Heterogeneity of impacts of high CO2 on the North Western European Shelf

The increase in atmospheric CO₂ is a dual threat to the marine environment: from one side it drives climate change leading to changes in water temperature, circulation patterns and stratification intensity; on the other side it causes a decrease in pH (Ocean Acidification or OA) due to the increase in dissolved CO₂. Assessing the combined impact of climate change and OA on marine ecosystems is a challenging task: the response of the ecosystem to a single driver is highly variable and still uncertain, as well as the interaction between these that could be either synergistic or antagonistic. In this work we use the coupled oceanographic-ecosystem model POLCOMS-ERSEM driven by climate forcing to study the interaction between climate change and OA. We focus in particular on primary production and nitrogen speciation. The model has been run in three different configurations in order to separate the impacts of ocean acidification from those due to climate change. The model shows significant interaction among the drivers and high variability in the spatial response of the ecosystem. Impacts of climate change and of OA on primary production have similar magnitude, compensating in some area and exacerbating in others. On the contrary, the direct impact of OA on nitrification is much lower than the one imposed by climate change.

Environmental controls on the Emiliania huxleyi calcite mass

Abstract. Although ocean acidification is expected to impact (bio)calcification by decreasing the seawater carbonate ion concentration, [CO₃²⁻], there exists evidence of non-uniform response of marine calcifying plankton to low seawater [CO₃²⁻]. This raises questions on the role of environmental factors other than acidification and on the complex physiological responses behind calcification. Here we investigate the synergistic effect of multiple environmental parameters, including temperature, nutrient (nitrate and phosphate) availability, and seawater carbonate chemistry on the coccolith calcite mass of the cosmopolitan coccolithophore Emiliania huxleyi, the most abundant species in the world ocean. We use a suite of surface (late Holocene) sediment samples from the South Atlantic and southwestern Indian Ocean taken from depths lying well above the modern lysocline. The coccolith calcite mass in our results presents a latitudinal distribution pattern that mimics the main oceanographic features, thereby pointing to the potential importance of phosphorus and temperature in determining coccolith mass by affecting primary calcification and possibly driving the E. huxleyi morphotype distribution. This evidence does not necessarily argue against the potentially important role of the rapidly changing seawater carbonate chemistry in the future, when unabated fossil fuel burning will likely perturb ocean chemistry beyond a critical point. Rather our study highlights the importance of evaluating the combined effect of several environmental stressors on calcifying organisms to project their physiological response(s) in a high CO₂ world and improve interpretation of paleorecords.

Ocean acidification alters the photosynthetic responses of a coccolithophorid to fluctuating UV and visible radiation

Mixing of seawater subjects phytoplankton to fluctuations in photosynthetically active radiation (PAR, 400-700nm) and ultraviolet radiation (UVR, 280-400nm). These irradiance fluctuations are now superimposed upon ocean acidification and thinning of the upper mixing layer through stratification, that alters mixing regimes. We therefore examined the photosynthetic carbon fixation and photochemical performance of a coccolithophore, Gephyrocapsa oceanica grown under high, future (1000 μatm) and low, current (390 μatm) CO2 levels, under regimes of fluctuating irradiances with or without UVR. Under both CO2 levels, fluctuating irradiances, as compared to constant irradiance, led to lower non-photochemical quenching (NPQ) and less UVR-induced inhibition of carbon fixation and PSII electron transport. The cells grown under high CO2 showed a lower photosynthetic carbon fixation rate, but lower NPQ and less UVB (280-315 nm)-induced inhibition. UVA (315-400 nm) led to less enhancement of the photosynthetic carbon fixation in the high CO2-grown cells under fluctuating irradiance. Our data suggest that ocean acidification and fast mixing or fluctuation of solar radiation will act synergistically to lower carbon fixation by G. oceanica, though ocean acidification may decrease UVB-related photochemical inhibition.

