine temperature reconstructions. *Clim. Past* 20:2081–101

Cubillos JC, Henderiks J, Beaufort L, Howard WR, Hallegraeff GM. 2012. Reconstructing calcification in ancient coccolithophores: individual coccolith weight and morphology of *Coccolithophores in Paleooceanography*
*Coccolithus pelagicus* (sensu lato). *Mar. Micropaleontol.* 92–93:29–39

de Vargas C, Aubry M-P, Probert I, Young J. 2007. Origin and evolution of coccolithophores: from coastal hunters to oceanic farmers. In *Evolution of Primary Producers in the Sea*, ed. PG Falkowski, AH Knoll, pp. 251–85. Amsterdam: Elsevier

Dedert M, Stoll H, Kars S, Young JR, Shimizu N, et al. 2014. Temporally variable diagenetic overgrowth on deep-sea nannofossil carbonates across Palaeogene hyperthermals and implications for isotopic analyses. *Mar. Micropaleontol.* 107:18–31

Dedert M, Stoll HM, Kroon D, Shimizu N, Kanamaru K, Ziveri P. 2012. Productivity response of calcareous nannoplankton to Eocene Thermal Maximum 2 (ETM2). *Clim. Past* 8:977–93

Diez Fernández S, Ruiz Encinar J, Sanz-Medel A, Isensee K, Stoll HM. 2015. Determination of low B/Ca ratios in carbonates using ICP-QQQ. *Geochem. Geophys. Geosyst.* 16:2005–14

Dittert N, Baumann K-H, Bickert T, Henrich R, Huber R, et al. 1999. Carbonate dissolution in the deep-sea: methods, quantification and paleoceanographic application. In *Use of Proxies in Paleoceanography: Examples from the South Atlantic*, ed. G Fischer, G Wefer, pp. 255–84. Berlin: Springer

Drury AJ, John CM. 2016. Exploring the potential of clumped isotope thermometry on coccolith-rich sediments as a sea surface temperature proxy. *Geochem. Geophys. Geosyst.* 17:4092–104

Dudley WC, Blackwelder P, Brand L, Duplessy JC. 1986. Stable isotopic composition of coccoliths. *Mar. Micropaleontol.* 10:1–8

Flores J-A, Bárcena M, Sierro F. 2000. Ocean-surface and wind dynamics in the Atlantic Ocean off Northwest Africa during the last 140 000 years. *Palaeogeogr. Palaeoclimatol. Palaeoecol.* 161:459–78

Flores J-A, Filippelli GM, Sierro FJ, Latimer J. 2012. The “White Ocean” hypothesis: a late Pleistocene Southern Ocean governed by coccolithophores and driven by phosphorus. *Front. Microbiol.* 3:233

Flores J-A, Marino M, Sierro FJ, Hodell DA, Charles CD. 2003. Calcareous plankton dissolution pattern and coccolithophore assemblages during the last 600 kyr at ODP Site 1089 (Cape Basin, South Atlantic): paleoceanographic implications. *Palaeogeogr. Palaeoclimatol. Palaeoecol.* 196:409–26
Frenz M, Baumann K-H, Boeckel B, Höppner R, Henrich R. 2005. Quantification of foraminifer and coccolith carbonate in South Atlantic surface sediments by means of carbonate grain-size distributions. *J. Sediment. Res.* 75:464–75

Freydier R, Michard A, De Lange G, Thomson J. 2001. Nd isotopic compositions of Eastern Mediterranean sediments: tracers of the Nile influence during sapropel S1 formation? *Mar. Geol.* 177:45–62

Fuertes M-Á, Flores J-A, Sierro FJ. 2014. The use of circularly polarized light for biometry, identification and estimation of mass of coccoliths. *Mar. Micropaleontol.* 113:44–55

Gibbs SJ, Bown PR, Ward BA, Alvarez SA, Kim H, et al. 2020. Algal plankton turn to hunting to survive and recover from end-Cretaceous impact darkness. *Sci. Adv.* 6:eabc9123

