Cell size, coccosphere geometry and growth in modern and fossil coccolithophores

Abstract

Coccolithophores are a key phytoplankton group that exhibit remarkable diversity in their biology, ecology, and in the highly distinctive morphological architecture of their calcite exoskeletons (coccospheres). Their extensive fossil record is testament to the crucial role that they play in the biogeochemical cycling of carbon through the production and export of inorganic coccoliths and organic matter. This fossil record provides an excellent archive of their biotic responses to environmental variability over thousands to millions of years that can be used to investigate the possible sensitivity of coccolithophores to potential changes in future climate. In this thesis, I explore how the fossil record of coccospheres can be utilized to investigate coccolithophore growth and physiology, providing a new cellular-level perspective on how we understand their interactions with global climate. This work focuses particularly on coccolithophores during the Paleogene, ~66 to ~23 million years ago, that was characterized by initially warm, high CO2 ‘greenhouse’ conditions that progressively cooled, involving substantial restructuring of marine systems. By imaging and measuring thousands of individual coccospheres, I have extensively documented the fundamentals of coccosphere architecture, including coccosphere size and shape and its relationship to coccolith size, number of coccoliths and their arrangement around each cell. This unprecedented dataset reveals the remarkable level of diversity in the architecture of Paleogene coccospheres for the first time, including multiple extinct species that had not previously been observed in this original form. Understanding what this dataset of coccosphere ‘geometry’ can tell us has necessitated the parallel exploration of modern coccolithophore biomineralisation and physiology. My culturing experiments on multiple modern species reveal that cell size and the number of coccoliths per cell is strongly regulated by cellular physiology, specifically responding to a decoupling between cellular division and calcification ability as populations transition between exponential and non-exponential phases of growth. Drawing direct comparisons between the coccosphere geometry of modern and fossil coccolithophores enables a proxy for growth phase to be developed that allows cellular physiology in the fossil record to be directly investigated. This is a potentially powerful new tool for understanding biotic-abiotic interactions in geological time. Furthermore, taxon-specific cellular geometry information provides us with a unique means to begin to reconstruct community-level cellular size structure and, crucially, its associated biovolume. These first reconstructions of community cell size structure across the transition from the Early Eocene greenhouse to the Early Oligocene icehouse demonstrate a massive shift in community biovolume distribution towards larger cells. This radically different-looking community must, in part, reflect the ability of the environment to support the demands of larger cells. Taken in conjunction with inferred changes in nutrient availability by the Late Eocene, this shift in population size structure was likely accompanied by an increase in community biomass, with potentially important implications for carbon export and size-specific grazing. Overall, my research illustrates that coccosphere geometry is a valuable tool for investigating fossil coccolithophore assemblages as populations of individual cells that are recording daily physiological responses to their immediate environment that ultimately determines the response of species and communities to environmental change.

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