Helen S. Findlay

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.

Sensitivity to ocean acidification parallels natural pCO2 gradients experienced by Arctic copepods under winter sea ice

Significance The Arctic Ocean is a bellwether for ocean acidification, yet few direct Arctic studies have been carried out and limited observations exist, especially in winter. We present unique under-ice physicochemical data showing the persistence of a mid water column area of high CO2 and low pH through late winter, Zooplankton data demonstrating that the dominant copepod species are distributed across these different physicochemical conditions, and empirical data demonstrating that these copepods show sensitivity to pCO2 that parallels the range of natural pCO2 they experience through their daily vertical migration behavior. Our data, collected as part of the Catlin Arctic Survey, provide unique insight into the link between environmental variability, behavior, and an organism’s physiological tolerance to CO2 in key Arctic biota. The Arctic Ocean already experiences areas of low pH and high CO2, and it is expected to be most rapidly affected by future ocean acidification (OA). Copepods comprise the dominant Arctic zooplankton; hence, their responses to OA have important implications for Arctic ecosystems, yet there is little data on their current under-ice winter ecology on which to base future monitoring or make predictions about climate-induced change. Here, we report results from Arctic under-ice investigations of copepod natural distributions associated with late-winter carbonate chemistry environmental data and their response to manipulated pCO2 conditions (OA exposures). Our data reveal that species and life stage sensitivities to manipulated OA conditions were correlated with their vertical migration behavior and with their natural exposures to different pCO2 ranges. Vertically migrating adult Calanus spp. crossed a pCO2 range of >140 μatm daily and showed only minor responses to manipulated high CO2. Oithona similis, which remained in the surface waters and experienced a pCO2 range of <75 μatm, showed significantly reduced adult and nauplii survival in high CO2 experiments. These results support the relatively untested hypothesis that the natural range of pCO2 experienced by an organism determines its sensitivity to future OA and highlight that the globally important copepod species, Oithona spp., may be more sensitive to future high pCO2 conditions compared with the more widely studied larger copepods.

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.

The societal challenge of ocean acidification.

The carbonate chemistry of the world’s oceans, including their pH, has been remarkably constant for hundreds of thousands of years (Pearson and Palmer, 2000), with typical surface ocean variations between ice ages and warm phases of no more than 0.2 pH units ([Sanyal et al., 1995], [Honisch and Hemming, 2005] and [Foster, 2008]). However, since the beginning of the industrial revolution, the oceans have taken up approximately 30% of the CO2 produced from fossil fuel burning, cement manufacture and land use changes (Sabine et al., 2004). While the invasion of CO2 into the ocean removes this greenhouse gas from the atmosphere and thereby dampens global warming, it forms carbonic acid in seawater and lowers ambient surface ocean pH (Broecker and Peng, 1982). Ocean acidification is the direct consequence of the excessive addition of CO2 to seawater (Broecker and Takahashi, 1977) and is therefore inherently more predictable than temperature and precipitation changes due to rising CO2 in the atmosphere. Changes are already measurable today ([Bates, 2001], [Bates et al., 2002], [Takahashi et al., 2003], [Keeling et al., 2004] and [Santana-Casiano et al., 2007]) and will become more pronounced as humankind emits more CO2 into the atmosphere, with surface ocean pH expected to decline by a further 0.3 pH units by the end of the century, corresponding to an approximately 100% increase in ocean acidity (hydrogen ion concentration [H+]), on top of the not, vert, similar0.1 pH unit decline to date ([Caldeira and Wickett, 2003], [Orr et al., 2005] and Solomon et al., 2007 In: S. Solomon et al., Editors, Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Fourth Assessment Report of the IPCC, Cambridge University Press, Cambridge (2007).[Solomon et al., 2007]) (Fig. 1). Such a rapid change in ocean pH has very likely not happened since the time the dinosaurs went extinct 65 million years ago ([van der Burgh et al., 1993], [Pearson and Palmer, 2000] and [Pagani et al., 2005]). While the dissolution of carbonate sediments on the bottom of the ocean and the weathering of rocks on land coupled with mixing of surface and deeper waters will eventually restore ocean pH to its pre-industrial state, this process will take up to a million years to complete ([Archer, 2005] and [Ridgwell and Zeebe, 2005]).

