Coralline algae (Rhodophyta) in a changing world: integrating ecological,physiological, and geochemical responses to global change

Coralline algae are globally distributed benthic primary producers that secrete calcium carbonate skeletons. In the context of ocean acidification, they have received much recent attention due to the potential vulnerability of their high‐Mg calcite skeletons and their many important ecological roles. Herein, we summarize what is known about coralline algal ecology and physiology, providing context to understand their responses to global climate change. We review the impacts of these changes, including ocean acidification, rising temperatures, and pollution, on coralline algal growth and calcification. We also assess the ongoing use of coralline algae as marine climate proxies via calibration of skeletal morphology and geochemistry to environmental conditions. Finally, we indicate critical gaps in our understanding of coralline algal calcification and physiology and highlight key areas for future research. These include analytical areas that recently have become more accessible, such as resolving phylogenetic relationships at all taxonomic ranks, elucidating the genes regulating algal photosynthesis and calcification, and calibrating skeletal geochemical metrics, as well as research directions that are broadly applicable to global change ecology, such as the importance of community‐scale and long‐term experiments in stress response.     

Investigating marine bio‐calcification mechanisms in a changing ocean with in vivo and high‐resolution ex vivo Raman spectroscopy

Ocean acidification poses a serious threat to marine calcifying organisms, yet experimental and field studies have found highly diverse responses among species and environments. Our understanding of the underlying drivers of differential responses to ocean acidification is currently limited by difficulties in directly observing and quantifying the mechanisms of bio‐calcification. Here, we present Raman spectroscopy techniques for characterizing the skeletal mineralogy and calcifying fluid chemistry of marine calcifying organisms such as corals, coralline algae, foraminifera, and fish (carbonate otoliths). First, our in vivo Raman technique is the ideal tool for investigating non‐classical mineralization pathways. This includes calcification by amorphous particle attachment, which has recently been controversially suggested as a mechanism by which corals resist the negative effects of ocean acidification. Second, high‐resolution ex vivo Raman mapping reveals complex banding structures in the mineralogy of marine calcifiers, and provides a tool to quantify calcification responses to environmental variability on various timescales from days to years. We describe the new insights into marine bio‐calcification that our techniques have already uncovered, and we consider the wide range of questions regarding calcifier responses to global change that can now be proposed and addressed with these new Raman spectroscopy tools.     

Coralline algae elevate pH at the site of calcification under ocean acidification

Coralline algae provide important ecosystem services but are susceptible to the impacts of ocean acidification. However, the mechanisms are uncertain, and the magnitude is species specific. Here, we assess whether species‐specific responses to ocean acidification of coralline algae are related to differences in pH at the site of calcification within the calcifying fluid/medium (pH_cf) using δ¹¹B as a proxy. Declines in δ¹¹B for all three species are consistent with shifts in δ¹¹B expected if B(OH)₄^? was incorporated during precipitation. In particular, the δ¹¹B ratio in Amphiroa anceps was too low to allow for reasonable pH_cf values if B(OH)₃ rather than B(OH)₄^? was directly incorporated from the calcifying fluid. This points towards δ¹¹B being a reliable proxy for pH_cf for coralline algal calcite and that if B(OH)₃ is present in detectable proportions, it can be attributed to secondary postincorporation transformation of B(OH)₄^?. We thus show that pH_cf is elevated during calcification and that the extent is species specific. The net calcification of two species of coralline algae (Sporolithon durum, and Amphiroa anceps) declined under elevated CO₂, as did their pH_cf. Neogoniolithon sp. had the highest pH_cf, and most constant calcification rates, with the decrease in pH_cf being ¼ that of seawater pH in the treatments, demonstrating a control of coralline algae on carbonate chemistry at their site of calcification. The discovery that coralline algae upregulate pH_cf under ocean acidification is physiologically important and should be included in future models involving calcification.     

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.     

