Biogeosciences, 14, 1493–1509, 2017 www.biogeosciences.net/14/1493/2017/ doi:10.5194/bg-14-1493-2017 © Author(s) 2017. CC Attribution 3.0 License. Physiology regulates the relationship between coccosphere geometry and growth phase in coccolithophores Rosie M. Sheward1,2, Alex J. Poulton3, Samantha J. Gibbs1, Chris J. Daniels3, and Paul R. Bown4 1Ocean and Earth Science, University of Southampton, National Oceanography Centre, Southampton, SO14 3ZH, UK 2Institute of Geosciences, Goethe University Frankfurt, 60438 Frankfurt am Main, Germany 3Ocean Biogeochemistry and Ecosystems, National Oceanography Centre, Southampton, SO14 3ZH, UK 4Department of Earth Sciences, University College London, Gower Street, London, WC1E 6BT, UK Correspondence to: Rosie M. Sheward ([email protected]) Received: 13 October 2016 – Discussion started: 1 November 2016 Revised: 10 February 2017 – Accepted: 24 February 2017 – Published: 24 March 2017 Abstract. Coccolithophores are an abundant phytoplankton on this, the direct comparison of coccosphere geometries group that exhibit remarkable diversity in their biology, ecol- in modern and fossil coccolithophores enables a proxy for ogy and calcitic exoskeletons (coccospheres). Their exten- growth phase to be developed that can be used to investigate sive fossil record is a testament to their important biogeo- growth responses to environmental change throughout their chemical role and is a valuable archive of biotic responses long evolutionary history. Our data also show that changes in to environmental change stretching back over 200 mil- growth rate and coccoliths per cell associated with growth- lion years. However, to realise the full potential of this phase shifts can substantially alter cellular calcite produc- archive for (palaeo-)biology and biogeochemistry requires tion. Coccosphere geometry is therefore a valuable tool for an understanding of the physiological processes that under- accessing growth information in the fossil record, providing pin coccosphere architecture. Using culturing experiments unprecedented insights into the response of species to envi- on four modern coccolithophore species (Calcidiscus lep- ronmental change and the potential biogeochemical conse- toporus, Calcidiscus quadriperforatus, Helicosphaera car- quences. teri and Coccolithus braarudii) from three long-lived fam- ilies, we investigate how coccosphere architecture responds to shifts from exponential (rapid cell division) to stationary 1 Introduction (slowed cell division) growth phases as cell physiology re- acts to nutrient depletion. These experiments reveal statisti- The fossil remains of biomineralised plankton provide com- cal differences in coccosphere size and the number of coc- prehensive records of their biogeography, ecology, diversity coliths per cell between these two growth phases, specif- and evolution that have significance for our understanding of ically that cells in exponential-phase growth are typically past ocean and climate systems and their influence on these smaller with fewer coccoliths, whereas cells experiencing microscopic organisms. Despite their small size (2 to 200 µm growth-limiting nutrient depletion have larger coccosphere for nanno- and microplankton), the vast numbers of pho- sizes and greater numbers of coccoliths per cell. Although tosynthesising plankton in the ocean drive many regional- the exact numbers are species-specific, these growth-phase to global-scale biogeochemical processes and comprise the shifts in coccosphere geometry demonstrate that the core biomass that sustains the ocean ecosystem (e.g. Menden- physiological responses of cells to nutrient depletion result Deuer and Kiørboe, 2016). Investigating the biological re- in increased coccosphere sizes and coccoliths per cell across sponse of plankton species to environmental variability is four different coccolithophore families (Calcidiscaceae, Coc- therefore a crucial step in understanding the potential con- colithaceae, Isochrysidaceae and Helicosphaeraceae), a rep- sequences of future climate change on marine systems. resentative diversity of this phytoplankton group. Building Published by Copernicus Publications on behalf of the European Geosciences Union. 