Planktic foraminifera are key producers of pelagic carbonate, and their shell weight is suggested to have been influenced by the environment in which they calcify. However, there is debate about the use of size-normalised weight (SNW) as a proxy, as some authors invoke a carbonate system control on calcification (and by extension SNW as a pCO2 proxy), while others suggest that species optimum conditions, nutrient concentration, or temperature drive shell weight. To better understand this proxy, we investigate what drives SNW and whether discrepancies in the proposed control on weight are due to differing data collection methodologies and/or regionally different drivers. We integrate new and published SNW data with environmental hindcast data from the CMIP6 modelling suite. Using Bayesian regression modelling, we find that the environment alone does not explain the variability in SNW across species. Although physiology likely modulates the response to the environment, we find little evidence of a unifying driver at the ecogroup level. Instead, we identify species-specific responses associated with drivers including (but not limited to) the carbonate system, which are likely different between ocean basins. We hypothesise that this is partly influenced by cryptic species and regional phenotypic plasticity in changes to shell weight that are not well understood, such as the thickness of calcite deposited during some species' reproductive phases. Consequently, which species to use as a pCO2 proxy or whether multiple species should be used in parallel to reduce uncertainty should be carefully considered. We strongly encourage the regional testing and calibration of pCO2–SNW relationships.

The Cenozoic shift from a hothouse to icehouse provides a natural experiment to explore how a changing climate and macroevolutionary trends control marine pelagic carbonate production and burial. In the modern ocean, the key components of pelagic carbonate burial — planktic foraminifera and coccolithophores — contribute approximately evenly. However, in the past, coccolithophores dominated open ocean inorganic carbon burial. Exactly when and why this shift away from a coccolithophore dominated ooze occurred is unresolved. To this end, we reconstructed a 65Myr record of foraminifer to nannofossil ratios from sites covering the Pacific, Southern, Indian, and Atlantic Ocean. To better understand the climate and macroevolutionary controls on carbonate production, we move away from the commonly reported bulk changes and instead investigate the individual components of carbonate production: foraminiferal and coccolithophore size, weight and abundance. We use a suite of methodologies to extract these data, including the novel application of imaging flow cytometry to rapidly and digitally reconstruct the fossil record of coccolithophore size and abundance. Our ratio data shows a shift towards calcareous zooplankton during the Neogene. Initial qualitative analysis reveals that coccolithophore size is relatively smaller in the modern part of the record, whilst automated microscopy shows that modern subtropical and tropical foraminiferal size is greater than recorded in the previous 65Myr. Foraminiferal size-normalised weight (SNW) is expected to be higher in the modern ocean than in the past due to its suggested carbonate system control (i.e. higher carbonate ion concentrations being conducive to heavier tests). However, SNW data from a high latitude site during the Palaeogene are similar to modern values for extant species – potentially implying something other than a carbonate system control on SNW.

Planktic foraminifera are a major contributor to global marine inorganic carbon production. They leave abundant calcium carbonate shells on the seafloor that serve as prime proxies for the physical and chemical attributes of past oceans. Despite their well-preserved fossil record and widespread use in palaeoceanography, our understanding of their ecology remains limited due to their low-standing stocks in the modern ocean and the challenges in culturing multiple generations under laboratory conditions, even after decades of data collection. This limitation affects our ability to interpret their fossil remains to describe past ecosystems and predict their responses to ongoing environmental changes. Trait-based ecology offers a powerful framework to characterise how and why foraminifera interact with their environment. Here, we review the current state of knowledge on key planktic foraminifera traits, including morphological, physiological, behavioural, and life history traits. Most spinose taxa are carnivorous, host to dinoflagellate photosymbionts, and are abundant and diverse in oligotrophic environments. In contrast, non-spinose taxa are typically herbivorous and most common in high-productivity regions. We highlight the potential of trait modelling to generate hypotheses testable in the field. Integration of trait-based modelling with metabarcoding, environmental DNA, and enhanced standardised data collection made openly available will help to fill critical gaps in our understanding of planktic foraminiferal ecology and allow us to use foraminifera as a key model organism for addressing fundamental ecological questions.

