Coccolithophore sensitivities to changing carbonate chemistry - an ecological framework

Coccolithophores are a group of unicellular phytoplankton species whose ability to calcify has a profound influence on biogeochemical element cycling. Calcification rates are controlled by a large variety of biotic and abiotic factors. Among these factors, carbonate chemistry has gained considerable attention during the last years as coccolithophores have been identified to be particularly sensitive to ocean acidification. Despite intense research in this area, a general concept harmonizing the numerous and sometimes (seemingly) contradictory responses of coccolithophores to changing carbonate chemistry is still lacking to date. Here, we present the "substrate-inhibitor concept" which describes the dependence of calcification rates on carbonate chemistry speciation. It is based on observations that calcification rate scales positively with bicarbonate (HCO3-), the primary substrate for calcification, and carbon dioxide (CO2), which can limit cell growth, whereas it is inhibited by protons (H+). This concept was implemented in a model equation, tested against experimental data, and then applied to understand and reconcile the diverging responses of coccolithophorid calcification rates to ocean acidification obtained in culture experiments. Furthermore, we (i) discuss how other important calcification-influencing factors (e.g. temperature and light) could be implemented in our concept and (ii) embed it in Hutchinson's niche theory, thereby providing a framework for how carbonate chemistry-induced changes in calcification rates could be linked with changing coccolithophore abundance in the oceans. Our results suggest that the projected increase of H+ in the near future (next couple of thousand years), paralleled by only a minor increase of inorganic carbon substrate, could impede calcification rates if coccolithophores are unable to fully adapt. However, if calcium carbonate (CaCO3) sediment dissolution and terrestrial weathering begin to increase the oceans' HCO3- and decrease its H+ concentrations in the far future (10 -100 kyears), coccolithophores could find themselves in carbonate chemistry conditions which may be more favorable for calcification than they were before the Anthropocene.

Experiment: changing carbonate chemistry influence on coccoliths formed by Emiliania huxleyi

The coccolithophore Emiliania huxleyi is a marine phytoplankton species capable of forming small calcium carbonate scales (coccoliths) which cover the organic part of the cell. Calcification rates of E. huxleyi are known to be sensitive to changes in seawater carbonate chemistry. It has, however, not yet been clearly determined how these changes are reflected in size and weight of individual coccoliths and which specific parameter(s) of the carbonate system drive morphological modifications. Here, we compare data on coccolith size, weight, and malformation from a set of five experiments with a large diversity of carbonate chemistry conditions. This diversity allows distinguishing the influence of individual carbonate chemistry parameters such as carbon dioxide (CO2), bicarbonate (HCO3- ), carbonate ion (CO32-), and protons (H+) on the measured parameters. Measurements of fine-scale morphological structures reveal an increase of coccolith malformation with decreasing pH suggesting that H+ is the major factor causing malformations. Coccolith distal shield area varies from about 5 to 11 µm2. Changes in size seem to be mainly induced by varying [HCO3- ] and [H+] although influence of [CO32-] cannot be entirely ruled out. Changes in coccolith weight were proportional to changes in size. Increasing CaCO3 production rates are reflected in an increase in coccolith weight and an increase of the number of coccoliths formed per unit time. The combined investigation of morphological features and coccolith production rates presented in this study may help to interpret data derived from sediment cores, where coccolith morphology is used to reconstruct calcification rates in the water column.