Altered neurotransmitter function in CO2-exposed stickleback (Gasterosteus aculeatus): a temperate model species for ocean acidification research

Studies on the consequences of ocean acidification for the marine ecosystem have revealed behavioural changes in coral reef fishes exposed to sustained near-future CO2 levels. The changes have been linked to altered function of GABAergic neurotransmitter systems, because the behavioural alterations can be reversed rapidly by treatment with the GABAA receptor antagonist gabazine. Characterization of the molecular mechanisms involved would be greatly aided if these can be examined in a well-characterized model organism with a sequenced genome. It was recently shown that CO2-induced behavioural alterations are not confined to tropical species, but also affect the three-spined stickleback, although an involvement of the GABAA receptor was not examined. Here, we show that loss of lateralization in the stickleback can be restored rapidly and completely by gabazine treatment. This points towards a worrying universality of disturbed GABAA function after high-CO2 exposure in fishes from tropical to temperate marine habitats. Importantly, the stickleback is a model species with a sequenced and annotated genome, which greatly facilitates future studies on underlying molecular mechanisms.

Colony-specific investigations reveal highly variable responses among individual corals to ocean acidification and warming

As anthropogenic climate change is an ongoing concern, scientific investigations on its impacts on coral reefs are increasing. Although impacts of combined ocean acidification (OA) and temperature stress (T) on reef-building scleractinian corals have been studied at the genus, species and population levels, there are little data available on how individual corals respond to combined OA and anomalous temperatures. In this study, we exposed individual colonies of Acropora digitifera, Montipora digitata and Porites cylindrica to four pCO2-temperature treatments including 400 µatm-28 °C, 400 µatm-31 °C, 1000 µatm-28 °C and 1000 µatm-31 °C for 26 days. Physiological parameters including calcification, protein content, maximum photosynthetic efficiency, Symbiodinium density, and chlorophyll content along with Symbiodinium type of each colony were examined. Along with intercolonial responses, responses of individual colonies versus pooled data to the treatments were investigated. The main results were: 1) responses to either OA or T or their combination were different between individual colonies when considering physiological functions; 2) tolerance to either OA or T was not synonymous with tolerance to the other parameter; 3) tolerance to both OA and T did not necessarily lead to tolerance of OA and T combined (OAT) at the same time; 4) OAT had negative, positive or no impacts on physiological functions of coral colonies; and 5) pooled data were not representative of responses of all individual colonies. Indeed, the pooled data obscured actual responses of individual colonies or presented a response that was not observed in any individual. From the results of this study we recommend improving experimental designs of studies investigating physiological responses of corals to climate change by complementing them with colony-specific examinations.

Two intertidal, non-calcifying macroalgae (Palmaria palmata and Saccharina latissima) show complex and variable responses to short-term CO2 acidification

Ocean acidification, the result of increased dissolution of carbon dioxide (CO2) in seawater, is a leading subject of current research. The effects of acidification on non-calcifying macroalgae are, however, still unclear. The current study reports two 1-month studies using two different macroalgae, the red alga Palmaria palmata (Rhodophyta) and the kelp Saccharina latissima (Phaeophyta), exposed to control (pHNBS = 8.04) and increased (pHNBS = 7.82) levels of CO2-induced seawater acidification. The impacts of both increased acidification and time of exposure on net primary production (NPP), respiration (R), dimethylsulphoniopropionate (DMSP) concentrations, and algal growth have been assessed. In P. palmata, although NPP significantly increased during the testing period, it significantly decreased with acidification, whereas R showed a significant decrease with acidification only. S. latissima significantly increased NPP with acidification but not with time, and significantly increased R with both acidification and time, suggesting a concomitant increase in gross primary production. The DMSP concentrations of both species remained unchanged by either acidification or through time during the experimental period. In contrast, algal growth differed markedly between the two experiments, in that P. palmata showed very little growth throughout the experiment, while S. latissima showed substantial growth during the course of the study, with the latter showing a significant difference between the acidified and control treatments. These two experiments suggest that the study species used here were resistant to a short-term exposure to ocean acidification, with some of the differences seen between species possibly linked to different nutrient concentrations between the experiments.

Acute survivorship of the deep-sea coral Lophelia pertusa from the Gulf of Mexico under acidification,warming,and deoxygenation

Changing global climate due to anthropogenic emissions of CO2 are driving rapid changes in the physical and chemical environment of the oceans via warming, deoxygenation, and acidification. These changes may threaten the persistence of species and populations across a range of latitudes and depths, including species that support diverse biological communities that in turn provide ecological stability and support commercial interests. Worldwide, but particularly in the North Atlantic and deep Gulf of Mexico, Lophelia pertusa forms expansive reefs that support biological communities whose diversity rivals that of tropical coral reefs. In this study, L. pertusa colonies were collected from the Viosca Knoll region in the Gulf of Mexico (390 to 450 m depth), genotyped using microsatellite markers, and exposed to a series of treatments testing survivorship responses to acidification, warming, and deoxygenation. All coral nubbins survived the acidification scenarios tested, between pH of 7.67 and 7.90 and aragonite saturation states of 0.92 and 1.47. However, calcification generally declined with respect to pH, though a disparate response was evident where select individuals net calcified and others exhibited net dissolution near a saturation state of 1. Warming and deoxygenation both had negative effects on survivorship, with up to 100% mortality observed at temperatures above 14ºC and oxygen concentrations of approximately 1.5 ml·l-1. These results suggest that, over the short-term, climate change and OA may negatively impact L. pertusa in the Gulf of Mexico, though the potential for acclimation and the effects of genetic background should be considered in future research.

