Biomineralization changes with food supply confer juvenile scallops (Argopecten purpuratus) resistance to ocean acidification

Future ocean acidification (OA) will affect physiological traits of marine species, with calcifying species being particularly vulnerable. As OA entails high energy demands, particularly during the rapid juvenile growth phase, food supply may play a key role in the response of marine organisms to OA. We experimentally evaluated the role of food supply in modulating physiological responses and biomineralization processes in juveniles of the Chilean scallop, Argopecten purpuratus, that were exposed to control (pH 8.0) and low pH (pH 7.6) conditions using three food supply treatments (high, intermediate, and low). We found that pH and food levels had additive effects on the physiological response of the juvenile scallops. Metabolic rates, shell growth, net calcification, and ingestion rates increased significantly at low pH conditions, independent of food. These physiological responses increased significantly in organisms exposed to intermediate and high levels of food supply. Hence, food supply seems to play a major role modulating organismal response by providing the energetic means to bolster the physiological response of OA stress. On the contrary, the relative expression of chitin synthase, a functional molecule for biomineralization, increased significantly in scallops exposed to low food supply and low pH, which resulted in a thicker periostracum enriched with chitin polysaccharides. Under reduced food and low pH conditions, the adaptive organismal response was to trade-off growth for the expression of biomineralization molecules and altering of the organic composition of shell periostracum, suggesting that the future performance of these calcifiers will depend on the trajectories of both OA and food supply. Thus, incorporating a suite of traits and multiple stressors in future studies of the adaptive organismal response may provide key insights on OA impacts on marine calcifiers.

Ocean acidification accelerates reef bioerosion

In the recent discussion how biotic systems may react to ocean acidification caused by the rapid rise in carbon dioxide partial pressure (pCO2) in the marine realm, substantial research is devoted to calcifiers such as stony corals. The antagonistic process-biologically induced carbonate dissolution via bioerosion- has largely been neglected. Unlike skeletal growth, we expect bioerosion by chemical means to be facilitated in a high-CO2 world. This study focuses on one of the most detrimental bioeroders, the sponge Cliona orientalis, which attacks and kills live corals on Australia's Great Barrier Reef. Experimental exposure to lowered and elevated levels of pCO2 confirms a significant enforcement of the sponges' bioerosion capacity with increasing pCO2 under more acidic conditions. Considering the substantial contribution of sponges to carbonate bioerosion, this finding implies that tropical reef ecosystems are facing the combined effects of weakened coral calcification and accelerated bioerosion, resulting in critical pressure on the dynamic balance between biogenic carbonate build-up and degradation.

Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO2-driven acidification during the initiation of calcification

The impact of ocean acidification (OA) on coral calcification, a subject of intense current interest, is poorly understood in part because of the presence of symbionts in adult corals. Early life history stages of Acropora spp. provide an opportunity to study the effects of elevated CO(2) on coral calcification without the complication of symbiont metabolism. Therefore, we used the Illumina RNAseq approach to study the effects of acute exposure to elevated CO(2) on gene expression in primary polyps of Acropora millepora, using as reference a novel comprehensive transcriptome assembly developed for this study. Gene ontology analysis of this whole transcriptome data set indicated that CO(2) -driven acidification strongly suppressed metabolism but enhanced extracellular organic matrix synthesis, whereas targeted analyses revealed complex effects on genes implicated in calcification. Unexpectedly, expression of most ion transport proteins was unaffected, while many membrane-associated or secreted carbonic anhydrases were expressed at lower levels. The most dramatic effect of CO(2) -driven acidification, however, was on genes encoding candidate and known components of the skeletal organic matrix that controls CaCO(3) deposition. The skeletal organic matrix effects included elevated expression of adult-type galaxins and some secreted acidic proteins, but down-regulation of other galaxins, secreted acidic proteins, SCRiPs and other coral-specific genes, suggesting specialized roles for the members of these protein families and complex impacts of OA on mineral deposition. This study is the first exhaustive exploration of the transcriptomic response of a scleractinian coral to acidification and provides an unbiased perspective on its effects during the early stages of calcification.

