Reviews and Syntheses: Responses of coccolithophores to ocean acidification: a meta-analysis

Concerning their sensitivity to ocean acidification, coccolithophores, a group of calcifying single-celled phytoplankton, are one of the best-studied groups of marine organisms. However, in spite of the large number of studies investigating coccolithophore physiological responses to ocean acidification, uncertainties still remain due to variable and partly contradictory results. In the present study we have used all existing data in a meta-analysis to estimate the effect size of future pCO2 changes on the rates of calcification and photosynthesis and the ratio of particulate inorganic to organic carbon (PIC / POC) in different coccolithophore species. Our results indicate that ocean acidification has a negative effect on calcification and the cellular PIC / POC ratio in the two most abundant coccolithophore species: Emiliania huxleyi and Gephyrocapsa oceanica. In contrast, the more heavily calcified species Coccolithus braarudii did not show a distinct response when exposed to elevated pCO2/reduced pH. Photosynthesis in Gephyrocapsa oceanica was positively affected by high CO2, while no effect was observed for the other coccolithophore species. There was no indication that the method of carbonate chemistry manipulation was responsible for the inconsistent results regarding observed responses in calcification and the PIC / POC ratio. The perturbation method, however, appears to affect photosynthesis, as responses varied significantly between total alkalinity (TA) and dissolved inorganic carbon (DIC) manipulations. These results emphasize that coccolithophore species respond differently to ocean acidification, both in terms of calcification and photosynthesis. Where negative effects occur, they become evident at CO2 levels in the range projected for this century in the case of unabated CO2 emissions. As the data sets used in this meta-analysis do not account for adaptive responses, ecological fitness and ecosystem interactions, the question remains as to how these physiological responses play out in the natural environment

Arctic Ocean turning corrosive

The cold waters of the polar seas are naturally low in carbonate saturation. As uptake of anthropogenic CO2 continues to acidify the oceans worldwide, the Arctic Ocean will be the first to pass the chemical threshold where surface seawater becomes undersaturated, i.e. corrosive for unprotected shells and skeletons of calcifying organisms. While the overall impacts of ocean acidification on the Arctic ecosystems are still unknown, the predicted changes in seawater chemistry are expected to make it increasingly difficult for calcareous organisms to inhabit these regions

Effects of ocean acidification on marine dissolved organic matter are not detectable over the succession of phytoplankton blooms

Marine dissolved organic matter (DOM) is one of the largest active organic carbon reservoirs on Earth, and changes in its pool size or composition could have a major impact on the global carbon cycle. Ocean acidification is a potential driver for these changes because it influences marine primary production and heterotrophic respiration. We simulated ocean acidification as expected for a “business-as-usual” emission scenario in the year 2100 in an unprecedented long-term mesocosm study. The large-scale experiments (50 m3 each) covered a full seasonal cycle of marine production in a Swedish Fjord. Five mesocosms were artificially enriched in CO2 to the partial pressure expected in the year 2100 (900 μatm), and five more served as controls (400 μatm). We applied ultrahigh-resolution mass spectrometry to monitor the succession of 7360 distinct DOM formulae over the course of the experiment. Plankton blooms had a clear effect on DOM concentration and molecular composition. This succession was reproducible across all 10 mesocosms, independent of CO2 treatment. In contrast to the temporal trend, there were no significant differences in DOM concentration and composition between present-day and year 2100 CO2 levels at any time point of the experiment. On the basis of our results, ocean acidification alone is unlikely to affect the seasonal accumulation of DOM in productive coastal environments

Effects of long-term high CO₂ exposure on two species of coccolithophores

The physiological performance of two coccolithophore species, Emiliania huxleyi and Coccolithus braarudii, was investigated during long-term exposure to elevated pCO2 levels. Mono-specific cultures were grown over 152 (E. huxleyi) and 65 (C. braarudii) generations while pCO2 was gradually increased to maximum levels of 1150 μatm (E. huxleyi) and 930 μatm (C. braarudii) and kept constant thereafter. Rates of cell growth and cell quotas of particulate organic carbon (POC), particulate inorganic carbon (PIC) and total particulate nitrogen (TPN) were determined repeatedly throughout the incubation period. Increasing pCO2 caused a decrease in cell growth rate of 9% and 29% in E. huxleyi and C. braarudii, respectively. In both species cellular PIC:TPN and PIC:POC ratios decreased in response to rising pCO2, whereas no change was observed in the POC:TPN ratios of E. huxleyi and C. braarudii. These results are consistent with those obtained in shorter-term high CO2 exposure experiments following abrupt pertubations of the seawater carbonate system and indicate that for the strains tested here a gradual CO2 increase does not alleviate CO2/pH sensitivity