Gibbs SJ, Bralower TJ, Bown PR, Zachos JC, Bybell LM. 2006. Shelf and open-ocean calcareous phytoplankton assemblages across the Paleocene–Eocene Thermal Maximum: implications for global productivity gradients. *Geology* 34:233–36

Gibbs SJ, Poulton AJ, Bown PR, Daniels CJ, Hopkins J, et al. 2013. Species-specific growth response of coccolithophores to Palaeocene–Eocene environmental change. *Nat. Geosci.* 6:218–22

Gibbs S, Shackleton N, Young J. 2004a. Orbitally forced climate signals in mid-Pliocene nannofossil assemblages. *Mar. Micropaleontol.* 51:39–56

Gibbs SJ, Shackleton NJ, Young JR. 2004b. Identification of dissolution patterns in nannofossil assemblages: a high-resolution comparison of synchronous records from Ceara Rise, ODP Leg 154. *Paleoceanography* 19:PA1029

Gibbs SJ, Stoll HM, Bown PR, Bralower TJ. 2010. Ocean acidification and surface water carbonate production across the Paleocene–Eocene thermal maximum. *Earth Planet. Sci. Lett.* 295:583–92

Godbillot C, Minoletti F, Bassinot F, Hermoso M. 2022. Parallel between the isotopic composition of coccolith calcite and carbon levels across Termination II: developing a new paleo-CO₂ probe. *Clim. Past* 18:449–64

González-Lanchas A, Hernández-Alméida I, Flores JA, Sierro F, Guitian J, Stoll H. 2021. Carbon isotopic fractionation of alkenones and *Gephyrocapsa* coccoliths over the late Quaternary (marine isotope stages 12–9) glacial-interglacial cycles at the western tropical

*Coccolithophores in Paleoceanography*
Atlantic. *Paleoceanogr. Paleoclimatol.* 36:e2020PA004175

González-Lemos S, Guitián J, Fuertes M-Á, Flores J-A, Stoll HM. 2018. An empirical method for absolute calibration of coccolith thickness. *Biogeosciences* 15:1079–91

Guerreiro C, Ziveri P, Cavaleiro C, Stuut J-B. 2024. Coccolith-calcite Sr/Ca as a proxy for transient export production related to Saharan dust deposition in the tropical North Atlantic. *Sci. Rep.* 14:4295

Guitián J, Dunkley Jones T, Hernández-Almeida I, Löffel T, Stoll HM. 2020. Adaptations of coccolithophore size to selective pressures during the Oligocene to Early Miocene high CO₂ world. *Paleoceanogr. Paleoclimatol.* 35:e2020PA003918

Guitián J, Fuertes MÁ, Flores J-A, Hernández-Almeida I, Stoll H. 2022. Variation in calcification of *Reticulofenestra* coccoliths over the Oligocene–Early Miocene. *Biogeosciences* 19:5007–19

Hannisdal B, Henderiks J, Liow LH. 2012. Long-term evolutionary and ecological responses of calcifying phytoplankton to changes in atmospheric CO₂. *Glob. Change Biol.* 18:3504–16

Henderiks J, Bartol M, Pige N, Karatsolis BT, Lougheed BC. 2020. Shifts in phytoplankton composition and stepwise climate change during the middle Miocene. *Paleoceanogr. Paleoclimatol.* 35:e2020PA003915

Henderiks J, Bollmann J. 2004. The *Gephyrocapsa* sea surface palaeothermometer put to the test: comparison with alkenone and foraminifera proxies off NW Africa. *Mar. Micropaleontol.* 50:161–84

Henderiks J, Pagani M. 2008. Coccolithophore cell size and the Paleogene decline in atmospheric CO₂. *Earth Planet. Sci. Lett.* 269:576–84

Henderiks J, Rickaby RE. 2007. A coccolithophore concept for constraining the Cenozoic carbon cycle. *Biogeosciences* 4:323–29

