Reconsidering the role of carbonate ion concentration in calcification by marine organisms

Marine organisms precipitate 0.5–2.0 Gt of carbon as calcium carbonate (CaCO3) every year with a profound impact on global biogeochemical element cycles. Biotic calcification relies on calcium ions (Ca2+) and generally on bicarbonate ions (HCO3−) as CaCO3 substrates and can be inhibited by high proton (H+) concentrations. The seawater concentration of carbonate ions (CO32−) and the CO32−-dependent CaCO3 saturation state (ΩCaCO3) seem to be irrelevant in this production process. Nevertheless, calcification rates and the success of calcifying organisms in the oceans often correlate surprisingly well with these two carbonate system parameters. This study addresses this dilemma through rearrangement of carbonate system equations which revealed an important proportionality between [CO32−] or ΩCaCO3 and the ratio of [HCO3−] to [H+]. Due to this proportionality, calcification rates will always correlate equally well with [HCO3−]/[H+] as with [CO32−] or ΩCaCO3 when temperature, salinity, and pressure are constant. Hence, [CO32−] and ΩCaCO3 may simply be very good proxies for the control by [HCO3−]/[H+] where [HCO3−] would be the inorganic carbon substrate and [H+] would function as calcification inhibitor. If the "substrate-inhibitor ratio" (i.e. [HCO3−]/[H+]) rather than [CO32−] or ΩCaCO3 controls CaCO3 formation then some of the most common paradigms in ocean acidification research need to be reviewed. For example, the absence of a latitudinal gradient in [HCO3−]/[H+] in contrast to [CO32−] and ΩCaCO3 could modify the common assumption that high latitudes are affected most severely by ocean acidification

Distinguishing between the effects of ocean acidification and ocean carbonation in the coccolithophore Emiliania huxleyi

The coccolithophore Emiliania huxleyi was cultured under a broad range of carbonate chemistry conditions to distinguish the effects of individual carbonate system parameters on growth, primary production, and calcification. In the first experiment, alkalinity was kept constant and the fugacity of CO2 (fCO2) varied from 2 to 600 Pa (1 Pa ≈ 10 µatm). In the second experiment, pH was kept constant (pHfree = 8) with fCO2 varying from 4 to 370 Pa. Results of the constant-alkalinity approach revealed physiological optima for growth, calcification, and organic carbon production at fCO2 values of ∼ 20 Pa, ∼ 40 Pa, and ∼ 80 Pa, respectively. Comparing this with the constant-pH approach showed that growth and organic carbon production increased similarly from low to intermediate CO2 levels but started to diverge towards higher CO2 levels. In the high CO2 range, growth rates and organic carbon production decreased steadily with declining pH at constant alkalinity while remaining consistently higher at constant pH. This suggests that growth and organic carbon production rates are directly related to CO2 at low (sub-saturating) concentrations, whereas towards higher CO2 levels they are adversely affected by the associated decrease in pH. A pH dependence at high fCO2 is also indicated for calcification rates, while the key carbonate system parameter determining calcification at low fCO2 remains unclear. These results imply that key metabolic processes in coccolithophores have their optima at different carbonate chemistry conditions and are influenced by different parameters of the carbonate system at both sides of the optimum

The Calcium Carbonate Shell of Emiliania huxleyi Provides Limited Protection Against Viral Infection

Coccolithophores are an important group of marine phytoplankton which cover themselves with the coccosphere – a shell composed of numerous calcium carbonate (CaCO3) platelets. Despite more than a century of coccolithophore research, it remains speculative why coccolithophores calcify. Resolving this question is essential to assess the competitive fitness of coccolithophores in the future ocean where changes in calcification are expected. Here, we used the Emiliania huxleyi – Emiliania huxleyi Virus 86 host-virus model system to test the hypothesis that the coccosphere serves as a physical barrier reducing viral infection. Therefore, we removed the coccosphere from living E. huxleyi cells and compared the infection progress relative to calcified cells in a series of 6 experiments under different growth conditions. We found that the coccosphere does not constitute an effective physical barrier against viral penetration, since non-growing calcified cells were susceptible to viral infection and lysis (growth stopped by light limitation). However, we also found that protection against the virus may depend on the daily growth cycle. E. huxleyi reached higher peak abundances when decalcified cells were allowed to rebuild their coccosphere before entering cell division phase and being exposed to the virus, thereby suggesting that rates of viral infection could be reduced by the coccosphere during the critical phase in the cell cycle. However, the benefit of this potential protection is arguably of limited ecological significance since the concentrations of both, calcified and decalcified E. huxleyi approached similar values until the end of the bloom. We conclude that the coccosphere provides at best a limited protection against infection with the EhV86

Can morphological features of coccolithophores serve as a reliable proxy to reconstruct environmental conditions of the past?