高浓度CO2引起的海水酸化对小珊瑚藻光合作用和钙化作用的影响

为了探讨CO2海底封存潜在的渗漏危险对于海洋生物的可能影响,以大型钙化藻类小珊瑚藻(Corallina pilulifera)为研究对象,在室内控光控温条件下,通过向培养海水充入CO2气体得到3种不同酸化程度的培养条件(pH 8.1、6.8和5.5),24h后比较藻体光合作用和钙化作用情况。结果显示:相对于自然海水培养条件(pH 8.1),在pH 6.8条件下培养的小珊瑚藻光合固碳速率得到了增强,而在pH 5.5条件下光合固碳速率则降低;随着酸化程度的增强,藻体的钙化固碳速率越来越低,在pH 5.5条件下甚至表现为负值[(-2.53±0.57)mg C g-1干重h-1];藻体颗粒无机碳(PIC)和颗粒有机碳(POC)含量的比值随着酸化程度的加强而降低,这反映了酸化对光合和钙化作用的综合效应。快速光反应曲线的测定结果显示:随着酸化程度的增强,强光引起的光抑制程度越来越强;在酸化条件下,藻体的光饱和点显著降低,但pH 6.8和5.5之间没有显著差异;低光下的电子传递速率在pH 8.1和6.8之间没有显著差异,pH 5.5培养条件下显著降低;最大电子传递速率在pH 6.8时最大,在pH 5.5时最低。以上结果说明,高浓度CO2引起的海水酸化显著地影响着小珊瑚藻的光合和钙化过程,不同的酸化程度下,藻体的光合、钙化反应不同,在较强的酸化程度下(pH 5.5),藻体的光合和钙化过程都将受到强烈的抑制,这些结果为认识CO2海底封存渗漏危险对海洋钙化藻类的可能影响提供了理论参考。     

TESTING THE EFFECTS OF OCEAN ACIDIFICATION ON ALGAL METABOLISM: CONSIDERATIONS FOR EXPERIMENTAL DESIGNS1

Ocean acidification describes changes in the carbonate chemistry of the ocean due to the increased absorption of anthropogenically released CO₂. Experiments to elucidate the biological effects of ocean acidification on algae are not straightforward because when pH is altered, the carbon speciation in seawater is altered, which has implications for photosynthesis and, for calcifying algae, calcification. Furthermore, photosynthesis, respiration, and calcification will themselves alter the pH of the seawater medium. In this review, algal physiologists and seawater carbonate chemists combine their knowledge to provide the fundamental information on carbon physiology and seawater carbonate chemistry required to comprehend the complexities of how ocean acidification might affect algae metabolism. A wide range in responses of algae to ocean acidification has been observed, which may be explained by differences in algal physiology, timescales of the responses measured, study duration, and the method employed to alter pH. Two methods have been widely used in a range of experimental systems: CO₂ bubbling and HCl/NaOH additions. These methods affect the speciation of carbonate ions in the culture medium differently; we discuss how this could influence the biological responses of algae and suggest a third method based on HCl/NaHCO₃ additions. We then discuss eight key points that should be considered prior to setting up experiments, including which method of manipulating pH to choose, monitoring during experiments, techniques for adding acidified seawater, biological side effects, and other environmental factors. Finally, we consider incubation timescales and prior conditioning of algae in terms of regulation, acclimation, and adaptation to ocean acidification.     

Diffusion Boundary Layers Ameliorate the Negative Effects of Ocean Acidification on the Temperate Coralline Macroalga Arthrocardia corymbosa