Hermoso M, Chan I, McClelland H, Heureux A, Rickaby R. 2016. Vanishing coccolith vital effects with alleviated carbon limitation. *Biogeosciences* 13:301–12

Hermoso M, Lecasble M. 2018. The effect of salinity on the biogeochemistry of the coccolithophores with implications for coccolith-based isotopic proxies. *Biogeosciences* 15:6761–72

Hermoso M, Lefeuvre B, Minoletti F, de Rafélis M. 2017. Extreme strontium concentrations
*Coccolithophores in Paleoceanography*
reveal specific biomineralization pathways in certain coccolithophores with implications for
the Sr/Ca paleoproductivity proxy. *PLOS ONE* 12:e0185655

Hermoso M, McClelland H-LO, Hirst JS, Minoletti F, Bonifacie M, Rickaby RE. 2020. Towards the use of the coccolith vital effects in palaeoceanography: a field investigation during the middle Miocene in the SW Pacific Ocean. *Deep-Sea Res. I* 160:103262

Hernández-Almeida I, Ausín B, Saavedra-Pellitero M, Baumann K-H, Stoll HM. 2019a. A dataset of modern and fossil distribution of coccolithophore species *Florisphaera profunda* in the world's ocean. *Data Brief* 22:826-29

Hernández-Almeida I, Ausín B, Saavedra-Pellitero M, Baumann K-H, Stoll HM. 2019b. Quantitative reconstruction of primary productivity in low latitudes during the last glacial maximum and the mid-to-late Holocene from a global *Florisphaera profunda* calibration dataset. *Quat. Sci. Rev.* 205:166-81

Herrmann S, Thierstein HR. 2012. Cenozoic coccolith size changes—evolutionary and/or ecological controls? *Palaeogeogr. Palaeoclimatol. Palaeoecol.* 333:92–106

Holtz L-M, Wolf-Gladrow D, Thoms S. 2017. Stable carbon isotope signals in particulate organic and inorganic carbon of coccolithophores—a numerical model study for *Emiliania huxleyi*. *J. Theor. Biol.* 420:117–27

Hönisch B, Royer DL, Breecker DO, Polissar PJ, Bowen GJ, et al. 2023. Toward a Cenozoic history of atmospheric CO₂. *Science* 382:eadi5177

Huntington KW, Petersen SV. 2023. Frontiers of carbonate clumped isotope thermometry. *Annu. Rev. Earth Planet. Sci.* 51:611–41

Imai R, Farida M, Sato T, Iryu Y. 2015. Evidence for eutrophication in the northwestern Pacific and eastern Indian oceans during the Miocene to Pleistocene based on the nannofossil accumulation rate, *Discoaster* abundance, and coccolith size distribution of *Reticulofenestra*. *Mar. Micropaleontol.* 116:15–27

Jin X, Liu C, Zhang H, Zhou C, Jiang X, et al. 2018. Evolutionary driven of *Gephyrocapsa* coccolith isotopic vital effects over the past 400 ka. *Earth Planet. Sci. Lett.* 503:236–47

Jin X, Wang X, Zhou X, Jiang X, Qiao P, Liu C. 2024. Precessional forcing of biogeochemical and nutrient cycling in the tropical western Pacific during the late Pleistocene. *Earth Planet. Sci. Lett.* 638:118759
Kameo K, Takayama T. 1999. Biostratigraphic significance of sequential size variations of the calcareous nannofossil genus *Reticulofenestra* in the Upper Pliocene of the North Atlantic. *Mar. Micropaleontol.* 37:41–52

Katz A, Bonifacie M, Hermoso M, Cartigny P, Calmels D. 2017. Laboratory-grown coccoliths exhibit no vital effect in clumped isotope (Δ47) composition on a range of geologically relevant temperatures. *Geochim. Cosmochim. Acta* 208:335–53

Knappertsbusch M. 2000. Morphologic evolution of the coccolithophorid *Calcidiscus leptoporus* from the Early Miocene to Recent. *J. Paleontol.* 74:712–30