Past warm events offer windows into the biotic response to extreme warmth. The early Eocene interval records the highest global average temperature and CO2 levels of the Cenozoic. Several transient global warming events occur within the Early Eocene Climatic Optimum (EECO, 53-49 Ma), offering an opportunity to investigate the impact of both long term and transient warm climatic conditions on planktic foraminifera. We analyse the planktic foraminiferal record across the EECO obtained from tropical Pacific ODP sites 1209-1210 (Shatsky Rise). These sites have an excellent age model and stable isotope ratios enabling linkage of the biotic data with the climate and carbon cycle spanning the EECO.We combine indicators of carbonate production and preservation [fragmentation index (FI) as a dissolution proxy, weight percent coarse fraction (CF) as foraminiferal production and preservation index, and Foraminiferal Mass Accumulation Rate (FMAR) as foraminiferal production proxy] with changes in planktic foraminiferal assemblages and test-size.At the EECO onset, the abundance of the genus Morozovella (53.28 Ma) and Chiloguembelina (52.85 Ma) decreased at Shatsky Rise sites, confirming previous Atlantic Ocean data and thus pointing towards global decline of these genera. We hypothesise that a reduction in foraminiferal mass accumulation and assemblage test-size would follow the drop in Morozovellids abundance, given their dominance and large size in early Eocene tropical assemblages. In contrast, we record a slight increase in test-size within assemblages and a relatively stable FMAR. These changes may be controlled by growing dominance of the genus Acarinina indicating an ability of this species to benefit from the environmental conditions. In addition, we observe a relatively stable FMAR at decreasing CF which may be linked to either increased carbonate dissolution or enhanced calcareous nannofossil productivity (or a combination of both) reducing foraminiferal relative contribution to the sediment.Even though the pronounced warming during the EECO strongly altered the planktic foraminiferal assemblage composition resulting in the decrease in abundance of some genera, species replacement within communities highlights the resilience of pelagic carbonate production.

Plain Language SummaryThe Early Eocene Climatic Optimum (EECO) is an interval of prolonged warmth that occurred ∼53 to 49 million years ago. Planktic foraminifera are important (alongside coccolithophores) for understanding the carbon cycle and determining export production in the ocean. To understand how foraminifera can be impacted by extreme heat, we analyzed samples from the Pacific Ocean through measuring changes in (a) the relative abundance, that is, the count of different taxa in a sample, and (b) body (shell) size of planktic foraminifera. At the start of the EECO, the abundance of the genera Morozovella and Chiloguembelina decreased. Despite this decline, the number of foraminifera being buried and the size of the largest shells in a sample does not change. We attribute this to the increased abundance of the genus Acarinina. In general, the accumulation of foraminifera remains stable while the relative abundance of foraminifera to coccolithophores decreases. Together, this implies that coccolithophores are increasing in abundance, and/or mass. During the EECO, one group of foraminifera was able to counterbalance the decrease in abundance of other genera. This highlights the resilience of open‐ocean carbonate production and the base of the marine food web.

Pronounced warming negatively impacts ecosystem resilience in modern oceans. To offer a long-term geological perspective of the calcareous plankton response to global warming, we present an integrated record, from two Tethyan sections (northeastern Italy), of the planktic foraminiferal and calcareous nannofossil response to the Eocene Thermal Maximum 2 hyperthermal (ETM2, similar to 54 Ma). Our study reveals pronounced changes in assemblage composition and a striking dwarfing of planktic foraminiferal tests of up to 40% during the event, impacting both surface and deeper dwellers. The increased abundance of small placoliths among calcareous nannofossils is interpreted as community size reduction. Literature and our foraminiferal size data from Sites 1263 and 1209 (Atlantic and Pacific Oceans) highlights that the pronounced dwarfism is restricted to the Tethyan area. The ETM2 is characterized by warm sea surface temperatures as indicated by our delta 18O data, but this warming is of global extent and cannot explain the unique dwarfism. Excluding evolutionary modifications, other potential drivers of dwarfism (eutrophication, deoxygenation, metabolic adaptation) cannot explain the exceptional dwarfism by themselves. The smallest sizes are in close temporal association with peaks in volcanic derived Hg/Th-Hg/Rb recorded just before and at the ETM2 which could not have been brought into our sections through weathering. In contrast, size reductions are absent below and above the ETM2 at Hg peaks where delta 18O data do not show warm conditions. We speculate that the local input of toxic metals from submarine volcanic emissions could have acted synergistically to warming, causing the unique dwarfism. Calcareous plankton size in the Tethys during the Eocene Thermal Maximum 2 (ETM2) reveals marked dwarfism Pronounced dwarfism was restricted to the Tethyan area, highlighting the importance of local signals in interpreting hyperthermals Calcareous plankton were highly unstable across the ETM2 but ultimately resilient

