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.

Predominance of heavily calcified coccolithophores at low CaCO3 saturation during winter in the Bay of Biscay

Coccolithophores are an important component of the Earth system, and, as calcifiers, their possible susceptibility to ocean acidification is of major concern. Laboratory studies at enhanced pCO₂ levels have produced divergent results without overall consensus. However, it has been predicted from these studies that, although calcification may not be depressed in all species, acidification will produce “a transition in dominance from more to less heavily calcified coccolithophores” [Ridgwell A, et al., (2009) Biogeosciences 6:2611–2623]. A recent observational study [Beaufort L, et al., (2011) Nature 476:80–83] also suggested that coccolithophores are less calcified in more acidic conditions. We present the results of a large observational study of coccolithophore morphology in the Bay of Biscay. Samples were collected once a month for over a year, along a 1,000-km-long transect. Our data clearly show that there is a pronounced seasonality in the morphotypes of Emiliania huxleyi, the most abundant coccolithophore species. Whereas pH and CaCO₃ saturation are lowest in winter, the E. huxleyi population shifts from <10% (summer) to >90% (winter) of the heavily calcified form. However, it is unlikely that the shifts in carbonate chemistry alone caused the morphotype shift. Our finding that the most heavily calcified morphotype dominates when conditions are most acidic is contrary to the earlier predictions and raises further questions about the fate of coccolithophores in a high-CO₂ world.

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.

Review of climate change impacts on marine fish and shellfish around the UK and Ireland

1. Recent and projected future changes in the temperature and chemistry of marine waters around the UK and Ireland are having, and will in the future have, effects on the phenology, productivity and distribution of marine fish and shellfish. However, the overall consequences are still hard to predict because behaviour, genetic adaptation, habitat dependency and the impacts of fishing on species, result in complex species’ responses that may be only partially explained by simple climate envelope predictions.
2. There is a broad body of evidence that climatic fluctuations are playing an important role in changing fish distributions and abundances, which is discernible against the background of trends in abundance due to fishing. During warm periods, southern species have tended to become more prominent and northern species less abundant. However, the changes in distribution are often more complicated than might be expected from a simple climate envelope approach, partly due to ocean circulation patterns which create invasion routes for southern water species into the North Sea from the south and from the north via the continental shelf west of Britain and Ireland.
3. The eventual population-scale impacts of ocean acidification on fish and shellfish are currently very difficult to predict. However, the scant evidence suggests that indirect food web effects arising from the enhanced sensitivity of calcifying planktonic organisms may be important, and the direct effect on fish sensory systems leading to subtle influences on behaviour with possible population-level implications are possible.
4. In British waters, the lesser sandeel (Ammodytes marinus) is identified as being at particular risk from climate change. Owing to its strict association with coarse sandy sediments it is unable to adapt its distribution to compensate for warming sea temperatures. Sandeels are a key link in the food web, linking primary and zooplankton production to top predators.

The carbonate system in the North Sea: sensitivity and model validation

The ocean plays an important role in regulating the climate, acting as a sink for carbon dioxide, perturbing the carbonate system and resulting in a slow decrease of seawater pH.

Understanding the dynamics of the carbonate system in shelf sea regions is necessary to evaluate the impact of ocean acidification (OA) in these societally important ecosystems. Complex hydrodynamic and ecosystem coupled models provide a method of capturing the significant heterogeneity of these areas. However rigorous validation is essential to properly assess the reliability of such models. The coupled model POLCOMS-ERSEM has been implemented in the North Western European shelf with a new parameterization for alkalinity explicitly accounting for riverine inputs and the influence of biological processes. The model has been validated in a like with like comparison with North Sea data from the CANOBA dataset. The model shows good to reasonable agreement for the principal variables, physical (temperature and salinity), biogeochemical (nutrients) and carbonate system (dissolved inorganic carbon and total alkalinity), but simulation of the derived variables, pH and pCO₂, are not yet fully satisfactory. This high uncertainty is attributed mostly to riverine forcing and primary production. This study suggests that the model is a useful tool to provide information on Ocean Acidification scenarios, but uncertainty on pH and pCO₂ need to be reduced, particularly when impacts of OA on ecosystem functions are included in the model systems.