Ocean acidification impacts on sperm mitochondrial membrane potential bring sperm swimming behaviour near its tipping point

Broadcast spawning marine invertebrates are susceptible to environmental stressors such as climate change, as their reproduction depends on the successful meeting and fertilization of gametes in the water column. Under near-future scenarios of ocean acidification, the swimming behaviour of marine invertebrate sperm is altered. We tested whether this was due to changes in sperm mitochondrial activity by investigating the effects of ocean acidification on sperm metabolism and swimming behaviour in the sea urchin Centrostephanus rodgersii. We used a fluorescent molecular probe (JC-1) and flow cytometry to visualize mitochondrial activity (measured as change in mitochondrial membrane potential, MMP). Sperm MMP was significantly reduced in delta pH -0.3 (35% reduction) and delta pH -0.5 (48% reduction) treatments, whereas sperm swimming behaviour was less sensitive with only slight changes (up to 11% decrease) observed overall. There was significant inter-individual variability in responses of sperm swimming behaviour and MMP to acidified seawater. We suggest it is likely that sperm exposed to these changes in pH are close to their tipping point in terms of physiological tolerance to acidity. Importantly, substantial inter-individual variation in responses of sperm swimming to ocean acidification may increase the scope for selection of resilient phenotypes, which, if heritable, could provide a basis for adaptation to future ocean acidification.

Ocean acidification decreases the light-use efficiency in an Antarctic diatom under dynamic but not constant light, link to supplementary data

There is increasing evidence that different light intensities strongly modulate the effects of ocean acidification (OA) on marine phytoplankton. The aim of the present study was to investigate interactive effects of OA and dynamic light, mimicking natural mixing regimes. The Antarctic diatom Chaetoceros debilis was grown under two pCO2 (390 and 1000 latm) and light conditions (constant and dynamic), the latter yielding the same integrated irradiance over the day. To characterize interactive effects between treatments, growth, elemental composition, primary production and photophysiology were investigated. Dynamic light reduced growth and strongly altered the effects of OA on primary production, being unaffected by elevated pCO2 under constant light, yet significantly reduced under dynamic light. Interactive effects between OA and light were also observed for Chl production and particulate organic carbon (POC) quotas. Response patterns can be explained by changes in the cellular energetic balance. While the energy transfer efficiency from photochemistry to biomass production (Phi_e,C) was not affected by OA under constant light, it was drastically reduced under dynamic light. Contrasting responses under different light conditions need to be considered when making predictions regarding a more stratified and acidified future ocean.

Impact of ocean acidification and warming on respiration, heart rate and acid-base status of Mytilus edulis from the North Sea

Anthropogenic climate change confronts marine organisms with rapid trends of concomitant warming and CO2 induced ocean acidification. The survival and distribution of species partly depend on their ability to exploit their physiological plasticity during acclimatization. Therefore, in laboratory studies the effects of simulated future ocean acidification on thermal tolerance, energy metabolism and acid-base regulation capacity of the North Sea population of the blue mussel Mytilus edulis were examined. Following one month of pre-acclimation to 10 °C and control CO2 levels, mussels were exposed for two weeks to control and projected oceanic CO2 levels (390, 750 and 1120 µatm) before being subjected to a stepwise warming protocol between 10 °C and 31 °C (+ 3 °C each night). Oxygen consumption and heart rates, anaerobic metabolite levels and haemolymph acid-base status were determined at each temperature. CO2 exposure left oxygen consumption rate unchanged at acclimation temperature but caused a somewhat stronger increase during acute warming and thus mildly higher Q10-values than seen in controls. Interestingly, the thermally induced limitation of oxygen consumption rate set in earlier in normocapnic than in hypercapnic (1120 µatm CO2) mussels (25.2 °C vs. 28.8 °C), likely due to an onset of metabolic depression in the control group following warming. However, the temperature induced increase in heart rate became limited above 25 °C in both groups indicating an unchanged pejus temperature regardless of CO2 treatment. An upper critical temperature was reached above 28 °C in both treatments indicated by the accumulation of anaerobic metabolites in the mantle tissue, paralleled by a strong increase in haemolymph PCO2 at 31 °C. Ocean acidification caused a decrease in haemolymph pH. The extracellular acidosis remained largely uncompensated despite some bicarbonate accumulation. In all treatments animals developed a progressive warming-induced extracellular acidosis. A stronger pH drop at around 25 °C was followed by stagnating heart rates. However, normocapnic mussels enhanced bicarbonate accumulation at the critical limit, a strategy no longer available to hypercapnic mussels. In conclusion, CO2 has small effects on the response patterns of mussels to warming, leaving thermal thresholds largely unaffected. High resilience of adult North Sea mussels to future ocean acidification indicates that sensitivity to thermal stress is more relevant in shaping the response to future climate change.