Past warm events offer windows into the biotic response to extreme warmth. The early Eocene interval records the highest global average temperature and CO2 levels of the Cenozoic. Several transient global warming events occur within the Early Eocene Climatic Optimum (EECO, 53-49 Ma), offering an opportunity to investigate the impact of both long term and transient warm climatic conditions on planktic foraminifera. We analyse the planktic foraminiferal record across the EECO obtained from tropical Pacific ODP sites 1209-1210 (Shatsky Rise). These sites have an excellent age model and stable isotope ratios enabling linkage of the biotic data with the climate and carbon cycle spanning the EECO. We combine indicators of carbonate production and preservation [fragmentation index (FI) as a dissolution proxy, weight percent coarse fraction (CF) as foraminiferal production and preservation index, and Foraminiferal Mass Accumulation Rate (FMAR) as foraminiferal production proxy] with changes in planktic foraminiferal assemblages and test-size. At the EECO onset, the abundance of the genus Morozovella (53.28 Ma) and Chiloguembelina (52.85 Ma) decreased at Shatsky Rise sites, confirming previous Atlantic Ocean data and thus pointing towards global decline of these genera. We hypothesise that a reduction in foraminiferal mass accumulation and assemblage test-size would follow the drop in Morozovellids abundance, given their dominance and large size in early Eocene tropical assemblages. In contrast, we record a slight increase in test-size within assemblages and a relatively stable FMAR. These changes may be controlled by growing dominance of the genus Acarinina indicating an ability of this species to benefit from the environmental conditions. In addition, we observe a relatively stable FMAR at decreasing CF which may be linked to either increased carbonate dissolution or enhanced calcareous nannofossil productivity (or a combination of both) reducing foraminiferal relative contribution to the sediment. Even though the pronounced warming during the EECO strongly altered the planktic foraminiferal assemblage composition resulting in the decrease in abundance of some genera, species replacement within communities highlights the resilience of pelagic carbonate production.

Size is fundamentally important in individual planktic foraminifers as it determines the number of offspring and hence reproductive success. Over evolutionary timescales, individuals tend to increase in size, altering the average size of assemblages; in the last million years, individuals were larger than at any other time in the geological record. This pattern is specifically driven by size increases in tropical and subtropical taxa in the Plio-Pleistocene. Here we use a taxon-free approach to assess what facilitated this novelty and to quantify the response of planktic foraminifers to both long and short time-scale environmental changes. We focus on the Pliocene, a time interval characterized by the closure of the Central American Seaway (CAS) and the short glaciation at marine isotope stage (MIS) M2. We measured size in foraminiferal assemblages using automated microscopy across 24 globally distributed PRISM locations, from subpolar to tropical environments. The 95th percentile was calculated on the maximum diameter measurements of 1.28 million specimens. Although there is a slight decrease in the average size of the assemblage in the high latitudes from the Early to Late Pliocene, with minimal changes in the tropics, results indicate little to no effect on foraminiferal size across MIS M2. The results show an unexpected stability and resilience against the reorganization of the tropical oceans associated with the closure of the CAS.

Carbonate‐forming organisms play an integral role in the marine inorganic carbon cycle, yet the links between carbonate production and the environment are insufficiently understood. Carbonate production is driven by the abundance of calcifiers and the amount of calcite produced by each individual (their size and weight). Here we investigate how foraminiferal carbonate production changes in the Atlantic, Pacific and Southern Ocean in response to a 4–5°C warming and a 0.3 surface ocean pH reduction during the Palaeocene‐Eocene Thermal Maximum (PETM). To put these local data into a global context, we apply a trait‐based plankton model (ForamEcoGEnIE) to the geologic record for the first time. Our data illustrates negligible change in the assemblage test size and abundance of foraminifers. ForamEcoGEnIE resolves small reductions in size and biomass, but these are short‐lived. The response of foraminifers shows spatial variability linked to a warming‐induced poleward migration and suggested differences in nutrient availability between open‐ocean and shelf locations. Despite low calcite saturation at high latitudes, we reconstruct stable foraminiferal size‐normalized weight. Based on these findings, we postulate that sea surface warming had a greater impact on foraminiferal carbonate production during the PETM than ocean acidification. Changes in the composition of bulk carbonate suggest a higher sensitivity of coccolithophores to environmental change during the PETM than foraminifers.

