Physiological advantages of dwarfing in surviving extinctions in high-CO2 oceans

Excessive CO2 in the present-day ocean-atmosphere system is causing ocean acidification, and is likely to cause a severe biodiversity decline in the future, mirroring effects in many past mass extinctions. Fossil records demonstrate that organisms surviving such events were often smaller than those before, a phenomenon called the Lilliput effect. Here, we show that two gastropod species adapted to acidified seawater at shallow-water CO2 seeps were smaller than those found in normal pH conditions and had higher mass-specific energy consumption but significantly lower whole-animal metabolic energy demand. These physiological changes allowed the animals to maintain calcification and to partially repair shell dissolution. These observations of the long-term chronic effects of increased CO2 levels forewarn of changes we can expect in marine ecosystems as CO2 emissions continue to rise unchecked, and support the hypothesis that ocean acidification contributed to past extinction events. The ability to adapt through dwarfing can confer physiological advantages as the rate of CO2 emissions continues to increase.

Foraging behaviour of the epaulette shark Hemiscyllium ocellatum is not affected by elevated CO2

Increased oceanic uptake of atmospheric carbon dioxide (CO2) is a threat to marine organisms and ecosystems. Among the most dramatic consequences predicted to date are behavioural impairments in marine fish which appear to be caused by the interference of elevated CO2 with a key neurotransmitter receptor in the brain. In this study, we tested the effects of elevated CO2 on the foraging and shelter-seeking behaviours of the reef-dwelling epaulette shark, Hemiscyllium ocellatum. Juvenile sharks were exposed for 30 d to control CO2 (400 µatm) and two elevated CO2 treatments (615 and 910 µatm), consistent with medium- and high-end projections for ocean pCO2 by 2100. Contrary to the effects observed in teleosts and in some other sharks, behaviour of the epaulette shark was unaffected by elevated CO2. A potential explanation is the remarkable adaptation of H. ocellatum to low environmental oxygen conditions (hypoxia) and diel fluctuations in CO2 encountered in their shallow reef habitat. This ability translates into behavioural tolerance of near-future ocean acidification, suggesting that behavioural tolerance and subsequent adaptation to projected future CO2 levels might be possible in some other fish, if adaptation can keep pace with the rate of rising CO2 levels.

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.

Increased CO2 modifies the carbon balance and the photosynthetic yield of two common Arctic brown seaweeds: Desmarestia aculeata and Alaria esculenta

Ocean acidification affects with special intensity Arctic ecosystems, being marine photosynthetic organisms a primary target, although the consequences of this process in the carbon fluxes of Arctic algae are still unknown. The alteration of the cellular carbon balance due to physiological acclimation to an increased CO2 concentration (1300 ppm) in the common Arctic brown seaweeds Desmarestia aculeata and Alaria esculenta from Kongsfjorden (Svalbard) was analysed. Growth rate of D. aculeata was negatively affected by CO2 enrichment, while A. esculenta was positively affected, as a result of a different reorganization of the cellular carbon budget in both species. Desmarestia aculeata showed increased respiration, enhanced accumulation of storage biomolecules and elevated release of dissolved organic carbon, whereas A. esculenta showed decreased respiration and lower accumulation of storage biomolecules. Gross photosynthesis (measured both as O2 evolution and 14C fixation) was not affected in any of them, suggesting that photosynthesis was already saturated at normal CO2 conditions and did not participate in the acclimation response. However, electron transport rate changed in both species in opposite directions, indicating different energy requirements between treatments and species specificity. High CO2 levels also affected the N-metabolism, and 13C isotopic discrimination values from algal tissue pointed to a deactivation of carbon concentrating mechanisms. Since increased CO2 has the potential to modify physiological mechanisms in different ways in the species studied, it is expected that this may lead to changes in the Arctic seaweed community, which may propagate to the rest of the food web.

The effect of elevated CO2 and increased temperature on in vitro fertilization success and initial embryonic development of single male:female crosses of broad-cast spawning corals at mid- and high-latitude locations

The impact of global climate change on coral reefs is expected to be most profound at the sea surface, where fertilization and embryonic development of broadcast-spawning corals takes place. We examined the effect of increased temperature and elevated CO2 levels on the in vitro fertilization success and initial embryonic development of broadcast-spawning corals using a single male:female cross of three different species from mid- and high-latitude locations: Lyudao, Taiwan (22° N) and Kochi, Japan (32° N). Eggs were fertilized under ambient conditions (27 °C and 500 µatm CO2) and under conditions predicted for 2100 (IPCC worst case scenario, 31 °C and 1000 µatm CO2). Fertilization success, abnormal development and early developmental success were determined for each sample. Increased temperature had a more profound influence than elevated CO2. In most cases, near-future warming caused a significant drop in early developmental success as a result of decreased fertilization success and/or increased abnormal development. The embryonic development of the male:female cross of A. hyacinthus from the high-latitude location was more sensitive to the increased temperature (+4 °C) than the male:female cross of A. hyacinthus from the mid-latitude location. The response to the elevated CO2 level was small and highly variable, ranging from positive to negative responses. These results suggest that global warming is a more significant and universal stressor than ocean acidification on the early embryonic development of corals from mid- and high-latitude locations.