Langer G, Gussone N, Nehrke G, Riebesell U, Eisenhauer A, et al. 2006. Coccolith strontium to calcium ratios in *Emiliania huxleyi*: the dependence on seawater strontium and calcium concentrations. *Limnol. Oceanogr.* 51:310–20

Le Guevel G, Minoletti F, Geisen C, Duong G, Rojas V, Hermoso M. 2024. Multispecies expression of coccolithophore vital effects with changing CO₂ concentrations and pH in the laboratory with insights for reconstructing CO₂ levels in geological history. EGUSphere https://doi.org/10.5194/egusphere-2024-1890

Le Moigne FA, Pabortsava K, Marcinko CL, Martin P, Sanders RJ. 2014. Where is mineral ballast important for surface export of particulate organic carbon in the ocean? *Geophys. Res. Lett.* 41:8460–68

Lees JA, Bown PR, Mattioli E. 2005. Problems with proxies? Cautionary tales of calcareous nannofossil paleoenvironmental indicators. *Micropaleontology* 51:333–43

Liu Y-W, Rokitta SD, Rost B, Eagle RA. 2021. Constraints on coccolithophores under ocean acidification obtained from boron and carbon geochemical approaches. *Geochim. Cosmochim. Acta* 315:317–32

Ma R, Aubry M-P, Bord D, Jin X, Liu C. 2024. Inferred nutrient forcing on the late middle Eocene to early Oligocene (~40–31 Ma) evolution of the coccolithophore *Reticulofenestra* (order Isochrysidales). *Paleobiology* 50:29–42

Marañón E. 2015. Cell size as a key determinant of phytoplankton metabolism and community structure. *Annu. Rev. Mar. Sci.* 7:241–64

Marañón E, Cermeño P, López-Sandoval DC, Rodríguez-Ramos T, Sobrino C, et al. 2013. Unimodal size scaling of phytoplankton growth and the size dependence of nutrient uptake
*Coccolithophores in Paleoceanography*
and use. *Ecol. Lett.* 16:371–79

Marino M, Maiorano P, Lirer F, Pelosi N. 2009. Response of calcareous nannofossil assemblages to paleoenvironmental changes through the mid-Pleistocene revolution at Site 1090 (Southern Ocean). *Palaeogeogr. Palaeoclimatol. Palaeoecol.* 280:333–49

Martínez-Ruiz F, Paytan A, Kastner M, González-Donoso J, Linares D, et al. 2003. A comparative study of the geochemical and mineralogical characteristics of the S1 sapropel in the western and eastern Mediterranean. *Palaeogeogr. Palaeoclimatol. Palaeoecol.* 190:23–37

Martini E. 1971. Standard Tertiary and Quaternary calcareous nannoplankton zonation. In *Proceedings Second Planktonic Conference, Rome*, pp. 739–85. Rome: Tecnoscienza

Matsuoka H. 1990. A new method to evaluate dissolution of CaCO₃ in the deep-sea sediments. *Trans. Proc. Paleontol. Soc. Jpn.* 157:430–34

McClelland H, Bruggeman J, Hermoso M, Rickaby R. 2017. The origin of carbon isotope vital effects in coccolith calcite. *Nat. Commun.* 8:14511

McIntyre A, McIntyre R. 1971. Coccolith concentrations and differential solution in oceanic sediments. In *The Micropaleontology of Oceans*, ed. BM Funnell, WR Riedel, pp. 253–61. Cambridge, UK: Cambridge Univ. Press

McIntyre A, Molfino B. 1996. Forcing of Atlantic equatorial and subpolar millennial cycles by precession. *Science* 274:1867–70

Mejía LM, Bernasconi SM, Fernandez A, Zhang H, Guitian J, et al. 2020. *Coccolith clumped isotopes suggest a more modest Miocene North Atlantic polar amplification*. Presented at Am. Geophys. Union Fall Meeting, Dec. 1–17