Buffer capacity of the coelomic fluid in echinoderms

The increase in atmospheric CO₂ due to anthropogenic activity results in an acidification of the surface waters of the oceans. The impact of these chemical changes depends on the considered organisms. In particular, it depends on the ability of the organism to control the pH of its inner fluids. Among echinoderms, this ability seems to differ significantly according to species or taxa. In the present paper, we investigated the buffer capacity of the coelomic fluid in different echinoderm taxa as well as factors modifying this capacity. Euechinoidea (sea urchins except Cidaroidea) present a very high buffer capacity of the coelomic fluid (from 0.8 to 1.8 mmol kg^- 1 SW above that of seawater) while Cidaroidea (other sea urchins), starfish and holothurians have a significantly lower one (from − 0.1 to 0.4 mmol kg^- 1 SW compared to seawater). We hypothesize that this is linked to the more efficient gas exchange structures present in the three last taxa whereas Euechinoidea evolved specific buffer systems to compensate lower gas exchange abilities. The constituents of the buffer capacity and the factors influencing it were investigated in the sea urchin Paracentrotus lividus and the starfish Asterias rubens. Buffer capacity is primarily due to the bicarbonate buffer system of seawater (representing about 63% for sea urchins and 92% for starfish). It is also partly due to coelomocytes present in the coelomic fluid (around 8% for both) and, in P. lividus only, a compound of an apparent size larger than 3 kDa is involved (about 15%). Feeding increased the buffer capacity in P. lividus (to a difference with seawater of about 2.3 mmol kg^- 1 SW compared to unfed ones who showed a difference of about 0.5 mmol kg^- 1 SW) but not in A. rubens (difference with seawater of about 0.2 for both conditions). In P. lividus, decreased seawater pH induced an increase of the buffer capacity of individuals maintained at pH 7.7 to about twice that of the control individuals and, for those at pH 7.4, about three times. This allowed a partial compensation of the coelomic fluid pH for individuals maintaind at pH 7.7 but not for those at pH 7.4.

Can the combination of decreased pH and increased temperature values induce oxidative stress in the clam Chamelea gallina and the mussel Mytilus galloprovincialis?

The combined effects of decreased pH and increased temperature values on antioxidant enzyme activities and lipid peroxidation were evaluated for the first time in the clam Chamelea gallina and the mussel Mytilus galloprovincialis, two bivalve species that are widespread along the northwestern coast of the Adriatic Sea. For 7 days, bivalves were exposed to three pH values (8.1, 7.7 and 7.4) at two temperatures (22 and 28 °C). Three independent experiments were carried out at salinity values of 28, 34 and 40 psu. Superoxide dismutase, catalase and glutathione S-transferase activities as well as lipid peroxidation were measured in the gills and digestive gland of the bivalves. The results demonstrated that the experimental conditions significantly influenced the biochemical parameters of the bivalves, although the variation pattern varied depending on the species and tissues analysed.

The response of nitrogen-limited marine phytoplankton to increasing carbon dioxide

With atmospheric carbon dioxide (CO2) concentrations rising rapidly as a result of anthropogenic emissions, understanding the potential of the ocean to store carbon is more important than ever. Nitrogen (N) limits primary production in large parts of the ocean, and hence the export of inorganic carbon to deep waters. The response of marine phytoplankton to this ongoing increase in CO2 is unknown, especially whether the critical C:N ratio of phytoplankton biomass will deviate from canonical values at high CO2. In regions of the ocean where nitrogen supply is limited, the C:N ratio of the phytoplankton biomass determines how much organic carbon can be exported from the surface to the deep, i.e. the efficiency of the biological pump. A change in C:N at high CO2 could lead to a significant feedback to increasing atmospheric CO2. In this thesis, I address the question of how C:N ratios of N-limited phytoplankton may change with CO2 concentration by conducting a combination of field work with natural populations of phytoplankton and laboratory experiments with model organisms under well defined conditions. The primary goals of this work were to identify trends in C:N ratios with CO2 under N-limiting conditions and to elucidate the underlying mechanisms responsible for any such trends. In the field, the C:N ratios of phytoplankton biomass showed a modest increase from low to high CO2 in 4 out of 5 N-limited experiments due chiefly to an increase in particulate organic carbon (POC). In contrast, parallel experiments under N-replete conditions showed no change in C:N ratios. Diatoms and coccolithophores accounted for an important fraction of the ambient phytoplankton population in the N-limited experiments that showed an effect of CO2 on the C:N ratio of the biomass, while cyanobacteria were dominant in the experiment that showed no effect. The concentration of Rubisco enzyme decreased at high CO2 in several N-limited experiments, but this decrease did not account for the change in C:N since it was only a small fraction of total protein. Contrary to the long-held assumption that Rubisco may account for up to half of total protein in phytoplankton, Rubisco concentrations represented less than 6% of total protein in laboratory cultures of eight species of microalgae and also in field experiments. Rubisco concentrations increased with growth rates. Theoretical calculations using our data suggest that phytoplankton contain the minimum amount of enzyme necessary to support their growth rates. Rubisco was also observed to decrease with increasing CO2 in some experiments, implying that the enzyme may not be completely saturated at ambient conditions. However, the low concentration of Rubisco in phytoplankton makes such a response to CO2 insignificant in terms of the overall C:N composition of the organisms. To follow-up on the field results, I investigated the effects of varying CO2 in continuous cultures of one coccolithophore and two diatoms under N-limitation. The C:N ratio of all species increased with decreasing growth rate as expected. As previously reported, the C:N ratio of the coccolithophore Emiliania huxleyi increased at high CO2 due to an increase in cellular carbon. Unexpectedly, I observed a significant increase in the C:N ratio of the two diatoms, Thalassiosira weissflogii and Thalassiosira oceanica, at very low CO2. However the C:N ratio remained essentially constant as the CO2 concentration was increased from current to greater values. Because diatoms are the major contributors to the biological pump and coccolithophores minor contributors, my results, if confirmed and generalizable to other species, imply that little change should be expected in the stoichiometry of the sinking biomass as CO2 increases in surface seawater. Contrary to land plants, marine phytoplankton are unlikely to increase the sequestration of CO2 and provide a negative feedback to the ongoing increase in atmospheric CO2. I note however, that the surprising increase in the C:N ratio of diatoms at low CO2 may be relevant to glacial/interglacial processes when the atmospheric CO2 concentration decreased below 200 parts per million (ppm), about half of what it is today.