Morphological changes in coccoliths, tiny calcite platelets covering the outer surface of coccolithophores, can be induced by physiological responses to environmental changes. Coccoliths recovered from sedimentary successions may therefore provide information on paleo-environmental conditions prevailing at the time when the coccolithophores were alive. To calibrate the biomineralization responses of ancient coccolithophore to environmental changes, studies often compared the biological responses of living coccolithophore species with paleo-data from calcareous nannofossils. However, there is uncertainty whether the morphological responses of living coccolithophores are representative of those of the fossilized ancestors. To investigate this, we exposed four living coccolithophore species (Emiliania huxleyi, Gephyrocapsa oceanica, Coccolithus pelagicus subsp. braarudii, and Pleurochrysis carterae) that have been evolutionarily distinct for hundreds of thousands to millions of years, to a range of environmental conditions (i.e., changing light intensity, Mg∕Ca ratio, nutrient availability, temperature, and carbonate chemistry) and evaluated their responses in coccolith morphology (i.e., size, length, width, malformation). The motivation for this study was to test if there is a consistent morphological response of the four species to changes in any of the tested abiotic environmental factors. If this was the case, then this could suggest that coccolith morphology can serve as a paleo-proxy for that specific factor because this response is conserved across species that have been evolutionary distinct over geological timescales. However, we found that the four species responded differently to changing light intensity, Mg∕Ca ratio, nutrient availability, and temperature in terms of coccolith morphology. The lack of a common response reveals the difficulties in using coccolith morphology as a paleo-proxy for these environmental drivers. However, a common response was observed under changing seawater carbonate chemistry (i.e., rising CO2), which consistently induced malformations. This commonality provides some confidence that malformations found in the sedimentary record could be indicative of adverse carbonate chemistry conditions

Technical Note: Sampling and processing of mesocosm sediment trap material for quantitative biogeochemical analysis

Sediment traps are the most common tool to investigate vertical particle flux in the marine realm. However, the spatial and temporal decoupling between particle formation in the surface ocean and particle collection in sediment traps at depth often handicaps reconciliation of production and sedimentation even within the euphotic zone. Pelagic mesocosms are restricted to the surface ocean, but have the advantage of being closed systems and are therefore ideally suited to studying how processes in natural plankton communities influence particle formation and settling in the ocean's surface. We therefore developed a protocol for efficient sample recovery and processing of quantitatively collected pelagic mesocosm sediment trap samples for biogeochemical analysis. Sedimented material was recovered by pumping it under gentle vacuum through a silicon tube to the sea surface. The particulate matter of these samples was subsequently separated from bulk seawater by passive settling, centrifugation or flocculation with ferric chloride, and we discuss the advantages and efficiencies of each approach. After concentration, samples were freeze-dried and ground with an easy to adapt procedure using standard lab equipment. Grain size of the finely ground samples ranged from fine to coarse silt (2–63 µm), which guarantees homogeneity for representative subsampling, a widespread problem in sediment trap research. Subsamples of the ground material were perfectly suitable for a variety of biogeochemical measurements, and even at very low particle fluxes we were able to get a detailed insight into various parameters characterizing the sinking particles. The methods and recommendations described here are a key improvement for sediment trap applications in mesocosms, as they facilitate the processing of large amounts of samples and allow for high-quality biogeochemical flux data

CO2 effects on diatoms: A Synthesis of more than a decade of ocean acidification experiments with natural communities

Diatoms account for 40 % of marine primary production and are considered to be key players in the biological carbon pump. Ocean acidification (OA) is expected to affect diatoms primarily by changing the availability of CO2 as a substrate for photosynthesis or through altered ecological interactions within the marine food web. Yet, there is little consensus how entire diatom communities will respond to increasing CO2. To address this question, we synthesized the literature from over a decade of OA-experiments with natural diatom communities to uncover: 1) if and how bulk diatom communities respond to elevated CO2; 2) if shifts within the diatom communities could be expected and how they are expressed with respect to taxonomic affiliation and size structure. We found that diatom communities responded to high CO2 in ~60 % of the experiments and in this case more often positively (56 %) than negatively (32 %; 12 % did not report the direction of change). Shifts among different diatom species were observed in 65 % of the experiments. Our synthesis supports the hypothesis that high CO2 particularly favors larger species as 12 out of 13 experiments which investigated cell size found a shift towards larger species. Unraveling winners and losers with respect to taxonomic affiliation was difficult due to a limited database, but there is evidence that the genus Pseudo-nitzschia could be among the losers. We conclude that OA-induced changes in diatom competitiveness and assemblage structure must be classified as a “risk for ecosystem services” due to the pivotal role diatoms play in trophic transfer and biogeochemical cycles

Neue Erkenntnisse über die Auswirkungen der Ozeanversauerung auf marine Lebensgemeinschaften

