Resolving the interactions of ocean acidification and temperature on coral calcification media pH

Coral Reefs - Ocean acidification typically reduces the calcification rates of massive Porites spp. corals, but increasing seawater temperatures (below the stress and bleaching threshold) can...     

Combined effects of warming and ocean acidification on coral reef Foraminifera Marginopora vertebralis and Heterostegina depressa

Warming and changes in ocean carbonate chemistry alter marine coastal ecosystems at an accelerating pace. The interaction between these stressors has been the subject of recent studies on reef organisms such as corals, bryozoa, molluscs, and crustose coralline algae. Here we investigated the combined effects of elevated sea surface temperatures and pCO₂ on two species of photosymbiont-bearing coral reef Foraminifera: Heterostegina depressa (hosting diatoms) and Marginopora vertebralis (hosting dinoflagellates). The effects of single and combined stressors were studied by monitoring survivorship, growth, and physiological parameters, such as respiration, photochemistry (pulse amplitude modulation fluorometry and oxygen production), and chl a content. Specimens were exposed in flow-through aquaria for up to seven weeks to combinations of two pCO₂ (~790 and ~490 µatm) and two temperature (28 and 31 °C) regimes. Elevated temperature had negative effects on the physiology of both species. Elevated pCO₂ had negative effects on growth and apparent photosynthetic rate in H.depressa but a positive effect on effective quantum yield. With increasing pCO₂, chl a content decreased in H. depressa and increased in M. vertebralis. The strongest stress responses were observed when the two stressors acted in combination. An interaction term was statistically significant in half of the measured parameters. Further exploration revealed that 75 % of these cases showed a synergistic (= larger than additive) interaction between the two stressors. These results indicate that negative physiological effects on photosymbiont-bearing coral reef Foraminifera are likely to be stronger under simultaneous acidification and temperature rise than what would be expected from the effect of each of the stressors individually.     

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 world''s 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.     

Effects of ocean acidification on learning in coral reef fishes

Ocean acidification has the potential to cause dramatic changes in marine ecosystems. Larval damselfish exposed to concentrations of CO(2) predicted to occur in the mid- to late-century show maladaptive responses to predator cues. However, there is considerable variation both within and between species in CO(2) effects, whereby some individuals are unaffected at particular CO(2) concentrations while others show maladaptive responses to predator odour. Our goal was to test whether learning via chemical or visual information would be impaired by ocean acidification and ultimately, whether learning can mitigate the effects of ocean acidification by restoring the appropriate responses of prey to predators. Using two highly efficient and widespread mechanisms for predator learning, we compared the behaviour of pre-settlement damselfish Pomacentrus amboinensis that were exposed to 440 μatm CO(2) (current day levels) or 850 μatm CO(2), a concentration predicted to occur in the ocean before the end of this century. We found that, regardless of the method of learning, damselfish exposed to elevated CO(2) failed to learn to respond appropriately to a common predator, the dottyback, Pseudochromis fuscus. To determine whether the lack of response was due to a failure in learning or rather a short-term shift in trade-offs preventing the fish from displaying overt antipredator responses, we conditioned 440 or 700 μatm-CO(2) fish to learn to recognize a dottyback as a predator using injured conspecific cues, as in Experiment 1. When tested one day post-conditioning, CO(2) exposed fish failed to respond to predator odour. When tested 5 days post-conditioning, CO(2) exposed fish still failed to show an antipredator response to the dottyback odour, despite the fact that both control and CO(2)-treated fish responded to a general risk cue (injured conspecific cues). These results indicate that exposure to CO(2) may alter the cognitive ability of juvenile fish and render learning ineffective.     

Differential response of two Mediterranean cold-water coral species to ocean acidification