Physiological response of the cold-water coral Desmophyllum dianthus to thermal stress and ocean acidification

Rising temperatures and ocean acidification driven by anthropogenic carbon emissions threaten both tropical and temperate corals. However, the synergistic effect of these stressors on coral physiology is still poorly understood, in particular for cold-water corals. This study assessed changes in key physiological parameters (calcification, respiration and ammonium excretion) of the widespread cold-water coral Desmophyllum dianthus maintained for 8 months at two temperatures (ambient 12 °C and elevated 15 °C) and two pCO2 conditions (ambient 390 ppm and elevated 750 ppm). At ambient temperatures no change in instantaneous calcification, respiration or ammonium excretion rates was observed at either pCO2 levels. Conversely, elevated temperature (15 °C) significantly reduced calcification rates, and combined elevated temperature and pCO2 significantly reduced respiration rates. Changes in the ratio of respired oxygen to excreted nitrogen (O:N), which provides information on the main sources of energy being metabolized, indicated a shift from mixed use of protein and carbohydrate/lipid as metabolic substrates under control conditions, to less efficient protein-dominated catabolism under both stressors. Overall, this study shows that the physiology of D. dianthus is more sensitive to thermal than pCO2 stress, and that the predicted combination of rising temperatures and ocean acidification in the coming decades may severely impact this cold-water coral species.

Functional consequences of prey acclimation to ocean acidification for the prey and its predator

Ocean acidification is the suite of chemical changes to the carbonate system of seawater as a consequence of anthropogenic carbon dioxide (CO2) emissions. Despite a growing body of evidences demonstrating the negative effects of ocean acidification on marine species, the consequences at the ecosystem level are still unclear. One factor limiting our ability to upscale from species to ecosystem is the poor mechanistic understanding of the functional consequences of the observed effects on organisms. This is particularly true in the context of species interactions. The aim of this work was to investigate the functional consequence of the exposure of a prey (the mussel Brachidontes pharaonis) to ocean acidification for both the prey and its predator (the crab Eriphia verrucosa). Mussels exposed to pH 7.5 for >4 weeks showed significant decreases in condition index and in mechanical properties (65% decrease in maximum breaking load) as compared with mussels acclimated to pH 8.0. This translated into negative consequences for the mussel in presence of the predator crab. The crab feeding efficiency increased through a significant 27% decrease in prey handling time when offered mussels acclimated to the lowest pH. The predator was also negatively impacted by the acclimation of the prey, probably as a consequence of a decreased food quality. When fed with prey acclimated under decreased pH for 3 months, crab assimilation efficiency significantly decreased by 30% and its growth rate was 5 times slower as compared with crab fed with mussels acclimated under high pH. Our results highlight the important to consider physiological endpoints in the context of species interactions.

Effects of seawater pCO2 and temperature on shell growth, shell stability, condition and cellular stress of Western Baltic Sea Mytilus edulis (L.) and Arctica islandica (L.)

Acidification of the World's oceans may directly impact reproduction, performance and shell formation of marine calcifying organisms. In addition, since shell production is costly and stress in general draws on an organism's energy budget, shell growth and stability of bivalves should indirectly be affected by environmental stress. The aim of this study was to investigate whether a combination of warming and acidification leads to increased physiological stress (lipofuscin accumulation and mortality) and affects the performance [shell growth, shell breaking force, condition index (Ci)] of young Mytilus edulis and Arctica islandica from the Baltic Sea. We cultured the bivalves in a fully-crossed 2-factorial experimental setup (seawater (sw) pCO2 levels "low", "medium" and "high" for both species, temperature levels 7.5, 10, 16, 20 and 25 °C for M. edulis and 7.5, 10 and 16 °C for A. islandica) for 13 weeks in summer. Mytilus edulis and A. islandica appeared to tolerate wide ranges of sw temperature and pCO2. Lipofuscin accumulation of M. edulis increased with temperature while the Ci decreased, but shell growth of the mussels only sharply decreased while its mortality increased between 20 and 25 °C. In A. islandica, lipofuscin accumulation increased with temperature, whereas the Ci, shell growth and shell breaking force decreased. The pCO2 treatment had only marginal effects on the measured parameters of both bivalve species. Shell growth of both bivalve species was not impaired by under-saturation of the sea water with respect to aragonite and calcite. Furthermore, independently of water temperatures shell breaking force of both species and shell growth of A. islandica remained unaffected by the applied elevated sw pCO2 for several months. Only at the highest temperature (25 °C), growth arrest of M. edulis was recorded at the high sw pCO2 treatment and the Ci of M. edulis was slightly higher at the medium sw pCO2 treatment than at the low and high sw pCO2 treatments. The only effect of elevated sw pCO2 on A. islandica was an increase in lipofuscin accumulation at the high sw pCO2 treatment compared to the medium sw pCO2 treatment. Our results show that, despite this robustness, growth of both M. edulis and A. islandica can be reduced if sw temperatures remain high for several weeks in summer. As large body size constitutes an escape from crab and sea star predation, this can make bivalves presumably more vulnerable to predation with possible negative consequences on population growth. In M. edulis, but not in A. islandica, this effect is amplified by elevated sw pCO2. We follow that combined effects of elevated sw pCO2 and ocean warming might cause shifts in future Western Baltic Sea community structures and ecosystem services; however, only if predators or other interacting species do not suffer as strong from these stressors.