Factors controlling the formation of marine snow and its sustained residence in surface waters

The formation of large marine snow macroflocs and stringers was monitored at a fixed station in the southern North Sea. During an 18-month investigation, large marine snow floes occurred in the water column on nine occasions for periods lasting between 5 and 16 d. Their formation coincided with both high phytoplankton biomass and low windspeeds. Retention of marine snow in the surface layer was related to slow sinking, neutral buoyancy, and rising of the large floes. Applying a specially developed instrument showed buoyancy to be caused by gas bubbles incorporated in the floes. Marine snow flotation coincided with periods of oxygen supersaturation in the water column, suggesting that oxygen production could be responsible for gas bubble formation within the floes. Disappearance of the large marine snow floes from the surface layer coincided with drastic increases in windspeed, indicating that enhanced wind-induced turbulent mixing in the surface layer could have resulted in the breakup of these floes. Formation and disappearance of marine snow had a marked influence on the light regime in the water

CO2 and HCO3- uptake in marine diatoms acclimated to different CO2 concentrations.

Rates of cellular uptake of CO2 and HCO3- during steady-state photosynthesis were measured in the marine diatoms Thalassiosira weissflogii and Phaeodactylum tricornutum, acclimated to CO2 partial pressures of 36, 180, 360, and 1,800 ppmv. In addition, in vivo activity of extracellular (eCA) and intracellular (iCA) carbonic anhydrase was determined in relation to CO2 availability. Both species responded to diminishing CO2 supply with an increase in eCA and iCA activity. In P. tricornutum, eCA activity was close to the detection limit at higher CO2 concentrations. Simultaneous uptake of CO2 and HCO3- was observed in both diatoms. At air-equilibrated CO2 levels (360 ppmv), T. weissflogii took up CO2 and HCO3- at approximately the same rate, whereas CO2 uptake exceeded HCO3- uptake by a factor of two in P. tricornutum. In both diatoms, CO2 :HCO3- uptake ratios progressively decreased with decreasing CO2 concentration, whereas substrate affinities of CO2 and HCO3- uptake increased. Half-saturation concentrations were always <=5 mM CO2 for CO2 uptake and <700 mM HCO3- for HCO3- uptake. Our results indicate the presence of highly efficient uptake systems for CO2 and HCO3- in both diatoms at concentrations typically encountered in ocean surface waters and the ability to adjust uptake rates to a wide range of inorganic carbon supply

CO2 perturbation experiments: similarities and differences between dissolved inorganic carbon and total alkalinity manipulations

Increasing atmospheric carbon dioxide (CO2) through human activities and invasion of anthropogenic CO2 into the surface ocean alters the seawater carbonate chemistry, increasing CO2 and bicarbonate (HCO3−) at the expense of carbonate ion (CO32−) concentrations. This redistribution in the dissolved inorganic carbon (DIC) pool decreases pH and carbonate saturation state (Ω). Several components of the carbonate system are considered potential key variables influencing for instance calcium carbonate precipitation in marine calcifiers such as coccolithophores, foraminifera, corals, mollusks and echinoderms. Unravelling the sensitivities of marine organisms and ecosystems to CO2 induced ocean acidification (OA) requires well-controlled experimental setups and accurate carbonate system manipulations. Here we describe and analyse the chemical changes involved in the two basic approaches for carbonate chemistry manipulation, i.e. changing DIC at constant total alkalinity (TA) and changing TA at constant DIC. Furthermore, we briefly introduce several methods to experimentally manipulate DIC and TA. Finally, we examine responses obtained with both approaches using published results for the coccolithophore Emiliania huxleyi. We conclude that under most experimental conditions in the context of ocean acidification DIC and TA manipulations yield similar changes in all parameters of the carbonate system, which implies direct comparability of data obtained with the two basic approaches for CO2 perturbation

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