The effect of chronic and acute low pH on the intracellular DMSP production and epithelial cell morphology of red coralline algae

The release of dimethylsulphoniopropionate (DMSP) by marine algae has major impacts on the global sulphur cycle and may influence local climate through the formation of dimethylsulphide (DMS). However, the effect of global change on DMSP/DMS (DMS(P)) production by algae is not well understood. This study examined the effect of low pH on DMS(P) production and epithelial cell morphology of the free-living red coralline alga Lithothamnion glaciale. Three pH treatments were used in the 80-day experiment: (1) current pH level (8.18, control), (2) low, chronic pH representing a 2100 ocean acidification (OA) scenario (7.70) and (3) low, acute pH (7.75, with a 3-day spike to 6.47), representing acute variable conditions that might be associated with leaks from carbon capture and storage infrastructure, at CO₂ vent sites or in areas of upwelling. DMS(P) production was not significantly enhanced under low, stable pH conditions, indicating that red coralline algae may have some resilience to OA. However, intracellular and water column DMS(P) concentrations were significantly higher than the control when pH was acutely spiked. Cracks were observed between the cell walls of the algal skeleton in both low pH treatments. It is proposed that this structural change may cause membrane damage that allows DMS(P) to leak from the cells into the water column, with subsequent implications for the cycling of DMS(P) in coralline algae habitats.

Biochemical, metabolic and morphological responses of the intertidal gastropod Littorina littorea to ocean acidification and increase temperature

Future changes to the pH and temperature of the oceans are predicted to impact the biodiversity of marine ecosystems, particularly those animals that rely on the process of calcification. The marine intertidal gastropod Littorina littorea can be used as a model of intertidal organism for investigating the effects of ocean acidification and high temperature, alone and in combination because its ability to be quickly adapt against environmental stressor. In the first study a single species population of L. littorea was used to test for physiological and biochemical effects underpinning organismal responses to climate change and ocean acidification. Compared with control conditions, snails decreased metabolic rates by 31% in response to elevated pCO2 while by 15% in response to combined pCO2 and temperature. Decreased metabolic rates were associated with metabolic depression, a strategy to match oxygen demand and availability, and an increase in end-product metabolites in the tissue under acidified treatments, indicating an increased reliance on anaerobic metabolism. This study also showed that anthropogenic alteration of CO2 and temperature may also lead to plastic responses, a fundamental mechanism of many marine gastropods to cope environmental variability. At low pH and elevated temperature in isolation or combined showing lower shell growth than individuals kept under control conditions. Percentage change in shell length and thicknesses was also lower under acidified and temperature in isolation or combined than control condition, making shells were more globular and desiccation rates were higher. Further studies to broader latitudinal ranges for six populations of L. littorea showed that shell growth decreased in all six populations under elevated pCO2 compared to control snails particularly those at range edges. Elevated pCO2 also affected to the reduction of shell length and width that causing shell aspect ratio to increase across latitudinal gradients except individuals from Millport, UK. Percentage changes of aperture width and aperture area were also decrease under elevated pCO2 with greater reduction of aperture area were found at populations in the mid-ranges which is assumed this response might be linked to local adaptation of the individual to microclimatic conditions. This study also showed that metabolic rates were negatively affected by high pCO2 and show non-linear trend across latitudinal gradients in compared to individual kept under normal pCO2 conditions. Metabolomic analysis showed that two northern populations of Trondheim and TromsØ were distinct from other populations when exposed to low temperature (15 °C) with elevated pCO2 due to, in part, high concentrations of thymine, uracil, valine and lysine. A similar separation also occurred under medium (25 °C) and high (35 °C) temperature exposure in which one of northern population (Trondheim) was distinct from other populations and had lower concentrations of alanine, betaine and taurine while higher of valine. These results suggest that populations at northern latitudes may apply different ionic transport mechanisms under elevated pCO2 and elevated temperatures and those populations are likely to vary in terms of their physiological responses to this environmental challenge.

Marine bivalve shell geochemistry and ultrastructure from modern low pH environments: environmental effect versus experimental bias (update)

Bivalve shells can provide excellent archives of past environmental change but have not been used to interpret ocean acidification events. We investigated carbon, oxygen and trace element records from different shell layers in the mussels Mytilus galloprovincialis combined with detailed investigations of the shell ultrastructure. Mussels from the harbour of Ischia (Mediterranean, Italy) were transplanted and grown in water with mean pHT 7.3 and mean pHT 8.1 near CO2 vents on the east coast of the island. Most prominently, the shells recorded the shock of transplantation, both in their shell ultrastructure, textural and geochemical record. Shell calcite, precipitated subsequently under acidified seawater responded to the pH gradient by an in part disturbed ultrastructure. Geochemical data from all test sites show a strong metabolic effect that exceeds the influence of the low-pH environment. These field experiments showed that care is needed when interpreting potential ocean acidification signals because various parameters affect shell chemistry and ultrastructure. Besides metabolic processes, seawater pH, factors such as salinity, water temperature, food availability and population density all affect the biogenic carbonate shell archive.