Effects of elevated CO2 on the reproduction of two calanoid copepods.

Some planktonic groups suffer negative effects from ocean acidification (OA), although copepods might be less sensitive. We investigated the effect of predicted CO2 levels (range 480-750ppm), on egg production and hatching success of two copepod species, Centropages typicus and Temora longicornis. In these short-term incubations there was no significant effect of high CO2 on these parameters. Additionally a very high CO2 treatment, (CO2=9830ppm), representative of carbon capture and storage scenarios, resulted in a reduction of egg production rate and hatching success of C. typicus, but not T. longicornis. In conclusion, reproduction of C. typicus was more sensitive to acute elevated seawater CO2 than that of T. longicornis, but neither species was affected by exposure to CO2 levels predicted for the year 2100. The duration and seasonal timing of exposures to high pCO2, however, might have a significant effect on the reproduction success of calanoid copepods.

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.

Can ocean acidification affect population dynamics of the barnacle Semibalanus balanoides at its southern range edge

The global ocean and atmosphere are warming. There is increasing evidence suggesting that, in addition to other environmental factors, climate change is affecting species distributions and local population dynamics. Additionally, as a consequence of the growing levels of atmospheric carbon dioxide (CO2), the oceans are taking up increasing amounts of this CO2, causing ocean pH to decrease (ocean acidification). The relative impacts of ocean acidification on population dynamics have yet to be investigated, despite many studies indicating that there will be at least a sublethal impact on many marine organisms, particularly key calcifying organisms. Using empirical data, we forced a barnacle (Semibalanus balanoides) population model to investigate the relative influence of sea surface temperature (SST) and ocean acidification on a population nearing the southern limit of its geographic distribution. Hindcast models were compared to observational data from Cellar Beach (southwestern United Kingdom). Results indicate that a declining pH trend (-0.0017 unit/yr), indicative of ocean acidification over the past 50 years, does not cause an observable impact on the population abundance relative to changes caused by fluctuations in temperature. Below the critical temperature (here T(crit) = 13.1 degrees C), pH has a more significant affect on population dynamics at this southern range edge. However, above this value, SST has the overriding influence. At lower SST, a decrease in pH (according to the National Bureau of Standards, pHNBs) from 8.2 to 7.8 can significantly decrease the population abundance. The lethal impacts of ocean acidification observed in experiments on early life stages reduce cumulative survival by approximately 25%, which again will significantly alter the population level at this southern limit. Furthermore, forecast predictions from this model suggest that combined acidification and warming cause this local population to die out 10 years earlier than would occur if there was only global warming and no concomitant decrease in pH.

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

Abstract 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.

Hidden impacts of ocean acidification to live and dead coral framework.

Cold-water corals, such as Lophelia pertusa, are key habitat-forming organisms found throughout the worlds oceans to 3000 m deep. The complex three-dimensional framework made by these vulnerable marine ecosystems support high biodiversity and commercially important species. Given their importance, a key question is how both the living and the dead framework will fare under projected climate change. Here, we demonstrate that over 12 months L. pertusa can physiologically acclimate to increased CO2, showing sustained net calcification. However, their new skeletal structure changes and exhibits decreased crystallographic and molecular-scale bonding organization. Although physiological acclimatization was evident, we also demonstrate that there is a negative correlation between increasing CO2 levels and breaking strength of exposed framework (approx. 20–30% weaker after 12 months), meaning the exposed bases of reefs will be less effective ‘load-bearers’, and will become more susceptible to bioerosion and mechanical damage by 2100.