Cold-water coral (CWC) reefs constitute one of the most complex deep-sea habitats harboring a vast diversity of associated species. Like other tropical or temperate framework builders, these systems are facing an uncertain future due to several threats, such as global warming and ocean acidification. In the case of Mediterranean CWC communities, the effect may be exacerbated due to the greater capacity of these waters to absorb atmospheric CO₂ compared to the global ocean. Calcification in these organisms is an energy-demanding process, and it is expected that energy requirements will be greater as seawater pH and the availability of carbonate ions decrease. Therefore, studies assessing the effect of a pH decrease in skeletal growth, and metabolic balance are critical to fully understand the potential responses of these organisms under a changing scenario. In this context, the present work aims to investigate the medium- to long-term effect of a low pH scenario on calcification and the biochemical composition of two CWCs from the Mediterranean, Dendrophyllia cornigera and Desmophyllum dianthus. After 314 d of exposure to acidified conditions, a significant decrease of 70 % was observed in Desmophyllum dianthus skeletal growth rate, while Dendrophyllia cornigera showed no differences between treatments. Instead, only subtle differences between treatments were observed in the organic matter amount, lipid content, skeletal microdensity, or porosity in both species, although due to the high variability of the results, these differences were not statistically significant. Our results also confirmed a heterogeneous effect of low pH on the skeletal growth rate of the organisms depending on their initial weight, suggesting that those specimens with high calcification rates may be the most susceptible to the negative effects of acidification.     

Future habitat suitability for coral reef ecosystems under global warming and ocean acidification

Rising atmospheric CO₂ concentrations are placing spatially divergent stresses on the world's tropical coral reefs through increasing ocean surface temperatures and ocean acidification. We show how these two stressors combine to alter the global habitat suitability for shallow coral reef ecosystems, using statistical Bioclimatic Envelope Models rather than basing projections on any a priori assumptions of physiological tolerances or fixed thresholds. We apply two different modeling approaches (Maximum Entropy and Boosted Regression Trees) with two levels of complexity (one a simplified and reduced environmental variable version of the other). Our models project a marked temperature‐driven decline in habitat suitability for many of the most significant and bio‐diverse tropical coral regions, particularly in the central Indo‐Pacific. This is accompanied by a temperature‐driven poleward range expansion of favorable conditions accelerating up to 40–70 km per decade by 2070. We find that ocean acidification is less influential for determining future habitat suitability than warming, and its deleterious effects are centered evenly in both hemispheres between 5° and 20° latitude. Contrary to expectations, the combined impact of ocean surface temperature rise and acidification leads to little, if any, degradation in future habitat suitability across much of the Atlantic and areas currently considered ‘marginal’ for tropical corals, such as the eastern Equatorial Pacific. These results are consistent with fossil evidence of range expansions during past warm periods. In addition, the simplified models are particularly sensitive to short‐term temperature variations and their projections correlate well with reported locations of bleaching events. Our approach offers new insights into the relative impact of two global environmental pressures associated with rising atmospheric CO₂ on potential future habitats, but greater understanding of past and current controls on coral reef ecosystems is essential to their conservation and management under a changing climate.     

Major cellular and physiological impacts of ocean acidification on a reef building coral

As atmospheric levels of CO(2) increase, reef-building corals are under greater stress from both increased sea surface temperatures and declining sea water pH. To date, most studies have focused on either coral bleaching due to warming oceans or declining calcification due to decreasing oceanic carbonate ion concentrations. Here, through the use of physiology measurements and cDNA microarrays, we show that changes in pH and ocean chemistry consistent with two scenarios put forward by the Intergovernmental Panel on Climate Change (IPCC) drive major changes in gene expression, respiration, photosynthesis and symbiosis of the coral, Acropora millepora, before affects on biomineralisation are apparent at the phenotype level. Under high CO(2) conditions corals at the phenotype level lost over half their Symbiodinium populations, and had a decrease in both photosynthesis and respiration. Changes in gene expression were consistent with metabolic suppression, an increase in oxidative stress, apoptosis and symbiont loss. Other expression patterns demonstrate upregulation of membrane transporters, as well as the regulation of genes involved in membrane cytoskeletal interactions and cytoskeletal remodeling. These widespread changes in gene expression emphasize the need to expand future studies of ocean acidification to include a wider spectrum of cellular processes, many of which may occur before impacts on calcification.     

Responses of a coral reef shark acutely exposed to ocean acidification conditions

Anthropogenic ocean acidification (OA) is a threat to coral reef fishes, but few studies have investigated responses of high-trophic-level predators, including sharks. We tested the effects of 72-hr exposure to OA-relevant elevated partial pressures of carbon dioxide (pCO₂) on oxygen uptake rates, acid–base status, and haematology of newborn tropical blacktip reef sharks (Carcharhinus melanopterus). Acute exposure to end-of-century pCO₂ levels resulted in elevated haematocrit (i.e. stress or compensation of oxygen uptake rates) and blood lactate concentrations (i.e. prolonged recovery) in the newborns. Conversely, whole blood and mean corpuscular haemoglobin concentrations, blood pH, estimates of standard and maximum metabolic rates, and aerobic scope remained unaffected. Taken together, newborn blacktip reef sharks appear physiologically robust to end-of-century pCO₂ levels, but less so than other, previously investigated, tropical carpet sharks. Our results suggest peak fluctuating pCO₂ levels in coral reef lagoons could still physiologically affect newborn reef sharks, but studies assessing the effects of long-term exposure and in combination with other anthropogenic stressors are needed.