Influence of changing carbonate chemistry on morphology and weight of 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 is, however, not yet understood how these changes are reflected in the morphology of coccoliths. 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 (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.

Prolonged exposure to elevated CO2 promotes growth of the algal symbiont Symbiodinium muscatinei in the intertidal sea anemone Anthopleura elegantissima

Some photosynthetic organisms benefit from elevated levels of carbon dioxide, but studies on the effects of elevated PCO₂ on the algal symbionts of animals are very few. This study investigated the impact of hypercapnia on a photosynthetic symbiosis between the anemone Anthopleura elegantissima and its zooxanthella Symbiodinium muscatinei. Anemones were maintained in the laboratory for 1 week at 37 Pa PCO₂ and pH 8.1. Clonal pairs were then divided into two groups and maintained for 6 weeks under conditions naturally experienced in their intertidal environment, 45 Pa PCO₂, pH 8.1 and 231 Pa PCO₂, pH 7.3. Respiration and photosynthesis were measured after the 1-week acclimation period and after 6 weeks in experimental conditions. Density of zooxanthellal cells, zooxanthellal cell size, mitotic index and chlorophyll content were compared between non-clonemate anemones after the 1-week acclimation period and clonal anemones at the end of the experiment. Anemones thrived in hypercapnia. After 6 weeks, A. elegantissima exhibited higher rates of photosynthesis at 45 Pa (4.2 µmol O₂ g⁻¹ h⁻¹) and 231 Pa (3.30 µmol O₂ g⁻¹ h⁻¹) than at the initial 37 Pa (1.53 µmol O₂ g⁻¹ h⁻¹). Likewise, anemones at 231 Pa received more of their respiratory carbon from zooxanthellae (CZAR  = 78.2%) than those at 37 Pa (CZAR  = 66.6%) but less than anemones at 45 Pa (CZAR  = 137.3%). The mitotic index of zooxanthellae was significantly greater in the hypercapnic anemones than in anemones at lower PCO₂. Excess zooxanthellae were expelled by their hosts, and cell densities, cell diameters and chlorophyll contents were not significantly different between the groups. The response of A. elegantissima to hypercapnic acidification reveals the potential adaptation of an intertidal, photosynthetic symbiosis for high PCO₂.

Acidification and warming affect both a calcifying predator and prey, but not their interaction

Both ocean warming and acidification have been demonstrated to affect the growth, performance and reproductive success of calcifying invertebrates. However, relatively little is known regarding how such environmental change may affect interspecific interactions. We separately treated green crabs Carcinus maenas and periwinkles Littorina littorea under conditions that mimicked either ambient conditions (control) or warming and acidification, both separately and in combination, for 5 mo. After 5 mo, the predators, prey and predator-prey interactions were screened for changes in response to environmental change. Acidification negatively affected the closer-muscle length of the crusher chela and correspondingly the claw-strength increment in C. maenas. The effects of warming and/or acidification on L. littorea were less consistent but indicated weaker shells in response to acidification. On the community level, however, we found no evidence that predator-prey interactions will change in the future. Further experiments exploring the impacts of warming and acidification on key ecological interactions are needed instead of basing predictions of ecosystem change solely on species-specific responses to environmental change.

Effects of ocean-acidification-induced morphological changes on larval swimming and feeding

Reduction in global ocean pH due to the uptake of increased atmospheric CO2 is expected to negatively affect calcifying organisms, including the planktonic larval stages of many marine invertebrates. Planktonic larvae play crucial roles in the benthic–pelagic life cycle of marine organisms by connecting and sustaining existing populations and colonizing new habitats. Calcified larvae are typically denser than seawater and rely on swimming to navigate vertically structured water columns. Larval sand dollars Dendraster excentricus have calcified skeletal rods supporting their bodies, and propel themselves with ciliated bands looped around projections called arms. Ciliated bands are also used in food capture, and filtration rate is correlated with band length. As a result, swimming and feeding performance are highly sensitive to morphological changes. When reared at an elevated PCO2 level (1000 ppm), larval sand dollars developed significantly narrower bodies at four and six-arm stages. Morphological changes also varied between four observed maternal lineages, suggesting within-population variation in sensitivity to changes in PCO2 level. Despite these morphological changes, PCO2 concentration alone had no significant effect on swimming speeds. However, acidified larvae had significantly smaller larval stomachs and bodies, suggesting reduced feeding performance. Adjustments to larval morphologies in response to ocean acidification may prioritize swimming over feeding, implying that negative consequences of ocean acidification are carried over to later developmental stages.