Anthropogenically-modulated reductions in pH, termed ocean acidification, could pose a major threat to the physiological performance, stocks, and biodiversity of calcifiers and may devalue their ecosystem services. Recent debate has focussed on the need to develop approaches to arrest the potential negative impacts of ocean acidification on ecosystems dominated by calcareous organisms. In this study, we demonstrate the role of a discrete (i.e. diffusion) boundary layer (DBL), formed at the surface of some calcifying species under slow flows, in buffering them from the corrosive effects of low pH seawater. The coralline macroalga Arthrocardia corymbosa was grown in a multifactorial experiment with two mean pH levels (8.05 ‘ambient’ and 7.65 a worst case ‘ocean acidification’ scenario projected for 2100), each with two levels of seawater flow (fast and slow, i.e. DBL thin or thick). Coralline algae grown under slow flows with thick DBLs (i.e., unstirred with regular replenishment of seawater to their surface) maintained net growth and calcification at pH 7.65 whereas those in higher flows with thin DBLs had net dissolution. Growth under ambient seawater pH (8.05) was not significantly different in thin and thick DBL treatments. No other measured diagnostic (recruit sizes and numbers, photosynthetic metrics, %C, %N, %MgCO₃) responded to the effects of reduced seawater pH. Thus, flow conditions that promote the formation of thick DBLs, may enhance the subsistence of calcifiers by creating localised hydrodynamic conditions where metabolic activity ameliorates the negative impacts of ocean acidification.     

Gene expression changes in the coccolithophore Emiliania huxleyi after 500 generations of selection to ocean acidification

Coccolithophores are unicellular marine algae that produce biogenic calcite scales and substantially contribute to marine primary production and carbon export to the deep ocean. Ongoing ocean acidification particularly impairs calcifying organisms, mostly resulting in decreased growth and calcification. Recent studies revealed that the immediate physiological response in the coccolithophore Emiliania huxleyi to ocean acidification may be partially compensated by evolutionary adaptation, yet the underlying molecular mechanisms are currently unknown. Here, we report on the expression levels of 10 candidate genes putatively relevant to pH regulation, carbon transport, calcification and photosynthesis in E. huxleyi populations short-term exposed to ocean acidification conditions after acclimation (physiological response) and after 500 generations of high CO₂ adaptation (adaptive response). The physiological response revealed downregulation of candidate genes, well reflecting the concomitant decrease of growth and calcification. In the adaptive response, putative pH regulation and carbon transport genes were up-regulated, matching partial restoration of growth and calcification in high CO₂-adapted populations. Adaptation to ocean acidification in E. huxleyi likely involved improved cellular pH regulation, presumably indirectly affecting calcification. Adaptive evolution may thus have the potential to partially restore cellular pH regulatory capacity and thereby mitigate adverse effects of ocean acidification.     

Microenvironmental changes support evidence of photosynthesis and calcification inhibition in Halimeda under ocean acidification and warming

The effects of elevated CO₂ and temperature on photosynthesis and calcification of two important calcifying reef algae (Halimeda macroloba and Halimeda cylindracea) were investigated with O₂ microsensors and chlorophyll a fluorometry through a combination of two pCO₂ (400 and 1,200 μatm) and two temperature treatments (28 and 32 °C) equivalent to the present and predicted conditions during the 2100 austral summer. Combined exposure to pCO₂ and elevated temperature impaired calcification and photosynthesis in the two Halimeda species due to changes in the microenvironment around the algal segments and a reduction in physiological performance. There were no significant changes in controls over the 5-week experiment, but there was a 50–70 % decrease in photochemical efficiency (maximum quantum yield), a 70–80 % decrease in O₂ production and a threefold reduction in calcification rate in the elevated CO₂ and high temperature treatment. Calcification in these species is closely coupled with photosynthesis, such that a decrease in photosynthetic efficiency leads to a decrease in calcification. Although pH seems to be the main factor affecting Halimeda species, heat stress also has an impact on their photosystem II photochemical efficiency. There was a strong combined effect of elevated CO₂ and temperature in both species, where exposure to elevated CO₂ or temperature alone decreased photosynthesis and calcification, but exposure to both elevated CO₂ and temperature caused a greater decline in photosynthesis and calcification than in each stress individually. Our study shows that ocean acidification and ocean warming are drivers of calcification and photosynthesis inhibition in Halimeda. Predicted climate change scenarios for 2100 would therefore severely affect the fitness of Halimeda, which can result in a strongly reduced production of carbonate sediments on coral reefs under such changed climate conditions.     

