Ocean acidification reduces growth and calcification in a marine dinoflagellate

Ocean acidification is considered a major threat to marine ecosystems and may particularly affect calcifying organisms such as corals, foraminifera and coccolithophores. Here we investigate the impact of elevated pCO₂ and lowered pH on growth and calcification in the common calcareous dinoflagellate Thoracosphaera heimii. We observe a substantial reduction in growth rate, calcification and cyst stability of T. heimii under elevated pCO₂. Furthermore, transcriptomic analyses reveal CO₂ sensitive regulation of many genes, particularly those being associated to inorganic carbon acquisition and calcification. Stable carbon isotope fractionation for organic carbon production increased with increasing pCO₂ whereas it decreased for calcification, which suggests interdependence between both processes. We also found a strong effect of pCO₂ on the stable oxygen isotopic composition of calcite, in line with earlier observations concerning another T. heimii strain. The observed changes in stable oxygen and carbon isotope composition of T. heimii cysts may provide an ideal tool for reconstructing past seawater carbonate chemistry, and ultimately past pCO₂. Although the function of calcification in T. heimii remains unresolved, this trait likely plays an important role in the ecological and evolutionary success of this species. Acting on calcification as well as growth, ocean acidification may therefore impose a great threat for T. heimii.

Reduced calcification and lack of acclimatization by coral colonies growing in areas of persistent natural acidification

As the surface ocean equilibrates with rising atmospheric CO₂, the pH of surface seawater is decreasing with potentially negative impacts on coral calcification. A critical question is whether corals will be able to adapt or acclimate to these changes in seawater chemistry. We use high precision CT scanning of skeletal cores of Porites astreoides, an important Caribbean reef-building coral, to show that calcification rates decrease significantly along a natural gradient in pH and aragonite saturation (Ω_arag). This decrease is accompanied by an increase in skeletal erosion and predation by boring organisms. The degree of sensitivity to reduced Ω_arag measured on our field corals is consistent with that exhibited by the same species in laboratory CO₂ manipulation experiments. We conclude that the Porites corals at our field site were not able to acclimatize enough to prevent the impacts of local ocean acidification on their skeletal growth and development, despite spending their entire lifespan in low pH, low Ω_arag seawater.

Response of benthic foraminifera to ocean acidification in their natural sediment environment: a long-term culturing experiment

Calcifying foraminifera are expected to be endangered by ocean acidification, However, the response of a complete community kept in natural sediment and over multiple generations under controlled laboratory conditions has not been constrained to date. During six month incubation, foraminiferal assemblages were treated with pCO₂ enriched seawater of 430, 907, 1865 and 3247 μatm pCO₂. The fauna was dominated by Ammonia aomoriensis and Elphidium species, whereas agglutinated species were rare. After 6 months incubation, pore water alkalinity was much higher in comparison to the overlying seawater. Consequently, the saturation state of Ω_calc was much higher in the sediment than in the water column in all pCO₂ treatments and remained close to saturation. As a result, the life cycle of living assemblages was largely unaffected by the tested pCO₂ treatments. Growth rates, reproduction and mortality, and therefore population densities and size-frequency distribution of Ammonia aomoriensis varied markedly during the experimental period. Growth rates varied between 25 and 50 μm per month, which corresponds to an addition of 1 or 2 new chambers per month. According to the size-frequency distribution, foraminifera start reproduction at a diameter of 250 μm. Mortality of large foraminifera was recognized, commencing at a test size of 285 μm at a pCO₂ ranging from 430 to 1865 μatm, and of 258 μm at 3247 μatm. The total organic content of living Ammonia aomoriensis has been determined to be 4.3% of dry weight. Living individuals had a calcium carbonate production rate of 0.47 g m⁻² yr⁻¹, whereas dead empty tests accumulated at a rate of 0.27 g m⁻² a⁻¹. Although Ω_calc was close to 1, some empty tests of Ammonia aomoriensis showed dissolution features at the end of incubation. In contrast, tests of the subdominant species, Elphidium incertum, stayed intact. This species specific response could be explained by differences in the elemental test composition, in particular the higher Mg-concentrations in Ammonia aomoriensis tests. Our results emphasize that the sensitivity to ocean acidification of endobenthic foraminifera in their natural sediment habitat is much lower compared to the experimental response of specimens isolated from the sediment.