During the Pliocene the planktic ecosystem, for the first time in its evolutionary history, experienced a separation of the tropical seaways. At the same time, low latitude planktic foraminifers reached sizes not seen for millions of years. We set out to examine whether the closure of the Central American Seaway (CAS) led to the reorganisation of the planktic food web and enabled this growth. As many plankton are not well preserved in the fossil record, we applied a trait-based ecosystem model for plankton – ForamEcoGEnIE – to an open and closed CAS Pliocene environment. ForamEcoGEnIE is an extension of the size-structured 3-D plankton ecosystem model, “EcoGEnIE” that includes non-spinose planktic foraminifers as a new functional group based on the costs and benefits of key traits (e.g. growth, grazing, calcification). We test whether the planktic food web and planktic foraminiferal physiology responded to this change in paleogeography by quantifying changes in plankton biomass and size. In large regions of the ocean, we observe no change in phytoplankton, zooplankton, or foraminiferal biomass in response to a closed CAS. However, we note an increase in biomass at the eastern equatorial Pacific and a decrease in the North Atlantic in response to the closure of the CAS. ForamEcoGEnIE predicts an increase in non-spinose foraminiferal body size at the eastern equatorial Pacific and a small decrease in the North Atlantic. We attribute the Pacific response to increased upwelling due to the closure of the CAS and in the North Atlantic we suggest the reduction in biomass and size is linked with the reorganisation of surface ocean currents. As much of the ocean shows no response, we tentatively conclude that the closure of the CAS did not induce a major reorganisation of the planktic ecosystem.

The scientific community is increasingly focused on the study of past climate analogues to better comprehend future implications of global warming on marine ecosystem and biogeochemical cycles. Through an integrated calcareous plankton and geochemical approach, we examined the Terche and Madeago (NE Italy) Tethyan sections, that encompass the hyperthermal Eocene Thermal Maximum 2 (ETM2, ~54 Ma). The ETM2 shares similarities with the current climate context such as global warming, carbon cycle perturbations, high pCO2 and ocean acidification, thus representing a key event in which investigate links between climate and biotic changes. Our planktic foraminiferal and calcareous nannofossil records show significant, though transient, changes in both the sections across this event. Our record of multiple dissolution proxies from both the sections ensures that dissolution did not affect calcareous plankton assemblages. Planktic foraminifera exhibit a marked increase in warm index surface-dweller Acarinina paralleled by a decline in abundance of the deeper-dweller chiloguembelinids and subbotinids. This implies that the ETM2 warming impacted the entire upper water column. Both chiloguembelinids and subbotinids, recognized as eutrophic and colder taxa, may have suffered, beside warming, of reduced food supply at the thermocline due to the increased surface-water remineralization of organic matter as induced by the significant warmth. Increase of Cretaceous calcareous nannofossils testifies reworking related to enhanced hydrological cycle that also generated input of nutrients from land. Surface water eutrophication during the ETM2 was inferred by rise in calcareous nannofossil eutrophic indices. This group proved to be more sensitive to the nutrient supply rather than warming. The ETM2 consequence on marine calcifiers test-size were not previously explored. We provide here new evidence of a striking test size reduction in planktic foraminiferal assemblages (up to 40%) during the ETM2 that involved both the surface and deeper-dweller taxa that is particularly marked at Madeago. Although loss of symbionts (bleaching) is known to affect test calcification, it cannot represent a likely cause in the studied case as both symbiotic and asymbiotic planktic foraminifera were affected at the same scale across the ETM2. The increased abundance of small placoliths Toweius and Ericsonia indicates that size reduction also impacted nannofossils, though to a lesser degree. We collected Hg (ppb), TOC (wt%) and Hg/TOC (ppb/wt%) data throughout our sections to test whether the reduction in size was related to environmental stressors not commonly linked to the ETM2. An increase in Hg was indeed detected in both sections at the base of the ETM2 and not corresponding to the intervals of reworking. Coeval submarine igneous events in this area might have introduced biolimiting metals thus involving the calcareous plankton productivity and possibly affecting test sizes. We hypothesize that the striking plankton dwarfism here recorded across the ETM2 is the result of the combined effect of paleoenvironmental perturbations induced by this event and increase in biolimiting metals. Our study alerts on possible consequences related to intense warming as associated to igneous events. Further data from different locations are needed to evaluate the geographic extension of impact on test-size variations in calcareous plankton assemblages.