One‐year experiment on the physiological response of the Mediterranean crustose coralline alga,Lithophyllum cabiochae,to elevated pCO2 and temperature

The response of respiration, photosynthesis, and calcification to elevated pCO₂ and temperature was investigated in isolation and in combination in the Mediterranean 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 μatm) or elevated pCO₂ (ca. 700 μatm). Respiration, photosynthesis, and net calcification showed a strong seasonal pattern following the seasonal variations of temperature and irradiance, with higher rates in summer than in winter. Respiration was unaffected by pCO₂ but showed a general trend of increase at elevated temperature at all seasons, except in summer under elevated pCO₂. Conversely, photosynthesis was strongly affected by pCO₂ with a decline under elevated pCO₂ in summer, autumn, and winter. In particular, photosynthetic efficiency was reduced under elevated pCO₂. Net calcification showed different responses depending on the season. In summer, net calcification increased with rising temperature under ambient pCO₂ but decreased with rising temperature under elevated pCO₂. Surprisingly, the highest rates in summer were found under elevated pCO₂ and ambient temperature. In autumn, winter, and spring, net calcification exhibited a positive or no response at elevated temperature but was unaffected by pCO₂. The rate of calcification of L. cabiochae was thus maintained or even enhanced under increased pCO₂. However, there is likely a trade‐off with other physiological processes. For example, photosynthesis declines in response to increased pCO₂ under ambient irradiance. The present study reports only on the physiological response of healthy specimens to ocean warming and acidification, however, these environmental changes may affect the vulnerability of coralline algae to other stresses such as pathogens and necroses that can cause major dissolution, which would have critical consequence for the sustainability of coralligenous habitats and the budgets of carbon and calcium carbonate in coastal Mediterranean ecosystems.     

Combined effects of ocean acidification and solar UV radiation on photosynthesis,growth, pigmentation and calcification of the coralline alga Corallina sessilis (Rhodophyta)

Previous studies have shown that increasing atmospheric CO₂ concentrations affect calcification in some planktonic and macroalgal calcifiers due to the changed carbonate chemistry of seawater. However, little is known regarding how calcifying algae respond to solar UV radiation (UVR, UVA+UVB, 280–400 nm). UVR may act synergistically, antagonistically or independently with ocean acidification (high CO₂/low pH of seawater) to affect their calcification processes. We cultured the articulated coralline alga Corallina sessilis Yendo at 380 ppmv (low) and 1000 ppmv (high) CO₂ levels while exposing the alga to solar radiation treatments with or without UVR. The presence of UVR inhibited the growth, photosynthetic O₂ evolution and calcification rates by13%, 6% and 3% in the low and by 47%, 20% and 8% in the high CO₂ concentrations, respectively, reflecting a synergistic effect of CO₂ enrichment with UVR. UVR induced significant decline of pH in the CO₂‐enriched cultures. The contents of key photosynthetic pigments, chlorophyll a and phycobiliproteins decreased, while UV‐absorptivity increased under the high pCO₂/low pH condition. Nevertheless, UV‐induced inhibition of photosynthesis increased when the ratio of particulate inorganic carbon/particulate organic carbon decreased under the influence of CO₂‐acidified seawater, suggesting that the calcified layer played a UV‐protective role. Both UVA and UVB negatively impacted photosynthesis and calcification, but the inhibition caused by UVB was about 2.5–2.6 times that caused by UVA. The results imply that coralline algae suffer from more damage caused by UVB as they calcify less and less with progressing ocean acidification.     

Metabolically induced pH fluctuations by some coastal calcifiers exceed projected 22nd century ocean acidification: a mechanism for differential susceptibility?