New insights into the impact of oceanic acidification on marine life communities: The pelagic realm is the largest interconnected ecosystem on our planet. It is inhabited by an enormous diversity of organisms, ranging from microscopic plankton to huge baleen whales. All these organisms interact either directly or indirectly with each other in a complex food-web. The stability of the food-web is currently challenged by major anthropogenic perturbations. Among these perturbations is ocean acidification – the absorption of anthropogenic CO2 which reacts with seawater and causes a profound decline in seawater pH. New studies with natural plankton communities show that ocean acidification can re-structure marine food-webs and modify elemental cycles with possible consequences for ecosystem services on which humans depend

The modulating effect of light intensity on the response of the coccolithophore Gephyrocapsa oceanicato ocean acidification

Global change leads to a multitude of simultaneous modifications in the marine realm among which shoaling of the upper mixed layer, leading to enhanced surface layer light intensities, as well as increased carbon dioxide (CO2) concentration are some of the most critical environmental alterations for phytoplankton. In this study, we investigated the responses of growth, photosynthetic carbon fixation and calcification of the coccolithophore Gephyrocapsa oceanica to elevated inline image (51 Pa, 105 Pa, and 152 Pa) (1 Pa ≈ 10 μatm) at a variety of light intensities (50–800 μmol photons m−2 s−1). By fitting the light response curve, our results showed that rising inline image reduced the maximum rates for growth, photosynthetic carbon fixation and calcification. Increasing light intensity enhanced the sensitivity of these rate responses to inline image, and shifted the inline image optima toward lower levels. Combining the results of this and a previous study (Sett et al. 2014) on the same strain indicates that both limiting low inline image and inhibiting high inline image levels (this study) induce similar responses, reducing growth, carbon fixation and calcification rates of G. oceanica. At limiting low light intensities the inline image optima for maximum growth, carbon fixation and calcification are shifted toward higher levels. Interacting effects of simultaneously occurring environmental changes, such as increasing light intensity and ocean acidification, need to be considered when trying to assess metabolic rates of marine phytoplankton under future ocean scenarios

Neue Erkenntnisse über die Auswirkungen der Ozeanversauerung auf marine Lebensgemeinschaften

New insights into the impact of oceanic acidification on marine life communities: The pelagic realm is the largest interconnected ecosystem on our planet. It is inhabited by an enormous diversity of organisms, ranging from microscopic plankton to huge baleen whales. All these organisms interact either directly or indirectly with each other in a complex food-web. The stability of the food-web is currently challenged by major anthropogenic perturbations. Among these perturbations is ocean acidification – the absorption of anthropogenic CO2 which reacts with seawater and causes a profound decline in seawater pH. New studies with natural plankton communities show that ocean acidification can re-structure marine food-webs and modify elemental cycles with possible consequences for ecosystem services on which humans depend

Influence of ocean acidification on plankton community structure during a winter-to-summer succession: An imaging approach indicates that copepods can benefit from elevated CO2 via indirect food web effects

Plankton communities play a key role in the marine food web and are expected to be highly sensitive to ongoing environmental change. Oceanic uptake of anthropogenic carbon dioxide (CO2) causes pronounced shifts in marine carbonate chemistry and a decrease in seawater pH. These changes–summarized by the term ocean acidification (OA)–can significantly affect the physiology of planktonic organisms. However, studies on the response of entire plankton communities to OA, which also include indirect effects via food-web interactions, are still relatively rare. Thus, it is presently unclear how OA could affect the functioning of entire ecosystems and biogeochemical element cycles. In this study, we report from a long-term in situ mesocosm experiment, where we investigated the response of natural plankton communities in temperate waters (Gullmarfjord, Sweden) to elevated CO2 concentrations and OA as expected for the end of the century (~760 μatm pCO2). Based on a plankton-imaging approach, we examined size structure, community composition and food web characteristics of the whole plankton assemblage, ranging from picoplankton to mesozooplankton, during an entire winter-to-summer succession. The plankton imaging system revealed pronounced temporal changes in the size structure of the copepod community over the course of the plankton bloom. The observed shift towards smaller individuals resulted in an overall decrease of copepod biomass by 25%, despite increasing numerical abundances. Furthermore, we observed distinct effects of elevated CO2 on biomass and size structure of the entire plankton community. Notably, the biomass of copepods, dominated by Pseudocalanus acuspes, displayed a tendency towards elevated biomass by up to 30–40% under simulated ocean acidification. This effect was significant for certain copepod size classes and was most likely driven by CO2-stimulated responses of primary producers and a complex interplay of trophic interactions that allowed this CO2 effect to propagate up the food web. Such OA-induced shifts in plankton community structure could have far-reaching consequences for food-web interactions, biomass transfer to higher trophic levels and biogeochemical cycling of marine ecosystems