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.

Cuttlebone morphometry measurements

Changes in seawater carbonate chemistry that accompany ongoing ocean acidification have been found to affect calcification processes in many marine invertebrates. In contrast to the response of most invertebrates, calcification rates increase in the cephalopod Sepia officials during long-term exposure to elevated seawater pCO2. The present trial investigated structural changes in the cuttlebones of S. officinalis calcified during 6 weeks of exposure to 615 Pa CO2. Cuttlebone mass increased sevenfold over the course of the growth trail, reaching a mean value of 0.71 ± 0.15 g. Depending on cuttlefish size (mantle lengths 44-56 mm), cuttlebones of CO2-incubated individuals accreted 22-55% more CaCO3 compared to controls at 64 Pa CO2. However, the height of the CO2- exposed cuttlebones was reduced. A decrease in spacing of the cuttlebone lamellae, from 384 ± 26 to 195 ± 38 lm, accounted for the height reduction The greater CaCO3 content of the CO2-incubated cuttlebones can be attributed to an increase in thickness of the lamellar and pillar walls. Particularly, pillar thickness increased from 2.6 ± 0.6 to 4.9 ± 2.2 lm. Interestingly, the incorporation of non-acidsoluble organic matrix (chitin) in the cuttlebones of CO2- exposed individuals was reduced by 30% on average. The apparent robustness of calcification processes in S. officials, and other powerful ion regulators such as decapod cructaceans, during exposure to elevated pCO2 is predicated to be closely connected to the increased extracellular [HCO3 -] maintained by these organisms to compensate extracellular pH. The potential negative impact of increased calcification in the cuttlebone of S. officials is discussed with regard to its function as a lightweight and highly porous buoyancy regulation device. Further studies working with lower seawater pCO2 values are necessary to evaluate if the observed phenomenon is of ecological relevance.

Effects of CO2-driven ocean acidification on early life stages of marine medaka (Oryzias melastigma)

The potential effects of elevated CO2 level and reduced carbonate saturation state in marine environment on fishes and other non-calcified organisms are still poorly known. In present study, we investigated the effects of ocean acidification on embryogenesis and organogenesis of newly hatched larvae of marine medaka (Oryzias melastigma) after 21 d exposure of eggs to different artificially acidified seawater (pH 7.6 and 7.2, respectively), and compared with those in control group (pH 8.2). Results showed that CO2-driven seawater acidification (pH 7.6 and 7.2) had no detectable effect on hatching time, hatching rate, and heart rate of embryos. However, the deformity rate of larvae in pH 7.2 treatment was significantly higher than that in control treatment. The left and right sagitta areas did not differ significantly from each other in each treatment. However, the mean sagitta area of larvae in pH 7.6 treatment was significantly smaller than that in the control (p = 0.024). These results suggest that although marine medaka might be more tolerant of elevated CO2 than some other fishes, the effect of elevated CO2 level on the calcification of otolith is likely to be the most susceptibly physiological process of pH regulation in early life stage of marine medaka.

Effects of ocean acidification caused by rising CO2 on the early development of three mollusks

Increasing atmospheric CO2 can decrease seawater pH and carbonate ions, which may adversely affect the larval survival of calcareous animals. In this study, we simulated future atmospheric CO2 concentrations (800, 1500, 2000 and 3000 ppm) and examined the effects of ocean acidification on the early development of 3 mollusks (the abalones Haliotis diversicolor and H. discus hannai and the oyster Crassostrea angulata). We showed that fertilization rate, hatching rate, larval shell length, trochophore development, veliger survival and metamorphosis all decreased significantly at different pCO2 levels (except oyster hatching). H. discus hannai were more tolerant of high CO2 compared to H. diversicolor. At 2000 ppm CO2, 79.2% of H. discus hannai veliger larvae developed normally, but only 13.3% of H. diversicolor veliger larvae. Tolerance of C. angulata to ocean acidification was greater than the 2 abalone species; 50.5% of its D-larvae developed normally at 3000 ppm CO2. This apparent resistance of C. angulata to ocean acidification may be attributed to their adaptability to estuarine environments. Mechanisms underlying the resistance to ocean acidification of both abalones requires further investigation. Our results suggest that ocean acidification may decrease the yield of these 3 economically important shellfish if increasing CO2 is a future trend.