Mejía LM, Bernasconi SM, Zhang H, Guitián J, Fernandez A, et al. 2023. Clumped isotopes in globally distributed Holocene coccoliths reveal their habitat depth. *Earth Planet. Sci. Lett.* 619:118313

Mejía LM, Paytan A, Eisenhauer A, Böhm F, Kolevica A, et al. 2018. Controls over δ<sup>44/40</sup>Ca and Sr/Ca variations in coccoliths: new perspectives from laboratory cultures and cellular models. *Earth Planet. Sci. Lett.* 481:48–60

Mejía LM, Ziveri P, Cagnetti M, Bolton C, Zahn R, et al. 2014. Effects of midlatitude westerlies on the paleoproductivity at the Agulhas Bank slope during the penultimate glacial cycle: evidence from coccolith Sr/Ca ratios. *Paleoceanography* 29:697–714
Meyer EM, Langer G, Brownlee C, Wheeler GL, Taylor AR. 2020. Sr in coccoliths of *Scyphosphaera apsteinii*: partitioning behavior and role in coccolith morphogenesis. *Geochim. Cosmochim. Acta* 285:41–54

Meyer J, Riebesell U. 2015. Reviews and syntheses: responses of coccolithophores to ocean acidification: a meta-analysis. *Biogeosciences* 12:1671–82

Minoletti F, Gardin S, Nicot E, Renard M, Spezzaferri S. 2001. Mise au point d'un protocole experimental de separation granulometrique d'assemblages de nannofossiles calcaires; applications paleoecologiques et geochimiques. *Bull. Soc. Géol. Fr.* 172:437-46

Minoletti F, Hermoso M, Gressier V. 2009. Separation of sedimentary micron-sized particles for palaeoceanography and calcareous nannoplankton biogeochemistry. *Nat. Protoc.* 4:14–24

Molfino B, McIntyre A. 1990. Precessional forcing of nutricline dynamics in the equatorial Atlantic. *Science* 249:766–69

Monteiro FM, Bach LT, Brownlee C, Bown P, Rickaby RE, et al. 2016. Why marine phytoplankton calcify. *Sci. Adv.* 2:e1501822

Müller MN, Kısakürek B, Buhl D, Gutperlet R, Kolevica A, et al. 2011. Response of the coccolithophores *Emiliania huxleyi* and *Coccolithus braarudii* to changing seawater Mg²⁺ and Ca²⁺ concentrations: Mg/Ca, Sr/Ca ratios and δ⁴⁴/⁴⁰Ca, δ²⁶/²⁴Mg of coccolith calcite. *Geochim. Cosmochim. Acta* 75:2088–102

Müller MN, Lebrato M, Riebesell U, Barcelos e Ramos J, Schulz KG, et al. 2014. Influence of temperature and CO₂ on the strontium and magnesium composition of coccolithophore calcite. *Biogeosciences* 11:1065–75

Neukermans G, Bach L, Butterley A, Sun Q, Claustre H, Fournier G. 2023. Quantitative and mechanistic understanding of the open ocean carbonate pump—perspectives for remote sensing and autonomous in situ observation. *Earth-Sci. Rev.* 239:104359

Okada H, Honjo S. 1973. The distribution of oceanic coccolithophorids in the Pacific. *Deep Sea Res. Oceanogr. Abstr.* 20:355–74

Pagani M, Huber M, Liu Z, Bohaty S, Henderiks J, et al. 2011. The role of carbon dioxide during the onset of Antarctic glaciation. *Science* 334:1261–64

Pillot Q, Suchéras-Marx B, Sarr AC, Bolton C, Donnadieu Y. 2023. A global reassessment of the spatial and temporal expression of the Late Miocene Biogenic Bloom. *Paleoceanogr.*

*Coccolithophores in Paleooceanography*
Poulton AJ, Adey TR, Balch WM, Holligan PM. 2007. Relating coccolithophore calcification rates to phytoplankton community dynamics: regional differences and implications for carbon export. *Deep-Sea Res. II* 54:538–57

