Calcifying plankton: From biomineralization to global change.

The cycling of calcium carbonate (CaCO3) in the ocean is closely linked to seawater alkalinity and the regulation of atmospheric CO2. In the modern pelagic ocean, almost all CaCO3 is produced by three groups of calcifying planktonic organisms: coccolithophores, foraminifers, and shelled pteropods. In this Review, we examine the differences in functional traits that define each group's distinctive role in the global carbon cycle and their sensitivity to climate change and ocean acidification. This synthesis reveals that a single representation of CaCO3 in climate models is unlikely to accurately reflect system dynamics or their impacts on biogeochemical cycling under climate change. We argue that understanding past and future CaCO3 cycle requires a better delineation of the traits that make up the diversity of calcifying plankton groups. Editor's summary: Calcifying planktonic organisms—coccolithophores, foraminifers, and shelled pteropods—are the linchpins of the marine carbonate cycle and key regulators of atmospheric carbon dioxide. What allows these tiny creatures to be such important players in the global carbon cycle? Ziveri et al. reviewed which of their functional traits make them so successful and how they respond to changes in climate and ocean chemistry. Knowing these properties is essential for better understanding their system dynamics and improving their representation in climate models. —Jesse Smith BACKGROUND: The production and dissolution of calcium carbonate (CaCO3) is a key component of the ocean carbon cycle. In the open ocean, nearly all CaCO3 is produced by three groups of calcifying plankton: coccolithophores, foraminifers, and pteropods. These taxonomically and functionally diverse organisms play a major role in ocean biogeochemistry by modulating air-sea CO2 exchange, and facilitating the export of carbon and alkalinity to depth. Despite their biogeochemical importance, these groups are typically considered separately, precluding an integrated understanding. Yet the pathways by which CaCO3 is produced and cycled through the ocean have important consequences for the carbon cycle and ecosystem functioning. Notably, none of the Earth system models included in the current Coupled Model Intercomparison Project (CMIP6) explicitly represents these groups of organisms. Here, we review the distinct functional traits of coccolithophores, foraminifers, and pteropods to elucidate how these traits shape their global distributions, vulnerabilities to climate change and acidification, and their role in modulating ocean chemistry and the Earth system. ADVANCES: Recent advances in data compilation at multiple levels offer a comprehensive but still incomplete view of the CaCO3 cycle, from biomineralization up to the global ocean, with different traits leading to differing vulnerabilities to environmental change. For example, coccolithophores, as primary producers, are relatively less affected by changes in oxygen concentration compared with heterotrophs, but are particularly sensitive to ocean acidification because of the proton load generated during intracellular calcification, which requires effective pH regulation and proton expulsion. Differing resource requirements contribute to the geographic distributions of each group, while traits such as body size and turnover rate are fundamentally linked to global production, export, dissolution, and burial. Compiling these data allows us to compare the markedly different fates of the CaCO3 produced by each group, from surface production through export to eventual sediment burial. A major imbalance exists in the global CaCO3 cycling related to each calcifying plankton group, with key uncertainties, especially in rates of group-specific production and shallow biologically mediated dissolution. Current best estimates indicate that a large fraction of coccolithophore-derived CaCO3—the dominant source of CaCO3 in the ocean—is dissolved and recycled in the upper ocean. This underscores the central role of ecological processes such as predation, particle aggregation, and microbial respiration in shaping ocean carbonate chemistry. We suggest that the overlooked process of shallow dissolution, mainly of coccolithophores, is also likely at play within the geological record of this group. OUTLOOK: The three major groups of calcifying plankton play essential but distinct roles within ocean ecosystems and the marine carbon cycle. Their diverse traits govern global distributions, production, export, and their differing response to environmental change. The magnitude of biologically mediated CaCO3 dissolution in the upper ocean remains broadly unrecognized, with implications for both the global alkalinity budget and interpretations of the fossil record. Sediment cores provide a fossil record going back 65 million years, revealing large variation in organism size and diversity likely linked to changes in seawater carbonate chemistry (acidification) and warming. The extent to which shallow, selective dissolution has biased this record remains an important unresolved question. Addressing discrepancies between CaCO3 production and export from the upper ocean will require renewed focus on both quantifying and understanding the individual and combined contribution of these groups, as well as the biological processes driving shallow dissolution. These efforts are also critical for incorporating a mechanistically resolved CaCO3 cycle into future climate models, thereby supporting a more integrated view of ocean biogeochemistry under climate change. Unresolved pathways in oceanic CaCO3 cycling: The role of calcifying plankton and shallow water dissolution. Three main calcifying plankton groups drive CaCO3 production and distinctively influence ocean alkalinity and biogeochemistry. Global CaCO3 fluxes reveal imbalances among production, export, and sediment burial. Biologically driven shallow water dissolution, mediated by predation, aggregation, and microbial respiration, plays a key yet often overlooked role. [ABSTRACT FROM AUTHOR]