Acid-base physiology response to ocean acidification of two ecologically and economically important holothuroids from contrasting habitats, Holothuria scabra and Holothuria parva

Sea cucumbers are dominant invertebrates in several ecosystems such as coral reefs, seagrass meadows and mangroves. As bioturbators, they have an important ecological role in making available calcium carbonate and nutrients to the rest of the community. However, due to their commercial value, they face overexploitation in the natural environment. On top of that, occurring ocean acidification could impact these organisms, considered sensitive as echinoderms are osmoconformers, high-magnesium calcite producers and have a low metabolism. As a first investigation of the impact of ocean acidification on sea cucumbers, we tested the impact of short-term (6 to 12 days) exposure to ocean acidification (seawater pH 7.7 and 7.4) on two sea cucumbers collected in SW Madagascar, Holothuria scabra, a high commercial value species living in the seagrass meadows, and H. parva, inhabiting the mangroves. The former lives in a habitat with moderate fluctuations of seawater chemistry (driven by day-night differences) while the second lives in a highly variable intertidal environment. In both species, pH of the coelomic fluid was significantly negatively affected by reduced seawater pH, with a pronounced extracellular acidosis in individuals maintained at pH 7.7 and 7.4. This acidosis was due to an increased dissolved inorganic carbon content and pCO2 of the coelomic fluid, indicating a limited diffusion of the CO2 towards the external medium. However, respiration and ammonium excretion rates were not affected. No evidence of accumulation of bicarbonate was observed to buffer the coelomic fluid pH. If this acidosis stays uncompensated for when facing long-term exposure, other processes could be affected in both species, eventually leading to impacts on their ecological role.

Combined effects of CO2 and temperature on carbon uptake and partitioning by the marine diatoms Thalassiosira weissflogii and Dactyliosolen fragilissimus

Carbon uptake and partitioning of two globally abundant diatom species, Thalassiosira weissflogii and Dactyliosolen fragilissimus, was investigated in batch culture experiments under four conditions: ambient (15°C, 400 µatm), high CO2 (15°C, 1000 µatm), high temperature (20°C, 400 µatm), and combined (20°C, 1000 µatm). The experiments were run from exponential growth into the stationary phase (six days after nitrogen depletion), allowing us to track biogeochemical dynamics analogous to bloom situations in the ocean. Elevated CO2 had a fertilizing effect and enhanced uptake of dissolved inorganic carbon (DIC) by about 8% for T. weissflogii and by up to 39% for D. fragilissimus. This was also reflected in higher cell numbers, build-up of particulate and dissolved organic matter, and transparent exopolymer particles. The CO2 effects were most prominent in the stationary phase when nitrogen was depleted and CO2(aq) concentrations were low. This indicates that diatoms in the high CO2 treatments could take up more DIC until CO2 concentrations in seawater became so low that carbon limitation occurs. These results suggest that, contrary to common assumptions, diatoms could be highly sensitive to ongoing changes in oceanic carbonate chemistry, particularly under nutrient limitation. Warming from 15 to 20 °C had a stimulating effect on one species but acted as a stressor on the other species, highlighting the importance of species-specific physiological optima and temperature ranges in the response to ocean warming. Overall, these sensitivities to CO2 and temperature could have profound impacts on diatoms blooms and the biological pump.

Physiological response to elevated temperature and pCO2 varies across four Pacific coral species: Understanding the unique host + symbiont response

The physiological response to individual and combined stressors of elevated temperature and pCO2 were measured over a 24-day period in four Pacific corals and their respective symbionts (Acropora millepora/Symbiodinium C21a, Pocillopora damicornis/Symbiodinium C1c-d-t, Montipora monasteriata/Symbiodinium C15, and Turbinaria reniformis/Symbiodinium trenchii). Multivariate analyses indicated that elevated temperature played a greater role in altering physiological response, with the greatest degree of change occurring within M. monasteriata and T. reniformis. Algal cellular volume, protein, and lipid content all increased for M. monasteriata. Likewise, S. trenchii volume and protein content in T. reniformis also increased with temperature. Despite decreases in maximal photochemical efficiency, few changes in biochemical composition (i.e. lipids, proteins, and carbohydrates) or cellular volume occurred at high temperature in the two thermally sensitive symbionts C21a and C1c-d-t. Intracellular carbonic anhydrase transcript abundance increased with temperature in A. millepora but not in P. damicornis, possibly reflecting differences in host mitigated carbon supply during thermal stress. Importantly, our results show that the host and symbiont response to climate change differs considerably across species and that greater physiological plasticity in response to elevated temperature may be an important strategy distinguishing thermally tolerant vs. thermally sensitive species.