Anthropogenically mediated decreases in pH, termed ocean acidification (OA), may be a major threat to marine organisms and communities. Research has focussed mainly on tropical coral reefs, but temperate reefs play a no less important ecological role in colder waters, where OA effects may first be manifest. Herein, we report that trends in pH at the surface of three ecologically important cold‐water calcifiers (a primary producer and herbivores), under a range of fluid flows, differ substantially from one another, and for two of the three calcifiers, the pH, during darkness, is lower than the mean projected pH due to OA for the surface waters of the global ocean beyond the year 2100. Using micro‐electrodes, we show that each calcifier had a different pH gradient between its surface and mainstream seawater, i.e. within the diffusion boundary layer (DBL) that appears to act as an environmental buffer to mainstream pH. Abalone encountered only mainstream seawater pH, whereas pH at the sea urchins’ surface was reduced by ~0.35 units. For coralline algae, pH was ~0.5 units higher in the light and ~0.35 units lower under darkness than in ambient mainstream seawater. This wide range of pH within the DBL of some calcifiers will probably affect their performance under projected future reductions in pH due to OA. Differing exposure to a range of surface pH may result in differential susceptibility of calcifiers to OA. Such fluctuations are no doubt regulated by the interplay of water movement, morphology and metabolic rates (e.g. respiration, calcification and/or photosynthesis). Our study, by considering physics (flow regime), chemistry (pH gradients vs. OA future projections) and biology (trophic level, physiology and morphology), reveals that predicting species‐specific responses and subsequent ecosystem restructuring to OA is complex and requires a holistic, eco‐mechanical, approach.     

Effects of multiple drivers of ocean global change on the physiology and functional gene expression of the coccolithophore Emiliania huxleyi

Ongoing ocean global change due to anthropogenic activities is causing multiple chemical and physical seawater properties to change simultaneously, which may affect the physiology of marine phytoplankton. The coccolithophore Emiliania huxleyi is a model species often employed in the study of the marine carbon cycle. The effect of ocean acidification (OA) on coccolithophore calcification has been extensively studied; however, physiological responses to multiple environmental drivers are still largely unknown. Here we examined two‐way and multiple driver effects of OA and other key environmental drivers—nitrate, phosphate, irradiance, and temperature—on the growth, photosynthetic, and calcification rates, and the elemental composition of E. huxleyi. In addition, changes in functional gene expression were examined to understand the molecular mechanisms underpinning the physiological responses. The single driver manipulation experiments suggest decreased nitrate supply being the most important driver regulating E. huxleyi physiology, by significantly reducing the growth, photosynthetic, and calcification rates. In addition, the interaction of OA and decreased nitrate supply (projected for year 2100) had more negative synergistic effects on E. huxleyi physiology than all other two‐way factorial manipulations, suggesting a linkage between the single dominant driver (nitrate) effects and interactive effects with other drivers. Simultaneous manipulation of all five environmental drivers to the conditions of the projected year 2100 had the largest negative effects on most of the physiological metrics. Furthermore, functional genes associated with inorganic carbon acquisition (RubisCO, AEL1, and δCA) and calcification (CAX3, AEL1, PATP, and NhaA2) were most downregulated by the multiple driver manipulation, revealing linkages between responses of functional gene expression and associated physiological metrics. These findings together indicate that for more holistic projections of coccolithophore responses to future ocean global change, it is necessary to understand the relative importance of environmental drivers both individually (i.e., mechanistic understanding) and interactively (i.e., cumulative effect) on coccolithophore physiology.     

Cell wall organic matrix composition and biomineralization across reef-building coralline algae under global change

Crustose coralline algae (CCA) are one of the most important benthic substrate consolidators on coral reefs through their ability to deposit calcium carbonate on an organic matrix in their cell walls. Discrete polysaccharides have been recognized for their role in biomineralization, yet little is known about the carbohydrate composition of organic matrices across CCA taxa and whether they have the capacity to modulate their organic matrix constituents amidst environmental change, particularly the threats of ocean acidification (OA) and warming. We simulated elevated pCO₂ and temperature (IPCC RCP 8.5) and subjected four mid-shelf Great Barrier Reef species of CCA to 2 months of experimentation. To assess the variability in surficial monosaccharide composition and biomineralization across species and treatments, we determined the monosaccharide composition of the polysaccharides present in the cell walls of surficial algal tissue and quantified calcification. Our results revealed dissimilarity among species' monosaccharide constituents, which suggests that organic matrices are composed of different polysaccharides across CCA taxa. We also observed that species differentially modulate composition in response to ocean acidification and warming. Our findings suggest that both variability in composition and ability to modulate monosaccharide abundance may play a crucial role in surficial biomineralization dynamics under the stress of OA and global warming.     