Effects of increased CO2 and nutrients on seagrass (Cymodocea nodosa) metabolism

Continuous global change leads to acidify ocean through increasing of atmospheric CO2 level which is major issue for our ecosysem now-a-days. Addressing this ocean acidification and ongoing anthropogenic problems of eutrophication with ocean temperature increase and teir cumulative impacts or interactive effects are still demanding a lot in research arena of oceanic environment. In this connection, this experiment conducted to investigate the effect of both nutrient and CO2 enrichment on the net community production (NCP) of Cymodocea nodosa beds collected from the western sector of the highly dynamic coastal lagoon Ria Formosa (south Portugal: 37° 01´ N, 7° 50´ W) in a mesocosm set up situated in Ramalhete Marine Station of University of Algarve where the open circulation of seawater exiss. To address the interaction with seagrass metabolism; two types of CO2 concentration (enriched: 700 ppm with pH 7.84 and control: existing 370 ppm with pH 8.12) and two types of nutrient concentration (enriched and control) were used with seawater. However, four types of different combinations from CO2 and nutrient concentration can explain effects of net community production for to complementary methods performed: light incubation and dark incubation. To estimate seagrass community metabolism, I measured change in calculated concentration of dissolved inorganic carbon (DIC) throughout photosynthesis and respiration from conducted twelve light incubations and nine dark incubations respectively in diferent days and times in order to catch possible wider range of underwater irradiances in case of light incubations. There were mild different trends suggesting increased production (± 38000 µmol C h-1 m-2) at underwater irradiance of ± 900 PAR µmol m-2 s-1 in the treatment of enriched nutrients and control CO2 concentration while decreased production (± 30000 µmol C h-1 m-2) found in the treatment with control CO2 and control nutrient at same irradiance. However, in consider to daytime, the net community production in afternoon found to differ a little bit after photoinhibition (observed at 13.30 h with ±1100 PAR µmol m-2 s-1) where maximum increased of NCP (± 35000 µmol C h-1 m-2) found at 17.00 h in the enriched (both in CO2 and nutrient) treatment. In all cases, average positive NCP values (from light) are found lower than the average negative NCP values (from dark) suggesting more community respiration in the equal day-night dates though the treatment with control CO2 and enriched nitrogen showed maximum net community production (around 60000 µmol C h-1 m-2) in the study place of south Portugal in the month of April-May when the daylight existed around 14 hours in a day. However, both CO2 and Nitrogen contents of seawater were not significantly affected yet in Cymodocea nodosa beds in generally even thouh there was significant difference (p = 0.002) among the daily average net community production of the four treatments. Further study should be carried out in order to better understand the underlying metabolic activities of C. nodosa leading to net community production in elevated CO2 and nutrients concentration to meet the upcoming global change.

Acclimation to ocean acidification during long-term CO2 exposure in the cold-water coral Lophelia pertusa

Ocean acidity has increased by 30% since preindustrial times due to the uptake of anthropogenic CO2 and is projected to rise by another 120% before 2100 if CO2 emissions continue at current rates. Ocean acidification is expected to have wide-ranging impacts on marine life, including reduced growth and net erosion of coral reefs. Our present understanding of the impacts of ocean acidification on marine life, however, relies heavily on results from short-term CO2 perturbation studies. Here we present results from the first long-term CO2 perturbation study on the dominant reef-building cold-water coral Lophelia pertusa and relate them to results from a short-term study to compare the effect of exposure time on the coral’s responses. Short-term (one week) high CO2 exposure resulted in a decline of calcification by 26-29% for a pH decrease of 0.1 units and net dissolution of calcium carbonate. In contrast, L. pertusa was capable to acclimate to acidified conditions in long-term (six months) incubations, leading to even slightly enhanced rates of calcification. Net growth is sustained even in waters sub-saturated with respect to aragonite. Acclimation to seawater acidification did not cause a measurable increase in metabolic rates. This is the first evidence of successful acclimation in a coral species to ocean acidification, emphasizing the general need for long-term incubations in ocean acidification research. To conclude on the sensitivity of cold-water coral reefs to future ocean acidification further ecophysiological studies are necessary which should also encompass the role of food availability and rising temperatures.

Acidification of subsurface coastal waters enhanced by eutrophication

Human inputs of nutrients to coastal waters can lead to the excessive production of algae, a process known as eutrophication. Microbial consumption of this organic matter lowers oxygen levels in the water1, 2, 3. In addition, the carbon dioxide produced during microbial respiration increases acidity. The dissolution of atmospheric carbon dioxide in ocean waters also raises acidity, a process known as ocean acidification. Here, we assess the combined impact of eutrophication and ocean acidification on acidity in the coastal ocean, using data collected in the northern Gulf of Mexico and the East China Sea—two regions heavily influenced by nutrient–laden rivers. We show that eutrophication in these waters is associated with the development of hypoxia and the acidification of subsurface waters, as expected. Model simulations, using data collected from the northern Gulf of Mexico, however, suggest that the drop in pH since pre-industrial times is greater than that expected from eutrophication and ocean acidification alone. We attribute the additional drop in pH—of 0.05 units—to a reduction in the ability of these carbon dioxide-rich waters to buffer changes in pH. We suggest that eutrophication could increase the susceptibility of coastal waters to ocean acidification.

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.