Stephen Widdicombe

Ocean acidification may increase calcification rates, but at a cost

Ocean acidification is the lowering of pH in the oceans as a result of increasing uptake of atmospheric carbon dioxide. Carbon dioxide is entering the oceans at a greater rate than ever before, reducing the oceans natural buffering capacity and lowering pH. Previous work on the biological consequences of ocean acidification has suggested that calcification and metabolic processes are compromised in acidified seawater. By contrast, here we show, using the ophiuroid brittlestar Amphiura filiformis as a model calcifying organism, that some organisms can increase the rates of many of their biological processes (in this case, metabolism and the ability to calcify to compensate for increased seawater acidity). However, this upregulation of metabolism and calcification, potentially ameliorating some of the effects of increased acidity comes at a substantial cost (muscle wastage) and is therefore unlikely to be sustainable in the long term.

Predicting ecosystem shifts requires new approaches that integrate the effects of climate change across entire systems.

Most studies that forecast the ecological consequences of climate change target a single species and a single life stage. Depending on climatic impacts on other life stages and on interacting species, however, the results from simple experiments may not translate into accurate predictions of future ecological change. Research needs to move beyond simple experimental studies and environmental envelope projections for single species towards identifying where ecosystem change is likely to occur and the drivers for this change. For this to happen, we advocate research directions that (i) identify the critical species within the target ecosystem, and the life stage(s) most susceptible to changing conditions and (ii) the key interactions between these species and components of their broader ecosystem. A combined approach using macroecology, experimentally derived data and modelling that incorporates energy budgets in life cycle models may identify critical abiotic conditions that disproportionately alter important ecological processes under forecasted climates.

A bioturbation classification of European marine infaunal invertebrates

Bioturbation, the biogenic modification of sediments through particle reworking and burrow ventilation, is a key mediator of many important geochemical processes in marine systems. In situ quantification of bioturbation can be achieved in a myriad of ways, requiring expert knowledge, technology, and resources not always available, and not feasible in some settings. Where dedicated research programmes do not exist, a practical alternative is the adoption of a trait-based approach to estimate community bioturbation potential (BPc). This index can be calculated from inventories of species, abundance and biomass data (routinely available for many systems), and a functional classification of organism traits associated with sediment mixing (less available). Presently, however, there is no agreed standard categorization for the reworking mode and mobility of benthic species. Based on information from the literature and expert opinion, we provide a functional classification for 1033 benthic invertebrate species from the northwest European continental shelf, as a tool to enable the standardized calculation of BPc in the region. Future uses of this classification table will increase the comparability and utility of large-scale assessments of ecosystem processes and functioning influenced by bioturbation (e.g., to support legislation). The key strengths, assumptions, and limitations of BPc as a metric are critically reviewed, offering guidelines for its calculation and application.

Scaling up experimental ocean acidification and warming research: from individuals to the ecosystem

Understanding long-term, ecosystem-level impacts of climate change is challenging because experimental research frequently focuses on short-term, individual-level impacts in isolation. We address this shortcoming first through an interdisciplinary ensemble of novel experimental techniques to investigate the impacts of 14-month exposure to ocean acidification and warming (OAW) on the physiology, activity, predatory behaviour and susceptibility to predation of an important marine gastropod (Nucella lapillus). We simultaneously estimated the potential impacts of these global drivers on N. lapillus population dynamics and dispersal parameters. We then used these data to parameterize a dynamic bioclimatic envelope model, to investigate the consequences of OAW on the distribution of the species in the wider NE Atlantic region by 2100. The model accounts also for changes in the distribution of resources, suitable habitat and environment simulated by finely resolved biogeochemical models, under three IPCC global emissions scenarios. The experiments showed that temperature had the greatest impact on individual-level responses, while acidification had a similarly important role in the mediation of predatory behaviour and susceptibility to predators. Changes in Nucella predatory behaviour appeared to serve as a strategy to mitigate individual-level impacts of acidification, but the development of this response may be limited in the presence of predators. The model projected significant large-scale changes in the distribution of Nucella by the year 2100 that were exacerbated by rising greenhouse gas emissions. These changes were spatially heterogeneous, as the degree of impact of OAW on the combination of responses considered by the model varied depending on local-environmental conditions and resource availability. Such changes in macro-scale distributions cannot be predicted by investigating individual-level impacts in isolation, or by considering climate stressors separately. Scaling up the results of experimental climate change research requires approaches that account for long-term, multiscale responses to multiple stressors, in an ecosystem context.