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.     

INTERACTIONS BETWEEN OCEAN ACIDIFICATION AND WARMING ON THE MORTALITY AND DISSOLUTION OF CORALLINE ALGAE1

Coralline algae are among the most sensitive calcifying organisms to ocean acidification as a result of increased atmospheric carbon dioxide (pCO₂). Little is known, however, about the combined impacts of increased pCO₂, ocean acidification, and sea surface temperature on tissue mortality and skeletal dissolution of coralline algae. To address this issue, we conducted factorial manipulative experiments of elevated CO₂ and temperature and examined the consequences on tissue survival and skeletal dissolution of the crustose coralline alga (CCA) Porolithon (=Hydrolithon) onkodes (Heydr.) Foslie (Corallinaceae, Rhodophyta) on the southern Great Barrier Reef (GBR), Australia. We observed that warming amplified the negative effects of high pCO₂ on the health of the algae: rates of advanced partial mortality of CCA increased from <1% to 9% under high CO₂ (from 400 to 1,100 ppm) and exacerbated to 15% under warming conditions (from 26°C to 29°C). Furthermore, the effect of pCO₂ on skeletal dissolution strongly depended on temperature. Dissolution of P. onkodes only occurred in the high‐pCO₂ treatment and was greater in the warm treatment. Enhanced skeletal dissolution was also associated with a significant increase in the abundance of endolithic algae. Our results demonstrate that P. onkodes is particularly sensitive to ocean acidification under warm conditions, suggesting that previous experiments focused on ocean acidification alone have underestimated the impact of future conditions on coralline algae. Given the central role that coralline algae play within coral reefs, these conclusions have serious ramifications for the integrity of coral‐reef ecosystems.     

Adaptive evolution in the coccolithophore Gephyrocapsa oceanica following 1,000 generations of selection under elevated CO2

Coccolithophores are important oceanic primary producers not only in terms of photosynthesis but also because they produce calcite plates called coccoliths. Ongoing ocean acidification associated with changing seawater carbonate chemistry may impair calcification and other metabolic functions in coccolithophores. While short‐term ocean acidification effects on calcification and other properties have been examined in a variety of coccolithophore species, long‐term adaptive responses have scarcely been documented, other than for the single species Emiliania huxleyi. Here, we investigated the effects of ocean acidification on another ecologically important coccolithophore species, Gephyrocapsa oceanica, following 1,000 generations of growth under elevated CO₂ conditions (1,000 μatm). High CO₂‐selected populations exhibited reduced growth rates and enhanced particulate organic carbon (POC) and nitrogen (PON) production, relative to populations selected under ambient CO₂ (400 μatm). Particulate inorganic carbon (PIC) and PIC/POC ratios decreased progressively throughout the selection period in high CO₂‐selected cell lines. All of these trait changes persisted when high CO₂‐grown populations were moved back to ambient CO₂ conditions for about 10 generations. The results suggest that the calcification of some coccolithophores may be more heavily impaired by ocean acidification than previously predicted based on short‐term studies, with potentially large implications for the ocean's carbon cycle under accelerating anthropogenic influences.     

Increased temperature mitigates the effects of ocean acidification in calcified green algae (Halimeda spp.)