Short-term acute hypercapnia affects cellular responses to trace metals in the hard clams Mercenaria mercenaria

Estuarine and coastal habitats experience large fluctuations of environmental factors such as temperature, salinity, partial pressure of CO₂ (P_CO2) and pH; they also serve as the natural sinks for trace metals. Benthic filter-feeding organisms such as bivalves are exposed to the elevated concentrations of metals in estuarine water and sediments that can strongly affect their physiology. The effects of metals on estuarine organisms may be exacerbated by other environmental factors. Thus, a decrease in pH caused by high P_CO2 (hypercapnia) can modulate the effects of trace metals by affecting metal bioavailability, accumulation or binding. To better understand the cellular mechanisms of interactions between P_CO2 and trace metals in marine bivalves, we exposed isolated mantle cells of the hard clams (Mercenaria mercenaria) to different levels of P_CO2 (0.05, 1.52 and 3.01 kPa) and two major trace metal pollutants – cadmium (Cd) and copper (Cu). Elevated P_CO2 resulted in a decrease in intracellular pH (pH_i) of the isolated mantle cells from 7.8 to 7.4. Elevated P_CO2 significantly but differently affected the trace metal accumulation by the cells. Cd uptake was suppressed at elevated P_CO2 levels while Cu accumulation has greatly accelerated under hypercapnic conditions. Interestingly, at higher extracellular Cd levels, labile intracellular Cd²⁺ concentration remained the same, while intracellular levels of free Zn²⁺ increased suggesting that Cd²⁺ substitutes bound Zn²⁺ in these cells. In contrast, Cu exposure did not affect intracellular Zn²⁺ but led to a profound increase in the intracellular levels of labile Cu²⁺ and Fe²⁺. An increase in the extracellular concentrations of Cd and Cu led to the elevated production of reactive oxygen species under the normocapnic conditions (0.05 kPa P_CO2); surprisingly, this effect was mitigated in hypercapnia (1.52 and 3.01 kPa). Overall, our data reveal complex and metal-specific interactions between the cellular effects of trace metals and P_CO2 in clams and indicate that variations in environmental P_CO2 may modulate the biological effects of trace metals in marine organisms.

The elemental composition of purple sea urchin (Strongylocentrotus purpuratus) calcite and potential effects of pCO2 during early life stages (update)

Ocean acidification will likely have negative impacts on invertebrates producing skeletons composed of calcium carbonate. Skeletal solubility is partly controlled by the incorporation of “foreign” ions (e.g. magnesium) into the crystal lattice of these skeletal structures, a process that is sensitive to a variety of biological and environmental factors. Here we explore effects of life stage, oceanographic region of origin, and changes in the partial pressure of carbon dioxide in seawater (pCO₂) on trace elemental composition in the purple sea urchin (Strongylocentrotus purpuratus). We show that, similar to other urchin taxa, adult purple sea urchins have the ability to precipitate skeleton composed of a range of biominerals spanning low- to high-Mg calcites. Mg / Ca and Sr / Ca ratios were substantially lower in adult spines compared to adult tests. On the other hand, trace elemental composition was invariant among adults collected from four oceanographically distinct regions spanning a range of carbonate chemistry conditions (Oregon, Northern California, Central California, and Southern California). Skeletons of newly settled juvenile urchins that originated from adults from the four regions exhibited intermediate Mg / Ca and Sr / Ca between adult spine and test endmembers, indicating that skeleton precipitated during early life stages is more soluble than adult spines and less soluble than adult tests. Mean skeletal Mg / Ca or Sr / Ca of juvenile skeleton did not vary with source region when larvae were reared under present-day, global-average seawater carbonate conditions (400 μatm; pH_T = 8.02 ± 0.03 1 SD; Ω_calcite = 3.3 ± 0.2 1 SD). However, when reared under elevated pCO₂ (900 μatm; pH_T = 7.73 ± 0.03; Ω_calcite = 1.8 ± 0.1), skeletal Sr / Ca in juveniles exhibited increased variance across the four regions. Although larvae from the northern populations (Oregon, Northern California, Central California) did not exhibit differences in Mg or Sr incorporation under elevated pCO₂ (Sr / Ca = 2.10 ± 0.06 mmol mol⁻¹; Mg / Ca = 67.4 ± 3.9 mmol mol⁻¹), juveniles of Southern California origin partitioned ~8% more Sr into their skeletons when exposed to higher pCO₂ (Sr / Ca = 2.26 ± 0.08 vs. 2.09 ± 0.005 mmol mol⁻¹ 1 SD). Together these results suggest that the diversity of carbonate minerologies present across different skeletal structures and life stages in purple sea urchins does not translate into an equivalent geochemical plasticity of response associated with geographic variation or temporal shifts in seawater properties. Rather, composition of S. purpuratus skeleton precipitated during both early and adult life history stages appears relatively robust to spatial gradients and predicted future changes in carbonate chemistry. An exception to this trend may arise during early life stages, where certain populations of purple sea urchins may alter skeletal mineral precipitation rates and composition beyond a given pCO₂ threshold. This potential for geochemical plasticity during early development in contrast to adult stage geochemical resilience adds to the growing body of evidence that ocean acidification can have differing effects across organismal life stages.