     

海洋酸化对珊瑚礁生态系统的影响研究进展

目前,大气CO2浓度的升高已导致海水pH值比工业革命前下降了约0.1,海水碳酸盐平衡体系随之变化,进而影响珊瑚礁生态系统的健康。近年来的研究表明海洋酸化导致造礁石珊瑚幼体补充和群落恢复更加困难,造礁石珊瑚和其它造礁生物(Reef-building organisms)钙化率降低甚至溶解,乃至影响珊瑚礁鱼类的生命活动。虽然海洋酸化对造礁石珊瑚光合作用的影响不显著,但珊瑚-虫黄藻共生体系会受到一定影响。建议选择典型海区进行长期系统监测,结合室内与原位模拟试验,从个体、种群、群落到系统不同层面,运用生理学和分子生物学技术,结合生态学研究手段,综合研究珊瑚的相应响应,以期深入认识海洋酸化对珊瑚礁生态系统健康(例如珊瑚白化)的影响及其效应。     

The reef-building coral Siderastrea siderea exhibits parabolic responses to ocean acidification and warming

Anthropogenic increases in atmospheric CO₂ over this century are predicted to cause global average surface ocean pH to decline by 0.1–0.3 pH units and sea surface temperature to increase by 1–4°C. We conducted controlled laboratory experiments to investigate the impacts of CO₂-induced ocean acidification (pCO₂ = 324, 477, 604, 2553 µatm) and warming (25, 28, 32°C) on the calcification rate of the zooxanthellate scleractinian coral Siderastrea siderea, a widespread, abundant and keystone reef-builder in the Caribbean Sea. We show that both acidification and warming cause a parabolic response in the calcification rate within this coral species. Moderate increases in pCO₂ and warming, relative to near-present-day values, enhanced coral calcification, with calcification rates declining under the highest pCO₂ and thermal conditions. Equivalent responses to acidification and warming were exhibited by colonies across reef zones and the parabolic nature of the corals'' response to these stressors was evident across all three of the experiment''s 30-day observational intervals. Furthermore, the warming projected by the Intergovernmental Panel on Climate Change for the end of the twenty-first century caused a fivefold decrease in the rate of coral calcification, while the acidification projected for the same interval had no statistically significant impact on the calcification rate—suggesting that ocean warming poses a more immediate threat than acidification for this important coral species.     

Opposite latitudinal gradients in projected ocean acidification and bleaching impacts on coral reefs

Coral reefs and the services they provide are seriously threatened by ocean acidification and climate change impacts like coral bleaching. Here, we present updated global projections for these key threats to coral reefs based on ensembles of IPCC AR5 climate models using the new Representative Concentration Pathway (RCP) experiments. For all tropical reef locations, we project absolute and percentage changes in aragonite saturation state (Ωarag) for the period between 2006 and the onset of annual severe bleaching (thermal stress >8 degree heating weeks); a point at which it is difficult to believe reefs can persist as we know them. Severe annual bleaching is projected to start 10–15 years later at high‐latitude reefs than for reefs in low latitudes under RCP8.5. In these 10–15 years, Ωarag keeps declining and thus any benefits for high‐latitude reefs of later onset of annual bleaching may be negated by the effects of acidification. There are no long‐term refugia from the effects of both acidification and bleaching. Of all reef locations, 90% are projected to experience severe bleaching annually by 2055. Furthermore, 5% declines in calcification are projected for all reef locations by 2034 under RCP8.5, assuming a 15% decline in calcification per unit of Ωarag. Drastic emissions cuts, such as those represented by RCP6.0, result in an average year for the onset of annual severe bleaching that is ~20 years later (2062 vs. 2044). However, global emissions are tracking above the current worst‐case scenario devised by the scientific community, as has happened in previous generations of emission scenarios. The projections here for conditions on coral reefs are dire, but provide the most up‐to‐date assessment of what the changing climate and ocean acidification mean for the persistence of coral reefs.     