Morphological plasticity of the coral skeleton under CO2-driven seawater acidification

Ocean acidification causes corals to calcify at reduced rates, but current understanding of the underlying processes is limited. Here, we conduct a mechanistic study into how seawater acidification alters skeletal growth of the coral Stylophora pistillata. Reductions in colony calcification rates are manifested as increases in skeletal porosity at lower pH, while linear extension of skeletons remains unchanged. Inspection of the microstructure of skeletons and measurements of pH at the site of calcification indicate that dissolution is not responsible for changes in skeletal porosity. Instead, changes occur by enlargement of corallite-calyxes and thinning of associated skeletal elements, constituting a modification in skeleton architecture. We also detect increases in the organic matrix protein content of skeletons formed under lower pH. Overall, our study reveals that seawater acidification not only causes decreases in calcification, but can also cause morphological change of the coral skeleton to a more porous and potentially fragile phenotype.

Decreased light availability can amplify negative impacts of ocean acidification on calcifying coral reef organisms

Coral reef organisms are increasingly and simultaneously affected by global and local stressors such as ocean acidification (OA) and reduced light availability. However, knowledge of the interplay between OA and light availability is scarce. We exposed 2 calcifying coral reef species (the scleractinian coral Acropora millepora and the green alga Halimeda opuntia) to combinations of ambient and increased pCO2 (427 and 1073 µatm, respectively), and 2 light intensities (35 and 150 µmol photons/m**2/s) for 16 d. We evaluated the individual and combined effects of these 2 stressors on weight increase, calcification rates, O2 fluxes and chlorophyll a content for the species investigated. Weight increase of A. millepora was significantly reduced by OA (48%) and low light intensity (96%) compared to controls. While OA did not affect coral calcification in the light, it decreased calcification in the dark by 155%, leading to dissolution of the skeleton. H. opuntia weight increase was not affected by OA, but decreased (40%) at low light. OA did not affect algae calcification in the light, but decreased calcification in the dark by 164%, leading to dissolution. Low light significantly reduced gross photosynthesis (56 and 57%), net photosynthesis (62 and 60%) and respiration (43 and 48%) of A. millepora and H. opuntia, respectively. In contrast to A. millepora, H. opuntia significantly increased chlorophyll content by 15% over the course of the experiment. No interactive effects of OA and low light intensity were found on any response variable for either organism. However, A. millepora exhibited additive effects of OA and low light, while H. opuntia was only affected by low light. Thus, this study suggests that negative effects of low light and OA are additive on corals, which may have implications for management of river discharge into coastal coral reefs.

Ocean acidification not likely to affect the survival and fitness of two yemperate benthic foraminiferal species: results from culture experiments

Specimens of Bolivina argentea and Bulimina marginata, two widely distributed temperate benthic foraminiferal species, were cultured at constant temperature and controlled pCO2 (ambient, 1000 ppmv, and 2000 ppmv) for six weeks to assess the effect of elevated atmospheric CO2 concentrations on survival and fitness using Adenosine Triphosphate (ATP) analyses and on shell microfabric using high-resolution SEM and image analysis. To characterize the carbonate chemistry of the incubation seawater, total alkalinity and dissolved inorganic carbon were measured approximately every two weeks. Survival and fitness were not directly affected by elevated pCO2 and the concomitant decrease in seawater pH and calcite saturation states (Omega c), even when seawater was undersaturated with respect to calcite. These results differ from some previous observations that ocean acidification can cause a variety of effects on benthic foraminifera, including test dissolution, decreased growth, and mottling (loss of symbiont color in symbiont-bearing species), suggesting that the benthic foraminiferal response to ocean acidification may be species specific. If so, this implies that ocean acidification may lead to ecological winners and losers even within the same taxonomic group.

Mesocosm experiment 2012 on warming and acidification effects on phytoplankton biomass and chemical composition

We investigated the impacts of predicted ocean acidification and future warming on the quantity and nutritional quality of a natural phytoplankton autumn bloom in a mesocosm experiment. Since the effects of CO2-enrichment and temperature have usually been studied independently, we were also interested in the interactive effects of both aspects of climate change. Therefore, we used a factorial design with two temperature and two acidification levels in a mesocosm experiment with a Baltic Sea phytoplankton community. Our results show a significant time-dependent influence of warming on phytoplankton carbon, chlorophyll a as well as POC. Phytoplankton carbon for instance decreased by more than a half with increasing temperature at bloom time. Additionally, elemental carbon to phosphorus ratios (C:P) increased significantly by approximately 5-8 % under warming. Impacts of CO2 or synergetic effects of warming and acidification could not be detected. We suggest that temperature-induced stronger grazing pressure was responsible for the significant decline in phytoplankton biomass. Our results suggest that biological effects of warming on Baltic Sea phytoplankton are considerable and will likely have fundamental consequences for the trophic transfer in the pelagic food-web.