Poulton AJ, Holligan PM, Charalampopoulou A, Adey TR. 2017. Coccolithophore ecology in the tropical and subtropical Atlantic Ocean: new perspectives from the Atlantic meridional transect (AMT) programme. *Prog. Oceanogr.* 158:150–70

Prentice K, Jones TD, Lees J, Young J, Bown P, et al. 2014. Trace metal (Mg/Ca and Sr/Ca) analyses of single coccoliths by secondary ion mass spectrometry. *Geochim. Cosmochim. Acta* 146:90–106

Raffi I, Backman J, Fornaciari E, Pälike H, Rio D, et al. 2006. A review of calcareous nannofossil astrobiochronology encompassing the past 25 million years. *Quat. Sci. Rev.* 25:3113–37

Raven JA, Giordano M, Beardall J, Maberly SC. 2012. Algal evolution in relation to atmospheric CO₂: carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles. *Philos. Trans. R. Soc. B* 367:493–507

Rickaby REM, Bard E, Sonzogni C, Rostek F, Beaufort L, et al. 2007. Coccolith chemistry reveals secular variations in the global ocean carbon cycle? *Earth Planet. Sci. Lett.* 253:83–95

Rickaby REM, Henderiks J, Young JN. 2010. Perturbing phytoplankton: response and isotopic fractionation with changing carbonate chemistry in two coccolithophore species. *Clim. Past* 6:771–85

Saavedra-Pellitero M, Baumann K-H. 2015. Comparison of living and surface sediment coccolithophore assemblages in the Pacific sector of the Southern Ocean. *Micropaleontology* 61:507–20

Saavedra-Pellitero M, Baumann K-H, Hernández-Almeida I, Flores JA, Sierro FJ. 2013. Modern sea surface productivity and temperature estimations off Chile as detected by coccolith accumulation rates. *Palaeogeogr. Palaeoclimatol. Palaeoecol.* 392:534–45

Saavedra-Pellitero M, Baumann K-H, Ullermann J, Lamy F. Marine Isotope Stage 11 in the Pacific sector of the Southern Ocean; a coccolithophore perspective. *Quaternary Science Coccolithophores in Paleoceanography*
*Reviews*. 2017 Feb 15; 158:1-4.

Saavedra-Pellitero M, Hernández-Almeida I, Cabarcos E, Baumann K-H, Dunkley Jones T, et al. 2022. Coupled coccolith-based temperature and productivity high-resolution reconstructions in the Eastern Equatorial Pacific during the last deglaciation and the Holocene. *Front. Mar. Sci.* 9:865846

Sheward RM. 2016. *Cell size, coccosphere geometry and growth in modern and fossil coccolithophores*. PhD Diss., Univ. Southampton, Southampton, UK

Si W, Rosenthal Y. 2019. Reduced continental weathering and marine calcification linked to late Neogene decline in atmospheric CO2. *Nat. Geosci.* 12:833–38

Sosdian SM, Lear CH, Tao K, Grossman EL, O'Dea A, Rosenthal Y. 2012. Cenozoic seawater Sr/Ca evolution. *Geochem. Geophys. Geosyst.* 13:Q10014

Spero HJ, Bijma J, Lea DW, Russell AD. 1999. Deconvolving glacial ocean carbonate chemistry from the planktonic foraminifera carbon isotope record. In *Reconstruction Ocean History*, ed. F Abrantes, AC Mix, pp. 329–42. Boston, MA: Springer

Stoll H, Langer G, Shimizu N, Kanamaru K. 2012. B/Ca in coccoliths and relationship to calcification vesicle pH and dissolved inorganic carbon concentrations. *Geochim. Cosmochim. Acta* 80:143–57

Stoll HM, Guitian J, Hernandez-Almeida I, Mejía LM, Phelps S, et al. 2019. Upregulation of phytoplankton carbon concentrating mechanisms during low CO₂ glacial periods and implications for the phytoplankton pCO₂ proxy. *Quat. Sci. Rev.* 208:1–20