Calcifying coral abundance near low-pH springs: implications for future ocean acidification

Rising atmospheric CO₂ and its equilibration with surface ocean seawater is lowering both the pH and carbonate saturation state (Ω) of the oceans. Numerous calcifying organisms, including reef-building corals, may be severely impacted by declining aragonite and calcite saturation, but the fate of coral reef ecosystems in response to ocean acidification remains largely unexplored. Naturally low saturation (Ω ~ 0.5) low pH (6.70–7.30) groundwater has been discharging for millennia at localized submarine springs (called “ojos”) at Puerto Morelos, México near the Mesoamerican Reef. This ecosystem provides insights into potential long term responses of coral ecosystems to low saturation conditions. In-situ chemical and biological data indicate that both coral species richness and coral colony size decline with increasing proximity to low-saturation, low-pH waters at the ojo centers. Only three scleractinian coral species (Porites astreoides, Porites divaricata, and Siderastrea radians) occur in undersaturated waters at all ojos examined. Because these three species are rarely major contributors to Caribbean reef framework, these data may indicate that today’s more complex frame-building species may be replaced by smaller, possibly patchy, colonies of only a few species along the Mesoamerican Barrier Reef. The growth of these scleractinian coral species at undersaturated conditions illustrates that the response to ocean acidification is likely to vary across species and environments; thus, our data emphasize the need to better understand the mechanisms of calcification to more accurately predict future impacts of ocean acidification.     

Similar controls on calcification under ocean acidification across unrelated coral reef taxa

Ocean acidification (OA) is a major threat to marine ecosystems, particularly coral reefs which are heavily reliant on calcareous species. OA decreases seawater pH and calcium carbonate saturation state (Ω), and increases the concentration of dissolved inorganic carbon (DIC). Intense scientific effort has attempted to determine the mechanisms via which ocean acidification (OA) influences calcification, led by early hypotheses that calcium carbonate saturation state (Ω) is the main driver. We grew corals and coralline algae for 8–21 weeks, under treatments where the seawater parameters Ω, pH, and DIC were manipulated to examine their differential effects on calcification rates and calcifying fluid chemistry (Ω_cf, pH_cf, and DIC_cf). Here, using long duration experiments, we provide geochemical evidence that differing physiological controls on carbonate chemistry at the site of calcification, rather than seawater Ω, are the main determinants of calcification. We found that changes in seawater pH and DIC rather than Ω had the greatest effects on calcification and calcifying fluid chemistry, though the effects of seawater carbonate chemistry were limited. Our results demonstrate the capacity of organisms from taxa with vastly different calcification mechanisms to regulate their internal chemistry under extreme chemical conditions. These findings provide an explanation for the resistance of some species to OA, while also demonstrating how changes in seawater DIC and pH under OA influence calcification of key coral reef taxa.     

Vulnerability of global coral reef habitat suitability to ocean warming,acidification and eutrophication

Coral reefs are threatened by global and local stressors. Yet, reefs appear to respond differently to different environmental stressors. Using a global dataset of coral reef occurrence as a proxy for the long‐term adaptation of corals to environmental conditions in combination with global environmental data, we show here how global (warming: sea surface temperature; acidification: aragonite saturation state, Ω_arag) and local (eutrophication: nitrate concentration, and phosphate concentration) stressors influence coral reef habitat suitability. We analyse the relative distance of coral communities to their regional environmental optima. In addition, we calculate the expected change of coral reef habitat suitability across the tropics in relation to an increase of 0.1°C in temperature, an increase of 0.02 μmol/L in nitrate, an increase of 0.01 μmol/L in phosphate and a decrease of 0.04 in Ω_arag. Our findings reveal that only 6% of the reefs worldwide will be unaffected by local and global stressors and can thus act as temporary refugia. Local stressors, driven by nutrient increase, will affect 22% of the reefs worldwide, whereas global stressors will affect 11% of these reefs. The remaining 61% of the reefs will be simultaneously affected by local and global stressors. Appropriate wastewater treatments can mitigate local eutrophication and could increase areas of temporary refugia to 28%, allowing us to ‘buy time’, while international agreements are found to abate global stressors.     