Coralline algal structure is more sensitive to rate, rather than the magnitude, of ocean acidification

Marine pCO2 enrichment via ocean acidification (OA), upwelling and release from carbon capture and storage (CCS) facilities is projected to have devastating impacts on marine biomineralisers and the services they provide. However, empirical studies using stable endpoint pCO2 concentrations find species exhibit variable biological and geochemical responses rather than the expected negative patterns. In addition, the carbonate chemistry of many marine systems is now being observed to be more variable than previously thought. To underpin more robust projections of future OA impacts on marine biomineralisers and their role in ecosystem service provision, we investigate coralline algal responses to realistically variable scenarios of marine pCO2 enrichment. Coralline algae are important in ecosystem function; providing habitats and nursery areas, hosting high biodiversity, stabilizing reef structures and contributing to the carbon cycle. Red coralline marine algae were exposed for 80 days to one of three pH treatments: (i) current pH (control); (ii) low pH (7.7) representing OA change; and (iii) an abrupt drop to low pH (7.7) representing the higher rates of pH change observed at natural vent systems, in areas of upwelling and during CCS releases. We demonstrate that red coralline algae respond differently to the rate and the magnitude of pH change induced by pCO2 enrichment. At low pH, coralline algae survived by increasing their calcification rates. However, when the change to low pH occurred at a fast rate we detected, using Raman spectroscopy, weaknesses in the calcite skeleton, with evidence of dissolution and molecular positional disorder. This suggests that, while coralline algae will continue to calcify, they may be structurally weakened, putting at risk the ecosystem services they provide. Notwithstanding evolutionary adaptation, the ability of coralline algae to cope with OA may thus be determined primarily by the rate, rather than magnitude, at which pCO2 enrichment occurs.

Experimental evidence for the role of Brissopsis lyrifera (Forbes, 1841) as a critical species in the maintenance of benthic diversity and the modification of sediment chemistry

Abstract The effects on infaunal diversity and sediment chemistry of bioturbation/feeding activity by different densities of the heart urchin Brissopsis lyrifera are quantified in an experiment conducted in the benthic mesocosm facility of the Norwegian Institute for Water Research at Solbergstrand, Norway. Using sediment from Bjornhordenbukta, a small, sheltered bay in Oslofjord, areas were subjected to 20 weeks of continuous disturbance from urchins at densities equivalent to 28 and 71 individuals m −2 , whilst other areas remained undisturbed. Low density treatments, reflecting the natural field densities observed during collection of the sediment, produced higher infaunal β diversity than the heavily disturbed or control treatments and this could be attributed to a decrease in competitive exclusion. This is consistent with the predictions of the intermediate disturbance hypothesis ( Connell, 1978 ). Bioturbation also caused a significant change in the chemistry of the surface sediment increasing oxygenation, decreasing the rates of denitrification and increasing the precipitation of phosphate. It is concluded that the disturbance activity of Brissopsis lyrifera may play a vital role in the maintenance of regional diversity and in the mediation of geochemical processes.

Comparing the impact of high CO2 on calcium carbonate structures in different marine organisms

Abstract Coastal seas are critical components of the global carbon cycle, yet little research has been conducted on the impact of ocean acidification on coastal benthic organisms. Calcifying marine organisms are predicted to be most vulnerable to a decline in oceanic pH (ocean acidification) based on the assumption that calcification will decrease as a result of changes in seawater carbonate chemistry, particularly reduced carbonate ion concentration (and associated saturation states). Net calcium carbonate production is dependent on an organisms ability to increase calcification sufficiently to counteract an increase in dissolution. Here, a critical appraisal of calcification in five benthic species showed, contrary to popular predictions, the deposition of calcium carbonate can be maintained or even increased in acidified seawater. This study measured changes in the concentration of calcium ions seen in shells taken from living animals exposed to acidified seawater. These data were compared with data from isolated shells that were not associated with living material to determine a species’ ability to maintain the physiological process of calcification under high carbon dioxide (CO2) conditions and characterize the importance of dissolution and abiotic influences associated with decreasing pH. Comparison with palaeoecological studies of past high CO2 events presents a similar picture. This conclusion implies that calcification may not be the physiological process that suffers most from ocean acidification; particularly as all species investigated displayed physiological trade-offs including increased metabolism, reduced health, and changes in behavioural responses in association with this calcification upregulation, which poses as great a threat to survival as an inability to calcify.