Effects of elevated pCO2 on the metabolism of a temperate rhodolith Lithothamnion corallioides grown under different temperatures

Coralline algae are considered among the most sensitive species to near future ocean acidification. We tested the effects of elevated pCO₂ on the metabolism of the free living coralline alga Lithothamnion corallioides (“maerl”) and the interactions with changes in temperature. Specimens were collected in North Brittany (France) and grown for 3 months at pCO₂ of 380 (ambient pCO₂), 550, 750 and 1000 μatm (elevated pCO₂) and at successive temperatures of 10°C (ambient temperature in winter), 16°C (ambient temperature in summer) and 19°C (ambient temperature in summer + 3°C). At each temperature, gross primary production, respiration (oxygen flux) and calcification (alkalinity flux) rates were assessed in the light and dark. Pigments were determined by HPLC. Chl a, carotene and zeaxanthin were the three major pigments found in L. corallioides thalli. Elevated pCO₂ did not affect pigment content while temperature slightly decreased zeaxanthin and carotene content at 10°C. Gross production was not affected by temperature but was significantly affected by pCO₂ with an increase between 380 and 550 μatm. Light, dark and diel (24 h) calcification rates strongly decreased with increasing pCO₂ regardless of the temperature. Although elevated pCO₂ only slightly affected gross production in L. corallioides, diel net calcification was reduced by up to 80 % under the 1000 μatm treatment. Our findings suggested that near future levels of CO₂ will have profound consequences for carbon and carbonate budgets in rhodolith beds and for the sustainability of these habitats.

Multistressor impacts of warming and acidification of the ocean on marine invertebrates’ life histories

Benthic marine invertebrates live in a multistressor world where stressor levels are, and will continue to be, exacerbated by global warming and increased atmospheric carbon dioxide. These changes are causing the oceans to warm, decrease in pH, become hypercapnic, and to become less saturated in carbonate minerals. These stressors have strong impacts on biological processes, but little is known about their combined effects on the development of marine invertebrates. Increasing temperature has a stimulatory effect on development, whereas hypercapnia can depress developmental processes. The pH, pCO₂, and CaCO₃ of seawater change simultaneously with temperature, challenging our ability to predict future outcomes for marine biota. The need to consider both warming and acidification is reflected in the recent increase in cross-factorial studies of the effects of these stressors on development of marine invertebrates. The outcomes and trends in these studies are synthesized here. Based on this compilation, significant additive or antagonistic effects of warming and acidification of the ocean are common (16 of 20 species studied), and synergistic negative effects also are reported. Fertilization can be robust to near-future warming and acidification, depending on the male–female mating pair. Although larvae and juveniles of some species tolerate near-future levels of warming and acidification (+2°C/pH 7.8), projected far-future conditions (ca. ≥4°C/ ≤pH 7.6) are widely deleterious, with a reduction in the size and survival of larvae. It appears that larvae that calcify are sensitive both to warming and acidification, whereas those that do not calcify are more sensitive to warming. Different sensitivities of life-history stages and species have implications for persistence and community function in a changing ocean. Some species are more resilient than others and may be potential “winners” in the climate-change stakes. As the ocean will change more gradually over coming decades than in “future shock” perturbation investigations, it is likely that some species, particularly those with short generation times, may be able to tolerate near-future oceanic change through acclimatization and/or adaption.