Sensitivity of coral calcification to ocean acidification: a meta‐analysis

To date, meta‐analyses of effects of acidification have focused on the overall strength of evidence for statistically significant responses; however, to anticipate likely consequences of ocean acidification, quantitative estimates of the magnitude of likely responses are also needed. Herein, we use random effects meta‐analysis to produce a systematically integrated measure of the distribution of magnitudes of the response of coral calcification to decreasing Ω_Arag. We also tested whether methodological and biological factors that have been hypothesized to drive variation in response magnitude explain a significant proportion of the among‐study variation. We found that the overall mean response of coral calcification is ~15% per unit decrease in Ω_Arag over the range 2 < Ω_Arag < 4. Among‐study variation is large (standard deviation of 8% per unit decrease in Ω_Arag). Neither differences in carbonate chemistry manipulation method, study duration, irradiance level, nor study species growth rate explained a significant proportion of the among‐study variation. However, studies employing buoyant weighting found significantly smaller decreases in calcification per unit Ω_Arag (~10%), compared with studies using the alkalinity anomaly technique (~25%). These differences may be due to the greater tendency for the former to integrate over light and dark calcification. If the existing body of experimental work is indeed representative of likely responses of corals in nature, our results imply that, under business as usual conditions, declines in coral calcification by end‐of‐century will be ~22%, on average, or ~15% if only studies integrating light and dark calcification are considered. These values are near the low end of published projections, but support the emerging view that variability due to local environmental conditions and species composition is likely to be substantial.     

Combined effects of two ocean change stressors, warming and acidification, on fertilization and early development of the Antarctic echinoid Sterechinus neumayeri

The effects of concurrent ocean warming and acidification on Antarctic marine benthos warrant investigation as little is known about potential synergies between these climate change stressors. We examined the interactive effects of warming and acidification on fertilization and embryonic development of the ecologically important sea urchin Sterechinus neumayeri reared from fertilization in elevated temperature (+1.5°C and 3°C) and decreased pH (?0.3 and ?0.5 pH units) treatments. Fertilization using gametes from multiple males and females, to represent populations of spawners, was resilient to acidification at ambient temperature (0°C). At elevated temperatures, there was a negative interactive effect of temperature and pH on percentage of fertilization (11% reduction at 3°C). For cleavage stage embryos, there was a significant, but small reduction (6%) in the percentage of normal embryos at pH 7.5. For blastulae, a 10–11% decrease in normal development occurred in the +3°C treatments across all pH levels. Our results highlight the importance of considering the impacts of both temperature and pH in assessing the life history response of S. neumayeri in a changing polar ocean. While fertilization and development to the blastula stage were robust to levels of temperature and pH change predicted over coming decades, deleterious interactive effects were evident between these stressors at levels projected to occur by 2100 and beyond.     

Effects of the ocean acidification on the functional structure of coral reef nematodes

Coral Reefs - A mesocosm experiment was designed to study the effects of acidification on the phytal nematofauna of a coral reef. We hypothesized that phytal nematodes are responsive to different...     

Response of Mediterranean coralline algae to ocean acidification and elevated temperature

The effects of elevated partial pressure of CO₂ ( p CO₂) and temperature, alone and in combination, on survival, calcification and dissolution were investigated in the crustose coralline alga Lithophyllum cabiochae . Algae were maintained in aquaria during 1 year at near-ambient conditions of irradiance, at ambient or elevated temperature (+3 °C) and at ambient [ca. 400 parts per million (ppm)] or elevated p CO₂ (ca. 700 ppm). Algal necroses appeared at the end of summer under elevated temperature first at 700 ppm (60% of the thallus surface) and then at 400 ppm (30%). The death of algae was observed only under elevated temperature and was two- to threefold higher under elevated p CO₂. During the first month of the experiment, net calcification was significantly reduced under elevated p CO₂. At the end of the summer period, net calcification decreased by 50% when both temperature and p CO₂ were elevated while no effect was found under elevated temperature and elevated p CO₂ alone. In autumn and winter, net calcification in healthy algae increased with increasing temperature, independently of the p CO₂ level, while necroses and death in the algal population caused a net dissolution at elevated temperature and p CO₂. The dissolution of dead algal thalli was affected by elevated p CO₂, being two- to fourfold higher than under ambient p CO₂. These results suggest that net dissolution is likely to exceed net calcification in L. cabiochae by the end of this century. This could have major consequences in terms of biodiversity and biogeochemistry in coralligenous communities dominated by these algae.