Impact of ocean acidification on benthic and water column ammonia oxidation

Ammonia oxidation is a key microbial process within the marine N-cycle. Sediment and water column samples from two contrasting sites in the English Channel (mud and sand) were incubated (up to 14 weeks) in CO2-acidified seawater ranging from pH 8.0 to pH 6.1. Additional observations were made off the island of Ischia (Mediterranean Sea), a natural analogue site, where long-term thermogenic CO2 ebullition occurs (from pH 8.2 to pH 7.6). Water column ammonia oxidation rates in English Channel samples decreased under low pH with near-complete inhibition at pH 6.5. Water column Ischia samples showed a similar though not statistically significant trend. However, sediment ammonia oxidation rates at all three locations were not affected by reduced pH. These observations may be explained by buffering within sediments or low-pH adaptation of the microbial ammonia oxidizing communities. Our observations have implications for modeling the future impact of ocean acidification on marine ecosystems.

Exposure to Elevated Temperature and Pco2 Reduces Respiration Rate and Energy Status in the Periwinkle Littorina littorea

In the future, marine organisms will face the challenge of coping with multiple environmental changes associated with increased levels of atmospheric Pco2, such as ocean warming and acidification. To predict how organisms may or may not meet these challenges, an in-depth understanding of the physiological and biochemical mechanisms underpinning organismal responses to climate change is needed. Here, we investigate the effects of elevated Pco2 and temperature on the whole-organism and cellular physiology of the periwinkle Littorina littorea. Metabolic rates (measured as respiration rates), adenylate energy nucleotide concentrations and indexes, and end-product metabolite concentrations were measured. Compared with values for control conditions, snails decreased their respiration rate by 31% in response to elevated Pco2 and by 15% in response to a combination of increased Pco2 and temperature. Decreased respiration rates were associated with metabolic reduction and an increase in end-product metabolites in acidified treatments, indicating an increased reliance on anaerobic metabolism. There was also an interactive effect of elevated Pco2 and temperature on total adenylate nucleotides, which was apparently compensated for by the maintenance of adenylate energy charge via AMP deaminase activity. Our findings suggest that marine intertidal organisms are likely to exhibit complex physiological responses to future environmental drivers, with likely negative effects on growth, population dynamics, and, ultimately, ecosystem processes.

Ocean acidification and rising temperatures may increase biofilm primary productivity but decrease grazer consumption

Climate change may cause ecosystems to become trophically restructured as a result of primary producers and consumers responding differently to increasing CO2 and temperature. This study used an integrative approach using a controlled microcosm experiment to investigate the combined effects of CO2 and temperature on key components of the intertidal system in the UK, biofilms and their consumers (Littorina littorea). In addition, to identify whether pre-exposure to experimental conditions can alter experimental outcomes we explicitly tested for differential effects on L. littorea pre-exposed to experimental conditions for two weeks and five months. In contrast to predictions based on metabolic theory, the combination of elevated temperature and CO2 over a five-week period caused a decrease in the amount of primary productivity consumed by grazers, while the abundance of biofilms increased. However, long-term pre-exposure to experimental conditions (five months) altered this effect, with grazing rates in these animals being greater than in animals exposed only for two weeks. We suggest that the structure of future ecosystems may not be predictable using short-term laboratory experiments alone owing to potentially confounding effects of exposure time and effects of being held in an artificial environment over prolonged time periods. A combination of laboratory (physiology responses) and large, long-term experiments (ecosystem responses) may therefore be necessary to adequately predict the complex and interactive effects of climate change as organisms may acclimate to conditions over the longer term.