Stoll HM, Rosenthal Y, Falkowski P. 2002a. Climate proxies from Sr/Ca of coccolith calcite: calibrations from continuous culture of *Emiliania huxleyi*. *Geochim. Cosmochim. Acta* 66:927–36

Stoll HM, Ruiz Encinar J, Ignacio Garcia Alonso J, Rosenthal Y, Probert I, Klaas C. 2001. A first look at paleotemperature prospects from Mg in coccolith carbonate: cleaning techniques and culture measurements. *Geochem. Geophys. Geosyst.* 2:1047

Stoll HM, Schrag DP. 2000. Coccolith Sr/Ca as a new indicator of coccolithophorid calcification and growth rate. *Geochem. Geophys. Geosyst.* 1:1006

Stoll HM, Shimizu N. 2009. Micropicking of nannofossils in preparation for analysis by secondary ion mass spectrometry. *Nat. Protoc.* 4:1038–43
Stoll HM, Shimizu N, Archer D, Ziveri P. 2007a. Coccolithophore productivity response to greenhouse event of the Paleocene–Eocene Thermal Maximum. *Earth Planet. Sci. Lett.* 258:192–206

Stoll HM, Shimizu N, Arevalos A, Matell N, Banasiak A, Zeren S. 2007b. Insights on coccolith chemistry from a new ion probe method for analysis of individually picked coccoliths. *Geochem. Geophys. Geosyst.* 8:Q06020

Stoll HM, Ziveri P. 2002. Separation of monospecific and restricted coccolith assemblages from sediments using differential settling velocity. *Mar. Micropaleontol.* 46:209–21

Stoll HM, Ziveri P, Geisen M, Probert I, Young JR. 2002b. Potential and limitations of Sr/Ca ratios in coccolith carbonate: new perspectives from cultures and monospecific samples from sediments. *Philos. Trans. R. Soc. A* 360:719–47

Stoll HM, Ziveri P, Shimizu N, Conte M, Theroux S. 2007c. Relationship between coccolith Sr/Ca ratios and coccolithophore production and export in the Arabian Sea and Sargasso Sea. *Deep-Sea Res. II* 54:581–600

Suchéras-Marx B, Giraud F, Daniel I, Rivard C, Aubry M-P, et al. 2021a. Origin of manganese in nannofossil calcite based on synchrotron nanoXRF and XANES. *Mar. Micropaleontol.* 163:101961

Suchéras-Marx B, Giraud F, Simionovici A, Daniel I, Tucoulou R. 2016. Perspectives on heterococcolith geochemical proxies based on high-resolution X-ray fluorescence mapping. *Geobiology* 14:390–403

Suchéras-Marx B, Giraud F, Simionovici A, Tucoulou R, Daniel I. 2021b. Evidence of high Sr/Ca in a Middle Jurassic murolith coccolith species. *Peer Commun. J.* 1:e25

Suchéras-Marx B, Henderiks J. 2014. Downsizing the pelagic carbonate factory: impacts of calcareous nannoplankton evolution on carbonate burial over the past 17 million years. *Glob. Planet. Change* 123:97–109

Suchéras-Marx B, Viseur S, Walker CE, Beaufort L, Probert I, Bolton C. 2022. Coccolith size rules—What controls the size of coccoliths during coccolithogenesis? *Mar. Micropaleontol.* 170:102080

Sulpis O, Jeansson E, Dinauer A, Lauvset SK, Middelburg JJ. 2021. Calcium carbonate dissolution patterns in the ocean. *Nat. Geosci.* 14:423–28
Šupraha L, Henderiks J. 2020. A 15-million-year-long record of phenotypic evolution in the heavily calcified coccolithophore *Helicosphaera* and its biogeochemical implications. *Biogeosciences* 17:2955–69

