A unifying concept of coccolithophore sensitivity to changing carbonate chemistry embedded in an ecological framework

Abstract

a b s t r a c tCoccolithophores 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 (HCO 3 À ), the primary substrate for calcification, and carbon dioxide (CO 2 ), 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 (CaCO 3 ) sediment dissolution and terrestrial weathering begin to increase the oceans' HCO 3 À 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.

A Conceptual Model for Projecting Coccolithophorid Growth, Calcification and Photosynthetic Carbon Fixation Rates in Response to Global Ocean Change

“…This analytical equation was later modified and improved for fitting calcification rates in Bach et al (2015). Although also a modified Michaelis-Menten equation, hydrogen ions (H + ), rather than f CO 2 , had been identified as the actual inhibiting factor influencing biological rates.…”

“…However, no decoupled data currently exists for G. oceanica. In order to test if Equation (8) could describe responses for coupled and decoupled carbonate chemistry we fitted the equation to data on coupled and decoupled E. huxleyi experiments as in Bach et al (2015). All data was first standardized following procedures described in section 2.2.…”

“…Contour lines were produced using Equation (8) and fit coefficients derived from E. huxleyi data presented in Bach et al (2015) (see section 2.9 for details). Colors indicate projected (contour lines) and measured (dots) calcification rates.…”

“…To test whether our conceptual model (Equation 8) could correctly fit responses to decoupled carbonate chemistry if data was available, it was applied to a combination of decoupled and coupled data of E. huxleyi used in Bach et al (2015) at constant light and temperature. For coupled carbonate systems (Constant TA) rates showed an optimum curve response (See constant TA line in Figure 7), while the decoupled carbonate chemistry system showed a Michaelis-Menten response curve (See constant pH line in Figure 7).…”

“…Previous studies (i.e., Bach et al, 2011;Sett et al, 2014;Bach et al, 2015), have established a unifying frame work where coccolithophore responses to carbonate chemistry can be described as a balance between the fertilizing effects of substrate (CO 2 and HCO − 3 ) availability (Bach et al, 2011) and the inhibiting effects of hydrogen ions (H + ) (Bach et al, 2011(Bach et al, , 2013. At one end of the scale, process-based numerical models describing intra-cellular inorganic carbon fluxes in response to changes in seawater carbonate chemistry and the resulting effects on coccolithophorid metabolic rates have been developed using this framework (Holtz et al, 2015a,b).…”