The singular and interactive effects of ocean acidification and temperature on the physiology of calcified green algae (Halimeda incrassata, H. opuntia, and H. simulans) were investigated in a fully factorial, 4-week mesocosm experiment. Individual aquaria replicated treatment combinations of two pH levels (7.6 and 8.0) and two temperatures (28 and 31 °C). Rates of photosynthesis, respiration, and calcification were measured for all species both prior to and after treatment exposure. Pre-treatment measurements revealed that H. incrassata displayed higher biomass-normalized rates of photosynthesis and calcification (by 55 and 81 %, respectively) relative to H. simulans and H. opuntia. Furthermore, prior to treatment exposure, photosynthesis was positively correlated to calcification, suggesting that the latter process may be controlled by photosynthetic activity in this group. After treatment exposure, net photosynthesis was unaltered by pH, yet significantly increased with elevated temperature by 58, 38, and 37 % for H. incrassata, H. simulans, and H. opuntia, respectively. Both pH and temperature influenced calcification, but in opposing directions. On average, calcification declined by 41 % in response to pH reduction, but increased by 49 % in response to elevated temperature. Within each pH treatment, elevated temperature increased calcification by 23 % (at pH 8.0) and 74 % (at pH 7.6). Interactions between pH, temperature, and/or species were not observed. This work demonstrates that, in contrast to prior studies, increased temperature may serve to enhance the metabolic performance (photosynthesis and calcification) of some marine calcifiers, despite elevated carbon dioxide concentrations. Thus, in certain cases, ocean warming may mitigate the negative effects of acidification.

     

Photosynthesis and calcification in the articulated coralline alga Ellisolandia elongata (Corallinales,Rhodophyta) from intertidal rock pools

Calcifying coralline algae are functionally important in many ecosystems but their existence is now threatened by global climate change. The aim of this study is to improve our understanding of coralline algal metabolic functions and their interactions by assessing the respiration, photosynthesis and calcification rates in an articulated (geniculate) coralline alga, Ellisolandia elongata. Algal samples selected for this case study were collected from an intertidal rock-pool on the coast of Brittany (France). Physiological rates were assessed in summer and winter by measuring the concentration of oxygen, dissolved inorganic carbon and total alkalinity fluxes at five irradiance levels and in the dark using incubation chambers.

Respiration, photosynthetic and calcification rates were strongly affected by seasonal changes. Respiration increased with temperature, being ten-fold higher in summer than in winter. Photosynthetic parameters of the photosynthesis-irradiance (P-E) curve, P_g^max, P_n^max and E_k, were two- to three-fold higher in summer relative to winter. Photoinhibition was observed under high irradiance indicating an acclimation of E. elongata to low irradiance levels. Parameters of the calcification-irradiance (G-E) curve, G^max and E_k, were approximately two-fold higher in summer compared with winter. In summer, calcification rates were more strongly inhibited under high irradiance than photosynthetic rates, suggesting a dynamic relationship between these metabolic processes. By inhabiting intertidal rock pools, E. elongata exhibits tolerance to a dynamic physico-chemical environment. Information on respiration, photosynthesis and calcification rates in a calcifying coralline alga inhabiting such dynamic environments in terms of pH and temperature is important in order to better understand how ocean acidification and warming will affect coralline algae in the future.     

海洋酸化生态学研究进展

工业革命以来,人类排放的大量二氧化碳引起温室效应的同时,也被海洋吸收使得全球海洋出现了严重的酸化。海洋酸化及伴随的海水碳酸盐化学体系的变化对海洋生物产生深远的影响。以海洋酸化对钙化作用和光合作用的影响为重点,总结了近年来关于海洋酸化的研究,介绍了海洋中不同生态系统对海洋酸化的响应。一方面,海水中CO23-浓度和碳酸钙饱和度的降低对海洋钙化生物造成严重损害,生活在高纬的冷水珊瑚和翼足目等文石生产者是最早的受害者;贝类和棘皮动物在钙化早期对海洋酸化尤其敏感,其幼体存活率受到海洋酸化的严重制约。另一方面,CO2浓度的增加能促进海洋植物的光合作用和生长,增加初级生产力,改变浮游植物的群落组成。此外,海洋酸化可以促进固氮和脱氮作用同时削弱硝化作用,改变溶氧浓度分布和金属的生物可利用性,从而对海洋生物产生间接影响。海洋酸化对海洋生态系统的影响机制复杂,影响程度深远。为了能准确的评估海洋酸化的生态学效应,需要更全面深入的研究。