Effects of ocean acidification and global warming on reef bioerosion-lessons from a clionaid sponge

Coral reefs are under threat, exerted by a number of interacting effects inherent to the present climate change, including ocean acidification and global warming. Bioerosion drives reef degradation by recycling carbonate skeletal material and is an important but understudied factor in this context. Twelve different combinations of pCO2 and temperature were applied to elucidate the consequences of ocean acidification and global warming on the physiological response and bioerosion rates of the zooxanthellate sponge Cliona orientalis-one of the most abundant and effective bioeroders on the Great Barrier Reef, Australia. Our results confirm a significant amplification of the sponges' bioerosion capacity with increasing pCO2, which is expressed by more carbonate being chemically dissolved by etching. The health of the sponges and their photosymbionts was not affected by changes in pCO2, in contrast to temperature, which had significant negative impacts at higher levels. However, we could not conclusively explain the relationship between temperature and bioerosion rates, which were slightly reduced at both colder as well as warmer temperatures than ambient. The present findings on the effects of ocean acidification on chemical bioerosion, however, will have significant implications for predicting future reef carbonate budgets, as sponges often contribute the lion's share of internal bioerosion on coral reefs.

Effects of reduced and business-as-usual CO2 emission scenarios on the algal territories of the damselfish Pomacentrus wardi (Pomacentridae)

Turf algae are a very important component of coral reefs, featuring high growth and turnover rates, whilst covering large areas of substrate. As food for many organisms, turf algae have an important role in the ecosystem. Farming damselfish can modify the species composition and productivity of such algal assemblages, while defending them against intruders. Like all organisms however, turf algae and damselfishes have the potential to be affected by future changes in seawater (SW) temperature and pCO2. In this study, algal assemblages, in the presence and absence of farming Pomacentrus wardi were exposed to two combinations of SW temperature and pCO2 levels projected for the austral spring of 2100 (the B1 "reduced" and the A1FI "business-as-usual" CO2 emission scenarios) at Heron Island (GBR, Australia). These assemblages were dominated by the presence of red algae and non-epiphytic cyanobacteria, i.e. cyanobacteria that grow attached to the substrate rather than on filamentous algae. The endpoint algal composition was mostly controlled by the presence/absence of farming damselfish, despite a large variability found between the algal assemblages of individual fish. Different scenarios appeared to be responsible for a mild, species specific change in community composition, observable in some brown and green algae, but only in the absence of farming fish. Farming fish appeared unaffected by the conditions to which they were exposed. Algal biomass reductions were found under "reduced" CO2 emission, but not "business-as-usual" scenarios. This suggests that action taken to limit CO2 emissions may, if the majority of algae behave similarly across all seasons, reduce the potential for phase shifts that lead to algal dominated communities. At the same time the availability of food resources to damselfish and other herbivores would be smaller under "reduced" emission scenarios.

Threatened Caribbean coral is able to mitigate the adverse effects of ocean acidification on calcification by increasing feeding rate

Global climate change threatens coral growth and reef ecosystem health via ocean warming and ocean acidification (OA). Whereas the negative impacts of these stressors are increasingly well-documented, studies identifying pathways to resilience are still poorly understood. Heterotrophy has been shown to help corals experiencing decreases in growth due to either thermal or OA stress; however, the mechanism by which it mitigates these decreases remains unclear. This study tested the ability of coral heterotrophy to mitigate reductions in growth due to climate change stress in the critically endangered Caribbean coral Acropora cervicornis via changes in feeding rate and lipid content. Corals were either fed or unfed and exposed to elevated temperature (30°C), enriched pCO2 (800 ppm), or both (30°C/800 ppm) as compared to a control (26°C/390 ppm) for 8 weeks. Feeding rate and lipid content both increased in corals experiencing OA vs. present-day conditions, and were significantly correlated. Fed corals were able to maintain ambient growth rates at both elevated temperature and elevated CO2, while unfed corals experienced significant decreases in growth with respect to fed conspecifics. Our results show for the first time that a threatened coral species can buffer OA-reduced calcification by increasing feeding rates and lipid content.