Effects of ocean acidification on growth and physiology of Ulva lactuca (Chlorophyta) in a rockpool-scenario

Rising atmospheric CO₂-concentrations will have severe consequences for a variety of biological processes. We investigated the responses of the green alga Ulva lactuca (Linnaeus) to rising CO₂-concentrations in a rockpool scenario. U. lactuca was cultured under aeration with air containing either preindustrial pCO₂ (280 μatm) or the pCO₂ predicted by the end of the 21st century (700 μatm) for 31 days. We addressed the following question: Will elevated CO₂-concentrations affect photosynthesis (net photosynthesis, maximum relative electron transport rate (rETR(max)), maximum quantum yield (Fv/Fm), pigment composition) and growth of U. lactuca in rockpools with limited water exchange? Two phases of the experiment were distinguished: In the initial phase (day 1–4) the Seawater Carbonate System (SWCS) of the culture medium could be adjusted to the selected atmospheric pCO₂ condition by continuous aeration with target pCO₂ values. In the second phase (day 4–31) the SWCS was largely determined by the metabolism of the growing U. lactuca biomass. In the initial phase, Fv/Fm and rETR(max) were only slightly elevated at high CO₂-concentrations, whereas growth was significantly enhanced. After 31 days the Chl a content of the thalli was significantly lower under future conditions and the photosynthesis of thalli grown under preindustrial conditions was not dependent on external carbonic anhydrase. Biomass increased significantly at high CO₂-concentrations. At low CO₂-concentrations most adult thalli disintegrated between day 14 and 21, whereas at high CO₂-concentrations most thalli remained integer until day 31. Thallus disintegration at low CO₂-concentrations was mirrored by a drastic decline in seawater dissolved inorganic carbon and HCO₃⁻. Accordingly, the SWCS differed significantly between the treatments. Our results indicated a slight enhancement of photosynthetic performance and significantly elevated growth of U. lactuca at future CO₂-concentrations. The accelerated thallus disintegration at high CO₂-concentrations under conditions of limited water exchange indicates additional CO₂ effects on the life cycle of U. lactuca when living in rockpools.

Sensitivity of Antarctic phytoplankton species to ocean acidification: growth, carbon acquisition, and species interaction

Despite the fact that ocean acidification is considered to be especially pronounced in the Southern Ocean, little is known about CO₂-dependent physiological processes and the interactions of Antarctic phytoplankton key species. We therefore studied the effects of CO₂ partial pressure (P_CO2) (16.2, 39.5, and 101.3 Pa) on growth and photosynthetic carbon acquisition in the bloom-forming species Chaetoceros debilis, Pseudo-nitzschia subcurvata, Fragilariopsis kerguelensis, and Phaeocystis antarctica. Using membrane-inlet mass spectrometry, photosynthetic O₂ evolution and inorganic carbon (C_i) fluxes were determined as a function of CO₂ concentration. Only the growth of C. debilis was enhanced under high P_CO2. Analysis of the carbon concentrating mechanism (CCM) revealed the operation of very efficient CCMs (i.e., high C_i affinities) in all species, but there were species-specific differences in CO₂-dependent regulation of individual CCM components (i.e., CO₂ and uptake kinetics, carbonic anhydrase activities). Gross CO₂ uptake rates appear to increase with the cell surface area to volume ratios. Species competition experiments with C. debilis and P. subcurvata under different P_CO2 levels confirmed the CO₂-stimulated growth of C. debilis observed in monospecific incubations, also in the presence of P. subcurvata. Independent of P_CO2, high initial cell abundances of P. subcurvata led to reduced growth rates of C. debilis. For a better understanding of future changes in phytoplankton communities, CO₂-sensitive physiological processes need to be identified, but also species interactions must be taken into account because their interplay determines the success of a species.

Effects of sub-lethal CO2(aq) concentrations on the performance of intensively reared gilthead seabream (Sparus aurata) in brackish water: flow-through experiments and full-scale RAS results

The effects sub-lethal CO_2(aq) concentrations were tested for the first time on gilthead seabream (Sparus aurata) juveniles (4 to 25 g; 64 growth days) and adult (∼300-400 g; 71 days) fish, both in fully controlled pilot tests and the latter also as part of full-scale RAS (recirculating aquaculture system) operation. In the pilot experiments (concentration range 5.2 to 56.3 mgCO₂/L) the specific growth rate, mortality rate, and physical fish disorders were monitored. In the full scale experiment, two groups of fish, originally from the same batch, were exposed for 197 days to controlled (by NaOH dosage) and uncontrolled pH conditions, resulting in exposure of the fish to significantly different CO_2(aq) concentrations. The pilot results showed, as expected, that the seabream fish grew faster at the lower CO₂ concentrations and that the growth rate of both juveniles and adult fish was only minimally inhibited up to roughly 20 mg CO₂/L (compared to a previously published curve). Mortality rate was considerable only at the highest CO₂ concentration (∼56 mgCO₂/L). Physical irregularities were not observed, apart from abnormally-high absence of swim bladder at the highest CO_2(aq) treatment. The (statistically significant) results from the full-scale RAS operation showed that growing gilthead seabream for 197 days at roughly constant and relatively low (∼16 mg/L) CO_2(aq) concentration resulted in fish with ∼10% larger mean weight relative to the fish grown in ponds in which CO_2(aq) was not controlled and its concentration fluctuated daily between 19 and 37 mg/L.

