Ocean warming, not acidification, controlled coccolithophore response during past greenhouse climate change

Current carbon dioxide emissions are an assumed threat to oceanic calcifying plankton (coccolithophores) not just due to rising sea-surface temperatures, but also because of ocean acidification (OA). This assessment is based on single species culture experiments that are now revealing complex, synergistic, and adaptive responses to such environmental change. Despite this complexity, there is still a widespread perception that coccolithophore calcification will be inhibited by OA. These plankton have an excellent fossil record, and so we can test for the impact of OA during geological carbon cycle events, providing the added advantages of exploring entire communities across real-world major climate perturbation and recovery. Here we target fossil coccolithophore groups (holococcoliths and braarudosphaerids) expected to exhibit greatest sensitivity to acidification because of their reliance on extracellular calcification. Across the Paleocene-Eocene Thermal Maximum (56 Ma) rapid warming event, the biogeography and abundance of these extracellular calcifiers shifted dramatically, disappearing entirely from low latitudes to become limited to cooler, lower saturation-state areas. By comparing these range shift data with the environmental parameters from an Earth system model, we show that the principal control on these range retractions was temperature, with survival maintained in high-latitude refugia, despite more adverse ocean chemistry conditions. Deleterious effects of OA were only evidenced when twinned with elevated temperatures. INTRODUCTION Increasing atmospheric CO2 is currently driving a decrease in surface ocean pH and carbonate saturation, a phenomena termed ocean acidification (OA; Royal Society, 2005). Continuing OA is expected to induce a range of adverse impacts on ocean ecosystem function, biodiversity, and marine biogeochemical cycles (Aze et al., 2014), with organisms that form shells from calcium carbonate (CaCO3) considered particularly at risk. The most widespread pelagic calcifiers are calcareous nannoplankton, predominantly coccolithophorid algae, with our current understanding of their response to OA predominantly based on observations of reduced calcification in short-term culture experiments (days to a year) (e.g., Riebesell et al., 2000). The interpretation of experimental results, however, is not straightforward, and they reveal a complex range of responses, including both higher and lower rates of calcification with acidification (Meyer and Riebesell, 2015), and synergistic effects with environmental parameters, such as temperature, modulating the acidification influence (Sett et al., 2014). More recent and sophisticated experiments have also shown that coccolithophore species may have the ability to adapt and evolve to OA over relatively short time scales (100 to thousands of generations) (Lohbeck et al., 2012). Because calcareous plankton have remarkably complete fossil records, we can now supplement experimental data by studying past climate change events that encompassed environmental changes relevant to the future, affording the opportunity to assess responses and complex net outcomes across entire calcareous nannoplankton populations. The Paleocene-Eocene Thermal Maximum (PETM, 56 Ma) was a transient carbon-release event characterized by 4–5 °C of surface ocean warming (Dunkley Jones et al., 2013) and an ~0.3 pH unit decrease (Penman et al., 2014), making it our closest geological analogue to modern fossil fuel burning (Hönisch et al., 2012). There is currently little substantive support for significant OA effects on calcifying plankton during this event, with some evidence of coccolith thinning (O’Dea et al., 2014) and putative skeletal malformation (Raffi and De Bernardi, 2008), but plentiful evidence for temperatureand nutrient availability–controlled migration and population composition changes (Bralower, 2002; Gibbs et al., 2006b). There is thus a need to identify diagnostic indicators that are sufficiently sensitive and selective to OA. Here we attempt to distinguish OA response by assessing a novel indicator of biomineralization function in coccolithophores, specifically the distribution of the extracellular calcifying holococcoliths (Figs. 1A–1C) and braarudosphaerids (Fig. 1D) across the PETM. Holococcoliths and heterococcoliths are the exoskeletal calcite plates of coccolithophores, produced during different life-cycle phases and generated by different biomineralization modes. Heterococcoliths form in the diploid life-cycle phase and comprise radial arrays of interlocking crystals with complex shapes (Fig. 1E), produced within the cytoplasm in a coccolith vesicle (Young and Henriksen, 2003). Their calcite is chemically distinct from abiotic calcite (Cros et al., 2013), implying a strong physiological control on the intracellular calcification processes (Mackinder et al., 2011), including a degree of buffering to external pH (Taylor et al., 2011). In contrast, holococcoliths form in the haploid life-cycle phase and comprise numerous minute crystallites (~0.1 μm; Figs. 1A–1C) produced within a membrane-bound space but outside the cell wall (Rowson et al., 1986). We therefore call these taxa extracellular coccolithophore calcifiers (ECCs). We also include in this ECC GEOLOGY, January 2016; v. 44; no. 1; p. 59–62 | Data Repository item 2016014 | doi:10.1130/G37273.1 | Published online 4 December 2015 © 2015 The Authors. Gold Open Access: This paper is published under the terms of the CC-BY license. Figure 1. Examples of extracellular and intra­ cellular calcifying calcareous nannoplankton, all imaged by scanning electron microscopy (SEM). A: Holococcolith Zygrhablithus bijugatus from Lodo Gulch (central California, USA), sample LO­03–29. B: Holococcolith Holodiscolithus solidus from Lodo Gulch, sam­ ple LO29. C: Holococcolith Semihololithus biskayae from Tanzania, sample TDP14/9–1. D: Braarudosphaera bigelowii (SEM) from Tanzania, sample TDP14/9–1. E: Toweius pertusus coccosphere (SEM), which includes an intracellularly forming protococcolith (high­ lighted in purple), from Bass River (New Jer­ sey, USA) sample BR27. on January 19, 2016 geology.gsapubs.org Downloaded from