Tangunan D, Baumann KH, Pätzold J, Henrich R, Kucera M, et al. 2017. Insolation forcing of coccolithophore productivity in the western tropical Indian Ocean over the last two glacial-interglacial cycles. *Paleoceanography* 32:692–709

Tanner T, Rae JWB, Hernandez-Almeida I, Zhang H, Jaggi M, et al. 2024. Multi-proxy estimates of sea surface temperature and CO₂ in the western Atlantic during the Late Miocene. *ESS Open Archive*. May 10, 2024. DOI: 10.22541/essoar.171535711.15687939/v1

Torres Romero I, Clark AJ, Wijker RS, Jaggi M, Zhang H, Stoll HM. 2024. Temperature-dependent carbon isotope fractionation in coccolithophores. *Front. Earth Sci.* 12:1331179

Tremblin M, Hermoso M, Minoletti F. 2016. Equatorial heat accumulation as a long-term trigger of permanent Antarctic ice sheets during the Cenozoic. *PNAS* 113:11782–87

Valença CR, Beaufort L, Hallegraeff GM, Müller MN. 2024. A comparison of methods for estimating coccolith mass. *Biogeosciences* 21:1601–11

Waite A, Gibbs S, Diester-Haass L, Rickaby R, Billups K. 2008. A top-down and bottom-up comparison of paleoproductivity proxies: calcareous nannofossil Sr/Ca ratios and benthic foraminiferal accumulation rates. *Geochem. Geophys. Geosyst.* 9:Q06005

Wells P, Okada H. 1997. Response of nannoplankton to major changes in sea-surface temperature and movements of hydrological fronts over Site DSDP 594 (south Chatham Rise, southeastern New Zealand), during the last 130 kyr. *Mar. Micropaleontol.* 32:341–63

Westerhold T, Marwan N, Drury AJ, Liebrand D, Agnini C, et al. 2020. An astronomically dated record of Earth's climate and its predictability over the last 66 million years. *Science* 369:1383–87

Young J. 1998. Neogene. In *Calcareous Nannofossil Biostratigraphy*, ed. PR Brown, pp. 225–65. Dordrecht, Neth.: Springer

Young J, Geisen M, Cros L, Kleijne A, Sprengel C, et al. 2003. A guide to extant coccolithophore taxonomy. *J. Nannoplankton Res. Spec. Issue* 1:1–132

Young J, Ziveri P. 2000. Calculation of coccolith volume and its use in calibration of carbonate flux estimates. *Deep-Sea Res. II* 47:1679–700
Young JR. 1990. Size variation of Neogene *Reticulofenestra* coccoliths from Indian Ocean DSDP cores. *J. Micropalaeontol.* 9:71–85

Young JR, Geisen M, Probert I. 2005. A review of selected aspects of coccolithophore biology with implications for paleobiodiversity estimation. *Micropaleontology* 51:267–88

Young JR, Henriksen K. 2003. Biomineralization within vesicles: the calcite of coccoliths. *Rev. Mineral. Geochem.* 54:189–215

Zhang H, Liu C, Mejía LM, Stoll H. 2021. Accelerate coccolith size separation via repeated centrifugation. *Biogeosciences* 18:1909–16

Zhang H, Stoll H, Bolton C, Jin X, Liu C. 2018. A refinement of coccolith separation methods: measuring the sinking characteristics of coccoliths. *Biogeosciences* 15:4759–75

Ziveri P, de Bernardi B, Baumann K-H, Stoll HM, Mortyn PG. 2007. Sinking of coccolith carbonate and potential contribution to organic carbon ballasting in the deep ocean. *Deep-Sea Res. II* 54:659–75

Ziveri P, Stoll HM, Probert I, Klaas C, Geisen M, et al. 2003. Stable isotope ‘vital effects’ in coccolith. *Earth Planet. Sci. Lett.* 210:137–49
<figure><img src="image_7.png" /><figcaption>**Supplementary Figure 1:** Map showing core site locations for all data shown and compiled in this paper. The map background shows sediment % CaCO₃ content, from Archer (1996).</figcaption></figure>