Negative effects of ocean acidification on calcification vary within the coccolithophore genus Calcidiscus

A large percentage of CO2 emitted into the atmosphere is absorbed by the oceans, causing chemical changes in surface waters known as ocean acidification (OA). Despite the high interest and increased pace of OA research to understand the effects of OA on marine organisms, many ecologically important organisms remain unstudied. Calcidiscus is a heavily calcified coccolithophore genus that is widespread and genetically and morphologically diverse. It contributes substantially to global calcium carbonate production, organic carbon production, oceanic carbon burial, and ocean-atmosphere CO2 exchange. Despite the importance of this genus, relatively little work has examined its responses to OA. We examined changes in growth, morphology, and carbon allocation in multiple strains of Calcidiscus leptoporus in response to ocean acidification. We also, for the first time, examined the OA response of Calcidiscus quadriperforatus, a larger and more heavily calcified Calcidiscus congener. All Calcidiscus coccolithophores responded negatively to OA with impaired coccolith morphology and a decreased ratio of particulate inorganic to organic carbon (PIC:POC). However, strains responded variably; C. quadriperforatus showed the most sensitivity, while the most lightly calcified strain of C. leptoporus showed little response to OA. Our findings suggest that calcium carbonate production relative to organic carbon production by Calcidiscus coccolithophores may decrease in future oceans and that Calcidiscus distributions may shift if more resilient strains and species become dominant in assemblages. This study demonstrates that variable responses to OA may be strain or species specific in a way that is closely linked to physiological traits, such as cellular calcite quota.

Seaweed fails to prevent ocean acidification impact on foraminifera along a shallow-water CO2 gradient

Ocean acidification causes biodiversity loss, alters ecosystems, and may impact food security, as shells of small organisms dissolve easily in corrosive waters. There is a suggestion that photosynthetic organisms could mitigate ocean acidification on a local scale, through seagrass protection or seaweed cultivation, as net ecosystem organic production raises the saturation state of calcium carbonate making seawater less corrosive. Here, we used a natural gradient in calcium carbonate saturation, caused by shallow-water CO2 seeps in the Mediterranean Sea, to assess whether seaweed that is resistant to acidification (Padina pavonica) could prevent adverse effects of acidification on epiphytic foraminifera. We found a reduction in the number of species of foraminifera as calcium carbonate saturation state fell and that the assemblage shifted from one dominated by calcareous species at reference sites (pH 8.19) to one dominated by agglutinated foraminifera at elevated levels of CO2 (pH 7.71). It is expected that ocean acidification will result in changes in foraminiferal assemblage composition and agglutinated forms may become more prevalent. Although Padina did not prevent adverse effects of ocean acidification, high biomass stands of seagrass or seaweed farms might be more successful in protecting epiphytic foraminifera.

Photochemical responses of the diatom Skeletonema costatum grown under elevated CO2 concentrations to short-term changes in pH

Variability in pH is a common occurrence in many aquatic environments, due to physical, chemical and biological processes. In coastal waters, lagoons, estuaries and inland waters, pH can change very rapidly (within seconds or hours) in addition to daily and seasonal changes. At the same time, progressive ocean acidification caused by anthropogenic CO2 emissions is superimposed on these spatial and temporal pH changes. Photosynthetic organisms are therefore unavoidably subject to significant pH variations at the cell surface. Whether this will affect their response to long-term ocean acidification is still unknown, nor is it known whether the short-term sensitivity to pH change is affected by the pCO2 to which the cells are acclimated. We posed the latter open question as our experimental hypothesis: Does acclimation to seawater acidification affect the response of phytoplankton to acute pH variations? The diatom Skeletonema costatum, commonly found in coastal and estuarine waters where short-term acute changes in pH frequently occur, was selected to test the hypothesis. Diatoms were grown at both 390 (pH 8.2, low CO2; LC) and 1000 (pH 7.9, high CO2; HC) µatm CO2 for at least 20 generations, and photosynthetic responses to short-term and acute changes in pH (between 8.2 and 7.6) were investigated. The effective quantum yield of LC-grown cells decreased by ca. 70% only when exposed to pH 7.6; this was not observed when exposed to pH 7.9 or 8.2. HC-grown cells did not show significant responses in any pH treatment. Non-photochemical quenching showed opposite trends. In general, our results indicate that while LC-grown cells are rather sensitive to acidification, HC-grown cells are relatively unresponsive in terms of photochemical performance.