1494 R. M. Sheward et al.: Physiology regulates growth-phase shifts in coccosphere geometry Coccolithophores are a major group of calcifying marine coccoliths per cell. Given this observation, can we reason- algae that first evolved more than 200 million years ago ably hypothesise that the growth–geometry relationship re- (Ma) during the Late Triassic (Janofske, 1992; Bown et al., ported by Gibbs et al. (2013) for two modern species is simi- 2004). The remains of their calcite cell coverings contribute lar across coccolithophores in general? If this is the case, then to the export of biogenic carbonate to deep-sea sediments coccosphere geometry could prove to be a valuable proxy (Broecker and Clark, 2009), forming a geographically and for growth phase and provide new insights into important temporally extensive fossil record that is mostly in the form fitness-related traits where growth rates cannot be measured of individual calcite plates called coccoliths. Spatial and tem- directly. One potential concern is that coccolithophores show poral analysis of coccoliths reveals the evolution, biogeog- pronounced species-specific and even strain-specific phys- raphy and ecology of past species (e.g. Haq and Lohmann, iological responses to a variety of environmental manipu- 1976; Knappertsbusch, 2000; Ziveri et al., 2004; Gibbs et al., lations such as carbonate chemistry and nutrient availabil- 2006; Baumann et al., 2016) and the response of species and ity in culture experiments (Langer et al., 2006, 2009; Krug communities to palaeoceanographic and palaeoclimatic vari- et al., 2011), which may extend to coccosphere variability. ability (e.g. Bollmann et al., 2002, 2009; Bown, 2005; Bown We therefore require coccosphere geometry data from multi- and Pearson, 2009). ple modern species experiencing different growth phases in Valuable new insights into past coccolithophore commu- order to further investigate the relationship between cocco- nities can also be provided by the study of intact fossil sphere geometry and growth. coccospheres that have not disarticulated into their compo- Here, we aim to determine the relationships (if any) be- nent coccoliths, providing intriguing snapshots of individ- tween growth phase and coccosphere geometry in three mod- ual cell growth in geological time (Gibbs et al., 2013; Bown ern coccolithophore species – Calcidiscus leptoporus, Cal- et al., 2014; O’Dea et al., 2014). Whilst the preservation of cidiscus quadriperforatus and Helicosphaera carteri – and intact coccospheres in sediments is generally uncommon, to integrate these new data with those previously determined recent investigations showcase a large diversity of cocco- by Gibbs et al. (2013) for Coccolithus and Emiliania. Cal- spheres from a range of ages, ocean basins and latitudes in cidiscus and Helicosphaera are particularly pertinent study numbers suitable for robust quantitative analyses (Gibbs et taxa, as they have widespread modern and geological occur- al., 2013; Bown et al., 2014). The discovery of relatively rences and are important components of mid- to low-latitude abundant fossil coccospheres in exceptionally well-preserved coccolithophore communities, preferring warmer temperate sedimentary deposits, inspired Gibbs et al. (2013) to first to tropical waters (Ziveri et al., 2004). These species are explore the quantitative links between coccosphere geome- also three of the largest and most heavily calcified of all try (coccosphere size, coccolith length and coccolith num- the modern species, along with Coccolithus pelagicus in the ber) and population growth. Their laboratory experiments us- high latitudes and Coccolithus braarudii in the mid- to high ing the modern species Coccolithus braarudii and Emiliania latitudes (Ziveri et al., 2004). They are therefore important huxleyi identified that cells undergoing rapid cell division contributors to the production (Daniels et al., 2014, 2016) (termed “exponential-phase” growth) were smaller and had and export of inorganic carbon to the deep ocean (Ziveri fewer coccoliths per coccosphere compared to cells dividing et al., 2007). Variability in coccosphere geometry in these slowly, or not at all (“stationary-phase” growth). This initial species, particularly the number of coccoliths per cell, could evidence of a relationship between growth phase and cocco- therefore substantially alter cellular calcite with significant sphere geometry was then used to reconstruct the response consequences for calcite production and export. The well- of fossil taxa (Coccolithus and Toweius) through an inter- documented fossil records of these genera extend back to the val of rapid warming ∼ 56 Ma called the Palaeocene–Eocene first occurrence of Calcidiscus ∼ 57 Ma (Bown et al., 2007) Thermal Maximum, PETM (Gibbs et al., 2013; O’Dea et al., and Helicosphaera ∼ 54 Ma (Perch-Nielsen, 1985). Along- 2014). As growth phases describe “states” of rapid or slowed side Coccolithus, they have been significant components of growth rates, these findings hint that coccosphere geometry coccolithophore communities over much of the last ∼ 55 Ma could provide opportunities for new insights into the ecolog- (Perch-Nielsen, 1985; Bown et al., 2007). ical “fitness” and subsequent evolutionary success of coccol- Helicosphaera and Calcidiscus also have distinct