Responses of the Emiliania huxleyi proteome to ocean acidification

Ocean acidification due to rising atmospheric CO2 is expected to affect the physiology of important calcifying marine organisms, but the nature and magnitude of change is yet to be established. In coccolithophores, different species and strains display varying calcification responses to ocean acidification, but the underlying biochemical properties remain unknown. We employed an approach combining tandem mass-spectrometry with isobaric tagging (iTRAQ) and multiple database searching to identify proteins that were differentially expressed in cells of the marine coccolithophore species Emiliania huxleyi (strain NZEH) between two CO2 conditions: 395 (~current day) and ~1340 p.p.m.v. CO2. Cells exposed to the higher CO2 condition contained more cellular particulate inorganic carbon (CaCO3) and particulate organic nitrogen and carbon than those maintained in present-day conditions. These results are linked with the observation that cells grew slower under elevated CO2, indicating cell cycle disruption. Under high CO2 conditions, coccospheres were larger and cells possessed bigger coccoliths that did not show any signs of malformation compared to those from cells grown under present-day CO2 levels. No differences in calcification rate, particulate organic carbon production or cellular organic carbon: nitrogen ratios were observed. Results were not related to nutrient limitation or acclimation status of cells. At least 46 homologous protein groups from a variety of functional processes were quantified in these experiments, of which four (histones H2A, H3, H4 and a chloroplastic 30S ribosomal protein S7) showed down-regulation in all replicates exposed to high CO2, perhaps reflecting the decrease in growth rate. We present evidence of cellular stress responses but proteins associated with many key metabolic processes remained unaltered. Our results therefore suggest that this E. huxleyi strain possesses some acclimation mechanisms to tolerate future CO2 scenarios, although the observed decline in growth rate may be an overriding factor affecting the success of this ecotype in future oceans.

Growth performance of microalgae exposed to CO2

The increase of CO₂ emission and other gases of greenhouse effect have caused global debates concerning climatic alterations, stimulating the development of mitigative strategies. Researches in this area include CO₂ kidnapping through aquatic microalgae production, as well as their use in the production of biofuels. The aim of this work was to determine the growth kinetics of microalgae (Chlorella sp, Scenedesmus spinosus, Scenedesmus acuminatus and Coelastrum sp.) exposed directly to CO₂. Measurements of microalgae growth and pH from medium were taken weekly. The results showed that carbon dioxide promoted growth inhibition in most microalgae. This condition should be considered for the developing of operational strategies and in projects of photobioreactors for the biological conversion of CO₂.

Synergism between elevated pCO2 and temperature on the Antarctic sea ice diatom Nitzschia lecointei

Polar oceans are particularly susceptible to ocean acidification and warming. Diatoms play a significant role in sea ice biogeochemistry and provide an important food source to grazers in ice-covered oceans, especially during early spring. However, the ecophysiology of ice living organisms has received little attention in terms of ocean acidification. In this study, the synergism between temperature and partial pressure of CO₂ (pCO₂) was investigated in relationship to the optimal growth temperature of the Antarctic sea ice diatom Nitzschia lecointei. Diatoms were kept in cultures at controlled levels of pCO₂ (∼390 and ∼960 μatm}) and temperature (−1.8 and 2.5 °C) for 14 days. Synergism between temperature and pCO₂ was detected in growth rate and acyl lipid fatty acid content. Carbon enrichment only promoted (3%) growth rate closer to the optimal growth, but not at the control temperature (−1.8 °C). Optimal growth rate was observed around 5 °C in a separate experiment. Polyunsaturated fatty acids (PUFA) comprised up to 98% of the total acyl lipid fatty acid pool at −1.8 °C. However, the total content of fatty acids was reduced by 39% at elevated pCO₂, but only at the control temperature. PUFAs were reduced by 30% at high pCO₂. Effects of carbon enrichment may be different depending on ocean warming scenario or season, e.g. reduced food quality for higher trophic levels during spring. Synergy between temperature and pCO₂ may be particularly important in polar areas since a narrow thermal window generally limits cold-water organisms.

Effects of ocean acidification on juvenile red king crab (Paralithodes camtschaticus) and tanner crab (Chionoecetes bairdi) growth, condition, calcification, and survival

Ocean acidification, a decrease in the pH in marine waters associated with rising atmospheric CO₂ levels, is a serious threat to marine ecosystems. In this paper, we determine the effects of long-term exposure to near-future levels of ocean acidification on the growth, condition, calcification, and survival of juvenile red king crabs, Paralithodes camtschaticus, and Tanner crabs, Chionoecetes bairdi. Juveniles were reared in individual containers for nearly 200 days in flowing control (pH 8.0), pH 7.8, and pH 7.5 seawater at ambient temperatures (range 4.4–11.9 °C). In both species, survival decreased with pH, with 100% mortality of red king crabs occurring after 95 days in pH 7.5 water. Though the morphology of neither species was affected by acidification, both species grew slower in acidified water. At the end of the experiment, calcium concentration was measured in each crab and the dry mass and condition index of each crab were determined. Ocean acidification did not affect the calcium content of red king crab but did decrease the condition index, while it had the opposite effect on Tanner crabs, decreasing calcium content but leaving the condition index unchanged. This suggests that red king crab may be able to maintain calcification rates, but at a high energetic cost. The decrease in survival and growth of each species is likely to have a serious negative effect on their populations in the absence of evolutionary adaptation or acclimatization over the coming decades.