Marine bivalve geochemistry and shell ultrastructure from modern low pH environments

Bivalve shells can provide excellent archives of past environmental change but have not been used to interpret ocean acidification events. We investigated carbon, oxygen and trace element records from different shell layers in the mussels Mytilus galloprovincialis (from the Mediterranean) and M. edulis (from the Wadden Sea) combined with detailed investigations of the shell ultrastructure. Mussels from the harbour of Ischia (Mediterranean, Italy) were transplanted and grown in water with mean pHT 7.3 and mean pHT 8.1 near CO2 vents on the east coast of the island of Ischia. The shells of transplanted mussels were compared with M. edulis collected at pH ~8.2 from Sylt (German Wadden Sea). Most prominently, the shells recorded the shock of transplantation, both in their shell ultrastructure, textural and geochemical record. Shell calcite, precipitated subsequently under acidified seawater responded to the pH gradient by an in part disturbed ultrastructure. Geochemical data from all test sites show a strong metabolic effect that exceeds the influence of the low-pH environment. These field experiments showed that care is needed when interpreting potential ocean acidification signals because various parameters affect shell chemistry and ultrastructure. Besides metabolic processes, seawater pH, factors such as salinity, water temperature, food availability and population density all affect the biogenic carbonate shell archive.

Temperate and cold water sea urchin species in an acidifying world: coping with change?

Anthropogenic carbon dioxide (CO2) emissions are increasing the atmospheric CO2 concentration and the oceans are absorbing around 1/3 them. The CO2 hydrolysis increases the H+ concentration, decreasing the pH, while the proportions of the HCO3- and CO32- ions are also affected. This process already led to a decrease of 0.1 pH units in surface seawater. According to “business-as-usual” models, provided by the Intergovernmental Panel on Climate Change (IPCC), the pH is expected to decrease 0.3-0.5 units by 2100 and 0.7-0.8 by 2300. As a result the surface ocean carbonates chemistry will also change: with increasing pCO2, dissolved inorganic carbon will increase and the equilibrium of the carbonate system will shift to higher CO2 and HCO3– levels, while CO32– concentration will decrease. Surface seawaters will progressively become less saturated towards calcite and aragonite saturation state and some particular polar and cold water regions could even become completely undersaturated within the next 50 years.

Responses of marine organisms to environmental hypercapnia, i.e. to an excess of CO2 in the aquatic environment, can be extremely variable and the degree of sensitivity varies between species and life stages. Sea urchins are key stone species in many marine ecosystems. They are considered to be particularly vulnerable to ocean acidification effects not only due to the nature of their skeleton (magnesium calcite) whose solubility is similar or higher than that of aragonite, but also because they lack an efficient ion regulatory machinery, being therefore considered poor acid-base regulators. Populations from polar regions are expected to be at an even higher risk since the carbonate chemical changes in surface ocean waters are happening there at a faster rate.

The goal of this work was to study the effects of low seawater pH exposure of different life stages of sea urchins, in order to better understand how species from different environments and/or geographic origins would respond and if there would be scope for possible adaptation and/or acclimatization.

Structural and geochemical alterations in the Mg calcite bryozoan Myriapora truncata under elevated seawater pCO2 simulating ocean acidification

The possible effects of ocean acidification on the calcareous skeleton of the Mediterranean bryozoan Myriapora truncata (Pallas, 1766) were studied by transplanting live and dead colonies into an area of natural volcanic CO2 vents at Ischia (Gulf of Naples, Tyrrhenian Sea), Italy. Morphology and geochemistry were compared between colonies from normal (mean pH = 8.07, min. pH 7.95), below-normal (mean pH 7.66, min. pH 7.32) and acidic (mean pH 7.43, min. pH 6.83) conditions after colonies had been exposed in situ for 45 and 128 days. Both distal (juvenile) and proximal (adult) parts of the branches were investigated. Skeletons of live colonies in acidic pH site after 45 days of exposure were less corroded than those of dead colonies, suggesting that the organic tissues enveloping the skeleton play a protective role. Colonies remained alive at the below-normal and acidic pH sites during the 45-day experiment but corrosion was very striking after 128 days, with colonies from the acidic site showing significant loss of skeleton. Compared to the control, these colonies also had lower levels of Mg (mean 8 versus 9.5 wt% Mg) within their skeletons. Electron microprobe mapping showed Mg to be higher in the outer layers of the skeletal walls in colonies from the normal pH site. Corrosion of outer layers of the walls probably explains the lower Mg level found in colonies exposed to acidic conditions. As solubility of calcite increases with Mg content, the enrichment of Mg in outer layers of the skeleton should enhance the vulnerability of Myriapora truncata to dissolution. These findings raise concerns over the survival of bryozoans with Mg calcite skeletons in the face of predicted decreases in oceanic pH levels.